Marcia Kyle

Shifts in Lake N:P Stoichiometry and Nutrient Limitation Driven by Atmospheric Nitrogen Deposition

Nitrogen Overload The cycling of essential nutrients in terrestrial ecosystems has been altered by human activities. Elser et al. (p. 835) report a comparative analysis of lakes in Norway, Sweden, and in the United States that suggests that this is also true in aquatic ecosystems such as lakes. Deposition of anthropogenically derived atmospheric nitrogen controls whether N or P is growth-limiting for phytoplankton. Under elevated conditions of atmospheric N inputs, lake phytoplankton become consistently P-limited because the N:P ratio is strongly distorted. This is in contrast to conditions of low N deposition when lake phytoplankton are N-limited. These effects are even observed in remote lakes, demonstrating the indirect yet wide-ranging effects of humans on global food webs. Deposition of anthropogenically derived nitrogen can cause phosphorus to become the limiting nutrient of lake phytoplankton. Human activities have more than doubled the amount of nitrogen (N) circulating in the biosphere. One major pathway of this anthropogenic N input into ecosystems has been increased regional deposition from the atmosphere. Here we show that atmospheric N deposition increased the stoichiometric ratio of N and phosphorus (P) in lakes in Norway, Sweden, and Colorado, United States, and, as a result, patterns of ecological nutrient limitation were shifted. Under low N deposition, phytoplankton growth is generally N-limited; however, in high–N deposition lakes, phytoplankton growth is consistently P-limited. Continued anthropogenic amplification of the global N cycle will further alter ecological processes, such as biogeochemical cycling, trophic dynamics, and biological diversity, in the world’s lakes, even in lakes far from direct human disturbance.

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.

Nutrient availability and phytoplankton nutrient limitation across a gradient of atmospheric nitrogen deposition

Atmospheric nitrogen (N) deposition to lakes and watersheds has been increasing steadily due to various anthropogenic activities. Because such anthropogenic N is widely distributed, even lakes relatively removed from direct human disturbance are potentially impacted. However, the effects of increased atmospheric N deposition on lakes are not well documented. We examined phytoplankton biomass, the absolute and relative abundance of limiting nutrients (N and phosphorus [P]), and phytoplankton nutrient limitation in alpine lakes of the Rocky Mountains of Colorado (USA) receiving elevated (> 6 kg N x ha(-1) x yr(-1)) or low (< 2 kg N x ha(-1) x yr(-1)) levels of atmospheric N deposition. High-deposition lakes had higher NO3-N and total N concentrations and higher total N : total P ratios. Concentrations of chlorophyll and seston carbon (C) were 2-2.5 times higher in high-deposition relative to low-deposition lakes, while high-deposition lakes also had higher seston C:N and C:P (but not N:P) ratios. Short-term enrichment bioassays indicated a qualitative shift in the nature of phytoplankton nutrient limitation due to N deposition, as high-deposition lakes had an increased frequency of primary P limitation and a decreased frequency and magnitude of response to N and to combined N and P enrichment. Thus elevated atmospheric N deposition appears to have shifted nutrient supply from a relatively balanced but predominantly N-deficient regime to a more consistently P-limited regime in Colorado alpine lakes. This adds to accumulating evidence that sustained N deposition may have important effects on lake phytoplankton communities and plankton-based food webs by shifting the quantitative and qualitative nature of nutrient limitation.

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.

Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity

Human activities have resulted in increased nitrogen deposition and atmospheric CO2 concentrations in the biosphere, potentially causing significant changes in many ecological processes. In addition to these ongoing perturbations of the abiotic environment, human-induced losses of biodiversity are also of major concern and may interact in important ways with biogeochemical perturbations to affect ecosystem structure and function. We have evaluated the effects of these perturbations on plant biomass stoichiometric composition (C:N:P ratios) within the framework of the BioCON experimental setup (biodiversity, CO2, N) conducted at the Cedar Creek Natural History Area, Minnesota. Here we present data for five plant species: Solidago rigida, Achillea millefolium, Amorpha canescens, Lespedeza capitata, and Lupinus perennis. We found significantly higher C:N and C:P ratios under elevated CO2 treatments, but species responded idiosyncratically to the treatment. Nitrogen addition decreased C:N ratios, but this response was greater in the ambient CO2 treatments than under elevated CO2. Higher plant species diversity generally lowered both C:N and C:P ratios. Importantly, increased diversity also led to a more modest increase in the C:N ratio with elevated CO2 levels. In addition, legumes exhibited lower C:N and higher C:P and N:P ratios than non-legumes, highlighting the effect of physiological characteristics defining plant functional types. These data suggest that atmospheric CO2 levels, N availability, and plant species diversity interact to affect both aboveground and belowground processes by altering plant elemental composition.

