The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities

1. This paper summarizes the salient features of the contributions to the workshop on The Role of Food Quality for Zooplankton. In this paper we attempt critically to evaluate our present knowledge in the light of new studies. 2. For the growth and reproduction of zooplankton, the existing literature considers two main limiting factors in the diet, i.e. phosphorus (homeostasis theory) and fatty acids. Nevertheless, interpretations and opinions regarding the importance of these two factors are the subject of controversy in the literature. No attempts have been made to link these two potentially limiting factors, let alone give a coherent view based on the mechanisms behind limitation. Aquaculture studies provide some direct evidence of the importance of the long-chained poly unsaturated fatty acids (PUFA) for zooplankton. The presence of PUFA in phytoplankton is reported to affect the growth rates of zooplankton significantly. 3. Field data on carbon and phosphorus indicate a greater constancy of the C : P ratios of zooplankton than of their food. Empirical data and modelling studies suggest that zooplankton, especially Daphnia spp., may maintain nutrient homeostasis by incorporating a greater proportion of the limiting nutrients ingested and releasing more of nutrients in excess supply. The need for conserving nutrients in short supply increases with the increase in growth rates. 4. Phosphorus certainly influences zooplankton food directly. Direct supplementation of the P-insufficient algal diet with PO₄-P alone discernibly improves the growth in daphnids. It is highly plausible that P limitation and fatty acid limitation are not mutually exclusive alternatives. The two, separately or in conjunction, can control growth of at least some lake zooplankters, especially daphnids. 5. Besides a shortage of nutrient (P), other environmental factors (irradiance, UV-radiation, temperature) can also adversely affect the zooplankton diet, including its digestibility and assimilation efficiency. 6. It is not yet clear if PUFA deficiency in the diet is in some way related to or caused by P deficiency. It is, however, now known that the EPA (eicosapentaenoic acid, 20 : 5ω3) content of certain algae is markedly reduced under P-limitation and that it differs significantly among the different taxonomic groups of phytoplankton. Diatoms and flagellates are generally considered as good-quality foods because of their high EPA content. On the contrary, cyanobacteria are low-quality food, having both low EPA and P content. 7. Recent experiments reveal that the relative importance of fatty acids for daphnids increases with a decreasing C : P ratio in the food, i.e. if P is no longer limiting, and vice versa. For daphnids, there is possibly a switch between P-limitation and PUFA limitation at intermediate C : P ratios. At higher C : P ratios, P is more important but at lower ratios PUFA are more crucial for growth and reproduction. 8. Lastly, the accumulating evidence for P limitation is stronger than that for fatty acid limitation.     

Linking elements to biochemicals: effects of nutrient supply ratios and growth rates on fatty acid composition of phytoplankton species

Three species of marine phytoplankton, Rhodomonas sp., Isochrysis galbana Parke, and Phaeodactylum tricornutum Bohlin, were cultivated in semicontinuous cultures to test biochemical responses (fatty acids; FAs) to five nitrogen (N):phosphorus (P) supply ratios and four growth rates (dilution rates). The characteristic FA profile was observed for each algal species (representing particular algal class), which remained relatively stable across the entire ranges of N:P supply ratios and growth rates. For all species, significant direct effects of N:P supply ratios on FAs were found at lower growth rates. The highest saturated and monounsaturated fatty acid (SFA and MUFA) contents were observed under N deficiency at the lowest growth rate in all three species, while responses of polyunsaturated fatty acids (PUFAs) revealed no consistent pattern. Total FAs (and SFAs and MUFAs) in all species showed significant negative correlations with N cell quota (Q_N) under N deficiency, but PUFAs had species‐specific correlations with Q_N. The results show that characteristic FA profiles of algal genus or species (representing particular algal classes) underlie fluctuations according to culture conditions. The significant correlation between FAs and Q_N under N deficiency suggests that elemental and biochemical limitation of phytoplankton should be considered mutually as determinants of food quality for zooplankton in marine ecosystems.     

