Paradoxes of enrichment: effects of increased light versus nutrient supply on pelagic producer-grazer systems

Energy-based plant-herbivore models produce the "paradox of enrichment," a destabilizing influence of enrichment on population dynamics. Because many plants change their carbon : nutrient stoichiometry in response to the light : nutrient supply ratio, enrichment with light can cause a mismatch between the elemental compositions of plants and their herbivores. Herbivore growth rates may then decrease with increased light supply, which is termed the "paradox of energy enrichment." I present a stoichiometric phytoplankton-grazer model that accounts for the dynamical vertical light gradient and explore how algal and grazer densities, mineral nutrient concentration, algal nutrient stoichiometry, and system stability respond to enrichment with light (through changes in irradiance, background turbidity, and water column depth) versus enrichment with nutrients. Parameterized for Daphnia, the model produces several "unusual" phenomena: multiple equilibria (with grazers extinct in spite of high algal biomass at one equilibrium), inconsistent light enrichment effects on stability (light enrichment first destabilizes and then stabilizes), and the paradox of energy enrichment. These phenomena are restricted to the low end of realistic nutrient supplies except in very shallow systems, where high sedimentation rates effectively deplete the water column of nutrients. At higher nutrient supplies, light enrichment produces the classical paradox of enrichment, leading first to an increase in grazers at a stable equilibrium and then to algae-grazer oscillations.     

Goose-mediated nutrient enrichment and planktonic grazer control in arctic freshwater ponds

A dramatic increase in the breeding population of geese has occurred over the past few decades at Svalbard. This may strongly impact the fragile ecosystems of the Arctic tundra because many of the ultra-oligotrophic freshwater systems experience enrichment from goose feces. We surveyed 21 shallow tundra ponds along a gradient of nutrient enrichment based on exposure to geese. Concentrations of total phosphorus (P) and dissolved inorganic nitrogen (DIN) in the tundra ponds ranged from 2–76 to 2–23 μg l⁻¹ respectively, yet there was no significant increase in phytoplankton biomass (measured as chlorophyll a; range: 0.6–7.3 μg l⁻¹) along the nutrient gradient. This lack of response may be the result of the trophic structure of these ecosystems, which consists of only a two-trophic level food chain with high biomasses of the efficient zooplankton grazer Daphnia in the absence of fish and scarcity of invertebrate predators. Our results indicate that this may cause a highly efficient grazing control of phytoplankton in all ponds, supported by the fact that large fractions of the nutrient pools were bound in zooplankton biomass. The median percentage of Daphnia–N and Daphnia–P content to particulate (sestonic) N and P was 338 and 3009%, respectively, which is extremely high compared to temperate lakes. Our data suggest that Daphnia in shallow arctic ponds is heavily subsidized by major inputs of energy from other food sources (bacteria, benthic biofilm), which may be crucial to the persistence of strong top–down control of pelagic algae by Daphnia.     

Larval salamander growth responds to enrichment of a nutrient poor headwater stream

While many studies have measured effects of nutrient enrichment on higher trophic levels in grazing food webs, few such studies exist for detritus-based systems. We measured effects of nitrogen and phosphorus addition on growth of larval Eurycea wilderae in a heterotrophic headwater stream using a repeated mark-recapture design. Growth estimates for 208 recaptured larvae (control stream n = 92; treatment stream n = 116) resulted in a growth rate of 0.0027 d⁻¹ in each stream prior to enrichment, whereas during enrichment treatment growth rates (g = 0.0069 d⁻¹ [±0.0019, 95% C.I.]) were significantly higher than control (g = 0.0043 d⁻¹ [±0.0007, 95% C.I.]). Results indicate that E. wilderae growth is tightly linked to the detrital resource and that growth may be indirectly affected by both quantity and quality of detritus. This study provides some of the first evidence that nutrient enrichment of detritus-based systems can influence multiple trophic levels in ways similar to autotrophic systems.     

Preparation of protoplasts and regeneration of intact cells ofStreptomyces cinnamonensis

Protoplasts were prepared and intact cells were regenerated inStreptomyces cinnamonensis— a monensin producer— to make genetic manipulations with this strain possible. 70–80% of protoplasts were formed and up to 90% of them could regenerate into intact cells.     

