Influence of food quality on growth and reproduction in Daphnia

SUMMARY. 1. Growth and reproduction were measured for Daphnia pulex (Leydig) fed Scenedesmus obliquus (Turp.) Kutz. grown with nitrogen-sufficient and nitrogen-deficient media. The incorporation of carbon into the body of D. pulex was traced using ¹⁴C-labelled algae and biochemical fractionation.
2. Scenedesmus cultured on N-defkient media allocated more carbon to lipid and less to protein than when cultured on N-sufficient media.
3. In a short-term feeding experiment, Daphnia accumulated more lipid when fed N-deficient algal cells high in lipid content than when fed algae grown on N-sufficient media that were lower in lipid.
4. Animals grew faster and produced larger broods when fed algae grown on an N-sufficient medium over an 8-day period. Daphnids fed N-deficient algae had higher quantities of body lipid, suggesting it was not a lack of energy which limited their growth and reproduction.
5. Daphnia fed algae grown on N-deficient media allocated more lipid to eggs, and their offspring lived longer under starvation conditions.     

Effects of UVB-irradiated algae on life history traits of Daphnia pulex

1. The impact of ultraviolet-B (UVB)-irradiated phytoplankton on the life history parameters of Daphnia was studied. Three species of Chlorophyceae ( Chlamydomonas reinhardtii, Scenedesmus acutus and S. subspicatus ) and one species of Cryptophyceae ( Cryptomonas pyrenoidifera ) were cultured with and without exposure to UVB radiation (biologically effective dose of 3 kJ m^–2 day^–1 DNA weighted) and fed to Daphnia pulex.
2. The daphnids feeding on UVB-irradiated algae tended to be smaller in size, to produce less and smaller offspring, and to have a reduced population growth rate.
3. Fatty acid (FA) analysis of the phytoplankton showed a reduced total FA content under UVB radiation for all four species. Changes in the content of unsaturated fatty acids (UFA) were species specific.
4. The results indicate that the energy transfer between the primary producers' and grazers' level might be negatively influenced by UVB radiation. Direct effects on food quality are modest but detectable, changes in quantity or species composition may be more important in the energy transfer.     

Dietary essential amino acids affect the reproduction of the keystone herbivore Daphnia pulex

Recent studies have indicated that nitrogen availability can be an important determinant of primary production in freshwater lakes and that herbivore growth can be limited by low dietary nitrogen availability. Furthermore, a lack of specific essential nitrogenous biochemicals (such as essential amino acids) might be another important constraint on the fitness of consumers. This might be of particular importance for cladoceran zooplankton, which can switch between two alternative reproductive strategies--the production of subitaneously developing and resting eggs. Here, we hypothesize that both the somatic growth and the type of reproduction of the aquatic keystone herbivore Daphnia is limited by the availability of specific essential amino acids in the diet. In laboratory experiments, we investigated this hypothesis by feeding a high quality phytoplankton organism (Cryptomonas) and a green alga of moderate nutritional quality (Chlamydomonas) to a clone of Daphnia pulex with and without the addition of essential amino acids. The somatic growth of D. pulex differed between the algae of different nutritional quality, but not dependent on the addition of dissolved amino acids. However, in reproduction experiments, where moderate crowding conditions at saturating food quantities were applied, addition of the essential amino acids arginine and histidine (but not lysine and threonine) increased the total number and the developmental stage of subitaneous eggs. While D. pulex did not produce resting eggs on Cryptomonas, relatively high numbers of resting eggs were released on Chlamydomonas. When arginine and histidine were added to the green algal diet, the production of resting eggs was effectively suppressed. This demonstrates the high, but previously overlooked importance of single essential amino acids for the reproductive strategy of the aquatic keystone herbivore Daphnia.     