Increased risk of phosphorus limitation at higher temperatures for Daphnia magna

Invertebrate herbivores frequently face growth rate constraints due to their high demands for phosphorus (P) and nitrogen (N). Temperature is a key modulator of growth rate, yet the interaction between temperature and P limitation on somatic growth rate is scarcely known. To investigate this interaction, we conducted a study on the somatic growth rate (SGR) of the cladoceran Daphnia magna, known to be susceptible to P-limitation. We determined the SGR across a broad range of dietary P content of algae (carbon (C):P ratios (125?C790), and at different temperatures (10?C25°C). There was a strong impact of both temperature and C:P ratio on the SGR of D. magna, and also a significant interaction between both factors was revealed. The negative effect of dietary C:P on growth rate was reduced with decreased temperature. We found no evidence of P limitation at lowest temperature, suggesting that enzyme kinetics or other measures of food quality overrides the demands for P to RNA and protein synthesis at low temperatures. These findings also indicate an increased risk of P limitation and thus reduced growth efficiency at high temperatures.     

Seasonal changes of C:P ratios of seston, bacteria, phytoplankton and zooplankton in a deep, mesotrophic lake

• 1 The C:P ratios of seston, bacteria, phytoplankton and zooplankton were measured twice a week in situ in mesotrophic, large and deep Lake Constance from April to December 1995. Except for zooplankton, a strong seasonality was exhibited with low C:P ratios during P‐enriched early spring conditions and high values during P‐depleted summer conditions.
• 2 Molar C:P ratios of seston varied between 180:1 and 460:1 demonstrating moderate phosphorus limitation in spring and during the clear‐water phase, and strong limitation for the rest of the season. The sestonic C:P ratio increased significantly during two decades of re‐oligotrophication of Lake Constance, reflecting an enhanced phosphorus limitation of the plankton community in summer. Molar C:P ratios of bacteria and phytoplankton varied seasonally between 50:1 and 130:1 and 180:1 and 500:1, respectively, and indicate carbon or light limitation in winter and phosphorus limitation in summer. Zooplankton had a molar C:P ratio of about 124:115 which was nearly constant throughout the seasons.
• 3 These differences in the C:P ratios of planktonic organisms have direct implications for phosphorus recycling within the food web as C:P ratios of excreta should be highly variable.

     

Does excess carbon affect respiration of the rotifer Brachionus calyciflorus Pallas?

1. Herbivorous zooplankton maintain a rather constant elemental composition in their body mass as compared with the variability commonly encountered in their food. Furthermore, their high phosphorus (P) and nitrogen (N) content means that they often face an excess of carbon (C) in their diet. Regulation of this surplus of energy may occur via modulation of assimilation efficiency, or postassimilation by increased respiration (CO₂) and/or excretion dissolved organic carbon, DOC. Whereas several studies have examined the effect of elemental imbalance in the genus Daphnia, few have examined other zooplankton taxa. 2. We investigated whether the rotifer Brachionus calyciflorus uses increased respiration as a means of stoichiometrically regulating excess dietary C. Growth rate and respiration were measured under different food qualities (C : N and C : P ratios). 3. Both C : N and C : P ratios in food had strong effects on growth rate, demonstrating strong nutrient limitation of rotifer growth when nutrient elements were depleted in the diet and indicating the need for stoichiometric regulation of excess ingested C. 4. Respiration measurements, supported by a stoichiometric model, indicated that excess C was not released as CO₂ in B. calyciflorus and that nutrient balance must therefore be maintained by other means such as excretion of DOC or egestion in faecal material.     

