Jessica R. Corman

Sustainability Challenges of Phosphorus and Food: Solutions from Closing the Human Phosphorus Cycle

The Green Revolution has led to a threefold growth in food production in the last 50 to 75 years, hut increases in crop production have required a concurrent increase in the use of inorganic phosphorus as fertilizer. A sustainable phosphorus supply is not assured, though, and food production depends on mineral phosphorus supplies that are nonrenewable and are being depleted. Phosphorus is effectively a nonsubstitutable necessity for all life. Because mineral phosphorus deposits are not distributed evenly, future phosphorus scarcity may have national security implications. Some projections show economically viable mineral reserves becoming depleted within a few decades. Phosphorus-induced food shortages are therefore a possibility, particularly in developing countries where farmers are more vulnerable to volatile fertilizer prices. Sustainable solutions to such future challenges exist, and involve closing the loop on the human phosphorus cycle. We review the current state of knowledge about human phosphorus use and dependence and present examples of these sustainable solutions.

Phosphorus in Phoenix: a budget and spatial representation of phosphorus in an urban ecosystem

As urban environments dominate the landscape, we need to examine how limiting nutrients such as phosphorus (P) cycle in these novel ecosystems. Sustainable management of P resources is necessary to ensure global food security and to minimize freshwater pollution. We used a spatially explicit budget to quantify the pools and fluxes of P in the Greater Phoenix Area in Arizona, USA, using the boundaries of the Central Arizona-Phoenix Long-Term Ecological Research site. Inputs were dominated by direct imports of food and fertilizer for local agriculture, while most outputs were small, including water, crops, and material destined for recycling. Internally, fluxes were dominated by transfers of food and feed from local agriculture and the recycling of human and animal excretion. Spatial correction of P dynamics across the city showed that human density and associated infrastructure, especially asphalt, dominated the distribution of P pools across the landscape. Phosphorus fluxes were dominated by agricultural production, with agricultural soils accumulating P. Human features (infrastructure, technology, and waste management decisions) and biophysical characteristics (soil properties, water fluxes, and storage) mediated P dynamics in Phoenix. P cycling was most notably affected by water management practices that conserve and recycle water, preventing the loss of waterborne P from the ecosystem. P is not intentionally managed, and as a result, changes in land use and demographics, particularly increased urbanization and declining agriculture, may lead to increased losses of P from this system. We suggest that city managers should minimize cross-boundary fluxes of P to the city. Reduced P fluxes may be accomplished through more efficient recycling of waste, therefore decreasing dependence on external nonrenewable P resources and minimizing aquatic pollution. Our spatial approach and consideration of both pools and fluxes across a heterogeneous urban ecosystem increases the utility of nutrient budgets for city managers. Our budget explicitly links processes that affect P cycling across space with the management of other resources (e.g., water). A holistic management strategy that deliberately couples the management of P and other resources should be a priority for cities in achieving urban sustainability.

The importance of lake-specific characteristics for water quality across the continental United States.

Lake water quality is affected by local and regional drivers, including lake physical characteristics, hydrology, landscape position, land cover, land use, geology, and climate. Here, we demonstrate the utility of hypothesis testing within the landscape limnology framework using a random forest algorithm on a national-scale, spatially explicit data set, the United States Environmental Protection Agencys 2007 National Lakes Assessment. For 1026 lakes, we tested the relative importance of water quality drivers across spatial scales, the importance of hydrologic connectivity in mediating water quality drivers, and how the importance of both spatial scale and connectivity differ across response variables for five important in-lake water quality metrics (total phosphorus, total nitrogen, dissolved organic carbon, turbidity, and conductivity). By modeling the effect of water quality predictors at different spatial scales, we found that lake-specific characteristics (e.g., depth, sediment area-to-volume ratio) were important for explaining water quality (54-60% variance explained), and that regionalization schemes were much less effective than lake specific metrics (28-39% variance explained). Basin-scale land use and land cover explained between 45-62% of variance, and forest cover and agricultural land uses were among the most important basin-scale predictors. Water quality drivers did not operate independently; in some cases, hydrologic connectivity (the presence of upstream surface water features) mediated the effect of regional-scale drivers. For example, for water quality in lakes with upstream lakes, regional classification schemes were much less effective predictors than lake-specific variables, in contrast to lakes with no upstream lakes or with no surface inflows. At the scale of the continental United States, conductivity was explained by drivers operating at larger spatial scales than for other water quality responses. The current regulatory practice of using regionalization schemes to guide water quality criteria could be improved by consideration of lake-specific characteristics, which were the most important predictors of water quality at the scale of the continental United States. The spatial extent and high quality of contextual data available for this analysis makes this work an unprecedented application of landscape limnology theory to water quality data. Further, the demonstrated importance of lake morphology over other controls on water quality is relevant to both aquatic scientists and managers.

