Stoichiometry, herbivory and competition for nutrients: simple models based on planktonic ecosystems

Models are examined in which two prey species compete for two nutrient resources, and are preyed upon by a predator that recycles both nutrients. Two factors determine the effective relative supply of the nutrients, hence competitive outcomes: the external nutrient supply ratio, and the relative recycling of the two nutrients within the system. This second factor is governed by predator stoichiometry--its relative requirements for nutrients in its own biomass. A model with nutrient resources that are essential for the competing prey is detailed. Criteria are given to identify the limiting nutrient for a food chain of one competitor with the predator. Increased supply of this limiting nutrient increases predator density and concentration of this nutrient at equilibrium, while decreasing the concentration of a non-limiting nutrient. Changes in supply or recycling of a non-limiting nutrient affect only the concentration of that nutrient. Criteria for the invasion of a second prey competitor are presented. When different nutrients limit growth of the resident prey and the invader, increased supply or recycling of the invader's limiting nutrient assists invasion, while increased supply or recycling of the resident's limiting nutrient hinders invasion. If the same nutrient limits both resident and invader, then changes in supply and recycling have complex effects on invasion, depending on species properties. In a parameterized model of a planktonic ecosystem, green algae and cyanobacteria coexist over a wide range of nitrogen:phosphorus supply ratios, without predators. When the herbivore Daphnia is added, coexistence is eliminated or greatly restricted, and green algae dominate over a wide range of supply conditions, because the effective supply of P is greatly reduced as Daphnia rapidly recycles N.     

Herbivorous animals can mitigate unfavourable ratios of energy and material supplies by enhancing nutrient recycling

Recent evidence shows that high supply ratios of light and nutrients limit planktonic herbivore growth by lowering the nutritional quality of algae. Over longer time scales, however, grazers may ameliorate this effect by their impact on nutrient cycling. We examine this possibility using two species of the herbivorous zooplankter Daphnia and its algal prey under different light intensities and low phosphorus supply in laboratory microcosms. At high light, Daphnia biomass was limited for a substantial period because of low P content of algal cells. However, a gradual increase in Daphnia density eventually improved food quality through grazing and nutrient cycling and via a novel process involving positive density dependence. Competitive exclusion of one of the two Daphnia species occurred under low light but not under high light when algae were nutritionally unsuitable. Such stoichiometrically mediated interactions among herbivorous animals may represent important mechanisms that affect community structure and material flows in ecosystems.     

Analytical solution for a hybrid Logistic-Monod cell growth model in batch and continuous stirred tank reactor culture

Monod and Logistic growth models have been widely used as basic equations to describe cell growth in bioprocess engineering. In the case of the Monod equation, the specific growth rate is governed by a limiting nutrient, with the mathematical form similar to the Michaelis–Menten equation. In the case of the Logistic equation, the specific growth rate is determined by the carrying capacity of the system, which could be growth-inhibiting factors (i.e., toxic chemical accumulation) other than the nutrient level. Both equations have been found valuable to guide us build unstructured kinetic models to analyze the fermentation process and understand cell physiology. In this work, we present a hybrid Logistic-Monod growth model, which accounts for multiple growth-dependent factors including both the limiting nutrient and the carrying capacity of the system. Coupled with substrate consumption and yield coefficient, we present the analytical solutions for this hybrid Logistic-Monod model in both batch and continuous stirred tank reactor (CSTR) culture. Under high biomass yield (Y_x/s) conditions, the analytical solution for this hybrid model is approaching to the Logistic equation; under low biomass yield condition, the analytical solution for this hybrid model converges to the Monod equation. This hybrid Logistic-Monod equation represents the cell growth transition from substrate-limiting condition to growth-inhibiting condition, which could be adopted to accurately describe the multi-phases of cell growth and may facilitate kinetic model construction, bioprocess optimization, and scale-up in industrial biotechnology.     

Use of dried algae as a food source for zooplankton growth and nutrient release experiments

Zooplankton growth and nutrient recycling are key processes in the operation of pelagic food webs. Most studies investigating these processes rely on complex methods and often require extensive laboratory facilities. Here we introduce a technique for preserving algae by rapid drying for later use in laboratory- or field-based growth and nutrient recycling experiments. Chemostat-grown Scenedesmus acutus was rapidly dried for later experiments evaluating its nutritional composition, suitability for animal growth and potential for use in nutrient release experiments. Reconstituted dried algae had slightly lower nitrogen (N), Phosphorus (P) and protein content (% dry weight) than fresh algae, but lipid content did not differ and elemental ratios were in the range considered to indicate favorable food quality. These elemental and biochemical differences did not appear functionally important, as Daphnia magna grew identically on fresh and dried food. Freeze-dried S.acutus did not work as an alternative to oven drying as it resulted in 100% mortality. NH4 and PO4 concentrations did not change over 24 h when dried algae were resuspended in normal media or boiled lake water. However, concentrations of PO4 decreased over 24 h, suggesting chemical adsorption of PO4 to the dried algae and reinforcing the need for animal-free controls in nutrient release experiments using this approach. N and P release rates for D.magna and natural zooplankton communities were estimated using dried algae, and values were comparable to published ones. Thus, dried algae may be a useful, simple technique for studying food quality and nutrient release in environments where maintaining active algal cultures may not be practical and a constant supply of consistent quality food is needed.      

