Relative Importance of Competition with Daphnia (Cladocera) and Nutrient Limitation on Anuraeopsis (Rotifera) Population Dynamics in a Laboratory Study

Freshwater Biology (2000) 44, 423±430 Relative importance of competition with Daphnia (Cladocera) and nutrient limitation on Anuraeopsis (Rotifera) population dynamics in a laboratory study

JOSEÂ M. CONDE-PORCUNA Institute of Water Research, University of Granada, E-18071 Granada, Spain

SUMMARY 1. In the laboratory, the growth and reproduction of Anuraeopsis fissa were measured when fed on Scenedesmus species grown in nutrient-sufficient, nitrogen-limited and phosphorus- limited media and in the presence or absence of one adult Daphnia longispina per vial. 2. Poor food quality may reduce the effect of competition on rotifers. Competition from Daphnia was stronger with nutrient sufficient algae than with nutrient limited algae. P- limitation significantly reduced Anuraeopsis population growth rate and fecundity. The effect of nutrient limitation on Anuraeopsis was stronger than that of competition with Daphnia. The Anuraeopsis population declined with P-limited food in both the presence and absence of Daphnia. 3. Exploitative competition by Daphnia on Anuraeopsis was stronger in the nutrient- sufficient treatment than in the N-limited one. Density, fecundity and population growth rate of Anuraeopsis were negatively affected by Daphnia in the nutrient-sufficient treatment, while only fecundity was reduced by Daphnia in the N-limited treatment. Consequently, in the N-limited treatment, mortality should be lower in the presence of Daphnia. This result could suggest that Anuraeopsis lives longer when short of nitrogen. 4. Nutrient limitation may affect to the competitive interactions between zooplankton species. P-limitation decreased the quality of algae as food for Anuraeopsis while N- limitation decreased the susceptibility of this rotifer species to exploitative competition by Daphnia. Keywords: zooplankton; Daphnia; competition; Anuraeopsis; nutrient limitation

Introduction tissues while releasing those present in excess of their requirements (Urabe, 1993; Carrillo, Reche & Cruz- Organisms differ in the proportions of major elements Pizarro, 1996). Algae have relatively high ratios of C:P that they contain. This includes N and P, which are and C:N and, under N or P limitation, the C:N:P ratio known to be highly dynamic and potentially limiting of phytoplankton varies considerably (Goldman, to production of aquatic ecosystems (Sterner & McCarthy & Peavy, 1979). Such biochemical responses Hessen, 1994). According to stoichiometric theory, of algae to resource limitation should affect their nutrient cycling, zooplankton growth and competition quality as food for animals. among grazers are all tightly coupled with resource Nitrogen and, particularly, P limitation reduce the nutrient ratios (Sterner & Hessen, 1994). Consumers quality of algae as food for Daphnia in laboratory incorporate most of a limiting nutrient into their own studies (Groeger, Schram & Marzolf, 1991; Sterner et al., 1993; Sterner & Robinson, 1994; Urabe, Clasen & Sterner, 1997; Van Donk et al., 1997; Weers & Gulati, 1997; DeMott, 1998; DeMott, Gulati & Siewertsen, 1998). The effects of algal nutrient limitation on Correspondence: Department of Animal Biology and Ecology, Faculty of Sciences, University of Granada, E-18071 Granada, algivorous rotifers are less well known, although Spain. E-mail: [email protected] Rothhaupt (1995) observed that N and, particularly, P

