Algal nutrient limitation affects rotifer growth rate but not ingestion rate
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1 Limnol. Oceanogr., 4(7), 1995, , by the American Society of Limnology and Oceanography, Inc. Algal nutrient limitation affects rotifer growth rate but not ingestion rate Karl. Rothhaupt Max-Planck-Institute of Limnology, Department of Physiological Ecology, P.O. Box 165, D-2432 Plijn, Germany Abstract The food algae Scenedesmus acutus and Cyclotella meneghiniana were grown in chemostats in a modified WC medium at identical growth rates (.4 d-l) but under different nutrient regimes. Nitrate or phosphate was reduced to produce N- or P-limited algae. Brachionus rubens did not differentiate between nonnutrientlimited and nutrient-limited Scenedesmus and ingested both at comparable rates. The rotifers reached highest maximum growth rates with nonnutricnt-limited Scenedesmus. N-limited Scenedesmus permitted similar growth rates at low food concentrations (below the incipient limiting level, ILL), but maximum growth rates at high food concentrations (above the ILL) were significantly reduced. With regard to the high N content of Brachionus, direct mineral N deficiency of the food appears to be possible. P-limited algae (Scenedesmus and Cyclotella) permitted no positive growth rates of the rotifers at all. P-limited algae that were short-term enriched with phosphate contained similar amounts of P as nonnutrient-limited algae but still were of lower nutritional quality, thus suggesting the importance of essential biochemical constituents. Herbiviorous zooplankton can be limited by the amount and the quality of their food resources (Lampert 1985). Algal species can differ in their nutritional quality if they are ingested differently due to their size or shape (Rothhaupt 199a) or if they differ in their biochemical composition (Ahlgren et al. 199). Blue-green algae (cyanobacteria) are known especially to often be a low-quality food (e.g. Arnold 1971; Lampert 1981). However, nutritional quality is determined not only by the taxonomic composition of the phytoplankton, but also by the growth conditions (Smith 1991). N limitation (Giani 1991) and especially P limitation (Sterner 1993) are known to reduce the nutritional quality of food algae for Daphnia. Since nutrient limitation is reflected by algal stoichiometry, the hypothesis of elemental limitation of the zooplankton has been put forward (Hessen 1992; Urabe and Watanabe 1992). Sterner and Robinson (1994) suggested that due to the differential partitioning between maintenance metabolism and growth, food quality effects may change with food concentration. Food lacking essential substances for growth may still supply enough energy for maintenance metabolism. By consequence, the difference between a low- and a high-quality food should be minor at low food concentrations when most of the assimilation is respired, but the difference should be great at high food concentrations when a large proportion is alloted to growth. The experiments I report here were done to investigate how N and P limitation of the coccale green alga Scenedesmus acutus affect the ingestion and population growth rates of the rotifer Brachionus rubens at various food concentrations. With regard to the effects of P limitation, I did, some comparative experiments with the diatom Cyclotel2a meneghiniana. Because I was mainly interested Acknowledgments Heinke Buhtz and Anita Bark provided technical assistance. Winfried Lampert, Alan Tessier, David Kirchman, and two anonymous referees helped to improve the manuscript. in the effects of the nature of nutrient limitation (N or P), I kept the intensity of growth limitation constant by growing the food algae in chemostats with identical dilution (=growth) rates. Methods Rotifers and algae-all cultivation and experimentation was done in temperature-controlled chambers at 2 t- 1 C. The rotifers as well as the algae were kept in WC (=MBL) medium (Guillard and Lorenzen 1972). B. rubens was from the zooplankton cultures at the Max-Planck- Institute in Pliin. Stock cultures were kept in 3-ml Erlenmeyer flasks; they were fed Scenedesmus (N 2.5 mg C liter- l) three times a week, and the medium was renewed every 2 weeks. The coccale green alga S. acutus (almost exclusively single cells; 6-pm equivalent spherical diameter, ESD) was from the culture collection at the Max-Planck-Institute in Plijn; the centric diatom C. meneghiniana (8.5- pm ESD) was from the culture collection at the University of Giittingen (culture number 12-1 a). Food algae were grown in chemostats at a dilution rate of.4 d-l. For P-limited algae, the phosphate concentration of the WC medium was reduced to 2 PM; for N-limited algae, the medium had a nitrate concentration of 4 PM. Unmodified WC medium has a phosphate concentration of 5,uM and a nitrate concentration of 1,,uM. The che- mostats had volumes of 75 or 2, ml and were continuously illuminated (- 1 pmol quanta mm2 s-l). Nutrient analyses - Particulate C and N were determined in a C/N analyzer (NA 15, Carlo Erba). Samples were filtered on precombusted (4-5 h at 45 C) glass-fiber filters (Whatman GF/C) and dried at 6 C overnight. Particulate P was determined on.2-pm membrane filters (cellulose nitrate, Sartorius) after acidic persulfate digestion (Koroleff 1976). Dissolved nutrients were analyzed according to standard procedures (Strickland and Parsons 121
