Differences between two species of Daphnia in the use of 10 - species of algae in Lake Washington

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1 Limnol. Oceanogr., 3(5), 1985, , by the American Society of Limnology and Oceanography, Inc. Differences between two species of Daphnia in the use of 1 species of algae in Lake Washington Aida Infante Apartado 47 16, Escuela de Biologia, Universidad Central, Caracas, 141 Venezuela Arni H. Litt Department of Zoology NJ 15, University of Washington, Seattle Abstract The ability of Daphnia pulicaria and Daphnia thorata to grow and reproduce when given the same concentrations of single species of algae was compared. The 1 algae selected included some of those most frequently found in the guts of Daphnia in Lake Washington. Clearing rates were determined and consumption of food expressed as number of cells ingested per day, cell volume, and carbon content. Cryptomonas and supported the highest egg production and increase in biomass. Colonial forms ( formosa,, Tabellaria, and ) were less favorable as food. Growth and reproduction were lowest with and tenuissima. Daphnia p&curia grew and reproduced faster than D. thorata with 7 of the 1 food species. The greater success of D. pulicaria than of D. thorata in the lake may be explained partly by its ability to use more effectively the energy available in a variety of foods. Daphnia pulicaria has been continuously present in Lake Washington since May 1976, forming relatively dense populations for a few weeks each year and becoming scarce in winter but not entirely disappearing. Other species of Daphnia have formed peaks at different times of year and have not been continuously present, most notably Daphnia thorata and, to a lesser extent, Daphnia galeata (Edmondson and Litt 1982). Our purpose here was to explore the question of how these differences could be related to food supply. For this, we compared the ability of D. pulicaria and D. thorata to use different species of algae. Studies of the feeding rate and rate of assimilation of different species of radioactively labeled algae by animals (Arnold 197 1; Infante 1973; Hayward and Gallup 1976) describe the ability to obtain and incorporate food, but cannot of themselves indicate the effect of a given species of food on the development and maintenance of a population. Because population dynamics are more directly related to growth rates and reproductive rates, we measured the early growth and reproduction of Daphnia when fed single species of algae. This work was supported by NSF grant DEB to W. T. Edmondson and by the Universidad Central de Venezuela. 153 We thank S. E. B. Abella for phytoplankton measurements and H. Hartmann for providing the culture of. Carbon and nitrogen were determined by D. E. Allison. We appreciated the use of M. Landry s carbon analyzer and the plankton wheels of B. Frost. Special thanks are due to W. T. Edmondson for inspiration and constant advice. Methods Cultures Daphnia cultures were started by placing single adult animals from Lake Washington in 15ml vials containing modified Woods Hole medium MBLB (Stemberger et al. 1979). The population density in each vial was maintained at two or three animals. Cultures were fed daily with a mixture of algae, supplemented every third day with bakers yeast. Trays of vials were placed in a growth chamber at 2 C (+.2 C), with continuous coolwhite fluorescent lighting. Most algae selected f& the experiments were those frequently found in the guts of Daphnia in Lake Washington during a very extensive survey of samples from all seasons of the years 1976l 98 (unpubl. data): formosa,,, tenuissima, astraea, S. hantz