Effects of stoichiometric dietary mixing on Daphnia growth and reproduction

Herbivores often encounter nutritional deficiencies in their diets because of low nutrient content of plant biomass. Consumption of various diet items with different nutrient contents can potentially alleviate these nutritional deficiencies. However, most laboratory studies and modeling of herbivorous animals have been done with diets in which all food has uniform nutrient content. It is not clear whether heterogeneous versus uniform food of equal overall nutrient content is of equivalent nutritional value. We tested the effects of dietary mixing on performance of a model organism, Daphnia. We fed two species of Daphnia ( D. galeata, D. pulicaria) with diets of equivalent bulk stoichiometric food quality (C:P) and studied whether they would produce equivalent performance when C:P was uniform among cells or when the diet involved a mixture of high C:P and low C:P cells. Daphnia were fed saturating and limiting concentrations of a uniform food of moderate C:P (UNI) or mixtures (MIX) of high C:P (LOP) and low C:P (HIP) algae prepared to match C:P in UNI. Daphnia were also fed HIP and LOP algae separately. Juvenile growth rate and adult fecundity were measured. D. galeata performance in UNI and MIX treatments did not differ, indicating that partitioning of C and P among particles did not affect dietary quality. Similarly, D. pulicaria‘s performance was similar in the MIX and UNI treatments but only at low food abundance. In the high food treatment, both growth and reproduction were higher in the MIX treatment, indicating some benefit of a more heterogeneous diet. The mechanisms for this improvement are unclear. Also, food quality affected growth and reproduction even at low food levels for both D. pulicaria and D. galeata. Our results indicate that some species of zooplankton can benefit from stoichiometric heterogeneity on diet.

Extensive natural intraspecific variation in stoichiometric (C:N:P) composition in two terrestrial insect species

Abstract Heterotrophic organisms must obtain essential elements in sufficient quantities from their food. Because plants naturally exhibit extensive variation in their elemental content, it is important to quantify the within-species stoichiometric variation of consumers. If extensive stoichiometric variation exists, it may help explain consumer variation in life-history strategy and fitness. To date, however, research on stoichiometric variation has focused on interspecific differences and assumed minimal intraspecific differences. Here this assumption is tested. Natural variation is quantified in body stoichiometry of two terrestrial insects: the generalist field cricket, Gryllus texensis Cade and Otte (Orthoptera: Gryllidae) and a specialist curculionid weevil, Sabinia setosa (Le Conte) (Coleoptera: Curculionidae). Both species exhibited extensive intraspecific stoichiometric variation. Cricket body nitrogen content ranged from 8–12% and there was a four-fold difference in body phosphorus content, ranging from 0.32–1.27%. Body size explained half this stoichiometric variation, with larger individuals containing less nitrogen and phosphorus. Weevils exhibited an almost three-fold difference in body phosphorus content, ranging from 0.38–0.97%. Overall, the variation observed within each of these species is comparable to the variation previously observed across almost all terrestrial insect species.