Temperature and the effects of elemental food quality on Daphnia

1. We examined the responses of two species of Daphnia to changes in food phosphorus (P) content, with animals reared at three different water temperatures. Specifically, we measured mass‐specific growth rate (MSGR), body P content and respiration rate of Daphnia magna and Daphnia pulex acclimatised to 10, 17.5 and 25 °C and fed food carbon : phosphorus (C : P) ratios of either 150 or 500. 2. The responses of these three physiological variables to temperature–food quality interactions were species‐specific. There was a significant interactive effect of temperature and food quality on D. magna, as the greatest proportional effect of food quality on growth was observed at 10 °C and reductions in body P because of low food P content were relatively greater at 25 °C. These effects may reflect the temperature dependence of mechanisms that reduce elemental constraints associated with food quality in D. magna. By contrast, there were no interactive effects between food quality and temperature on MSGR, body P or mass‐specific respiration of D. pulex. 3. It thus appears that temperature can alter food quality effects on Daphnia but the nature of these alterations depends upon the daphniid species and its thermal adaptability. Significant temperature–food quality interactions will complicate efforts to understand zooplankton nutrition in nature and warrant future consideration.     

Atmospheric nitrogen deposition is associated with elevated phosphorus limitation of lake zooplankton

Here, we present data that for the first time suggests that the effects of atmospheric nitrogen (N) deposition on nutrient limitation extend into the food web. We used a novel and sensitive assay for an enzyme that is over‐expressed in animals growing under dietary phosphorus (P) deficiency (alkaline phosphatase activity, APA) to assess the nutritional status of major crustacean zooplankton taxa in lakes across a gradient of atmospheric N deposition in Norway. Lakes receiving high N deposition had suspended organic matter (seston) with significantly elevated carbon:P and N:P ratios, indicative of amplified phytoplankton P limitation. This P limitation appeared to be transferred up the food chain, as the cosmopolitan seston‐feeding zooplankton taxa Daphnia and Holopedium had significantly increased APA. These results indicate that N deposition can impair the efficiency of trophic interactions by accentuating stoichiometric food quality constraints in lake food webs.     

Bacteria as a source of phosphorus for zooplankton

The utilization of bacterial phosphorus in zooplankton metabolism was investigated using radio-phosphorus labelled natural bacteria as food source for zooplankton in feeding experiments. Incorporation of labelled bacteria was clearly related to the species' ability to graze on bacteria, with the cladoceran Daphnia reaching the highest biomass-specific activity and the copepod Acanthodiaptomus the lowest. Within Daphnia, juveniles had a higher biomass-specific uptake of phosphorus than adults. This was presumably caused by higher growth rates of the juveniles rather than age-specific differences in the ability to feed on bacteria, supported by the observation that the juveniles had the highest specific P-content. Retention of ingested ³²P from labelled particles exceeded 80%, indicating higher assimilation efficiencies on phosphorus compared with carbon. In the investigated humic lake, approximately 75% of the phosphorus in grazable particles was bound in bacterial cells, making bacteria the most important source of P to the bacterivore zooplankton species.     

CHARACTERISTICS OF PHOSPHORUS LIMITATION IN CHLAMYDOMONAS REINHARDTH (CHLOROPHYCEAE) AND ITS PALMELLOIDS1

Chlamydomonas reinhardtii Dang, was grown in a chemostat culture under phosphate limitation. The steady state concentration of phosphate was below the detection limit (< 1 μg P/L) in all runs. The cellular content of phosphorus (Q_p), polyphosphate (Q_pp) and chlorophyll a increased with increasing dilution rate, and the growth rate of the alga was described by Q_p as well as Q_pp in the Droop model. The ratio Q_pp/Q_p and the activity of alkaline phosphatase were maximal at high and low growth rates, respectively. Palmelloids of Chlamydomonas were found at high dilution rates (D > 0.12 h^?1) and became attached to the wall of the culture vessel. They differed from the vegetative stage in both chemical composition and growth rate. Their contents of phosphorus and chlorophyll a were low, as in the vegetative cells, which grew at a low growth rate, whereas the ration Q_pp/Q_p and the activity of alkaline phosphatase were comparable with those of fast growing vegetative cells. The growth rate of the palmelloids was 0.03 h^?1 whereas maximum growth rate (μ_m) for the vegetative cells was 0.21 h^?1.     