2 154 Infante and Litt schii, niagarae, and Tabellaria. We also used Chlorella sp. and Cryptomonas var. reflexa. The taxonomy of the genus is under review. (Hakansson and Locker 198 1). All species were isolated from Lake Washington except for C. var. reflexa, which was provided by R. Stemberger. Single cells or colonies were isolated from plankton samples and passed through 1 washes of sterile medium. The algae were grown in MBLB medium under the same light and temperature conditions as the Daphnia. The cultures were not axenic, but sterile techniques, glassware, and culture medium were used throughout to minimize contamination with laboratory bacteria. Growth experiments The experiments were started when the feeding animals were 2 days old and had attained a mean length of 878 (+ 5) pm for D. pulicaria and 778 (+38) pm for D. thorata. At this stage, mortality from handling is less than with younger Daphnia and the animals eat algae > 1, pm3 in volume. Each animal was kept in sterile medium for 1 h to assure that the filtering apparatus was clear of unwanted algae. Two Daphnia were placed in each of five 125ml Pyrex glassstoppered reagent bottles (actually containing 135 ml) filled with medium containing a suspension of algae. The bottles, on a wheel rotating at 1.3 rpm to prevent sedimentation of food, we:e incubated for 7 days at 2 C under contmuous light to prevent diurnal changes in oxygen and ph and to maintain continued growth. Two control bottles were used, one con taining algae without Daphnia and the other Daphnia without algae. The experiment was repeated, giving a total of 2 fed Daphnia. In all bottles bubbles appeared and grew during the 7 days, indicating that photosynthesis must have maintained oxygeh concentration at levels close to saturation. Chemical analysis of additional bottles held for 7 days, showed oxygen saturation in the water and nitrate and phosphate levels adequate to maintain continued growth of the algae. This design did not permit as much control of food density as would one with daily renewal, but we thought it important to minimize handling of the animals since there seems to be a dis:inct speciesspecific difference in hardiness. Daphnia thorata was more susceptible to handling damage and its mortality was higher. The bottles were observed daily and the number of dead animals recorded. The initial concentration of algae (1, cells ml ) was the same for all species used with the exception of S. niagarae (1, cells mll) and T. (5, cells mll), which never grew to the desired densities in the cultures. We felt that the concentrations were high enough to minimize the effect of changes in abundance of food that developed during the experiment (Porter et al. 1982; Infante 1973). Since Chlorella is small we used two concentrations 1, and 2, cells mll. After 7 days, adults, juveniles, and embryos were counted and measured. Lengths of animals were measured from the top of the head to the base of the tail spine. The dry weights of groups of Daphnia of known length (lo2 animals of each size group) were determined with a Cahn model 29 electrobalance (sensitivity 1 pg). Biomass was calculated from a regression of dry weight (y, hg) on length (x, mm) of the form In y = In a + b In x; for D. pulicaria a = 5. and b = 3.24, for D. thorata, a = 3.16 and b = The regression was based on 326 D. pulicaria and 228 D. thorata. The dry weight of the embryos was determined for several different stages of different size, but these data could not be included in the regression because there was a measurable loss of weight during development. Green (1956) found a 1625% diminution in dry weight during the embryonic development in Daphnia magna and Daphnia curvirostris, and a similar loss was observed in Daphnia middendorfiana by Edmondson (1955). The embryos increased in dry weight before their release from the brood chamber. This increase rais es the possibility that late embryos can feed on particles in the water contained in the brood chamber. Embryos of D. pulicaria from Lake Washington of about stage 22 (Lei and Clifford 1974) could be seen making rapid peristaltic movements of the esophagus. The lumen of the digestive tract

3 Daphnia nutrition 155 Table 1. Survival, growth, and reproduction of Daphnia pulicaria and Daphnia thorata fed during 7 days with 1 species of algae from Lake Washington. APercentage of mortality; Bmean length of adults (pm); Cnumber of juveniles; Dmean length of juveniles (pm); Enumber of embryos; Fmean size of embryos (pm); Gtotal offspring; Htotal biomass (pg); Iincrease factor (total biomass/initial biomass). (SD in parentheses.) Food organism (cells ml ) firmosa tenuissima niagarae (1 x 13) TabelIaria (5x13) (2 x 15) Cryptomonas A B C D E F G H I D. pulicaria 25 1,316(53) 2 87(93) 17 29(2) 19 D. thorata 4 1,416(28) 4 69(66) 3 261(g) 34 D. pulicaria D. thorata 45 1,75(15) 1,147(4) D. pulicaria 5 1,541(32) 