Cascading predator control interacts with productivity to determine the trophic level of biomass accumulation in a benthic food web

Large-scale exploitation of higher trophic levels by humans, together with global-scale nutrient enrichment, highlights the need to explore interactions between predator loss and resource availability. The hypothesis of exploitation ecosystems suggests that top–down and bottom–up control alternate between trophic levels, resulting in a positive relationship between primary production and the abundance of every second trophic level. Specifically, in food webs with three effective trophic levels, primary producers and predators should increase with primary production, while in food webs with two trophic levels, only herbivores should increase. We provided short-term experimental support for these model predictions in a natural benthic community with three effective trophic levels, where the number of algal recruits, but not the biomass of gastropod grazers, increased with algal production. In contrast, when the food web was reduced to two trophic levels by removing larger predators, the number of algal recruits was unchanged while gastropod grazer biomass increased with algal production. Predator removal only affected the consumer-controlled early life-stages of algae, indicating that both the number of trophic levels and the life-stage development of the producer trophic level determine the propagation of trophic cascades in benthic systems. Our results support the hypothesis that predators interact with resource availability to determine food-web structure.     

Invasive carp and prey community composition disrupt trophic cascades in eutrophic ponds

The role of trophic cascades in structuring freshwater communities has been extensively studied. Most of this work, however, has been conducted in oligotrophic northern lakes that contain highly vulnerable cyprinid prey: aquatic communities where trophic interactions are likely to be stronger than in many other systems. Fewer studies have been conducted in eutrophic systems or have examined the bottom-up effects of benthivorous fishes, and none have directly compared these effects to those of piscivores on ecosystem structure and function. We conducted enclosure experiments in eutrophic ponds to examine trophic effects of invasive benthivores (common carp—Cyprinus carpio L.), native piscivores (largemouth bass—Micropterus salmoides [Lacepède]), and their interactions with common centrarchid prey with well-developed anti-predatory behaviors (age-1 bluegill—Lepomis macrochirus Rafinesque and young-of-year largemouth bass). At the end of the 60-day experiment, common carp had strong bottom-up effects that increased total phosphorus and turbidity while decreasing chlorophyll a biomass and macrophyte cover that resulted in decreased macroinvertebrate biomass and also decreased growth in both juvenile largemouth bass and bluegill. Piscivorous largemouth bass, however, did not affect the survival of either planktivorous juvenile largemouth bass or bluegill. Growth of juvenile largemouth bass was also not affected, but juvenile bluegill growth was significantly diminished, possibly due to nonconsumptive effects of predation. Our results suggest that, in a centrarchid-dominated eutrophic system, top-down effects of predators are overwhelmed by common carp-mediated bottom-up effects. These bottom-up effects strongly affected multiple trophic levels, thus altering aquatic community structure and function.     

Dominance of autochthonous autotrophic carbon in food webs of heterotrophic rivers

This paper addresses the river heterotrophy paradox, “How can animal biomass within riverine food webs be fueled primarily by autochthonous autotrophic production if the ecosystem as a whole is heterotrophic?”. Reviewed, stable isotope data from tropical, temperate, and arctic rivers provide evidence consistent with the revised riverine productivity model (RPM): “The primary, annual energy source supporting overall metazoan production and species diversity in mid‐ to higher‐trophic levels of most rivers (≥4th order) is autochthonous primary production entering food webs via algal‐grazer and decomposer pathways”. The revised RPM does not conflict with the heterotrophy paradox because: (a) the decomposer (microbial loop) food pathway processes most of the transported, allochthonous and autochthonous carbon and, with algal respiration in some cases, is primarily responsible for a river's heterotrophic state (P/R<1); but (b) biomass production of mid‐ to higher‐trophic levels is principally supported by an algal‐grazer (phytoplankton and benthic microalgae) pathway that is only weakly linked to the decomposer pathway. The reason the algal‐grazer pathway supports the majority of metazoan biomass is that allochthonous carbon is mostly recalcitrant, whereas carbon from autochthonous primary production, though much less plentiful, is commonly more labile (easier to assimilate), contains more energy per unit mass, and is typically preferred by metazoa.     