Changes in food quality of the green alga Scenedesmus induced by Daphnia infochemicals: biochemical composition and morphology

1. The effects of Daphnia infochemicals on the morphology and biochemical composition of Scenedesmus were studied and subsequently their influence on Daphnia life history. Three species of Scenedesmus ( S. acutus, S. obliquus and S. subspicatus ) were tested for Daphnia -induced colony formation. Life history experiments were performed with Daphnia cucullata and D. magna feeding on unicellular or colonial S. acutus.
2. Colony formation was promoted when S. acutus and S. obliquus were exposed to filtered water from a D. magna culture. S. subspicatus did not form colonies when exposed to culture water, but showed some colony formation when exposed to live D. magna.
3. No clear differences were found in total lipid, protein or carbohydrate content between the unicellular and colonial ecomorphs of the three Scenedesmus species. However, fatty acid (FA) concentration and composition were changed. Total FA as a percentage of frozen dry weight (DW) were increased in colonies. The ratio of monounsaturated (MUFA) and polyunsaturated fatty acids (PUFA) and the ratio of ω3 : ω6 fatty acids decreased in colonies.
4. A short-term grazing experiment with three size classes of Scenedesmus revealed lower clearance rates for small Daphnia when feeding on large colonial Scenedesmus.
5. Life history parameters of both Daphnia species were influenced by food type. The intrinsic rate of population increase ( r) was significantly lower for daphnids feeding on colonies.
6. The negative influence of colonial Scenedesmus on population growth of Daphnia seems to be determined by algal morphology rather than biochemical composition.     

Effects of algal food quality on fecundity and population growth rates of Daphnia

1. Food quality was at least as important as food quantity for both fecundity and population growth responses of the cladoceran Daphnia pulicaria fed the green alga Ankistrodesmus falcatus grown under N limitation, P limitation, or non-limited condition.
2. The fecundity of D. pulicaria was reduced under conditions of low food quality (low N or low P) compared with that for animals fed control non-limited algae regardless of ration size. The reduced fecundity of D. pulicaria fed P-limited food could be partially alleviated by increasing the ration (hence, compensation), but such was not the case for animals fed N-limited food.
3. Population growth rates of D. pulicaria ( r _max) were significantly reduced under conditions of low-quality food for both N-limited and P-limited algae. Population growth rates were unaffected by ration size, indicating no compensation.     

The relative importance of algae and bacteria as food for Daphnia longispina (Cladocera) in a polyhumic lake

SUMMARY. 1. Grazing on algae and bacteria by the planktonic cladoceran, Daphnia longispina , was studied in a small polyhumic lake with low phytoplankton primary production in southern Finland.
2. D. longispina filtered algae at average rates of 0.09-0.82 ml ind⁻¹ h⁻¹. The filtering rates on bacteria were 26-92% of those on algae in parallel experiments.
3. From June to August algae, including mixotrophic and heterotrophic forms, comprised 56-93% of the food ingested by D. longispina. In mid-September and early October, when the Daphnia population was declining and the algal biomass was low, bacteria comprised 73% and 55% respectively of the food of Daphnia.
4. For D. longispina , an energy pathway via bacteria and bactivorous flagellates is probably a more important link to allochthonous organic matter than direct utilization of epilimnetic bacteria.     

Relationships between heterotrophic nanoflagellates and the demographic response of Daphnia longispina in a eutrophic lake with poor food quality conditions

1. Based on both field data and laboratory studies, the summer population of Daphnia longispina living in a stratified eutrophic lake was examined in relation to the abundance of algae, nanoflagellates and picocyanobacteria.
2. In early July, the Daphnia population replaced Bosmina and remained the dominant zooplankter during summer 1994. Its development in July was concomitant with an increase of edible algae but, despite the apparent abundance in available food, the Daphnia population decreased throughout August suggesting poor food conditions.
3. From mid-August to the beginning of September, the biomass of inedible phytoplankton was greater than that of the smaller, edible fraction. Consequently the average rate of increase, birth rates and fecundity of Daphnia remained low. Although the biomass of heterotrophic nanoflagellates was consistently low, the demographic parameters of Daphnia were correlated throughout this period with these protozoans.
4. Life table experiments run in the laboratory showed that epilimnetic food supported both the growth in length of individual Daphnia and an increase in fecundity, but metalimnetic food supported only individual growth. D. longispina probably failed to reproduce because of the abundance of detritus mixed with the heterotrophic nanoflagellates in the metalimnetic water at that period of the year. The vertical migration of Daphnia into these deeper layers could be caused by a predator avoidance mechanism.     