8 D. thorata 2 1,197(48) 2 D. pulicaria 3 1,262(49) D. thorata 7 945(36) D. pulicaria 1 1,161(67) D. thorata 3 1,285(49) 12 D. pulicaria 5 1,816(34) D. thorata I. 5 1,394(57) D. pulicaria 1 D. thorata 1 D. pulicaria 5 1,716(44) D. thorata 25 1,277(52) D. pulicaria 4 1,613(42) D. thorata 35 1,366(57) D. pulicaria 2 1,328(56) D. thorata D. pulicaria 3 1,115(39) 1,819(46) D. thorata 15 1,427(57) (2 1) 2 581(O) 881(98) 61(1) 959(O) 777(41) (56) (76) (53) (48) (69) (3) (12) (64) (32) 54 39(13) ) (5) 959(29) ) 72(22) (2 1) (55) (56) 285(79) 5 233(4 1) 15 22(13) (38) 58 27(7) ,92.g contained many small (34 pm) rodshaped particles that looked like bacteria. Massed together, they had a slightly pink appearance. The gut of one embryo contained a single S. (4.5 pm in diameter). At the end of the 7day growth period, the total biomass present was calculated by adding the dry weight of the embryos to the dry weight of the postembryonic stages and the increment calculated on the basis of the weight of the two initial individuals. The concentration of food before and after the experiments was determined by duplicate direct counts in a SedgwickRafter chamber. and S. were counted in a hemocytometer because the cells were too small for accurate counting with the SedgwickRafter. The gut contents of the Daphnia were examined after the experiments to observe the conditions of the cells. When algae were counted and gut contents analyzed after experiments, the bottles were also examined microscopically for bacterial growth. Clearing rates of Daphnia (milliliters cleared per individual per day) were calculated from the concentrations in the experimental and control bottles at the end of the experiment (Rigler 197 1). Feeding rates (cells consumed per individual per day) were calculated by multiplying the clearing rate by the mean concentration of cells during the experiment, using the exponential model of Edmondson (1965). Results were not used from bottles in which both Daphnia did not survive through the sixth day. Grazing by juveniles was assumed to be insignificant. The amount of carbon and nitrogen in

4 156 Infante and Litt Table 2. Cell dimensions, cell volume, carbon and nitrogen content per individual cell, and carbon and nitrogen content per cubic meter of algal cultures. (LLength; Wwidth; Ddepth; ddiameter.) Algal species formosa niagarae Tabellaria tenuissima Cryptomonas Cell dimensions Cell vol C content c vol N content N vol OLmJ) (m3) (pg cell ) (Pg m7 (pg cell ) (pg m9 C:N L=63.6 D=4.2 1, L=77. W=3.8 1, d=8.7 W= d=7.45 w= d=33 D=2.8 11,213 1, L=52.8 L=2.9 L=39.1 d=1.7 L=23.4 W=7.8 D= 12. d=7.5 d=6.2 W=ll.O , , , the different foods was measured with a Carlo Erba C&N analyzer. Results As measured by increase in biomass, D. pulicaria was more successful than D. thorata with 7 of the 1 food species (Table 1). Daphnia thorata grew about 1.1 times as much as D. pulicaria with A. formosa and S. astraea. Results were the same when reproduction was used as the criterion, except that Chlorella supported production of more eggs by D. thorata even though its growth was less than that of D. pulicaria. Mortality of D. thorata was generally higher than that of D. pulicaria, except that mortality was essentially equal at the low concentration of Chlorella and neither species survived on a diet of S. niagarae. Cryptomonas is an excellent food, the best of the 1 for both species of Daphnia. The small S. is also very favorable, ranking second for both species. Individual cells of S. astraea are a good size for Daph nia to handle but the cellsclumped together during the experiments and we could not disperse them even with strong shaking. Under these conditions, the diatom was not a very favorable food, ranking ninth for D. pulicaria and fifth for D. thorata. Stephano discus niagarae is a special case because of its large size. In Lake Washington, D. pu licaria larger than 1.4 mm can ingest entire cells, although most cells are broken. The fragments of S. niagarae found in the guts of small Daphnia (5 1.4 mm) in the lake are evidently ingested as fragments. Small Daphnia grown in cultures of S. niagarae could not break the cells and did not survive for more than 4 days. No S. niagarae was found in the guts. formosa and F. make an interesting contrast