ã 2000 Blackwell Science Ltd. 423 424 J. M. Conde-Porcuna limitation in algae decreased the population growth Methods rate of Brachionus rubens (Ehrenberg). Anuraeopsis fissa and Daphnia longispina (MuÈ ller) Sterner & Robinson (1994) suggested that, due to were cultured using Scenedesmus acutus as food the differential partitioning between maintenance source for more than 1 month before starting the metabolism and growth, the effect of food quality experiments. Scenedesmus was grown in batch may change with food concentration. The difference cultures using a modified Beijerinck medium between low and high quality food should be less at (Table 1). low food concentration when most of the assimilate is For this study, a single clone of Scenedesmus was respired, but greater at high food concentration when grown for 5 days in several batch cultures using most is allocated to growth. three types of the growth medium (Table 1) with N Rothhaupt (1995) showed that N limitation of and P adjusted to produce N-limiting (200 mm N: rotifers occurs only at high food concentration when, 100 mm P, N:P = 2), P-limiting (606 mm N: 4 mm P, despite of loss respiratory carbon, the stoichiometry of N:P = 151.5) and nutrient-sufficient (606 mm N: the food available for growth remains unfavourable. 100 mm P, N:P = 6.1) conditions. Consequently, However, more studies are needed to assess the three types of Scenedesmus were used in the present importance of nutrient limitation on other rotifers. On study. Temperature was 20 °C. Log-phase algae the other hand, several studies have suggested the were harvested after being centrifuged at ca. 3 000 importance of biotic factors in determining the r.p.m. for 10 min. structure of rotifer plankton (Dumont, 1977; Lampert Experiments were conducted in 50-mL plastic vials & Rothhaupt, 1991; Urabe, 1992; Paul & Schindler, containing 50 mL of dechlorinated tap-water with an 1994; Conde-Porcuna, 1998; Conde-Porcuna & initial algal density of 4 ´ 105 cells ml±1 for each Declerck, 1998). Daphnia can affect rotifer populations treatment (N-limited, P-limited and nutrient-sufficient negatively through exploitative and/or interference algae). The food concentration is near the threshold competition (mechanical and/or chemical interfer- for population growth of that clone of A. fissa fed on ence) (Burns & Gilbert, 1986; Gilbert, 1988; MacIsaac & Scenedesmus (Dumont, Sarma & Ali, 1995; Sarma, Gilbert, 1991a,b; Conde-Porcuna, Morales-Baquero & Nandini & Dumont, 1996). Cruz-Pizarro, 1994; Sarnelle, 1997; Conde-Porcuna, The effects of nutrient limitation were tested in the 1998). presence and absence of one adult of Daphnia to check In natural situations, Daphnia may reduce the for the relative importance of nutrient limitation and density of phytoplankton-suppressing herbivorous competition by Daphnia. rotifers through exploitative competition and Forty-five individuals of A. fissa were inoculated in mechanical interference. Both mechanisms are stron- the vials (900 ind L±1). The initial rotifer population ger at low food concentration (Gilbert, 1988). In included adults (egg-bearing and nonegg-bearing) addition, phytoplankton in the field can occasionally be nutrient limited. As a consequence, the relative Table 1 Composition of the algal growth medium (modified importance for rotifer populations of competition by from Stein, 1966) Daphnia (including exploitative and interference competition) and nutrient limitation need to be Compound Final medium (mg L±1) analysed. Sommer (1992) found, under certain cir- NH4NO3 As needed (see text) cumstances, intraspecific facilitation instead of com- KH2PO4 As needed (see text) petition when the animals were limited by food MgSO4 4.500 quality. This occurred because reduction of algal H3BO3 0.715 . density by grazing increased the per capita P income ZnSO4 7H2O 0.055 . CuSO4 5H2O 0.020 of the algae and therefore improved their quality as . MnSO4 7H2O 0.635 food source. . Co(NO3)2 6H2O 0.015 In this paper, I try to verify the relative importance . (NH4)6Mo7O24 4H2O 0.004 . of competition by Daphnia and nutrient limitation CaCl2 6H2O 1.075 . effects on Anuraeopsis fissa (Gosse), a cosmopolitan C6H5FeO7 H2O 1.325 C H O .H O 1.325 rotifer species. 6 8 7 2