2 122 Rothhaupt 1972). All particulate and dissolved nutrient analyses were duplicated. The food concentrations are given in carbon equivalents (mg C liter-l). Food suspensions were mixed according to previously established calibration curves of extinction (8 nm) vs. carbon content.for each limitation type. If not mentioned otherwise, food suspensions of N- or P-limited algae were prepared with medium lacking the respective nutrient to avoid subsequent uptake. The phosphate uptake of P-limited algae was tested by adding phosphate to algal suspensions of known carbon content (Scenedesmus: 1 mg C liter- + 8 PM PO,; Cyclotella: 2.5 mg C liter- + 2 PM POJ. I estimated the P uptake and the change in the C : P ratio of the algae from the decline of the phosphate concentration in the medium. The algal cultures were not axenic. Nevertheless, bacterial P uptake should have played a minor role, because P partitioning between algae and bacteria is known to be concentration-dependent. Although bacteria have high affinities at low nutrient concentrations, algae are superior with regard to maximum uptake rates at high nutrient concentrations. In tracer experiments with comparable phytoplankton cultures, P uptake in unenriched cultures was dominated by bacteria. A phosphate addition of.25 PM already led to >9% uptake by phytoplankton, and the share of the phytoplankton even increased with higher enrichments (Rothhaupt and Glide 1992). Determination of ingestion rates-because the food uptake of herbivorous zooplankton depends on the longterm adaptation of the animals (several days; Rothhaupt and Lampert 1992), I preadapted the rotifers under identical conditions. They were kept at a food concentration of.5 mg C liter-l (Scenedesmus, not nutrient limited) for 4 d. The animals were incubated in slowly rotating bottles and transferred into fresh.food suspensions every day. Ingestion and clearance rates were determined with 14Clabeled algae. I incubated 1 ml of algal suspension with 3.7 MBq NaH14C3 for h. Labeled algae were centrifuged twice and resuspended in WC medium. Feeding experiments were run in duplicate jars. About 5 animals were pipetted into lo-ml unlabeled food suspension of the desired concentration and allowed to adapt for at least 1 h. Then 25 ml of labeled food suspension of the same concentration was added. After a feeding time of 1 min, the animals were separated with 52-pm nets, narcotized in carbonated water (3 s), rinsed with deionized water, and fixed in a Petri dish with a few drops of formaldehyde. Groups of 12 animals were then transferred into scintillation vials. Animals were dissolved in.3 ml of tissue solubilizer (Soluene 35) and counted with 5 ml of toluene scintillator; 2 ml of the food suspension was counted with 3.5 ml of water-absorbing scintillation cocktail (Instagel II + 5% Carbosorb, all chemicals by Packard). The activity of all samples was determined in a Packard Tri-Carb 15 scintillation counter. Clearance and ingestion rates were calculated according to Peters (1984). Determination ofpopulation growth rates-three stoppered glass tubes (35-ml volume) for each food type and concentration received 3 animals each and were kept in the dark on a slowly rotating wheel at - 1 rpm. At most 25%, but usually much less, of the food suspension was cleared per day. At 24-h intervals, the food suspension was completely renewed. The rotifers were counted and classified to the type (subitaneous, male, resting eggs) and number of eggs carried by removing individuals with micropipettes under a dissecting microscope. Thirty rotifers (or the remaining ones in the case of negative growth rates) were pipetted back into the culture tube. I took care not to change the population structure and therefore put back proportionate numbers of female animals without eggs, with male eggs, with resting eggs, and with 1,2, etc. subitaneous eggs. Mictic females (with male or resting eggs) always were < 1% of the total population. When percent increase or decrease had stabilized for at least 3 d (C.V. I O.l), the experiment was terminated. Intrinsic growth rates for daily intervals were calculated as r = In(iV,) - ln(n,-,). Here r is the intrinsic growth rate (d-l), and N,-,,, is animal numbers on consecutive days. The functional relationships between food densities and growth rates were expressed as modified Monod curves (Monod 195) with a threshold for zero population growth (Rothhaupt 199a): r = r,,,(s - S,)/(S - So + K,). r max is the maximum growth rate (d-l), S is the food concentration (mg C liter- ), So is the threshold for zero growth (mg C liter-l), and