Biological Stoichiometry in Human Cancer

Background A growing tumor in the body can be considered a complex ecological and evolutionary system. A new eco-evolutionary hypothesis (the “Growth Rate Hypothesis”, GRH) proposes that tumors have elevated phosphorus (P) demands due to increased allocation to P-rich nucleic acids, especially ribosomal RNA, to meet the protein synthesis demands of accelerated proliferation. Methodology/Principal Findings We determined the elemental (C, N, P) and nucleic acid contents of paired malignant and normal tissues from colon, lung, liver, or kidney for 121 patients. Consistent with the GRH, lung and colon tumors were significantly higher (by approximately two-fold) in P content (fraction of dry weight) and RNA content and lower in nitrogen (N):P ratio than paired normal tissue, and P in RNA contributed a significantly larger fraction of total biomass P in malignant relative to normal tissues. Furthermore, patient-specific differences for %P between malignant and normal tissues were positively correlated with such differences for %RNA, both for the overall data and within three of the four organ sites. However, significant differences in %P and %RNA between malignant and normal tissues were not seen in liver and kidney and, overall, RNA contributed only ∼11% of total tissue P content. Conclusions/Significance Data for lung and colon tumors provide support for the GRH in human cancer. The two-fold amplification of P content in colon and lung tumors may set the stage for potential P-limitation of their proliferation, as such differences often do for rapidly growing biota in ecosystems. However, data for kidney and liver do not support the GRH. To account for these conflicting observations, we suggest that local environments in some organs select for neoplastic cells bearing mutations increasing cell division rate (“r-selected,” as in colon and lung) while conditions elsewhere may select for reduced mortality rate (“K-selected,” as in liver and kidney).

Effects of light and nutrients on plankton stoichiometry and biomass in a P-limited lake

A field enclosure experiment was performed over 12 weeks in a P-limited lake to test the hypothesis that light:nutrient balance affects pelagic communities by altering the C:P stoichiometry of seston and by influencing exudation of labile DOC by algae. Three levels of light intensity (ambient, 50% of ambient, 25% of ambient) were cross-classified with three levels of nutrients in a factorial design (n=2). Dissolved nutrient concentrations, seston C concentration and C:P ratios in small (<1 μm) and larger (1–85 μm) size fractions were monitored, along with chlorophyll a concentration, abundance of bacteria and protozoa, and biomass and P-content of macrozooplankton. Algal exudation of recently-fixed C into the dissolved pool was also measured at the end of the experiment in selected enclosures. Treatments had no effect on seston C concentration but reduction of light intensity significantly decreased whole seston and large (1–85 μm) seston C:P ratios. However, the magnitude of these effects was modest and not likely to be ecologically significant. There were no effects of nutrient addition or light×nutrient interaction on seston stoichiometry. Algae tended to release a higher percentage of fixed C as DOC in high light enclosures but this difference was not statistically significant. There were no effects of treatments on the abundance of bacteria or protozoa but nutrient enrichment led to a statistically significant but generally modest increase in macrozooplankton biomass. No effects on zooplankton community composition or P-content were observed. Comparison of effect sizes and treatment variances indicated a high probability of type II error and thus our confidence in failing to reject the null hypothesis in most of the above cases was low. Thus, our data provide support for only some aspects of the light:nutrient hypothesis but more appropriate tests of the hypothesis should involve stronger treatments and/or increased replication in order to be better able to evaluate its validity.

Effects of zooplankton on nutrient availability and seston C : N : P stoichiometry in inshore waters of Lake Biwa, Japan

Abstract Forty-eight-hour experimental manipulations of zooplankton biomass were performed to examine the potential effects of zooplankton on nutrient availability and phytoplankton biomass (as measured by seston concentration) and C : N : P stoichiometry in eutrophic nearshore waters of Lake Biwa, Japan. Increasing zooplankton, both mixed-species communities and Daphnia alone, consistently reduced seston concentration, indicating that nearshore phytoplankton were generally edible. The zooplankton clearance rates of inshore phytoplankton were similar to rates measured previously for offshore phytoplankton. Increased zooplankton biomass led to increased concentrations of nutrients (NH4-N, soluble reactive phosphorus [SRP]). Net release rates were higher than those found in previous measurements made offshore, reflecting the nutrient-rich nature of inshore seston. Zooplankton nutrient recycling consistently decreased TIN : SRP ratios (TIN = NH4 + NO3 + NO2). This effect probably resulted from the low N : P ratios of nearshore seston, which were lower than those commonly found in crustacean zooplankton and thus resulted in low retention efficiency of P (relative to N) by the zooplankton. Thus, zooplankton grazing inshore may ameliorate algal blooms due to direct consumption but tends to create nutrient supply conditions with low N : P, potentially favoring cyanobacteria. In comparison with previous findings for offshore, it appears that potential zooplankton effects on phytoplankton and nutrient dynamics differ qualitatively in inshore and offshore regions of Lake Biwa.