Positive feedbacks between bottom-up and top-down controls promote the formation and toxicity of ecosystem disruptive algal blooms: A modeling study

Harmful algal blooms that disrupt and degrade ecosystems (ecosystem disruptive algal blooms, EDABs) are occurring with greater frequency and severity with eutrophication and other adverse anthropogenic alterations of coastal systems. EDAB events have been hypothesized to be caused by positive feedback interactions involving differential growth of competing algal species, low grazing mortality rates on EDAB species, and resulting decreases in nutrient inputs from grazer-mediated nutrient cycling as the EDAB event progresses. Here we develop a stoichiometric nutrient–phytoplankton–zooplankton (NPZ) model to test a conceptual positive feedback mechanism linked to increased cell toxicity and resultant decreases in grazing mortality rates in EDAB species under nutrient limitation of growth rate. As our model EDAB alga, we chose the slow-growing, toxic dinoflagellate Karenia brevis, whose toxin levels have been shown to increase with nutrient (nitrogen) limitation of specific growth rate. This species was competed with two high-nutrient adapted, faster-growing diatoms (Thalassiosira pseudonana and Thalassiosira weissflogii) using recently published data for relationships among nutrient (ammonium) concentration, carbon normalized ammonium uptake rates, cellular nitrogen:carbon (N:C) ratios, and specific growth rate. The model results support the proposed positive feedback mechanism for EDAB formation and toxicity. In all cases the toxic bloom was preceded by one or more pre-blooms of fast-growing diatoms, which drew dissolved nutrients to low growth rate-limiting levels, and stimulated the population growth of zooplankton grazers. Low specific grazing rates on the toxic, nutrient-limited EDAB species then promoted the population growth of this species, which further decreased grazing rates, grazing-linked nutrient recycling, nutrient concentrations, and algal specific growth rates. The nutrient limitation of growth rate further increased toxin concentrations in the EDAB algae, which further decreased grazing-linked nutrient recycling rates and nutrient concentrations, and caused an even greater nutrient limitation of growth rate and even higher toxin levels in the EDAB algae. This chain of interactions represented a positive feedback that resulted in the formation of a high-biomass toxic bloom, with low, nutrient-limited specific growth rates and associated high cellular C:N and toxin:C ratios. Together the elevated C:N and toxin:C ratios in the EDAB algae resulted in very high bloom toxicity. The positive feedbacks and resulting bloom formation and toxicity were increased by long water residence times, which increased the relative importance of grazing-linked nutrient recycling to the overall supply of limiting nutrient (N).     

Multiple resource limitation theory applied to herbivorous consumers: Liebig's minimum rule vs. interactive co-limitation

There is growing consensus that the growth of herbivorous consumers is frequently limited by more than one nutrient simultaneously. This understanding, however, is based primarily on theoretical considerations and the applicability of existing concepts of co-limitation has rarely been tested experimentally. Here, we assessed the suitability of two contrasting concepts of resource limitation, i.e. Liebig's minimum rule and the multiple limitation hypothesis, to describe nutrient-dependent growth responses of a freshwater herbivore (Daphnia magna) in a system with two potentially limiting nutrients (cholesterol and eicosapentaenoic acid). The results indicated that these essential nutrients interact, and do not strictly follow Liebig's minimum rule, which consistently overestimates growth at co-limiting conditions and thus is not applicable to describe multiple nutrient limitation of herbivorous consumers. We infer that the outcome of resource-based modelling approaches assessing herbivore population dynamics strongly depends on the applied concept of co-limitation.     

Evidence of phosphorus-limited individual and population growth of Daphnia in a Canadian Shield lake

We performed bag experiments in a Canadian Shield lake with generally high seston (suspended food particles mainly composed of algae) carbon (C):phosphorus (P) ratios, and investigated the responses of individual and population growth of herbivorous Daphnia dentifera on their abundance with (+P) and without (−P) a phosphorus enrichment to lake water. In both treatments, increased abundance of D. dentifera reduced seston C concentration and was accompanied by decreases in population and individual growth rates. However, P-enrichment increased seston P concentration and then reduced seston C:P ratio from 400–700 to ca 100 (by atoms). As a result, both individual and population growth rates were significantly higher in the +P treatment at all animal abundances even though seston C concentrations were similar between the treatments. The magnitude of the growth enhancement by the P-enrichment was independent of animal abundance. Stepwise regression analyses revealed that 71 and 90% of the variance in the population and individual growth rates, respectively, were explained by seston C and P concentrations, and that the contribution of the seston P concentration was roughly the same as that of seston C. Such joint effects of seston C and P indicate that food quality (P content) as well as food quantity (C concentration) can influence Daphnia not only at the level of individual growth but also at the level of population dynamics in P-limited lakes. Our results thus strongly corroborate the hypothesis that the population development of a key herbivore Daphnia in P-limited Canadian Shield lakes is inhibited by the direct effects of P-limited food on individual growth, which weaken the strength of trophic cascading interactions starting from piscivorous fish through planktivorous fish and zooplankton to algae.     

