Energy Reserves of Three Zoop Ankton Species from Two Lakes with Different Meta Concentrations
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Energy Reserves of Three Zoop ankton Species from Two Lakes with Different Meta Concentrations Michael T. Arts and W. Gary Sprules Dep~ftrnenbof Zoologv, Erlndaie College, Un~r/ersityof Toronto, Mi,>r>~auga,Ont. C5b IC6 Arts, tM. T., and W. G. Sprules. 1987. Energy reserves of three zooplankton species from two lakes with different metal concentrations. Can. 1. Fish. Aquat. Sci. 44: 458-466. Dry weight and lipid content sf three zooplankton species in two lakes differing in concentrations of copper, nic keB, and aluminum were assayed for tiyo consecutive summers. Epischura 1,acustris ;and Wolopediurn gibberurn had lower lipid levels and were generally lighter in the lake with elevated metals. 'The lipid droplet in eggs of H. gibberurn was 21 % smaller in the lake with elevated metal [evels. Total body burdens sf copper in W. gibberurn were twice as high in the lake with elevated metals. There was ~CPdifference in dry weight and levels of energy reserves of Didpeomu minutus between the lakes. Lower lipid content and decreased weight of E. lacustris and W. gibberuns fraamr Round Lake could wot be explained by lowered food availability, since both the edible portion of phytoplankton biomass and abundance of small Bosmirsa were similar in the two lakes. Since there were ns differences in food levels for E. lacujtrij and H. gibberurn in the two lakes, eve attributed lower energy reserves in these species to effects of heavy metal contamination. Pendant deux 6tes consecutifs, on a d6termine le poids sec et la teneur en lipides de trois espPces de mooplanston pekeplant deux lacs & diffkrentes concentrations de cuivre, de nickel et d'alurniniurn. Dans Be lac A concentration @leveede metaux, Epischura lacustris et Molopedium gibberurn avaient des teneurs en lipides moins @leveeset leur psids etait en general plus faible. Bans les oeufs de H. gibberurn, les gouttelettes lipidiques Gtaient 21 % plus petites dans le cas du lac 2 concentration klevge de metaux. Les charges corporel[es totales de cuivre chez H. gibbeaunl 6taient deux fois plus elevkes dans ce dernier lac. Aucune difference relative au poids sec ou aux niveaux de reserves energetiques chez Biaptornus rnirautus n'a 6te relevee d'un lac ii J'autre. Une plus faible disponibilite de nourriture n'a pu expliquer la faible teneur en lipides et le poids inf6rieur de E. lacuseris et de H. gibberurn du lac Round car la partie comestible de la biornasse phytoplanctonique et I'abondance de petites Bosmir~a6taient semblables dans Bes deux lacs. Conime il n'existe aucune diiikrence' quant 2 la quantite de nourriture disponible pour E. Ic2custri_iet PI. gibberurn d'un lac B I'autre, on attribue les faibles r6serves her- getiques chez ces espPces aux effets de la contamination par des rn6taux Isurds. Received November 6 5, 7 986 Accepted October 22, 1986 ( J85 70 ) riacylglycerols predominate as an energy reserve in vivo synthesis of triacylglycerols, in organisms from bacteria freshwater zoopiankton (Golaiden and Hsrniy 1980; to man, have shown that this enzyme can contain up to 98 Fagkas et al. 898 1; Gcserlden and Henry 1984). These sulfiydryl groups (Burton et a!. 1968, rats and pigeons). Hsu energy resenes play a critical role during periods of et al. (1965) demonstrated that the enzyme was susceptible to starvation (Lee and Barnes 19'75) and affect competitive ability heavy metal inactivation, since chelating agents such as EDTA among neonates (Gosslden and Henry 1984). Zooplankton sue- stimulated activity in the presence of heavy metals as much as cum$ quickly to starvation (Threlkeld 1976); thus, any inter- 200% over controls without EDTA. Thus, uptake sf heavy ference in the accumulation or synthesis sf these energy re- metals capable of inactivating the kitty acid synthetase complex serves could have important ecological consequences. occurs directly in the intestinal tissue. the major site of tri- Triacylglycerol synthesis may represent a target site for met- acylglycerol synthesis. The dry weight of some species, for al cations. Metal ions often exert their toxic effect on aquatic example Dlsphnisi Bairagna, is reduced in solutions of copper or organisms by binding to enzymes and forming transition-metal nickel (Biesinger and Christensen 1972) and nickel alone (Hall complexes, with complex stability largely determining the tox- 19801, and since triacylglycerols can contribute significantly to icity of the metal ion (Shaw 1961). Effects of metal poisoning the total dry weight (up to 25% in Hkalopediurn gibberurn). it on enzyme systems have been documented for sea urchin em- seems likely that some of this weight loss could be explained bryos (Tirnourian and Watchmaker 19729, crayfish (Hub- by fat loss. Alternatively, reduction in filtration rates in zoo- schman L967), and fishes (Crandall and Goodnight 1963; plankton exposed to metals (Flickinger et al. 1982) could result McKim et al. 1970; Jackirn et al. 1970; Jackirn 1973: Bryan in reduced food gathering ability and thus lower lipid levels. 