Analysis of a predator-prey system with predator switching

In this paper, we consider an interaction of prey and predator species where prey species have the ability of group defence. Thresholds, equilibria and stabilities are determined for the system of ordinary differential equations. Taking carrying capacity as a bifurcation parameter, it is shown that a Hopf bifurcation can occur implying that if the carrying capacity is made sufficiently large by enrichment of the environment, the model predicts the eventual extinction of the predator providing strong support for the so-called ‘paradox of enrichment’.     

Nutrient limitation of the primary production of phytoplankton in Lake Baikal

Nutrient limitation of the primary production of phytoplankton at some stations in southern and central Lake Baikal was studied by nutrient enrichment experiments in August 2002. Chlorophyll (Chl.) a concentrations ranged from 0.7 to 5.8μgl⁻¹. Inorganic nutrient concentrations were low: soluble reactive phosphorus ranged from 0.05 to 0.20μmoll⁻¹, ammonia from 0.21 to 0.41μmoll⁻¹, and nitrite plus nitrate from 0.33 to 0.37μmoll⁻¹. In the five enrichment experiments, phosphate spikes and phosphate plus nitrate spikes always stimulated primary production. Nitrate spikes also stimulated primary production in four of the experiments. Significant differences were detected between the controls and phosphate spikes and between the controls and phosphate plus nitrate spikes. Thus, the first limiting nutrient is thought to be phosphorus, but once phosphorus is supplied to the surface water, the limiting nutrient will quickly shift from phosphorus to nitrogen.     

Linking limitation to species composition: importance of inter- and intra-specific variation in grazing resistance

Short-term responses of producers highlight that key nutrients (e.g., N, P)—or combinations of these nutrients—limit primary production in aquatic and terrestrial ecosystems. These discoveries continue to provide highly valuable insights, but it remains important to ask whether nutrients always predominantly limit producers despite wide variation in nutrient supply and herbivory among systems. After all, predictions from simple food chain models (derived here) readily predict that limitation by grazers can exceed that by nutrients, given sufficient enrichment. However, shifts in composition of producers and/or increasing dominance of invulnerable stages of a producer can, in theory, reduce grazer limitation and retain primacy of nutrient limitation along nutrient supply gradients. We observed both mechanisms (inter- and intra-species variation in vulnerability to herbivory) working in a two-part mesocosm experiment. We incubated diverse benthic algal assemblages for several months either in the presence or absence of benthic macro-grazers in mesocosms that spread a broad range of nutrient supply. We then conducted short-term assays of nutrient and grazer limitation on these communities. In the “historically grazed” assemblages, we found shifts from more edible, better competitors to more resistant producers over enrichment gradients (as anticipated by the food web model built with a tradeoff in resistance vs. competitive abilities). However, contrary to our expectations, “historically ungrazed” assemblages became dominated by producers with vulnerable juvenile forms but inedible adult forms (long filaments). Consequently, we observed higher resource limitation rather than grazer limitation over this nutrient supply gradient in both “historically grazed” (expected) and “historically ungrazed” (not initially expected). Thus, via multiple, general mechanisms involving resistance to grazing (changes in species composition or variation in stage-structured vulnerability), producer assemblages should remain more strongly or as strongly limited by nutrients than grazers, even over large enrichment gradients. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Nutrient Enrichment and Food Web Composition Affect Ecosystem Metabolism in an Experimental Seagrass Habitat

Background

Food web composition and resource levels can influence ecosystem properties such as productivity and elemental cycles. In particular, herbivores occupy a central place in food webs as the species richness and composition of this trophic level may simultaneously influence the transmission of resource and predator effects to higher and lower trophic levels, respectively. Yet, these interactions are poorly understood.

Methodology/Principal Findings

Using an experimental seagrass mesocosm system, we factorially manipulated water column nutrient concentrations, food chain length, and diversity of crustacean grazers to address two questions: (1) Does food web composition modulate the effects of nutrient enrichment on plant and grazer biomasses and stoichiometry? (2) Do ecosystem fluxes of dissolved oxygen and nutrients more closely reflect above-ground biomass and community structure or sediment processes? Nutrient enrichment and grazer presence generally had strong effects on biomass accumulation, stoichiometry, and ecosystem fluxes, whereas predator effects were weaker or absent. Nutrient enrichment had little effect on producer biomass or net ecosystem production but strongly increased seagrass nutrient content, ecosystem flux rates, and grazer secondary production, suggesting that enhanced production was efficiently transferred from producers to herbivores. Gross ecosystem production (oxygen evolution) correlated positively with above-ground plant biomass, whereas inorganic nutrient fluxes were unrelated to plant or grazer biomasses, suggesting dominance by sediment microbial processes. Finally, grazer richness significantly stabilized ecosystem processes, as predators decreased ecosystem production and respiration only in the zero- and one- species grazer treatments.