Threshold elemental ratios for carbon versus phosphorus limitation in Daphnia

1. The transition from carbon (C) to phosphorus (P) limited growth in Daphnia depends not only on the C : P ratio in seston, i.e. food quality, but also on food quantity. Carbon is commonly believed to be limiting at low food because of the energetic demands of basal metabolism. The critical C : P ratio in seston (otherwise known as the threshold elemental ratio, TER) above which P is limiting would then be high when food is scarce. 2. A new model that differentiates between the C : P requirements for growth and maintenance is presented that includes terms for both C and P in basal metabolism. At low food the calculated TERs for Daphnia of around 230 are only slightly higher than values of 200 or so at high intake. Seston C : P often exceeds 230, particularly in oligotrophic lakes where phytoplankton concentration is low and detritus dominates the diet, indicating the potential for limitation by P. 3. The analysis highlights the importance of P, as well as C, in maintenance metabolism and the overall metabolic budget, such that food quality is of importance even when intake is low. Further measurements of C and P metabolism at low food, in particular basal respiration and excretion rates, are needed in order to improve our understanding of the interacting roles of food quantity and quality in zooplankton nutrition.     

Adaptation of soil microbial growth to temperature: Using a tropical elevation gradient to predict future changes

Terrestrial biogeochemical feedbacks to the climate are strongly modulated by the temperature response of soil microorganisms. Tropical forests, in particular, exert a major influence on global climate because they are the most productive terrestrial ecosystem. We used an elevation gradient across tropical forest in the Andes (a gradient of 20°C mean annual temperature, MAT), to test whether soil bacterial and fungal community growth responses are adapted to long‐term temperature differences. We evaluated the temperature dependency of soil bacterial and fungal growth using the leucine‐ and acetate‐incorporation methods, respectively, and determined indices for the temperature response of growth: Q₁₀ (temperature sensitivity over a given 10oC range) and T_min (the minimum temperature for growth). For both bacterial and fungal communities, increased MAT (decreased elevation) resulted in increases in Q₁₀ and T_min of growth. Across a MAT range from 6°C to 26°C, the Q₁₀ and T_min varied for bacterial growth (Q_10–20 = 2.4 to 3.5; T_min = ?8°C to ?1.5°C) and fungal growth (Q_10–20 = 2.6 to 3.6; T_min = ?6°C to ?1°C). Thus, bacteria and fungi did not differ significantly in their growth temperature responses with changes in MAT. Our findings indicate that across natural temperature gradients, each increase in MAT by 1°C results in increases in T_min of microbial growth by approximately 0.3°C and Q_10–20 by 0.05, consistent with long‐term temperature adaptation of soil microbial communities. A 2°C warming would increase microbial activity across a MAT gradient of 6°C to 26°C by 28% to 15%, respectively, and temperature adaptation of microbial communities would further increase activity by 1.2% to 0.3%. The impact of warming on microbial activity, and the related impact on soil carbon cycling, is thus greater in regions with lower MAT. These results can be used to predict future changes in the temperature response of microbial activity over different levels of warming and over large temperature ranges, extending to tropical regions.     

Inter- and intra-annual variability in the phytoplankton community of a high mountain lake: the influence of external (atmospheric) and internal (recycled) sources of phosphorus