1976). Triacylglycersl synthesis occurs primarily in the cells of Numerous estimates of lethal metal concentrations have been the intestinal wall (Gsulden and Henry 1984), an important site made using organisms such as Dsag~huia!(Bieseazger and Chris- of uptake for metals such as nickel (Hall 1980). Studies on the tensen 1972; Baudouin and Scoppa 1974; Winner and Fan-ell ubiiqtriitous fatty acid synthetase complex responsible for the in 1976; Shcherban 1977) and trout (Brown and Dalton 1970; 458 Can. 9. Fish. Ayuut. Sc-i., Vd.44, 1987 McKim and Benoit 197 1; Dmmmond et al. 1973). While these nizer. Centrifugation at 4588 x g for 15 min removed heavy studies outlined conditions associated uith short-term survival, carapace components. Triacylglycerols were separated by thin- chronic effects of toxins have rarely been assessed (however, layer chromatography on silica gel plates (kieselgel 606. E. see Winner and Fanell 1976; Borgmann et al. 1980). especially Merck Co.). The solvent system used was 90: 10: 1 6v/v) pe- under field conditions (Yan and Stms 1980). troleum ether - diethyl ether - glacial acetic acid (Malins and We measured triacylglycerol energy reserves (storage fats) Mangold 1960). Triacylglycerols were detected with iodine in three zooplankton species, Episcshlrr6~luc-srstv-is Forbes, and quantified calorimetrically (Pye Unisarn SP6) using a sul- Diaptcrmlrs minutus Lilljeborg. and Holspediscrn gibberams furic acid - dichromate reagent (Arn~enta1964). Trjipalmitin Zaddach. common to a metal-contanainated and an uncon- standard was used for calibration. taminated Iake in central Ontario. These species occur in 65, The availability of food naturally affects energy reserves in 43, and 6292, respectively. sf 666 lakes in norfheastem North organisms. Therefore, for both lakes. in 1982, we estimated America (Carter et al. 1980). Because of its wide geographical density of Bosmina lorzgir-sstris (8. F. hjuller), a small clado- range (Carter et al. 1980) and presence in acid and metal- ceran that is the major component sf the diet of E. 1ac.lrsrri.s stressed lakes (Spmles 1975: Yan and Strus 1980B, Dominutus (Wong 198 1 ). Roughly every 2 wk, two metered-hauls using appears to be a tolerant species. Based on geographical distri- the Wisconsin-style townet from bottom to surface over the bution, we predict that if chronic exposure to elevated metal center of the deepest basin were combined and preserved visith concentration affects triacylglycerols. then E. bacustris and H. 5% formalin. A microcon~puter-based measuring device gibbsr~nawould have Bower levels of triacylglycerols in the (Spmles et al. 1981) coupled to a dissecting microscope was metal-contaminated lake whereas B. ~nis~utaaswould show little used to determine densities of B. Iongirostv-is. or no difference between the lakes. Egg and fat droplet diameters of H. gibbpsraun were measured using a dissecting microscope (Wild-Leitz, M5) with an ocular Methods micrometer. As a rough index of algal food available to the herbivorous Two lakes were chosen for comparative purposes: Blue D. sninutus and H. gibb~rurra,the biolgaass of edible algae Chalk Lake in the Muskoka district of south-central Ontario, (<30 pm) was determined in both lakes. Samples were taken which has metal levels at or below the limits of detection of with a weighted Tygon tube 66 m x 1 cm) over the deepest standard atomic absorption methods. and Round Lake, 1-4 krn basin in the lake at approximately 2-wk intervals in 1981 southwest of Sudbury, Ontario, with substantially higher levels (May-August). Ten such integrated hauls were combined in a of copper, nickel, and aluminum. plastic bucket. A 100-mL aliquot was removed for phyto- Zooplankton for lipid analyses were obtained at roughly plankton analyses and preserved with Lugol's acidified iodine 2-wk intervals, from May to October in 1981 and May to solution. Five millilitres from this bottle was settled overnight August in 1982, by unmetered vertical townet hauls from bot- onto a microscope slide that had been pretreated with a gel to tom to surface at the center of the deepest basin. The large enhance adhesion of settled algae (Knoechel and Kalff 1976). zooplankters E. Bacustv-is and H. gibbsruraa were collected with Slides were desiccated over silica gel for 24 h. A drop of 10% a tapered net, length I .5 m with a 1-rn' opening, and 1 mm glycerol in water was added after which slides were preserved mesh (Nero 1982). This net was used to advantage for E. by sealing the edges of the coverslip with nailpolish. Counting lacaastris, since this species can avoid smaller nets and rarely was done by transects on a binocular. inverted, conapound achieves densities in excess of 1.5 animals/&. A Wisconsin- microscope (Leitz b'etzlar, Diavert). Phytoplankton were di- style townet with 30- and 45-cm hoops and 153-pm mesh was vided into four groups - unicells.