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 423±430 Competition and nutrient limitation effects on Anuraeopsis 425 and neonates. The experimental vials were main- Results tained at 19 ‹ 1 °C in a well illuminated (103 ´ 10± Anuraeopsis density increased with time in both the 3 Wm±2; 14 h light/10 h dark photoperiod) room. For nutrient-sufficient and N-limited treatments, particu- Daphnia treatments, one adult of Daphnia longispina larly in the former (Fig. 1). Rotifer fecundity declined (» 1.4 mm) was placed in each vial (20 ind L±1). Three replicates were used for each treatment, so the experimental set up consisted of a total of 18 vials (three food types ´ presence or absence of Daphnia ´ three replicates). In all cases, every 2± 3 days rotifers and eggs were counted and the vials were cleaned. After counting, rotifers were trans- ferred into the vials containing 20 mL of fresh medium with Scenedesmus (4 ´ 105 cells ml±1) and 30 mL of the `old` medium. As a consequence, 40% of the medium was replaced with fresh medium and algae. Because just 40% of the medium was changed, food limitation effects due to Daphnia and rotifer feeding were maintained during the experi- ment. New-born Daphnia were removed from the vials during the experiment. The rate of increase (day±1)ofAnuraeopsis was calculated using the exponential rate of population increase:

r = (ln Nt ±lnN0)/t where Nt and N0 are population densities at times t and 0, and t is time in days. Fecundity of A. fissa was estimated as the number of eggs per female. Statistical analyses were performed using the STATISTICA program (Statsoft, Inc. 1998). Two-way repeated measures ANOVAs were used to determine differences in the density, fecundity and population growth rate of Anuraeopsis in time. To avoid temporal pseudoreplication these analyses are recommended when using repeated measures designs (time) with replicate treatments (Hulbert & White, 1993). Homo- geneity of variances and normality were checked by Bartlett`s test and the Kolmogorov±Smirnov-test, respectively (Sokal & Rohlf, 1981). Density and fecundity of A. fissa were logarithmic transformed to comply with these assumptions for ANOVA, while no transformation was needed for the rate of population increase. The effect of the presence of Daphnia for each nutrient treatment was tested with a least-significant- difference test, LSD (planned comparisons: compar- isons were planned before the experiment had been carried out and the results obtained), and probability values were adjusted for the number of simultaneous Fig. 1 Population density of A. fissa as a function of nutrient limitation and Daphnia presence during this study; (X) without tests using the sequential Bonferroni method (Rice, Daphnia,(B) with Daphnia. Each value is mean ‹ SE based on 1989). three replicates.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 423±430 426 J. M. Conde-Porcuna in the P-limited treatment while fluctuating patterns ment, population growth rate declined in the presence were observed in the N-limited and nutrient-sufficient and absence of Daphnia while, in the nutrient- treatments (Fig. 2). Anuraeopsis growth rate declined sufficient treatment, growth rate clearly declined in in time in the nutrient-sufficient treatment when the presence of Daphnia (Fig. 3). Daphnia was present (Fig. 3). In the P-limited treat-

Fig. 2 Changes in the fecundity of Anuraeopsis (no. of eggs per Fig. 3 Variations in growth rates (r)ofAnuraeopsis as a function female) as a function of nutrient limitation and Daphnia presence of nutrient limitation and Daphnia presence during this study; during this study; (X) without Daphnia,(B) with Daphnia. Each (X) without Daphnia,(B) with Daphnia. Each value is mean ‹ SE value is mean ‹ SE based on three replicates. based on three replicates.

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 423±430 Competition and nutrient limitation effects on Anuraeopsis 427 Table 2 Analyses of variance with repeated measures demonstrating the effects of D. longispina and nutrient treatment (C = nutrient- sufficient; NL = N-limited; PL = P-limited) on the density, fecundity and growth rate of A. fissa population. All MS and F-values are rounded to two significant digits

Density Fecundity Growth rate

Effects d.f. MS FP MS FP MS FP Daphnia 1 0.52 2.38 < 0.149 0.05 7.72 < 0.017 0.15 6.51 < 0.025 Nutrient treatment 2 2.30 10.54 < 0.01 0.17 28.67 < 0.0001 0.34 14.39 < 0.0001 Daphnia ´ nutrient 2 0.43 1.98 < 0.181 0.00 0.53 < 0.603 0.02 0.87 < 0.445 Error 12 0.22 0.01 0.02 Time 4 1.35 35.61 < 0.0001 0.08 14.37 < 0.0001 0.34 28.45 < 0.0001 Daphnia ´ time 4 0.38 10.06 < 0.0001 0.02 4.59 < 0.01 0.09 7.78 < 0.0001 Nutrient treatment ´ time 8 0.65 17.29 < 0.0001 0.01 1.65 < 0.136 0.09 7.42 < 0.0001 Daphnia ´ nutrient ´ time 8 0.06 1.51 < 0.179 0.01 1.52 < 0.175 0.03 2.28 < 0.038 Error 48 0.04 0.01 0.01

Nutrient effect: planned comparisons (LSD test) probabilities ranked from low to high average value of the different demographic traits: density PL < C NS NL; fecundity PL < < C NS NL; growth rate PL < C NS NL. Planned comparisons: < , significantly smaller at P < 0.01; < < , significantly smaller at P < 0.001; NS not significantly different.