1. The inter‐ and intra‐annual changes in the biomass, elemental (carbon (C), nitrogen (N) and phosphorus (P)) and taxonomical composition of the phytoplankton in a high mountain lake in Spain were studied during 3 years with different physical (fluctuating hydrological regime) and chemical conditions. The importance of internal and external sources of P to the phytoplankton was estimated as the amount of P supplied via zooplankton recycling (internal) or through ice‐melting and atmospheric deposition (external). 2. Inter‐annual differences in phytoplankton biomass were associated with temperature and total dissolved phosphorus. In 1995, phytoplankton biomass was positively correlated with total dissolved phosphorus. In contrast, the negative relationship between zooplankton and seston biomass (direct predatory effects) and the positive relationship between zooplankton P excretion and phytoplankton biomass in 1997 (indirect P‐recycling effects), reinforces the primary role of zooplankton in regulating the total biomass of phytoplankton but, at the same time, encouraging its growth via P‐recycling. 3. Year‐to‐year variations in seston C : P and N : P ratios exceeded intra‐annual variations. The C : P and N : P ratios were high in 1995, indicating strong P limitation. In contrast, in 1996 and 1997, these ratios were low during ice‐out (C : P < 100 and N : P < 10) and increased markedly as the season progressed. Atmospheric P load to the lake was responsible for the decline in C : P and N : P ratios. 4. Intra‐annual variations in zooplankton stoichiometry were more pronounced than the overall differences between 1995 and 1996. Thus, the zooplankton N : P ratio ranged from 6.9 to 40.1 (mean 21.4) in 1995, and from 10.4 to 42.2 (mean 24.9) in 1996. The zooplankton N : P ratio tended to be low after ice‐out, when the zooplankton community was dominated by copepod nauplii, and high towards mid‐ and late‐season, when these were replaced by copepodites and adults. 5. In 1995, the minimum demands for P of phytoplankton were satisfied by ice‐melting, atmospheric loading and zooplankton recycling over 100%. In order of importance, atmospheric inputs (> 1000%), zooplankton recycling (9–542%), and ice‐melting processes (0.37–5.16%) satisfied the minimum demand for P of phytoplankton during 1996 and 1997. Although the effect of external forces was rather sporadic and unpredictable in comparison with biologically driven recycle processes, both may affect phytoplankton structure and elemental composition. 6. We identified three conceptual models representing the seasonal phosphorus flux among the major compartments of the pelagic zone. While ice‐melting processes dominated the nutrient flow at the thaw, biologically driven processes such as zooplankton recycling became relevant as the season and zooplankton ontogeny progressed. The stochastic nature of P inputs associated with atmospheric events can promote rapid transitional changes between a community limited by internal recycling and one regulated by external load. 7. The elemental composition of the zooplankton explains changes in phytoplankton taxonomic and elemental composition. The elemental negative balance (seston N : P < zooplankton N : P, low N : P recycled) during the thaw, would promote a community dominated by species with a high demand for P (Cryptophyceae). The shift to an elemental positive balance (seston N : P > zooplankton N : P, high N : P recycled) in mid‐season would skew the N : P ratio of the recycled nutrients, favouring dominance by chrysophytes. The return to negative balance, as a consequence of the ontogenetic increase in zooplankton N : P ratio and the external P inputs towards the end of the ice‐free season, could alleviate the limitation of P and account for the appearance of other phytoplankton classes (Chlorophyceae or Dinophyceae).     

Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils

The relative activities of soil enzymes involved in mineralizing organic carbon (C), nitrogen (N), and phosphorus (P) reveal stoichiometric and energetic constraints on microbial biomass growth. Although tropical forests and grasslands are a major component of the global C cycle, the effects of soil nutrient availability on microbial activity and C dynamics in these ecosystems are poorly understood. To explore potential microbial nutrient limitation in relation to enzyme allocation in low latitude ecosystems, we performed a meta-analysis of acid/alkaline phosphatase (AP), β-1,4-glucosidase (BG), and β-1,4-N-acetyl-glucosaminidase (NAG) activities in tropical soils. We found that BG:AP and NAG:AP ratios in tropical soils are significantly lower than those of temperate ecosystems overall. The lowest BG:AP and NAG:AP ratios were associated with old or acid soils, consistent with greater biological phosphorus demand relative to P availability. Additionally, correlations between enzyme activities and mean annual temperature and precipitation suggest some climatic regulation of microbial enzyme allocation in tropical soils. We used the results of our analysis in conjunction with previously published data on soil and biomass C:N:P stoichiometry to parameterize a biogeochemical equilibrium model that relates microbial growth efficiency to extracellular enzyme activity. The model predicts low microbial growth efficiencies in P-limited soils, indicating that P availability may influence C cycling in the highly weathered soils that underlie many tropical ecosystems. Therefore, we suggest that P availability be included in models that simulate microbial enzyme allocation, biomass growth, and C mineralization.     