Population growth rates of two closely related rotifer species: effects of food quantity, particle size, and nutritional quality

SUMMARY. 1. The relationship between population growth rates and the concentrations of several algal species was determined in laboratory experiments with the rotifers Brachionus rubens and B. calyciflorus .
2. The effects of food quantity were well described by a modified Monod model with a threshold for zero population growth. The model parameters depended on particle size and nutritional quality of the food algae. Differences between the rotifer species were significant and reflected their varying food-size preferences.
3. For each rotifer species, thresholds were lowest for algae in the most readily ingested size range. The lowest thresholds were 0.07–0.09 mgC 1⁻¹ with algae of about 5 μm equivalent spherical diameter (ESD) for B. rubens , and 0.19 mgC 1⁻¹ with algae of about 10 μm ESD for B. calyciflorus .
4. Maximal growth rates ( r _max) were slightly below 0.8 day⁻¹ for both rotifers with most algal species. The highest r _max values for both rotifers were observed when Cyclotella meneghiniana was provided as food. With this alga, B. calyciflorus had a significantly higher r_max (1.02 day⁻¹) than B. rubens (0.838 day⁻¹).
5. From a comparison of the relationship between growth rates and ingestion rates, Chlamydomonas reinhardii appeared to be of low nutritional quality for B. rubens .
6. Egg ratios were related to growth rate and were not influenced by the algal food used. Egg development times and average mortality rates were estimated from the relationship between egg ratio and growth rate. B. calyciflorus appeared to have a high average mortality rate (0.383 day⁻¹) compared to B. rubens (0.083 day⁻¹).     

Behavioural response of Daphnia to olfactory cues from food, competitors and predators

The behavioural response of the freshwater zooplankter Daphniato chemicals from its food, the green alga Scenedesmus, to algalcells, to the green colour from chlorophyll, to chemicals releasedfrom congeners and conspecifics, and to chemicals released frominvertebrate (Chaoborus) and vertebrate predators (Leuciscus)was investigated in a Y-tube olfactometer. No preference wasobserved either for medium that had contained algae, or formedium with algal cells or with the green colour of algae, offeredas alternatives to clean medium. In contrast, swimming speedwas significantly reduced at high algal concentrations and inthe presence of green colour. Moreover, starved animals hadlost their rheotaxis. Neither Daphnia magna nor Daphnia pulexhad a preference for either clean medium or medium that hadcontained conspecifics, but D. magna significantly chose cleanmedium when medium which had been inhabited by D. pulex wasthe alternative. No avoidance of medium from Chaoborus cultureswas found, but D. magna significantly avoided medium that hadbeen inhabited by ides (Leuciscus idus L.). The responses observedcould result in aggregation of animals by reduced swimming speedat high algal densities and by avoidance of areas with predators.When these cues have become less important due to food depletionand decreased predation pressure, the interspecific-competitor-relatedcues might result in desegregation.     

Invasibility of a reservoir to exotic Daphnia lumholtzi: experimental assessment of diet selection and life history responses to cyanobacteria

SUMMARY 1. In reservoirs of the south-central United States, the exotic cladoceran Daphnia lumholtzi is common during warm midsummer conditions, when cyanobacteria are abundant and native Daphnia are rare. In the current study, we employed surveys, field experiments, and a life table experiment to investigate the role of food quality in explaining the distribution and phenology of D. lumholtzi , relative to two native species ( Daphnia parvula and Daphnia mendotae ).
2. During May–September 2000 in eutrophic McDaniel Lake, Missouri U.S.A., cyanobacteria (primarily Oscillatoria ) first appeared at 6-m depth and then became abundant throughout the epilimnion.
3. During the May field experiment, D. lumholtzi , D. parvula and D. mendotae all consumed a similar diet of algae, showing positive selection for small greens (chlorophytes and cryptophytes <20 μm). During the July experiment, when the epilimnion exceeded 25 °C and cyanobacteria were common in the lake, D. lumholtzi consumed significantly more total algae and more cyanobacteria than the two native species. Although the Daphnia selected against cyanobacteria, all three species consumed about 25% of this food in their diet.
4. A life table experiment compared the responses of D. lumholtzi and D. parvula with variation in density of high-quality food ( Ankistrodesmus ) and concentration of a toxic strain of cyanobacteria ( Anabaena flos-aquae ). Both Daphnia species showed reduced survivorship, fertility and intrinsic rates of increase in response to elevated concentrations of cyanobacteria, particularly at the higher food level.
5. The results suggest that D. lumholtzi shows similar inhibition from cyanobacteria as does the native Daphnia . However, their continued high in situ feeding rates imply that D. lumholtzi is less affected by midsummer conditions in warm-water reservoirs than are native Daphnia .     