Conclusions/Significance

Overall, our results indicate that consumer presence and species composition strongly influence ecosystem responses to nutrient enrichment, and that increasing herbivore diversity can stabilize ecosystem flux rates in the face of perturbations.     

Bioassay Method in Evaluation of Trophic Conditions and Nutrient Limitation in the Danube Wetland Waters (1388–1426 r. km)

The algal growth potential (AGP) in water samples of the Danube wetland waters (1388–1426 r. km) as well as the effect of nitrogen (in final concentration of 0.16 g l⁻¹) and phosphorus enrichment (in final concentration of 0.02 g l⁻¹) on the AGP was investigated by miniaturized bioassay method. Values of the total biomass of Chlorella kessleri up to the 14th day of incubation were suitable for the evaluation of trophic conditions according to the classification of AGP. On the basis of the AGP results, trophic conditions in 55% of the samples were oligo-mesotrophic and in 46% of the samples meso-eutrophic. A statistically significant correlation (r = 0.34) was established between the AGP of C. kessleri in original water samples and NO₃ concentrations in situ. The TN/TP ratio in the wetland waters indicated a greater limitation due to nitrogen than phosphorous. Significantly lower TSI_TN than TSI_SD, TSI_Chla and TSI_TP indicated nitrogen limited conditions. In order to quantify established nutrient limitation by the bioassay method, the effect of added N and P concentrations on the growth rate of C. kessleri was expressed as the degree of nutrient limitation (Δr d⁻¹) during 7 days of incubation. In the Danube wetland waters only N limitation was established in June and July; N and P limitation in May and September while in August and October 2003 neither of the tested nutrients were limiting. From May to October 2003 the significantly highest degree of nitrogen (Δr = 0.736 d⁻¹) and phosphorus limitation (Δr = 0.474 d⁻¹) was determined in Lake Sakadaš.     

Food web structure of a shallow eutrophic lake (Lake Taihu,China) assessed by stable isotope analysis

Lake Taihu is a large, shallow, and eutrophic lake in China. It has provided local communities with valuable fisheries for centuries, but little is known of the trophodynamics, or of its faunal communities. Carbon and nitrogen isotopic composition was used to assess its trophic pathways and the food web structure [food sources and trophic levels (TL)]. Basal food sources were distinguishable based on their δ¹³C values, ranging from −27.2 to −15.2‰. Consumers were also well separated in δ¹³C (−26.9 to −17.9‰ for invertebrates and −25.7 to −18.1‰ for fishes), which allowed for an effective discrimination of carbon sources between these fauna. An average trophic enrichment factor of 3.4‰ was used to calculate the TLs based on δ¹⁵N of zooplankton, with results indicating a food web having four TLs. Although δ¹⁵N values overlap and cover a large range within trophic compartments, the isotopic signatures of the species assessed revealed a general trend of ¹⁵N enrichment with increasing TL. Stable isotope signatures were also used to establish a general food web scheme in which five main trophic pathways were analyzed.     

Prey diversity and prey identity affect herbivore performance on different time scales in a long term aquatic food‐web experiment