GROWTH AND PHOSPHORUS UPTAKE BY THE TOXIC DINOFLAGELLATE ALEXANDRIUM CATENELLA (DINOPHYCEAE) IN RESPONSE TO PHOSPHATE LIMITATION1

Alexandrium catenella (Whedon et Kof.) Balech has exhibited seasonal recurrent blooms in the Thau lagoon (South of France) since first reported in 1995. Its appearance followed a strong decrease (90%) in phosphate (PO₄^3?) concentrations in this environment over the 1970–1995 period. To determine if this dinoflagellate species has a competitive advantage in PO₄^3?‐limited conditions in terms of nutrient acquisition, semicontinuous cultures were carried out to characterize phosphorus (P) uptake by A. catenella cells along a P‐limitation gradient using different dilution rates (DRs). Use of both inorganic and organic P was investigated from measurements of ³³PO₄^3? uptake and alkaline phosphatase activity (APA), respectively. P status was estimated from cellular P and carbon contents (Q_P and Q_C). Shifts in trends of Q_P/Q_C and Q_P per cell (Q_P·cell?1) along the DR gradient allowed the definition of successive P‐stress thresholds for A. catenella cells. The maximal uptake rate of ³³PO₄^3? increased strongly with the decrease in DR and the decrease in Q_P/Q_C, displaying physiological acclimations to PO₄^3? limitation. Concerning maximal APA per cell, the observation of an all‐or‐nothing pattern along the dilution gradient suggests that synthesis of AP was induced and maximized at the cellular scale as soon as PO₄^3? limitation set in. APA variations revealed that the synthesis of AP was repressed over a PO₄^3? threshold between 0.4 and 1 μM. As lower PO₄^3? concentrations are regularly observed during A. catenella blooms in Thau lagoon, a significant portion of P uptake by A. catenella cells in the field may come from organic compounds.     

SPECIES‐SPECIFIC RESPONSE IN ALKALINE PHOSPHATASE ACTIVITY OF FRESHWATER PHYTOPLANKTON IN A NUTRIENT ENRICHMENT EXPERIMENT

A new method was utilized to study species‐specific responses of phytoplankton to phosphorus limitation in a nutrient enrichment experiment. A substrate, ELF, produces a fluorescent precipitate at the sites of alkaline phosphatase (AP), which makes it possible to visually detect phosphorus (P) limitation in individual cells of multiple species. Lake water was incubated in the laboratory to induce nitrogen (N) or P limitation. Initially, little or no ELF labeling was observed for any of the phytoplankton species, indicating a general lack of P limitation. This observation was supported by low bulk AP activity in the initial field samples. During the experiment, several chlorophyte taxa (Coelastrum, Eudorina, a solitary spiny coccoid) were driven to P limitation, as evidenced by a high percentage of cells displaying ELF labeling when inorganic N was added. Taxa such as Actinastrum and Dictyosphaerium, on the contrary, were never P limited. Little or no ELF was observed in cyanobacterial species, suggesting that P limitation was not achieved in these organisms. Using traditional bulk AP activity, significantly higher levels of AP activity were observed in treatments with inorganic N additions, compared to those with phosphate additions. ELF labeling generally followed the trend of bulk AP, except in species that did not dominate the biomass. Finally, we noted that all species observed were ELF labeled at least on one occasion, except for fragile flagellates which did not withstand the labeling procedure.     