K, is the Monod constant (mg C liter-l). Because numerical and functional responses were determined at identical food concentrations, the modified Monod model was also used to express the relationship between ingestion rates and growth rates. Curves were fitted to data by iterative nonlinear regression (STSC Inc. 1985). Results Algalgrowth limitation andparticulate nutrient ratios- The type of algal growth limitation (e.g. N, P) is determined by the nutrient that is in minimum supply relative to other nutrients or to light. The intensity of nutrient limitation of chemostat-grown algae is determined by the dilution rate (=steady state growth rate). The input concentration of the limiting nutrient influences the biomass attained but not the intensity of nutrient limitation. Maximum growth rates in batch cultures with nonlimiting nutrient concentrations were 1.2 d-l for Scenedesmus and.9 d-l for Cyclotella (unpubl. results). Hence, Scenedesmus grew with 33% and Cyclotella grew with 45% of its maximum growth rate under steady state conditions in the chemostats when the dilution rate was.4 d-l. In the chemostats with nutrient-reduced media, algal
3 Nutrient-limited rotlyer food 123 Table 1. Particulate nutrient concentrations in the algal cultures (values of duplicate measurements) and average atomic C : N: P ratios. One nitrogen measurement failed in both Cyclotella cultures. C N P (mg liter - I) C:N:P Scenedesmus 43.3i / :3.7:1 Scenedesmus N lim 6.6i6.6.52/ / :8.3: 1 Scenedesmus P lim 21.4/ ' / :72.7:1 Cyclotella 2.5i /-.485/ : 12.6: 1 Cyclotella P lim 15.8/ /-.62/ :57.:1 growth was limited by the concentration of the respective nutrient in short supply. In P-limited cultures of Scenedesmus and Cyclotella, soluble reactive P was at or below the limit of detectability (-. 15 PM), and in the N-limited Scenedesmus culture, the inorganic N concentration (NH4 + NOz + N3) was as low as 1.4 PM. The growthlimiting factor was not evident in the chemostats with a full medium. Here, algal growth may have been limited by the availability of light or of inorganic C. The nature of algal growth limitation was reflected by the particulate nutrient ratios (Table 1). C : P ratios were highest for P-limited algae, and N-limited Scenedesmus had the highest C : N ratio. Body stoichiometry of Brachionus-Body contents of C, N, and P were estimated from a rotifer population that had reached a high density at a high food concentration (Table 2). Brachionus differed from its food algae mainly due to a high N content. Influence of nutrient limitation on the ingestion of Scenedesmus- Ingestion rates were determined at increasing food concentrations of.125,.25,.5, 1,2, and 4 mg C liter- l. For all three limitation types of Scenedesmus, Brachionus showed similar functional responses with increasing food concentration that corresponded well to a rectilinear Blackman model with maximum clearance rates below and maximum ingestion rates above a critical food concentration (incipient limiting level, ILL; Rigler 1961) of - 1 mg C liter-l (Fig. 1). To judge the influence of the type of algal growth limitation on the food uptake by Brachionus, I therefore compared the maximum clearance rates below the ILL (.125,.25, and.5 mg C liter- ) and the maximum ingestion rates above the ILL (2 and 4 mg C liter- ) by means of one-way ANOVA. The maximum clearance rates (F = 1.O 12; 2, 15 dfi P =.387) as well as the maximum ingestion rates (F= 2.933; Table 2. Body contents of C, N, and P (values of duplicate measurements) and average atomic nutrient ratios of Brachionus rubens. C N P (ng ind- I) C:N:P 173.4/ i / :22.7:1 2, 9 df; P =.15) were not significantly different for the three food qualities. Influence of nutrient limitation of the food algae on the population growth rates ofbrachionus-population growth rates of Brachionus were determined at the same Scenedesmus concentrations as the feeding rates. Population growth rates increased hyperbolically with the food concentration when both nonnutrient-limited and N-limited Scenedesmus were fed to the rotifers (Fig. 2). The relationship in both cases was well described by the modified Monod model (Table 3). Brachionus reached higher maximum growth rates with the nonnutrient-limited Scenedesmus as a food alga (Fig. 2). A two-way ANOVA with interaction term showed that both main effects (the food concentration and the type of limitation of the food algae) as well as the interaction term were highly significant (Table 4). Pairwise comparisons of the growth rates on nonnutrient-limited and on N-limited food at identical food concentrations by means of Bonferroni-adjusted t-tests confirmed the original impression that only the growth rates at the two highest food concentrations (2 and 4 mg C liter- I) were significantly different between both foods (Table 5). LLI G a F a* i V 3 Q V V V FOOD CONCENTRATION (mg C liter- ) Fig. 1. Ingestion rates by Brachionus rubens of Scenedesmus in varying states of limitation. Nonnutrient limited-e; N limited-; P limited-v.