Essential fatty acid content and the phosphorus to carbon ratio in cultured algae as indicators of food quality for Daphnia

1. A series of experiments examined growth of Daphnia magna on three algal diets ( Rhodomonas minuta , Scenedesmus acutus and Synechococcus sp.) at varying physiological states [nitrogen and phosphorus (P) limitations] to test whether variation in algal fatty acid and/or elemental composition can predict Daphnia growth.
2. These algae differed widely in their essential fatty acid (EFA) composition while phosphorus (P) or nitrogen limitation had only a small influence on their ω3-polyunsaturated fatty acid (PUFA) content.
3. Individually, algal ω3-PUFA content explained 69% of the variation in the normalised growth of D. magna, while algal phosphorus content explained 11% of the variation. Quantitative models for D. magna growth used both algal ω3-PUFA content and algal C : P ratio as food quality indices. Together, algal ω3-PUFA content and C : P ratio explained 70% of the variation in the normalised growth rate of D. magna .
4. Our results indicate that EFA influenced algal food quality much more strongly than P. The EFA and mineral P impacts appear to be independent.     

Predator–prey instability: individual-level mechanisms for population-level results

1. In previous work we established that increasing temperature led to a destabilization of the population dynamics of the invertebrate carnivore Mesostoma ehrenbergii and its prey Daphnia pulex , which ultimately resulted in the local extinction of Daphnia at higher temperatures. Two mechanisms are proposed to explain the population-level phenomena: (1) quantitative changes in carnivore vital rates with increasing temperature led to stronger functional and numerical response and (2) qualitative changes in the dynamic allocation of energy to reproduction by the predator with increasing temperature introduces inverse density dependence in the predator's response.
2. The growth of individual M. ehrenbergii was monitored under various food conditions to determine the effect of two temperatures (18 and 24 °C) and five food levels on rates of growth, prey consumption and reproduction and on reproductive allocation patterns.
3. The first mechanism was supported by both higher consumption rates (stronger functional response) and faster growth rates with earlier age at maturity and shorter generation time (stronger numerical response).
4. Evidence for mechanism two was also provided by an alteration of the reproductive allocation pattern with temperature. Viviparous (subitaneous) eggs were more likely to be produced by this carnivore at low food levels at 24 °C, while at 18 °C, high food levels were required before individuals made this switch. This shift actually introduces inverse density dependence in the predator's numerical response which is highly destabilizing.
5. Based on the results of this study, the differential effect of M. ehrenbergii on the dynamics and structure of its D. pulex prey populations can be attributed to changes in both physiological rates and reproductive allocation patterns with temperature.     

Allochtonous input and trophic level heterogeneity: impact on an aquatic food web

The impact of food web complexity in open and closed food webs was explored experimentally under controlled laboratory conditions. We used an aquatic model community consisting of two forms of primary producers, phytoplankton ( Scenedesmus obtusiuscusculus ) and periphyton ( Nitzschia perminuta ) and two types of consumers, Daphnia pulex feeding on phytoplankton and Chydorous sphaericus feeding on both periphyton and phytoplankton. Three different food webs all having the phytoplankton and periphyton, but having either one of the consumers or both were set up. These food webs were studied in an open and closed treatment. In the open treatment, phytoplankton was continuously flowing through the aquaria whereas in the closed system all the phytoplankton was delivered at the start of the experiment.
D. pulex had a positive effect on the density of C. sphaericus in both the open and closed treatments. In the open treatment C. sphaericus increased to very high numbers and was able to depress phytoplankton and thereby negatively affect D. pulex . Our study shows that the explicit handling of the population dynamics of both grazers allowed us to show how a compensatory increase in one primary producer due to increased grazing on another primary producer creates a negative feedback between consumers: C. sphaericus increased and negatively affected D. pulex .     