The effects of top–down versus bottom–up control on benthic coral reef community structure

While climate change and associated increases in sea surface temperature and ocean acidification, are among the most important global stressors to coral reefs, overfishing and nutrient pollution are among the most significant local threats. Here we examined the independent and interactive effects of reduced grazing pressure and nutrient enrichment using settlement tiles on a coral-dominated reef via long-term manipulative experimentation. We found that unique assemblages developed in each treatment combination confirming that both nutrients and herbivores are important drivers of reef community structure. When herbivores were removed, fleshy algae dominated, while crustose coralline algae (CCA) and coral were more abundant when herbivores were present. The effects of fertilization varied depending on herbivore treatment; without herbivores fleshy algae increased in abundance and with herbivores, CCA increased. Coral recruits only persisted in treatments exposed to grazers. Herbivore removal resulted in rapid changes in community structure while there was a lag in response to fertilization. Lastly, re-exposure of communities to natural herbivore populations caused reversals in benthic community trajectories but the effects of fertilization remained for at least 2 months. These results suggest that increasing herbivore populations on degraded reefs may be an effective strategy for restoring ecosystem structure and function and in reversing coral–algal phase-shifts but that this strategy may be most effective in the absence of other confounding disturbances such as nutrient pollution.     

Life history consequences for Daphnia pulex feeding on nutrient-limited phytoplankton

1. The growth and feeding of Daphnia pulex De Geer on different algal species was examined. The green algae Chlamydomonas reinhardtii Dangeard and Scenedesmus acutus Meyen, the diatom Synedra tenuissima Kützing, the cryptophyte Cryptomonas pyrenoidifera Geitler and the cyanobacterium Microcystis aeruginosa Kützing were cultured in non-limiting and in N- or P-limiting medium and used as food for D. pulex.
2. Growth limitations were reflected in the elemental and biochemical composition and the morphological characteristics of the algal resources.
3. The clearance rates of D. pulex feeding on nutrient-limited algae were reduced. This was not observed when nutrient-limited mutant Chlamydomonas cells without cell walls were used as food, indicating that the cell wall may play an important part.
4. In comparison with animals grown on nutrient-sufficient cells, nutrient-limited algae resulted in smaller body length, reduced brood sizes, reduced size at maturity, increased age at first reproduction and, consequently, in reduced Daphnia population growth rates.
5. Daphnia population growth rates ( r ) were negatively correlated with the C : P ratio and the carbohydrate content of the food. Moreover, significant correlations between r and clearance rates were found.
6. The observed differences in the grazing and the life history parameters of Daphnia feeding on non-limited and nutrient-limited algae may be the result of both reduced nutritional value and reduced digestibility of nutrient-limited algae.     

Mitigation of adverse effects of rising CO2 on a planktonic herbivore by mixed algal diets

Putative future increase in atmospheric CO₂ is expected to adversely affect herbivore growth due to decrease in contents of key nutrients such as nitrogen and phosphorus (P) relative to carbon in primary producers including plant and algal species. However, as many herbivores are polyphagous and as the response of primary producers to elevated CO₂ is highly species-specific, effects of elevated CO₂ on herbivore growth may differ between feeding conditions with monospecific and multiproducer diets. To examine this possibility, we performed CO₂ manipulation experiments under a P-limited condition with a planktonic herbivore, Daphnia , and three algal species, Scenedesmus obliquus (green algae), Cyclotella sp. (diatoms) and Synechococcus sp. (cyanobacteria). Semibatch cultures with single algal species (monocultures) and multiple algal species (mixed cultures) were grown at ambient (360 ppm) and high CO₂ levels (2000 ppm) that were within the natural range in lakes. Both in the mono- and mixed cultures, algal steady state abundance increased but algal P : C and N : C ratios decreased when they were grown at high CO₂. As expected, Daphnia fed monospecific algae cultured at high CO₂ had decreased growth rates despite increased algal abundance. However, when fed mixed algae cultured at high CO₂, especially consisting of diatoms and cyanobacteria or the three algal species, Daphnia maintained high growth rates despite lowered P and N contents relative to C in the algal diets. These results imply that algal diets composed of multiple species can mitigate the adverse effects of elevated CO₂ on herbivore performance, although the magnitude of this mitigation depends on the composition of algal species involved in the diets.