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5 Nutrient-limited rotifer food 125 Table 5. Pair-wise comparison of the growth rates of Brachionus rubens with nonnutrient- and N-limited Scenedesmus as a food. Asterisks: *- significant differences (P <.5) in the Bonferroni-adjusted t-tests. 1 Food concn (mg C liter- ) t df P <O.OOl <.1* Y a 25 mitted lower maximum growth rates at high concentrations of food; no positive population growth was possible with P-limited Scenedesmus as a food. There are three possible explanations for these different qualities of food. First, P-limited Scenedesmus resist digestion and therefore are of low nutritional quality. Second, nutrient-limited algae deviate in their cell stoichiometries from the demands of the rotifers; consequently, like their food, the animals are limited by mineral nutrients. Third, nutrient-limited algae have lower contents of certain biochemical constituents, such as amino acids, unsaturated fatty acids, or vitamins; consequently, the rotifers are limited by essential biochemical constituents. 2 3 DAYS Fig. 3. Population growth of Brachionus rubens with a food concentration of 1 mg C liter- l. Symbols are means (+ SE; n = 3) of the animal numbers reached after 1 d. Due to the routine schedule, numbers were reduced to the original densities (3 animals) when the population growth was positive. The food was nonnutrient-limited Scenedesmus in medium without P (O), P-limited Scenedesmus in medium with P (O), and P-limited Scenedesmus in medium without P (). 1 I I I I I o DAYS Fig. 4. As Fig. 3, but with Cyclotella as food (2.5 mg C liter-i). Due to the routine schedule, numbers were reduced to the original densities (5 animals) when the population growth was positive. Grazing resistance and nutritional quality-van Donk and Hessen (1993) supposed the resistance to digestion by Daphnia to be due to changes in the structure of the cell wall in P-limited coccale green algae. However, it seems that this does not explain the low nutritional quality of P-limited algae for Brachionus, because the diatom Cyclotella as well as the green alga Scenedesmus were unsuitable foods when they had been grown under P limitation. Cell walls of green algae consist of cellulose and pectin, while diatom cell walls consist of silica, It is therefore unlikely that both groups have evolved similar mechanisms of digestion resistance. Diatoms do, however, frequently excrete excess C in the form of mucuslike compounds. This effect may be epecially pronounced under P or N deficiency and may also block digestive enzymes. Elemental or biochemical limitation of Brachionus - To judge the possibility of the rotifers direct mineral nutrient limitation due to the different cell stoichiometries of Scenedesmus, I plotted the population growth rates against ingestion rates for the elements C, N, and P that had been determined at identical food concentrations and qualities (Fig. 5). As expected, there is no simple relationship explaining the growth rates by the ingestion rates ofjust one element. When the relationships between growth rates and ingestion rates are expressed as modified Monod models, the fits for the whole data set are relatively poor (C ingestion: R 2 =.265; N ingestion: R2 =.35 1; P ingestion: R2 =.41). When the data for P-limited food are omitted, the fits for the C- and N-ingestion models are improved (C ingestion: R2 =.768; N ingestion: R2 =.843). Similarly, the fit for the P-ingestion model is improved when the data for N-limited food are omitted (R2 =.86). It thus seems that the growth rates
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7 Nutrient-limited rotifer food 127 food quality for Brachionus when they had been grown Table 6. Estimated production efficiencies (production : inunder P limitation, the content of eicosapentaenoic acid gestion) of Brachionus rubens with nonnutrient- and N-limited probably was not the limiting factor for the rotifers. Scenedesmus as a food at food concentrations >ILL. The superiority of nonnutrient-limited over N-limited Scenedesmus at food concentrations above the ILL may Nutrient Production efficiency for bc due to direct N deficiency in the N-limited algae. A limitation C N high N content was measured in the body mass of Bra- None chionus. The C : N ratio is equivalent to