Allocation strategies in crustacean stoichiometry: the potential role of phosphorus in the limitation of reproduction

1. Elemental composition (carbon : nitrogen : phosphorus, C : N : P) was analysed in eggs and juveniles of two crustaceans, Daphnia magna (Cladocera) and the crayfish Astacus astacus (Decapoda). Stoichiometry was also analysed for the carapace, muscle tissue, hepatopanchreas and gills of Astacus. 2. For both species the C : P ratio was significantly higher in eggs than juveniles, but there was a constant, homeostatic elemental ratio in eggs during embryogenesis (Astacus) and with different C : N : P in maternal food (Daphnia). 3. Differences in the stoichiometry of major tissue categories in Astacus suggest that there are distinct allocation strategies of elements to various somatic tissues as well as to reproduction versus somatic tissues overall. 4. There are strong ontogenetic shifts in the allocation of energy and elements in both species, as for crustaceans in general. During maturity there may be a trade‐off with regard to the allocation of C, N or P to somatic or reproductive tissue, and poor food quality (high C : P in food) could pose other constraints on reproductive capacity than does food shortage (low C). 5. Egg production may be at least as sensitive to low P as is somatic growth and could result in a marked decrease in overall population growth rate more severe than would be expected from individual growth rate alone.     

The stoichiometry of N and P in the pelagic zone of Castle Lake, California

We measured the concentrations, as well as lake-wide amounts,of nitrogen (N) and phosphorus (P) in dissolved, seston andzooplankton pools throughout the water column of Castle Lake,California, during summer, 1991. This allowed us to determinethe stoichiometric ratios of important elements in each pool(C:N, C:P, N:P) as well as for the entire lake. Dissolved andseston pools were the predominant storage compartments for bothN and P; zooplankton never contained >5% of N or 10% of Plake wide. However, by late summer, the concentrations of Pin seston and in zooplankton were similar in the upper portionsof the water column, suggesting that changes in food web structurethat alter zooplankton biomass and community composition (andhence elemental storage in the zooplankton) may produce significantshifts in nutrient storage among pelagic pools. Lake-wide levelsof dissolved N were largely constant over the study period;however, lake-wide dissolved P increased. These dynamics suggestedthat the majority of nutrients stored in dissolved pools wereunavailable for phytoplankton growth. N:P and C:P ratios indicatedthat Castle Lake phytoplankton became severely deficient inP during the course of our observations. These ratios also greatlyexceeded recently reported threshold values for elemental constraintson growth and reproduction for several species of zooplankton.The ratio of N to P in the zooplankton pool was relatively constantand consistently lower than that in the sestion. As a result,the predicted N:P ratio of zooplankton-regenerated nutrientsexceeded the N:P ratio of the seston, implying that zooplanktonnutrient regeneration further skewed N and P supply ratios,and potentially enhanced P limitation of phytoplankton in CastleLake. ¹Present address: Department of Biology, Box 19498, Universityof Texas at Arlington, Arlington, TX 76019, USA     