Two-way repeated measures ANOVA show that last day shows a tendency for an effect of Daphnia on nutrient limitation significantly affected the demo- Anuraeopsis density for the N-limited treatment, this graphic traits of A. fissa (Table 2). This effect was comparison was not statistically significant. However, mainly due to P limitation, since there were no Anuraeopsis fecundity was reduced by Daphnia not differences between nutrient-sufficient and N-limited only in the nutrient-sufficient but also in the N-limited treatments (Table 2). Anuraeopsis population growth treatments after the day 7 (Fig. 2; Table 3). As a and density also varied through time in different consequence, Anuraeopsis density was only reduced Daphnia (Daphnia ´ time) and nutrient (nutrient ´ - by Daphnia in the nutrient-sufficient treatment and time) treatments. Daphnia had no overall direct effect Anuraeopsis fecundity was reduced by Daphnia in both on Anuraeopsis density. Fecundity of Anuraeopsis was nutrient-sufficient and N-limited treatments. also negatively affected by P limitation and by Daphnia. Contrast analyses of the population parameters of Discussion Anuraeopsis with and without Daphnia but with identical food types show that the growth rate and Studies dealing with the influence of food quality on density of Anuraeopsis were significantly reduced by rotifer populations are very scarce (Rothhaupt, 1990, Daphnia in the nutrient-sufficient treatment after day 7 1995). It is possible to imagine situations where slight (Figs 1 and 3; Table 3), particularly at day 13 (LSD competition, combined with other adverse conditions test, P = 0.005). On the contrary, growth rate and (such as poor food quality), would cause extinction. density of Anuraeopsis were not reduced by Daphnia in Although several studies have considered the impor- the N-limited and P-limited treatments. Although the tance of the different types of competition by Daphnia on rotifer populations (Gilbert, 1988; MacIsaac & Table 3 Planned comparisons (contrast analyses, LSD test) of the Gilbert, 1991a,b; Conde-Porcuna et al., 1994; Fuss- density, fecundity and growth rate of Anuraeopsis in the presence mann, 1996; Conde-Porcuna, 1998), however, no and absence of Daphnia after day 7 (days 10 and 13) previous attempt has been made to assess the relative Density Fecundity Growth rate importance for rotifer dynamic of competition by

Food type PP P Daphnia and nutrient limitation. Nutrient-sufficient 0.012* 0.002* 0.016* In the present study, Anuraeopsis populations were N-limited 0.331 0.007* 0.209 mainly affected by nutrient limitation, particularly P-limited 0.773 0.612 0.055 phosphorus. This effect increased with time. This *Significant differences (P < 0.05) in the sequential Bonferroni confirms the results of previous studies showing the test. importance of P-limitation on several zooplankton