a nitrogen content N limited of 12.3% in dry weight under the assumption that the carbon content corresponds to -45% of dry weight. Similarly high N contents were reported by Schliiter (1984) approach, Sommer (1988) found that in the moderately for B. rubens (12-14% N in dry wt) and by Scott (198) eutrophic Schiihsee (northern Germany), N and P limifor Brachionus plicatilis (12.4% N in dry wt). The following is an attempt to estimate the N and C yields (K, ; production : ingestion) of Brachionus for N-limited and nonnutrient-limited Scenedesmus at food concentrations above the ILL with a significantly different quality of each food. Rotifer C : N ratios for lower food concentrations were not determined. Daily production rates for N and C can be calculated from the population growth rates of the rotifers (Fig. 2) and their body contents of N and C (Table 2). Ingestion rates for N and C are known from the feeding experiments (Fig. 5). Even though the yields calculated from these data can be regarded only as rough estimates and especially for N appear to be too high, they suggest that nitrogen was better utilized than carbon (Table 6). The N-limited food algae resulted in an especially low C yield of the rotifers. Direct N limitation of Brachionus at high concentrations of N-limited food is thus conceivable. Schliiter (1984) found a dry-weight-related yield of.43 and a nitrogen yield of.86 for B. rubens. Consistent with this study, his food algae had lower N contents than did the rotifers. Droop and Scott (1978) worked with an experimental system in which B. plicatilis was limited by cyanocobalamine (vitamin B,,). They reported a carbon yield of.225, a nitrogen yield of.16 1, and a B,, yield of.743 for the limiting cyanocobalamine. Interaction of food quantity and food quality-the growth rate patterns with nonnutrient- and N-limited food closely resemble a hypothetical relationship proposed by Sterner and Robinson (1994; cf. their fig. 1): The lowquality food is equal to the high-quality food at low to moderate concentrations of food but has a lower plateau at high concentrations of food. At low concentrations of food, maintenance metabolism forms a significant part of the total food ingestion (Sterner and Robinson 1994). If mainly substrates without N (lipids, carbohydrates) are respired, this raises the share of N in the assimilated food that is actually available for production and so may prevent N limitation at low concentrations of food. N limitation would occur only at high concentrations of food, when, in spite of respiratory carbon losses, the stoichiometry of the food available for growth remains unfavorable. Relevance to the natural situation-phytoplankton in the field can be nutrient limited at times. Using a biotest tation of single algal species was discontinuous in time and mostly weak to moderate. Short periods of severe limitation- however, did occur. In early June 1986, for example, the growth of Rhodomonas sp. in the lake was severly P limited (< 25% of the maximum growth rate), as was the case for the whole phytoplankton fraction < 1 pm (N 5% reduction of the average growth rate)-the probable food base for rotifers. In the shallow hypertrophic Binnensee (northern Germany), P was limiting for the growth of most phytoplankton species in May and early June 1987 (Sommer 1989). N limitation prevailed later in the year and often severely reduced the growth rates of the dominating coccale green algae (Scenedesmus spp. and Monoraphidium spp.). There are several species of Brachionus (B. rubens, B. calyctjlorus, B. quadridentatus) in the lake (unpubl. data), and the system thus appears to be comparable to my laboratory study. During 1987, Brachionus first appeared in the lake in late June after the end of the early phase of P limitation (Lampcrt and Rothhaupt 1991). In conclusion, the experiments reported here support the view that algal nutrient limitation can constrain grazer production. N limitation and particularly P limitation decreased the food quality of algae for the rotifer B. rubens. Field data suggest that at least occasionally, this may also apply to rotifers in nature. References AHLGREN, G., L. LUNDSTEDT, M. BRETT, AND C. FORSBERG Lipid composition and food quality of some freshwater phytoplankton for cladoceran zooplankters. J. Plankton Rcs. 12: ARNOLD, D. E Ingestion, assimilation, survival, and reproduction by Daphnia pulex fed seven species of bluegreen algae. Limnol. Oceanogr. 16: DROOP, M. R., AND J. M. SCOTT Steady-state energetics of a planktonic herbivore. J. Mar. Biol. Assoc. U.K. 58: GIANI, A Implications of phytoplankton chemical composition for zooplankton production: Experimental evidence. Oecologia 87: GUILLARD, R. R. L., AND C. J. LORENZEN Yellow-green algae with chlorophyllide c. J. Phycol. 8: HARRISON, P. J., P. A. THOMPSON, AND G. S. CALDERWOOD Effects of nutrient and light limitation on the biochemical composition of phytoplankton. J. Appl. Phycol. 2:
8 128 Rothhaupt HESSEN, D Nutrient element limitation of zooplankton production. Am. Nat. 14: KIBRBOE, T Phytoplankton growth rate and nitrogen content: Implications for feeding and fecundity in a herbivorous copepod. Mar. Ecol. Prog. Ser. 55: KOROLEFF, F Determination of phosphorus, p In K. Grasshoff [ed.], Methods of seawater analysis. Verlag Chemie. LAMPERT, W Inhibitory and toxic effects of blue-green algae on Daphnia. Int. Rev. Gesamten Hydrobiol. 66: Food limitation and the structure of zooplankton communities. Ergeb. Limnol. 21: 497 p. -, AND K.. ROTHHAUPT Alternating dynamics of rotifers and Daphnia magna in a shallow lake. Arch. Hydrobiol. 12: MONOD, J La technique de culture continue. Theorie et application. Ann. Inst. Pasteur 79: MILLER-NAVARRA, D Quantifizierung von Nahrungsqualitat fur herbivores Zooplankton. Ph.D. thesis, Christian-Albrechts Univ. 135 p Evidence that a highly unsaturated fatty acid limits Daphnia growth in nature. Arch. Hydobiol. 132: PETERS, R. H Methods for the study of feeding, grazing and assimilation by zooplankton, p In J. A. Downing und F. H. Rigler [eds.], A manual on methods for the assessment of secondary productivity in fresh waters, 2nd ed. IBP Handbook 17. Blackwell. RIGLER, F. H The relation between concentration of food and filtering rate of Daphnia magna Straus. Can. J. Zool. 39: ROTHHAUPT, K.. 199a. Population growth rates of two closely related rotifer species: Effects of food quantity, particle size, and nutritional quality. Freshwater Biol. 23: 56 l b. Changes of the functional responses of the rotifers Brachionus rubens and Brachionus calyciflorus with particle sizes. Limnol. Oceanogr. 35: , AND H. GLADE The influence of spatial and temporal concentration gradients on phosphate partitioning between different size fractions of plankton: Further evidence and possible causes. Limnol. Oceanogr. 37: , AND W. LAMPERT Growth-rate dependent feed- ing rates in Daphnia pulicaria and Brachionus rubens: Adaptation to intermediate time-scale variations in food abundance. J. Plankton Res. 14: SCHL~~TER, M Kontinuierliche Massenkultur des planktischen Rotators Brachionus rubens. Ber. KFA Jiilich No SCOTT, J. M Effect of growth rate of the food alga on the growth/ingestion efficiency of a marine herbivore. J. Mar. Biol. Assoc. U.K. 6: SMITH, V. H Competition between consumers. Limnol. Oceanogr. 36: SOMMER, U Does nutrient competition among phytoplankton occur in situ? Int. Ver. Theor. Angew. Limnol. Verh. 23: Nutrient status and nutrient competition ofphytoplankton in a shallow, hypertrophic lake. Limnol. Oceanogr. 34: 1162-l 173. STERNER, R. W Daphnia growth on varying quality of Scenedesmus: Mineral limitation of zooplankton. Ecology 74: 235 l-236. AND J. L. ROBINSON Thresholds for growth in Dhphnia magna with high and low phosphorus. Limnol. Oceanogr. 39: AND R. F. SMITH Clearance, ingestion and release of N and P by Daphnia pulex feeding on Scenedesmus acutus of varying nutritional quality. Bull. Mar. Sci. 53: STBTTRUP, J. G., AND J. JENSEN Influence of algal diet on feeding and egg-production of the Calanoid copepod Acartia tonsa Dana. J. Exp. Mar. Biol. Ecol. 141: STRICKLAND, J. D. H., AND T. R. PARSONS A practical handbook of seawater analysis, 2nd ed. Bull. Fish. Res. Bd. Can STSC, INC Statgraphics: Statistical graphics system. URABE, J., AND Y. WATANABE Possibility of N or P limitation for planktonic cladocerans: An experimental test. Limnol. Oceanogr. 37: VAN DONK, E., AND D.. HESSEN Grazing-resistance in nutrient-stressed phytoplankton. Oecologia 93: Submitted: 12 October 1994 Accepted: 1 May 1995 Amended: 1 June 1995
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