Zooplankton,and related phytoplankton cycles,in a eutrophic lake

The seasonal cycles of zooplankton were determined for 18 consecutive months in a sewage-enriched lake in northern Canada and were related to algal availability and utilization, food consumption, temperature and the density of predators. Most of the common species (Daphnia pulex, Daphnia middenorffiana, Keratella cochlearis, Keratella quadrata, Polyarthra vulgaris) increased in abundance in May and June, reached a mid-summer maximum, and declined sharply in the fall. Phytoplankton densities increased sharply in May, peaked early in June and gradually decreased through the summer and fall. Since the quantity of algae in the guts remained constant during this period, algal availability and utilization had no direct impact on the seasonal cycles of any species. Furthermore, the amount of ingested material in D. pulex and D. middendorffiana was similar regardless of time of year, implying that the total quantity of food in the environment did not restrict development. Although temperature was the most important factor influencing variations in the densities of all species, predation by Cyclops spp. probably had little effect on the population dynamics of the fauna.     

Food effects on life history traits and seasonal dynamics of Ceriodaphnia pulchella

1. This paper describes the effects of differences in food quantity and quality on selected life history traits of Ceriodaphnia pulchella . Animals were fed with four concentrations of two green algae, Scenedesmus obliquus and Chlamydomonas globosa , given separately as well as in a 1 : 1 mixture.
2. In most cases growth, reproduction and condition of the animals and consequently the rate of population increase, r , increased with food concentration. Life history parameters of animals raised on S. obliquus were lowest, whereas no significant differences were found between animals fed with C. globosa and with the mixture of the two algal species.
3. In contrast to the large effects of food quantity and quality found in the laboratory, an analysis of the population dynamics of C. pulchella in Lake Tjeukemeer showed that the effect of changes in food conditions during the growing season of this species was limited, although overall food levels seemed to be poor throughout the year.
4. Changes in the birth rate of the population are mainly governed by changes in temperature, and possibly by changes in the densities of the invertebrate predator Leptodora kindtii .     

Food effects on life history traits and seasonal dynamics of Ceriodaphnia pulchella

1. This paper describes the effects of differences in food quantity and quality on selected life history traits of Ceriodaphnia pulchella . Animals were fed with four concentrations of two green algae, Scenedesmus obliquus and Chlamydomonas globosa , given separately as well as in a 1 : 1 mixture.
2. In most cases growth, reproduction and condition of the animals and consequently the rate of population increase, r , increased with food concentration. Life history parameters of animals raised on S. obliquus were lowest, whereas no significant differences were found between animals fed with C. globosa and with the mixture of the two algal species.
3. In contrast to the large effects of food quantity and quality found in the laboratory, an analysis of the population dynamics of C. pulchella in Lake Tjeukemeer showed that the effect of changes in food conditions during the growing season of this species was limited, although overall food levels seemed to be poor throughout the year.
4. Changes in the birth rate of the population are mainly governed by changes in temperature, and possibly by changes in the densities of the invertebrate predator Leptodora kindtii .     

Zooplankton-phytoplankton interactions: the case for refining methods, measurements and models

Many of the classic experiments on the interactions between animals and their food supply were performed using laboratory cultures of Daphnia but comparable predator-prey cycles have seldom been recorded in the field. In this paper, we report the results of a field experiment designed to examine the effect of seasonal variations in the supply of edible algae on the population dynamics of Daphnia hyalina var lacustris. The experiment was performed in a large (45 m diameter) enclosure that was fertilised at regular intervals to sustain phytoplankton production. The results demonstrate that predator prey interactions of the kind recorded in culture can be detected in the field if large numbers of samples are collected and the results analysed using appropriate methods. Analyses using the numbers of Daphnia collected at a single station and chlorophyll a as a measure of food availability produced inconclusive results. Similarly, Daphnia birth rates calculated using the total number of individuals provided a poor measure of the animals reproductive response to changes in the supply of food. The clearest evidence of systematic plant-herbivore interactions was obtained when improved estimates of Daphnia numbers and adult birth rates were combined with estimates of edible rather than total algal biomass. Daphnia birth rates were then positively correlated with the estimated amount of ingestible carbon (r = 0.77) and the proportion of gravid adults decreased dramatically when the concentration of food fell below 0.10 mg C l^-1. Measurements and models of phytoplankton loss rates were then used to assess the impact of Daphnia grazing on the growth and decline of three species of edible algae. The results demonstrated that most species were able to sustain positive growth rates despite short-term increases in the population filtration rate. For much of the summer, the Daphnia appeared to behave as non-interactive grazers and had very little effect on the growth rate of their main phytoplankton food. Their grazing activity did, however, arrest the growth of a late summer population of Chlorella when the Daphnia were estimated to be filtering all the water contained in the enclosure in less than a day.     