because the cells are similar in size and shape, but the colony form is very different. As a food, expressed in terms of growth (Table l), A. formosa ranked third for D. thorata, eighth for D. pulicaria. By contrast, ranked third for D. pulicaria and only ninth for D. thorata. Daphnia thorata apparently can handle colonies of A. formosa more easily than the ribbonshaped colonies of F., and do it better than D. pulicaria. is eaten in great numbers by both species of Daphnia in Lake Wash ington. In the experiments, it supported adequate growth and reproduction of both species, although it is near the middle of the list on a relative basis. tenuissima is seen less often in gut contents, and it was poor food in the experiments: none of the D. thorata developed to maturity, and D. pulicaria produced very few offspring. Direct observation showed that both species

5 Daphnia nutrition 157 Table 3. Experimental concentrations of the different food types (mean values of two sets). ABottles with Daphnia pulicaria; B bottles with Daphnia thorata. Initial concentrations: 1 x lo4 cells mll (Tabellariafinestrata: 5 x 13 cells ml ). Final concentrations are shown with SE of estimate as percent (in parentheses). Algal species formosa Tabellaria Cryptomonas Control 17,392 26,972 21,568 36,284 9,872 27,5 95, * Mean C concentration (pg C ml ) in parcnthescs. Final concn (cells ml ) Mean concn of cells during exp.* (a A B A B 9,452(12.5) 9,53( 19.2) 9,786(.579) 9,764(.577) 18,87(14.7) 25,87(24.6) 13,969(1.113) 16,673(1.328) 2,5() 3,75() 5,41(.186) 6,372(.213) 2,26(4.1) 8,41(36.3) 5,171(.151) 9,179(.268) 254(31.3) 1,344(57.4) 1,592(.361) 2,783(.728) 6,5(38.3) 6,(4.8) 8,126(1.18) 7,831(.981) 76,137(3.8) 62,868(28.7) of Daphnia had difficulty handling the filaments, and rejection movements were more frequent. The cells of M. italica are more easily separated and ingested than those of M. italica tenuissima, which have interlocking spines. The increase (Table 1, Col. I) value of Chlorella at the lower concentration equals the increase value of A. formosa for D. pu Zicaria. Distinctly lower growth and reproductive values were obtained for both species of Daphnia when fed with the higher concentration of ; this was to be expected because of the inhibitory effect of Chlorella (Ryther 1954) and because of the decrease of filtering rates and maximum feeding rate with increasing concentrations of Chlorella (McMahon and Rigler 1965). Although bacteria were not counted, they were evidently not important as a source of nutrition for Daphnia. Bacteria were never seen during the cell counts of the cultures at the end of each experiment. Pace et al. (1983) found that a population of aquatic bacteria as dense as 2 x lo7 cells ml 1 was unable to support growth of Daphnia. The fact that all our animals died on a diet of S. niagarae also suggests that bacterial biomass in the experimental vessels was too low to support 2dayold animals. On the basis of cell dimensions and the volume and appearance of food inside the gut of the animals, the 1 algae we used can be divided into two groups. The first group includes C., S., S. astraea, and, all of which can be swallowed whole. The remaining six species require separation of the cells from the colony and sometimes breakage before ingestion; if cellular material is lost through fragmentation, feeding rates will underestimate the actual carbon intake. Lampert (1978a) found up to 17% of carbon to be lost from algae broken during feeding. In addition to size and shape, the food organisms we used differed in their chemical properties (Table 2). The two food species with the highest carbon and nitrogen content per cell (S. niagarae and T. ) were not the best foods. Reasons for the better food quality of C. and S. could include their solitary condition, form, and size, despite their relatively low amounts of carbon and nitrogen. We expected changes in food concentration during the experiments due to reproduction of algal cells and consumption by the animals. We calculated the mean concentration of algae (m during the 7 days and also the mean carbon concentrations (Table 3). The algal concentrations of the controls doubled or tripled during the experiments, so that food was maintained at a high level in the bottles with Daphnia. Carbon supply remained at levels above the threshold concentration for egg production

