Jotaro Urabe

The stoichiometry of consumer-driven nutrient recycling : theory, observations, and consequences

Ecologists are increasingly recognizing the importance of consumers in reg- ulating ecosystem processes such as nutrient cycling. Ecologists have recently made con- siderable progress in understanding nutrient cycling and trophic interactions in pelagic systems by application of a new concept, ecological stoichiometry, to consumer-driven processes. In this paper we synthesize these conceptual advances within pelagic ecology and attempt to illustrate how they may be usefully applied in other ecosystems. Stoichi- ometric theory shows that both grazer and algal elemental composition are critical param- eters influencing rates and ratios of nutrient release. Thus, the stoichiometry of nutrient recycling is a feedback mechanism linking grazer dynamics and algal nutritional status. Incorporation of such effects into a fully dynamic stoichiometric model generates profound changes in the predicted dynamics of algae and grazers, suggesting that adoption of a stoichiometric view may substantively alter our view of the interaction between trophic dynamics and nutrient cycling. The basic predictions of stoichiometric models of nutrient release are generally supported by experimental data showing that N:P release ratios are primarily a function of algal N:P ratio and secondarily a function of grazer N:P ratio, and that rates of P release by grazers are also related to food P:C. Furthermore, evidence for effects of nutrient release stoichiometry on phytoplankton communities and pelagic eco- system function is accumulating, including data showing consistent alterations in algal physiological status and ecosystem-scale changes in N fixation in response to altered grazer community structure and elemental composition. As the general features of the stoichi- ometry of algae-zooplankton interactions reflect fundamental biological processes linked to plant and animal mineral nutrition, the stoichiometric view of consumer-driven nutrient recycling can easily be applied to other ecosystems, including terrestrial and benthic food webs. A suite of potential applications of stoichiometric thinking to benthic and terrestrial habitats is suggested.

NUTRIENT LIMITATION REDUCES FOOD QUALITY FOR ZOOPLANKTON: DAPHNIA RESPONSE TO SESTON PHOSPHORUS ENRICHMENT

Laboratory studies are increasingly indicating that the quality of nutrient-limited algae is suboptimal for zooplankton production. However, little is known about how quality is affected by nutrient limitation of phytoplankton in more natural situations. To test for phosphorus (P) limitation of zooplankton growth under realistic food conditions, we performed a set of 5-d experiments using Daphnia dentifera and suspended particulate matter (seston) from three lakes at the Experimental Lakes Area (Ontario, Canada). Neonate Daphnia fed for 6 h per day on freshly collected seston enriched or unenriched with PO4 and spent the rest of the day feeding on unaltered natural seston. PO4 enrichment did not affect food abundance or concentrations and composition of essential fatty acids but dramatically lowered seston C:P ratio and significantly stimulated Daphnia growth. These results demonstrate that, even with field-collected seston, the effects of algal phosphorus limitation can extend to herbivores through reduc...

Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers

Animals encountering nutritionally imbalanced foods should release elements in excess of requirements in order to maintain overall homeostasis. Quantifying these excesses and predicting their fate is, however, problematic. A new model of the stoichiometry of consumers is formulated that incorporates the separate terms in the metabolic budget, namely, assimilation of ingested substrates and associated costs, protein turnover, other basal costs, such as osmoregulation, and the use of remaining substrates for production. The model indicates that release of excess C and nonlimiting nutrients may often be a significant fraction of the total metabolic budget of animals consuming the nutrient‐deficient forages that are common in terrestrial and aquatic systems. The cost of maintenance, in terms of not just C but also N and P, is considerable, such that food quality is important even when intake is low. Many generalist consumers experience short‐term and unpredictable fluctuations in their diets. Comparison of model output with data for one such consumer, Daphnia, indicates that mechanisms operating postabsorption in the gut are likely the primary means of regulating excess C, N, and P in these organisms, notably respiration decoupled from biochemical or mechanical work and excretion of carbon and nutrients. This stoichiometrically regulated release may often be in organic rather than inorganic form, with important consequences for the balance of autotrophic and heterotrophic processes in ecosystems.