TEMPERATURE EFFECTS ON SILICON- AND PHOSPHORUS-LIMITED GROWTH AND COMPETITIVE INTERACTIONS AMONG THREE DIATOMS1

Three diatom species, Stephanodiscus hantzschii (Ehr.) Grun., Asterionella formosa Hass. and Fragilaria crotonensis Kitt. Hass. were isolated from Lake Maarsseveen where they are dominant and show a successional sequence. The physiological responses of each species to temperature and limitation by silicon and phosphorus were determined over the temperature range of 5° to 20° C using short-term batch culture methods. Stephanodiscus hantzschii had higher maximum growth rates than the other two species at all temperatures, and the maximum growth rates of all species increased with increasing temperature. Temperature affected not only maximum growth rates but also half-saturation constants (K_s) and the minimum cell quotas. S. hantzschii had low silicon requirements for growth under Si-limiting conditions, and A. formosa and F. crotonensis had higher and nearly identical silicon requirements. The K_s values for silicon for S. hantzschii were essentially constant from 5° to 20° C but varied greatly for the other two species. A. formosa had the lowest requirements for growth under phosphorus limitation, F. crotonensis was intermediate and S. hantzschii had the highest growth requirements for phosphorus. The K₁ values for phosphorus were constant over the temperature range for both A. formosa and F. crotonensis and were much higher and variable for S. hantzschii. Nutrient competition experiments were performed in continuous cultures at four temperatures and various Si:P ratios. The results generally, but not always, confirmed the predictions based on the Monod relationships for each species. Results not in agreement with predictions were usually because of similar physiological properties of A. formosa and F. crotonensis or because of decreased loss rates for F. crotonensis due to wall growth. In cultures with all three species phosphorus-limited (Si:P > 75), A. formosa often dominated as predicted, although F. crotonensis was sometimes the most abundant species. As predicted, S. hantzschii never dominated at high Si:P ratios. At intermediate Si:P ratios when A. formosa and F. crotonensis were both Si-limited and S. hantzschii P-limited, all three species coexisted because A. formosa and F. crotonensis have almost identical silicon requirements, although sometimes F. crotonensis was more abundant than predicted. At 10°C the results agreed best with the predictions; A. formosa dominated at high Si:P ratios and S. hantzschii dominated as predicted at low Si:P ratios when all three species were Si-limited.     

Phosphorus acquisition and competitive abilities of two herbivorous zooplankton, <Emphasis Type="Italic">Daphnia pulex</Emphasis> and <Emphasis Type="Italic">Ceriodaphnia quadrangula</Emphasis>

Contrary to an expectation from the size-efficiency hypothesis, small herbivore zooplankton such as Ceriodaphnia often competitively predominate against large species such as Daphnia. However, little is known about critical feeding conditions favoring Ceriodaphnia over Daphnia. To elucidate these conditions, a series of growth experiments was performed with various types of foods in terms of phosphorus (P) contents and composition (algae and bacteria). An experiment with P-rich algae showed that the threshold food level, at which an individual’s growth rate equals zero, was not significantly different between the two species. However, the food P:C ratio, at which the growth rate becomes zero, was lower for Daphnia than for Ceriodaphnia, suggesting that the latter species is rather disfavored by P-poor algae. Ceriodaphnia showed a higher growth rate than Daphnia only when a substantial amount of bacteria was supplied together with a low amount of P-poor algae as food. These results suggest that an abundance of bacteria relative to algae plays a crucial role in favoring Ceriodaphnia over Daphnia because these are an important food resource for the former species but not for the latter.     

Modeling soil CO<Subscript>2</Subscript> emissions from ecosystems

We present a new soil respiration model, describe a formal model testing procedure, and compare our model with five alternative models using an extensive data set of observed soil respiration. Gas flux data from rangeland soils that included a large number of measurements at low temperatures were used to model soil CO₂ emissions as a function of soil temperature and water content. Our arctangent temperature function predicts that Q₁₀ values vary inversely with temperature and that CO₂ fluxes are significant below 0 °C. Independent data representing a broad range of ecosystems and temperature values were used for model testing. The effects of plant phenology, differences in substrate availability among sites, and water limitation were accounted for so that the temperature equations could be fairly evaluated. Four of the six tested models did equally well at simulating the observed soil CO₂ respiration rates. However, the arctangent variable Q₁₀ model agreed closely with observed Q₁₀ values over a wide range of temperatures (r² = 0.94) and was superior to published variable Q₁₀ equations using the Akaike information criterion (AIC). The arctangent temperature equation explained 16–85% of the observed intra-site variability in CO₂ flux rates. Including a water stress factor yielded a stronger correlation than temperature alone only in the dryland soils. The observed change in Q₁₀ with increasing temperature was the same for data sets that included only heterotrophic respiration and data sets that included both heterotrophic and autotrophic respiration.