The question whether and how diversity‐mediated productivity at the base of food‐webs influences adjacent trophic levels is still unclear. Experiments revealed negative effects on consumers due to the increasing dominance of inedible species under grazing pressure, and positive effects due to a greater variety of prey resources. We experimentally investigate two more hypotheses, which have not been addressed in detail so far: first, more diverse primary producer communities potentially use limiting resources more efficiently, and are, therefore, more productive. This effect can be considered functionally similar to a direct enrichment with limiting resources, potentially resulting in a higher stochastic risk of herbivore extinction (‘paradox of enrichment’). Second, in a stable environment, enclosed primary producer communities should evolve towards a ‘climax state’, eventually dominated by one or few prey species. Therefore, long‐term diversity effects in producer communities should more likely result from the specific traits of the dominating species, than from complementarity. To address these hypotheses, we conducted long‐term laboratory experiments, exposing the freshwater grazer Daphnia magna to a gradient of algal species richness (1, 2, 4 or 8 edible chlorophyte species). The experiments were run in batch cultures, without exchange of growth medium after the start of the experiment. Six parameters related to Daphnia population demography, biomass accrual, and stability were followed and determined over a period of up to 263 days. Producer diversity exhibited strong positive effects on the short‐term performance of grazers (first reproduction, first population peak), and on grazer mean standing stocks. However, herbivore long‐term dynamics (day of extinction and temporal stability) depended on prey species identity, namely the presence of Chlamydomonas reinhardtii. Our experiments suggest that both prey diversity and identity can have positive effects on consumer performance, but act on different time scales.     

Competing Effects of Toxin-Producing Phytoplankton on Overall Plankton Populations in the Bay of Bengal

The coexistence of a large number of phytoplankton species on a seemingly limited variety of resources is a classical problem in ecology, known as ‘the paradox of the plankton’. Strong fluctuations in species abundance due to the external factors or competitive interactions leading to oscillations, chaos and short-term equilibria have been cited so far to explain multi-species coexistence and biodiversity of phytoplankton. However, none of the explanations has been universally accepted. The qualitative view and statistical analysis of our field data establish two distinct roles of toxin-producing phytoplankton (TPP): toxin allelopathy weakens the interspecific competition among phytoplankton groups and the inhibition due to ingestion of toxic substances reduces the abundance of the grazer zooplankton. Structuring the overall plankton population as a combination of nontoxic phytoplankton (NTP), toxic phytoplankton, and zooplankton, here we offer a novel solution to the plankton paradox governed by the activity of TPP. We demonstrate our findings through qualitative analysis of our sample data followed by analysis of a mathematical model.     

DNA amounts in the nuclei ofParamecium aurelia andTetrahymena pyriformis

DNA amounts have been determined in the micronuclei and macronuclei of 8 strains ofParamecium aurelia and 6 strains ofTetrahymena pyriformis. In the case ofTetrahymena a distribution of values for the amount of DNA in the macronuclei of all the strains was observed but the lowest values were approximately the same, viz. 1.17×10⁻¹¹ g. There are two groups of strains in relation to micronuclear DNA values ofTetrahymena, one giving an average of 0.36×10⁻¹² g and the other 0.815×10⁻¹² g. The ratio of MIC/MAC DNA varies in the two groups.Paramecium again has a range of macronuclear values within each stock—lowest value 2.51×10⁻¹⁰ g—and the micronuclear values are similar in all stocks—approximately 0.613×10⁻¹² g. The ratio of MIC/MAC DNA is similar in each stock.—The haploid genome values calculated from these data show excellent agreement with the values obtained by DNA renaturation studies. Supported by a Research Grant B/SR/8276 from the Science Research Council. The Vickers densitometer was purchased with a grant from the Medical Research Council.     

Periphyton removal related to phosphorus and grazer biomass level

1. The proliferation of nuisance periphyton in enriched streams may be dependent on the biomass of the grazing macroinvertebrates present. In the present study, the effectiveness of grazer size and biomass in controlling periphyton and the extent to which grazing effectiveness was affected by enrichment level were determined. 2. Two sets of experiments with two caddisfly grazers were conducted in laboratory channels during spring and summer 1995 and 1996. The first set tested the combined effect of phosphorus enrichment and grazing, while the second set tested the effect of variable grazer biomass on periphyton biomass. 3. Grazing reduced periphyton biomass in excess of 80%, compared to ungrazed controls. Grazers were equally effective in controlling filamentous green algae, Stigeoclonium, diatoms and small colonial greens. Near complete removal of periphyton biomass by grazing occurred at even at the lowest grazer biomass level (750 mg m^??2, i.e. approximately one-third of natural levels). 4. Grazing controlled periphyton biomass more than did enrichment with soluble reactive phosphorus (SRP). 5. Grazing rates in the phosphorus-grazing interaction experiments averaged about 6 mg chl a g invertebrate^??1 day^??1, which was similar to past work in these channels and elsewhere, while rates were about five-fold higher in the variable grazer biomass experiments. 6. Simulating effects of SRP and grazing with a calibrated model suggests that higher SRP levels would be necessary to exceed a nuisance periphyton biomass level if grazers were present. However, if grazer biomass was more than 1500 mg m^??2, a nuisance level would probably not be exceeded at any SRP.     