REDUCED LIGHT INCREASES HERBIVORE PRODUCTION DUE TO STOICHIOMETRIC EFFECTS OF LIGHT/NUTRIENT BALANCE

Ecological common sense says that decreased solar energy should reduce herbivore production because of reduced energy flow through primary producers. However, a field experiment in a phosphorus-limited lake showed that production of zooplankton herbivores was increased by shading. This paradoxical outcome was caused by a decoupling of producer carbon fixation and nutrient uptake under high light that reduced food quality for herbivores. At low nutrient supplies, shading increased nutrient contents relative to carbon within algal food, outweighing effects of decreased primary production. Thus, light/ nutrient balance affects the degree of mismatch between primary producers and herbivores in nature, which in turn influences mass-transfer efficiencies along food chains. To predict how energy transfer efficiency and biological interactions will respond to perturbations, it is essential to take into account changes in light/nutrient balance and its effects on the stoichiometry of autotroph-herbivore interactions.

N and P Cycling Coupled by Grazers' Activities: Food Quality and Nutrient Release by Zooplankton

In order to clarify the role of zooplankton in the cycling of elements and its subsequent effect on algal populations, food elimination and nutrient release rates by zooplankton in a small pond dominated by daphnids were estimated for nitrogen and phosphorus from April to September. Comparison of the elemental contents of food and zooplankton showed that N was the element in shortest supply in the food sources utilized by zooplankton. The net clearance rate of the zooplankton was higher for N than for P and C throughout the study period, indicating that these organisms can eliminate the scarcest element from the food pool with a higher efficiency. Soluble N and P released by the zooplankton consisted mainly of ammonium nitrogen and soluble reactive phosphorus, and on a dry mass basis N release ranged from 0.27 to 1.05 tig mg-I h-I and P release from 0.045 to 0.30 jig mg-I h-i. Statistical analysis revealed that the N release rate was most affected by food abundance, whereas the P release rate and N: P release ratio were affected by the N: P ratio of the food. The net production rate of the zooplankton, estimated from the difference between elimination and release rates, showed a quite similar N: P ratio to that of the body tissue, indicating that zooplankton can keep their elemental composition roughly constant even if the N: P ratio of their food supply varies. Thus, the N and P release rates of zooplankton are linked through processes maintaining the elemental composition of body tissues. The present results indicate that the cycling rate of an element in pelagic systems depends highly on the grazers requirements as well as the relative abundances of other elements. Zooplankton can modify the nutritional environment for algae through accumulation and regeneration processes, as suggested by recent theoretical models.

The influence of fluctuating light intensities on species composition and diversity of natural phytoplankton communities

Abstract. The influence of fluctuating light intensities on phytoplankton composition and diversity was investigated for 49xa0days under semi-continuous culture conditions with sufficient nutrient supply, using phytoplankton assemblages from Lake Biwa, Japan. Light conditions were either periodically changed from high intensity (100xa0µmol photons m–2 s–1) to low intensity (20xa0µmol photonsxa0m–2 s–1) at intervals of 1, 3, 6 and 12xa0days, or fixed to constant intensities (permanent high and low light levels). All treatments additionally experienced a day:night cycle of 16:8xa0h.Phytoplankton abundance increased and reached a saturation level on day 19 of the treatment with permanent high light, but increased continuously until the end of the experiment (day 49) in the treatment with permanent low light intensity. In treatments with periodically changing light intensities, the phytoplankton abundance reached saturation levels between these dates. Under phytoplankton abundance saturation, chlorophytes predominated in the treatment with permanent high light, while either cyanophytes or diatoms were abundant under permanent low light intensity. Treatments with changing light supply had chlorophyte- and cyanobacteria-dominated replicates as well as replicates with balanced proportions of both. Furthermore, species diversity, measured by the Shannon index, was low in cultures under permanent light intensity, while slow fluctuating light at the scale of 3 –12xa0days resulted in an increased diversity index.These results indicate that species composition and diversity of the phytoplankton were affected by the periodically changing light regime in the order of days, and suggest that temporal changes in weather conditions are a major impediment to competitive exclusion of phytoplankton species in nature.