6 158 Infante and Litt Table 4. Clearing rates, cells eaten per individual per day, volume of cells ingested, and carbon consumption of Daphnia pulicaria and Daphnia thorata fed with different foods. AClearing rates (ml indl dl); Bcells eaten (cells ind dl); Cvolume consumed (pm3 dl); Dcarbon consumption (pg C ind dl). Algal species formosa Tabellaria Ctyptomonas D. pulicaria D. thorata A B C D A B C D , , , , , , , , , , , , , , given by Lampert (1978b) for Daphnia pulex and unialgal cultures of Scenedesmus acus as.1 mg C literl. Rates of feeding were different for the various foods (Table 4). Daily cell consumption ranged from 44 to 129 x 1 O3 cells ind l d l by D. pulicaria and from 6 to 12 x 1 O3 by D. thorata. Data for the two species of Daphnia were remarkably similar for two of the algae (A. formosa and C. ) and fairly similar for others: within a factor of two for T., S., and S. astraea. The highest carbon consumption by both species of Daphnia was provided by C.. TabeZZaria followed with an unexpectedly high carbon consumption; this calculation may be an overestimate, because of the loss of carbon from broken cells. The calculations are based on the assumption that whole cells are consumed and may result in overestimates for A. formosa and F. as well. The daily carbon ingestion of S. is lower than that of C., but the number of S. astraea cells eaten per day was higher. With the exceptions discussed above, the calculated daily carbon consumption on a given food was similar for the two species of Daphnia. Nevertheless, growth and reproduction were lower for D. thorata than for D. pulicaria on 7 out of the 1 foods. Daphnia p&curia is present in Lake Washington during the entire year; D. thorata is restricted to a shorter period (Edmondson and Litt 1982). This success of D. pulicaria may be explained partly by its ability to use more effectively a wide variety of food organisms. References ARNOLD, D. E Ingestion, assimilation, survival, and reproduction by Daphnia pulex fed seven species of bluegreen algae. Limnol. Oceanogr. 16: EDMONDSON, W. T The seasonal life history of Daphnia in an arctic lake. Ecology 36: Reproductive rate of planktonic rotifers as related to food and temperature in nature. Ecol. Monogr. 35: 6 ll 11., AND A. H. LITT Daphnia in Lake Washington. Limnol. Oceanogr. 27: GREEN, J Growth, size and reproduction in Daphnia (Crustacea: Cladocera). Proc. R. Sot. Lond. 126: HAKANSSON, H., AND S. LOCKER Ehrenberg, 1846, a revision of the species described by Ehrenberg. Nova Hedwigia 35, p HAYWARD, R. S., AND D. N. GALLUP Feeding, filtering and assimilation in Daphnia schoedleri Sars as affected by environmental conditions. Arch. Hydrobiol. 77: INFANTE, A Untersuchungen fiber die Ausnutzbarkeit verschiedener Algen durch das Zooplankton. Arch. Hydrobiol. Supp1.42, p LAMPERT, W. 1978a. Release of dissolved organic carbon by grazing zooplankton. Limnol. Oceanogr. 23: b. A field study on the dependence of the fecundity of Daphnia spec. on food concentration. Oecologia 36: LEI, C., AND H. F. CLIFFORD Field and laboratory studies of Daphnia schoedleri Sars from a

7 Daphnia nutrition 159 winterkill lake ofalberta. Nat. Mus. Nat. Sci. (Can.) Publ. Zool p. MCMAHON, J. W., AND F.H. RIGLER Feeding rate of Daphnia magna Straus in different foods labeled with radioactive phosphorus. Limnol. Oceanogr. 1: 15l 13. PACE, M. L., K. G. PORTER, AND Y. S. FEIG Species and agespecific differences in bacterial resource utilization by two cooccurring cladocerans. Ecology 64: PORTER, K. G.,J. GERRITSEN, AND J. D. ORCUTT,JR The effect of food concentration on swimming patterns, feeding behavior, ingestion, assimilation, and respiration by Daphnia. Limnol. Oceanogr. 27: RIGLER, F. H Feeding rates, p In W. T. Edmondson and G. G. Winberg [eds.], Secondary productivity in fresh waters. IBP Handbook 17. Blackwell. RYTHER, J. H Inhibitory effects of phytoplankton upon the feeding of Daphnia magna with reference to growth, reproduction and survival. Ecology 35: STEMBERGER, R.S.,D.R. FULLER,AND A.M. BEETON &Role of predacious rotifers in Great Lakes plankton dynamics. Natl. Ocean. Atmos. Admin. Final Rep. Univ. Mich. 57. Submitted: 28 July 1983 Accepted: 22 March 1985