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 423±430 428 J. M. Conde-Porcuna populations (Sommer, 1992; Sterner et al., 1993; Urabe, changes of the cell wall in P-limited green algae that 1993; Rothhaupt, 1995; Urabe et al., 1997; Weers & could explain resistance to digestion by Daphnia.In Gulati, 1997; DeMott et al., 1998; DeMott, 1998). contrast, N-limitation had only minor effects on cell Rothhaupt (1995) showed that N-limited Scenedes- morphology and digestibility (Sterner & Hessen, mus allowed similar rotifer growth rates at low to 1994). The decrease in food quality using P-limited moderate concentrations of food. According to this, algae could be a direct effect of P, as well as an Anuraeopsis population growth rate and density were indirect effect caused by changes in both biochemistry not affected by N-limited food (Table 2) at the levels of and cell wall morphology (Weers & Gulati, 1997). food supplied in this study, the latter being considered However, DeMott et al. (1998) obtained data that low for Anuraeopsis by Dumont et al. (1995). conflict with the notion that P-limited green algae With respect to the competitive effects of Daphnia, are resistant to digestion. Their data support stoichio- MacIsaac & Gilbert (1991a) observed that mechanical metric theory and the elemental limitation hypothesis. interference by Daphnia was especially important Sterner & Robinson (1994) found that P-sufficient and initially but declined thereafter, while exploitative P-limited Scenedesmus were equal in quality at low competition increased with time. In the present study, food concentration near the food quantity threshold evidence of competition by Daphnia did not become for growth. In contrast P-limited Scenedesmus were a marked until after day 7, and the overall mean poor food at high concentrations. These results are Anuraeopsis density was not significantly affected by also predicted by stoichiometric theory but further Daphnia. Moreover, Conde-Porcuna et al. (1994) have contradict the notion of a defence against digestion in already shown that Anuraeopsis population density P-limited Scenedesmus. In the present study, however, was not affected by mechanical interference by P-limited Scenedesmus were a poor food for Anuraeop- Daphnia at a higher density than those in the present sis at the food concentrations of the experiment. study. All these aspects suggest that mechanical P-limitation could have affected the individual interference should be negligible in this study. growth of Daphnia and this could have been a factor The negative effect of Daphnia increased with time, in this study. However, Daphnia survival was high in so exploitative competition and chemical interference all treatments (» 82%) and Daphnia mortality was by Daphnia could have been important in the experi- observed only during the first days of the experiment. ment. Conde-Porcuna (1998) observed that the pre- At the end of the experiment Daphnia individuals sence of Daphnia-mediated chemicals induced a lower were preserved in formalin and measured fecundity and a decrease in the intrinsic rate of (mean ‹ SD: 1.8 ‹ 0.2 mm). No significant differences population growth in the rotifer Keratella. However, in were found between treatments for the size of Daphnia that study the densities of Daphnia were much higher at the end of the experiment (ANOVA: d.f. = 2,6; than those in the present study. In addition, in the F = 1.36; P = 0.33). A contrast analysis between the present experiment 40% of the medium was replaced final size of Daphnia in the control treatment and that every 2±3 days, so chemical interference would have in the P-limited treatment shows that there was no been minimised. As a consequence, the negative significant difference (P = 0.20). As a consequence, for impact of Daphnia on Anuraeopsis during the experi- the length and conditions of the experiment, the ment was probably due to exploitative competition. P- individual growth of Daphnia was not affected by limitation was the main factor controlling Anuraeopsis nutrient limitation. Rotifers should be more sensitive dynamics during this study. Furthermore, there was to P-limitation than Daphnia, and the Daphnia popula- no significant effect of Daphnia in the P treatment, tion would need to be exposed to longer periods of which suggests that Anuraeopsis declined strongly, nutrient limitation before starting to decline. because of P-limitation, before any shortage of food It is a general phenomenon of phytoplankton that in due to Daphnia feeding could have been relevant. This nutrient-limited cells, the content of highly unsaturated could be related to the low digestibility of P-limited fatty acids decreases while saturated fatty acids may Scenedesmus, which can pass through the guts of increase (Harrison, Thompson & Calderwood, 1990). A Daphnia undamaged (Sterner & Smith, 1993; Sterner high percentage of unsaturated fatty acids has been et al., 1993; Van Donk & Hessen, 1993; Van Donk et al., related to a high nutritional quality of the algae 1997). Van Donk & Hessen (1993) showed structural (Ahlgren et al., 1990). However, Gulati & DeMott