Evidence of coprophagy in freshwater zooplankton

1. Vertical transport of nutrients in sedimenting faecal material is greatly reduced by coprophageous organisms. Unfortunately, nearly all work on faecal production, sedimentation and coprophagy has dealt with copepods in marine ecosystems. Here, we report the first evidence of coprophagy in freshwater zooplankton from oligotrophic and eutrophic lakes. We used ¹⁴C‐labelled algae and faecal material to estimate the rates of algal clearance and coprophagy. 2. Measured feeding rates per individual on faecal material were similar (Daphnia pulex, D. rosea, Leptodiaptomus tyrelli) or even higher (D. lumholtzi) than filtering rates on phytoplankton. This finding does not necessarily implicate active selection of faeces over algae because: (i) we did not use the same food concentrations for faeces and algae, and (ii) grazers of slightly different sizes were used in each test. 3. Weight‐specific clearance rates of L. tyrelli and Holopedium gibberum on faecal matter (0.084–0.089 mL μg^?1 h^?1) were higher than in the daphniids (0.026 mL μg^?1 h^?1). 4. The data indicate that coprophagy in freshwater ecosystems is an important mechanism of nutrient recycling, and this process should be taken into account when studying nutrient fluxes within lakes and reservoirs.     

Stoichiometric food quality and herbivore dynamics

Herbivores may grow with nutrient or energy limitation, depending on food abundance and the chemical composition of their food. We present a model that describes herbivore growth as a continuous function of two limiting factors. This function uses the synthesizing unit concept, has the hyperbolic Monod model as a limiting case, and has the same number of parameters as the Monod model coupled to Liebig's discontinuous minimum rule. We use the model to explore nutrient-limited herbivore growth in a closed system with algae, Daphnia and phosphorus as the limiting nutrient. Phosphorus in algae may substantially influence Daphnia growth. This influence changes over time and is most pronounced when algae and Daphnia populations fluctuate strongly. Relative to classic models that only consider food quantity as a determinant of Daphnia growth, our model shows richer dynamical behaviour. In addition to the standard positive equilibrium, which may be stable or unstable depending on nutrient availability, a new positive equilibrium may arise in our model when mortality rates are relatively high. This equilibrium is unstable and reduces the likelihood of long-term persistence of Daphnia in the system.     

Comparing grazing by Dreissena polymorpha on phytoplankton in the presence of toxic and non-toxic cyanobacteria

SUMMARY 1. The feeding behaviour of the zebra mussel ( Dreissena polymorpha ) was studied in the laboratory on different combinations of food, including a green alga ( Chlamydomonas reinhardtii ) and toxic and non-toxic strains of the cyanobacterium Microcystis aeruginosa .
2. The highest clearance rate of phytoplankton by zebra mussels was found when the mussels were feeding on a mixture of Chlamydomonas and non-toxic Microcystis , the lowest on a mixture of Chlamydomonas and toxic Microcystis .
3. The differences found in the clearance rates between food combinations can be partly explained by the production of pseudofaeces containing live phytoplankton cells. Zebra mussels expelled significantly more live phytoplankton cells in the presence of toxic Microcystis than in the presence of non-toxic Microcystis . The pseudofaeces contained predominantly live Chlamydomonas cells. Proportionately much less live Microcystis cells were encountered in the pseudofaeces.
4. Consequently, grazing of zebra mussels on a combination of Chlamydomonas and Microcystis may finally result in a dominance of Chlamydomonas over Microcystis . The presence of toxic Microcystis may even strengthen this shift.