Experimental determination of nitrogen kinetic isotope fractionation: Some principles; illustration for the denitrification and nitrification processes

Summary A few principles relative to the presentation and use of nitrogen stable isotopic data are briefly reviewed. Some classical relationships between the isotope composition of a substrate undergoing a single-step unidirectional reaction, are introduced. They are illustrated through controlled experiments on denitrification in a soil, and through nitrification by pure cultures ofNitrosomonas europaea. In the latter case, the isotope fractionation is calculated from the isotopic composition of the residual substrate, then of the product and the result is shown to be statistically the same for the two procedures. The isotopic enrichment factor for denitrification is −29.4±2.4‰ at 20°C, and −24.6±0.9‰ at 30°C; for nitrification this factor is −34.7±2.5‰ under the experimental conditions employed.     

Indirect food web interactions: sea otters and kelp forest fishes in the Aleutian archipelago

Although trophic cascades—the effect of apex predators on progressively lower trophic level species through top-down forcing—have been demonstrated in diverse ecosystems, the broader potential influences of trophic cascades on other species and ecosystem processes are not well studied. We used the overexploitation, recovery and subsequent collapse of sea otter (Enhydra lutris) populations in the Aleutian archipelago to explore if and how the abundance and diet of kelp forest fishes are influenced by a trophic cascade linking sea otters with sea urchins and fleshy macroalgae. We measured the abundance of sea urchins (biomass density), kelp (numerical density) and fish (Catch per unit effort) at four islands in the mid-1980s (when otters were abundant at two of the islands and rare at the two others) and in 2000 (after otters had become rare at all four islands). Our fish studies focused on rock greenling (Hexagrammos lagocephalus), the numerically dominant species in this region. In the mid-1980s, the two islands with high-density otter populations supported dense kelp forests, relatively few urchins, and abundant rock greenling whereas the opposite pattern (abundant urchins, sparse kelp forests, and relatively few rock greenling) occurred at islands where otters were rare. In the 2000, the abundances of urchins, kelp and greenling were grossly unchanged at islands where otters were initially rare but had shifted to the characteristic pattern of otter-free systems at islands where otters were initially abundant. Significant changes in greenling diet occurred between the mid-1980s and the 2000 although the reasons for these changes were difficult to assess because of strong island-specific effects. Whereas urchin-dominated communities supported more diverse fish assemblages than kelp-dominated communities, this was not a simple effect of the otter-induced trophic cascade because all islands supported more diverse fish assemblages in 2000 than in the mid-1980s.     

Nutritional value of algae: a critical control on the stability of Daphnia-algal systems

In Daphnia–algal systems, the effect of nutrient enrichmenton stability is an important ecological issue. Here I considera system of Daphnia and two potential prey; one prey termedprimary algae, which are preferentially consumed, and the othersecondary algae, which yield less nutrition and are more resistantto the grazer. The presence of secondary algae is a key to thestability, but their nutritional value has not been clearlydefined in the previous theory and the actual value varies.Here I use a simple mathematical model defining explicitly thenutritional values of algae and examine the stability of thesystems as a function of phosphorus enrichment. Whether or notall three species can stably coexist depended on the combinationof the algal species used for simulation. In systems where allthe species coexist in a stable manner, in which enrichmentdoes not necessarily lead to destabilization, there is alwaysa critical nutritional value of the secondary algae. Empiricalwork supports the possibility that the unknown nutritional valueof secondary algae takes a value close to the critical one.Furthermore, at the critical nutritional value, the populationresponse in the systems to enrichment is consistent with theobserved trend in natural systems. This suggests that Daphnia–algalsystems in nature can maintain stability in the face of enrichment,without requiring specific assumptions such as spatial heterogeneity.