ã 2000 Blackwell Science Ltd, Freshwater Biology, 44, 423±430 Competition and nutrient limitation effects on Anuraeopsis 429 (1997) consider that P limitation and fatty acid limita- tion growth is high. Predation, low food abundance tion are not mutually exclusive alternatives. The two, (not due to grazing) and low food quality should separately or in conjunction, can control growth of at reduce the potential for competition. These aspects least some lake zooplankters. In any case, the accumu- should be taking in account when studying interac- lating evidence for P limitation is stronger than that for tions between rotifers and other zooplankton. fatty acid limitation (Gulati & DeMott, 1997). There were significant effects of Daphnia on demo- Acknowledgments graphic traits of Anuraeopsis in the N-limited and nutrient-sufficient treatments, and especially in the Financial support was provided from a PP grant latter. Scenedesmus cultures on N-limited media (University of Granada, Spain) and from CICYT project allocated more carbon to lipid and less to protein AMB97-0996 (Spain). I am grateful for the use of than when cultured on N-sufficient media (Groeger facilities at the Laboratory of Animal Ecology (Uni- et al., 1991). Groeger et al. (1991) showed that Daphnia versity of Ghent, Belgium). I thank two anonymous fed algae grown on N-deficient media allocated more referees for improving the manuscript. I also thank to lipid to eggs, and their offspring lived longer under Dr S.S.S. Sarma for providing the A. fissa stock. starvation conditions. Probably, rotifer offspring in N- limited situations could also live longer under food References limited conditions, as does Daphnia. This could explain the different effects of Daphnia (exploitative Ahlgren G., Lundstedt L., Brett M. & Forsberg C. (1990) Lipid composition and food quality of some freshwater competition) on Anuraeopsis in the N-limited and phytoplankton for cladoceran zooplankters. Journal of nutrient-sufficient treatments. In the last days of the Plankton Research, 12, 809±818. experiment (after day 7), fecundity of Anuraeopsis was Burns C.W. & Gilbert J.J. (1986) Effects of daphnid size and significantly reduced by Daphnia in both treatments, density on interference between Daphnia and Keratella while density and growth rate were not reduced in the cochlearis. Limnology and Oceanography, 31, 848±858. N-limited treatment (Fig. 1; Table 3). According to Carrillo P., Reche I. & Cruz-Pizarro L. (1996) Intraspecific this, survival of Anuraeopsis should be higher in the N- stoichiometric variability and the ratio of nitrogen to limited treatment than that in the high-quality food phosphorus resupplied by zooplankton. Freshwater treatment when Daphnia is present. Consequently, at Biology, 36, 363±374. the degree of N-limitation used in the present Conde-Porcuna J.M. (1998) Chemical interference by experiment, Anuraeopsis is less susceptible to exploi- Daphnia on Keratella: a life table experiment. Journal of tative competition by Daphnia when growing on N- Plankton Research, 20, 1637±1644. Conde-Porcuna J.M. & Declerck S. (1998) Regulation of limited algae. rotifer species by invertebrate predators in a hyper- In summary, this experiment shows that P-limita- trophic lake: selective predation on egg-bearing fe- tion decreased the quality of algae as food for A. fissa, males and induction of morphological defences. Journal and that nutrient limitation reduced the effect of of Plankton Research, 20, 605±618. Daphnia competition. N-limitation decreased the Conde-Porcuna J.M., Morales-Baquero R. & Cruz-Pizarro susceptibility of A. fissa to exploitative competition L. (1994) Effects of Daphnia longispina on rotifer by Daphnia. Rothhaupt (1995) indicated that field data populations in a natural environment: relative impor- suggest that, at least occasionally, nutrient limitation tance of food limitation and interference competition. may also apply to rotifers in nature. Some rotifer Journal of Plankton Research, 16, 691±706. species, at least, should be more sensitive to P DeMott W.R. (1998) Utilization of a cyanobacterium and limitation than Daphnia. In the present experiment a phosphorus-deficient green alga as complementary there was no evidence of any effect of P limitation on resources by daphnids. Ecology, 79, 2463±2481. DeMott W.R., Gulati R.D. & Siewertsen K. (1998) Effects the individual growth and survival of Daphnia, for 13 of phosphorus-deficient diets on the carbon and d, while Anuraeopsis was clearly affected by P phosphorus balance of Daphnia magna. Limnology and limitation. It is important to study how food quality Oceanography, 43, 1147±1161. may influence the strength, importance and outcome Dumont H.J. (1977) Biotic factors in the population of competition. In general, the potential for competi- dynamics of rotifers. Archive fuÈr Hydrobiologie Beihefte tion should be higher when the potential for popula- Ergebnisse der Limnologie, 8, 126±129.

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