Genotype × environment interactions, stoichiometric food quality effects, and clonal coexistence in Daphnia pulex

The role of stoichiometric food quality in influencing genotype coexistence and competitive interactions between clones of the freshwater microcrustacean, Daphnia pulex, was examined in controlled laboratory microcosm experiments. Two genetically distinct clones of D. pulex, which show variation in their ribosomal (r)DNA structure, as well as differences in a number of previously characterized growth-rate-related features (i.e., life-history features), were allowed to compete in two different arenas: (1) batch cultures differing in algal food quality (i.e., high vs. low carbon:phosphorus (C:P ratio) in the green alga, Scenedesmus acutus); (2) continuous flow microcosms receiving different light levels (i.e., photosynthetically active radiation) that affected algal C:P ratios. In experiment 1, a clear genotypexa0×xa0environment interaction was determined with clone 1 out-competing clone 2 under high nutrient (i.e., low food C:P) conditions, while the exact opposite pattern was observed under low nutrient (i.e., high C:P) conditions. In experiment 2, clone 1 dominated over clone 2 under high light (higher C:P) conditions, but clonal coexistence was observed under low light (low C:P) conditions. These results indicate that food (nutrient) quality effects (hitherto an often overlooked factor) may play a role in microevolutionary (genotypic) responses to changing stoichiometric conditions in natural populations.

Temporal and Vertical Difference in Factors Limiting Growth Rate of Heterotrophic Bacteria in Lake Biwa.

A bstractDilution bioassays were performed to examine the seasonal and vertical difference in the relative importance of factors limiting growth of heterotrophic bacteria in Lake Biwa. The lake water diluted by 0.2 μm lake filtrate (1:6.6) was enriched either with glucose (C), inorganic phosphorus (P), ammonium nitrogen (N), amino acids (AA), or a combination of these, and incubated for 2 days at the depths where lake water was collected (2.5, 20 and 30 m depths). Experiments showed that at 2.5 m, P was the most deficient resource for bacterial growth, but the magnitude of P limitation depended on water temperature. Among others, amino acids showed a slight but significant stimulation of bacterial growth rates during the fall. At 20 and 30 m, however, growth stimulation by resource addition was rarely detected. Vertically reciprocal translocation experiments revealed that the growth rate was limited by low temperature rather than resource supply at the greater depths. The results support a simple view that bacterial growth rate is basically regulated by water temperature, but high growth rate is not realized in summer because of resource depletion. The present study suggests that both temperature and P supply play a crucial role in biogeochemical cycling of organic matter in Lake Biwa through the bacterial growth rate.

Assessment of ‘top-down’ and ‘bottom-up’ forces as determinants of rotifer distribution among lakes in Ontario, Canada

Predation and food supply are generally perceived as important determinants of spatial and temporal variations of populations. The population dynamics of freshwater rotifers have been well researched in this aspect. However, their spatial variations have attracted less attention and have not been studied by simultaneously considering both predation and food supply. We studied spatial variations of rotifer abundance among 34 Canadian boreal lakes. A large part of the variance of rotifer abundance was associated with variables related to trophic status including chlorophyll a and total phosphorus. However, abundances of mesozooplankton such as potential predators and competitors did not correlate with rotifer abundance and did not explain the residual of the regression between rotifer abundance and chlorophyll a. The results of the present study indicated that variation in rotifer abundance among lakes was caused by ‘bottom-up’ forces related to food supply and not by ‘top-down’ predatory interactions. This provides a contrast to previous empiric and experimental studies that reported that temporal variations of rotifer abundance were mainly regulated by ‘top-down’ interactions. This discrepancy suggests that overall differences in rotifer abundance among lakes are mainly determined by ‘bottom-up’ forces while temporal changes in single lakes are shaped by ‘top-down’ forces. Meanwhile, the composition of rotifer species was correlated with mesozooplankton abundance as well as trophic status. Rotifer species with long spines or rigid loricae were found in the lakes where mesozooplankton were abundant, which suggests that defensive morphology could have affected the rotifer species distribution among the study lakes.

Phytoplankton growth rate as a function of cell size: an experimental test in Lake Biwa

Abstract It is well known that algal growth rates decrease with increasing cell size. Most of these findings were, however, obtained under laboratory conditions. It is not clear if these allometric relationships are also applicable to in situ conditions. In the present study, the relationship between growth rates and cell size of algal species was examined seasonally in Lake Biwa by in situ dilution bioassays. The bioassays revealed that the highest growth rate of each species throughout the experiments was negatively correlated with cell size consistent with known allometric relationships. At each incubation experiment, however, growth rates were not necessarily correlated with cell size. This was true even when both macro- and micronutrients were added, although a substantial number of species responded to nutrient enrichment. These results showed that nutrient supplies affected algal species differently regardless of cell size and that factors other than nutrient supplies limited the growth rate of some algal species. Due to such species-specific differences in limiting factors, at any given time in situ growth rates of algae are not determined exclusively by cell size.