Response of a Stoichiometrically Imbalanced Ecosystem to Manipulation of Nutrient Supplies and Ratios

Cuatro Ciénegas Basin (CCB) is a desert ecosystem that hosts a large diversity of water bodies. Many surface waters in this basin have imbalanced nitrogen (N) to phosphorus (P) stoichiometry (total N:P > 100 by atoms), where P is likely to be a limiting nutrient. To investigate the effects of nutrient stoichiometry on planktonic and sediment ecosystem components and processes, we conducted a replicated in situ mesocosm experiment in Lagunita, a shallow pond located in the southwest region of the basin. Inorganic N and P were periodically added to mesocosms under three different N:P regimes (P only, N:P = 16 and N:P = 75) while the control mesocosms were left unamended. After three weeks of fertilization, more than two thirds of the applied P was immobilized into seston or sediment. The rapid uptake of P significantly decreased biomass C:P and N:P ratios, supporting the hypothesis that Lagunita is P-limited. Meanwhile, simultaneous N and P enrichment significantly enhanced planktonic growth, increasing total planktonic biomass by more than 2-fold compared to the unenriched control. With up to 76% of added N sequestered into the seston, it is suspected that the Lagunita microbial community also experienced strong N-limitation. However, when N and P were applied at N:P = 75, the microbes remained in a P-limitation state as in the untreated control. Two weeks after the last fertilizer application, seston C:P and N:P ratios returned to initial levels but chlorophyll a and seston C concentrations remained elevated. Additionally, no P release from the sediment was observed in the fertilized mesocosms. Overall, this study provides evidence that Lagunita is highly sensitive to nutrient perturbation because the biota is primarily P-limited and experiences a secondary N-limitation despite its high TN:TP ratio. This study serves as a strong basis to justify the need for protection of CCB ecosystems and other low-nutrient microbe-dominated systems from anthropogenic inputs of both N and P.

Interaction between lithification and resource availability in the microbialites of Río Mesquites, Cuatro Ciénegas, México

Lithified microbial structures (microbialites) have been present on Earth for billions of years. Lithification may impose unique constraints on microbes. For instance, when CaCO3 forms, phosphate may be captured via coprecipitation and/or adsorption and potentially rendered unavailable for biological uptake. Therefore, the growth of microbes associated with CaCO3 may be phosphorus-limited. In this study, we compared the effects of resource addition on biogeochemical functions of microbial communities associated with microbialites and photoautotrophic microbial communities not associated with CaCO3 deposition in Río Mesquites, Cuatro Ciénegas, México. We also manipulated rates of CaCO3 deposition in microbialites to determine whether lithification reduces the bioavailability of phosphorus (P). We found that P additions significantly increased rates of gross primary production (F2,13 = 103.9, P < 0.001), net primary production (F2,13 = 129.6, P < 0.0001) and ecosystem respiration (F2,13 = 6.44, P < 0.05) in the microbialites, while P addition had no effect on photoautotrophic production in the non-CaCO3 -associated microbial communities. Growth of the non-CaCO3-associated phototrophs was only marginally stimulated when nitrogen and P were added simultaneously (F1,36 = 3.98, P = 0.053). In the microbialites, resource additions led to some shifts in the abundance of Proteobacteria, Bacteroidetes and Cyanobacteria but mostly had little effect on bacterial community composition. Ca(2+) uptake rates increased significantly with organic carbon additions (F1,13 = 8.02, P < 0.05). Lowering of CaCO3 deposition by decreasing calcium concentrations in the water led to increased microbial biomass accumulation rates in terms of both organic carbon (F4,48 = 5.23, P < 0.01) and P (F6,48 = 13.91, P < 0.001). These results provide strong evidence in support of a role of lithification in controlling P limitation of microbialite communities.

Effects of Volcanic Pumice Inputs on Microbial Community Composition and Dissolved C/P Ratios in Lake Waters: an Experimental Approach

Volcanic eruptions discharge massive amounts of ash and pumice that decrease light penetration in lakes and lead to concomitant increases in phosphorus (P) concentrations and shifts in soluble C/P ratios. The consequences of these sudden changes for bacteria community composition, metabolism, and enzymatic activity remain unclear, especially for the dynamic period immediately after pumice deposition. Thus, the main aim of our study was to determine how ambient bacterial communities respond to pumice inputs in lakes that differ in dissolved organic carbon (DOC) and P concentrations and to what extent these responses are moderated by substrate C/P stoichiometry. We performed an outdoor experiment with natural lake water from two lakes that differed in dissolved organic carbon (DOC) concentration. We measured nutrient concentrations, alkaline phosphatase activity (APA), and DOC consumption rates and assessed different components of bacterial community structure using next-generation sequencing of the 16S rRNA gene. Pumice inputs caused a decrease in the C/P ratio of dissolved resources, a decrease in APA, and an increase in DOC consumption, indicating reduced P limitation. These changes in bacteria metabolism were coupled with modifications in the assemblage composition and an increase in diversity, with increases in bacterial taxa associated with biofilm and sediments, in predatory bacteria, and in bacteria with gliding motility. Our results confirm that volcanic eruptions have the potential to alter nutrient partitioning and light penetration in receiving waterways which can have dramatic impacts on microbial community dynamics.

Nutrient dynamics and phytoplankton resource limitation in a deep tropical mountain lake

Abstract Managing lake eutrophication requires a clear understanding of resource limitation of primary productivity, yet historically research on this subject has focused on temperate lakes. In 2010, we quantified several metrics of resource limitation in Lake Atitlán, Guatemala, Central America’s deepest tropical mountain lake that has recently experienced extensive phytoplankton blooms. In contrast to many temperate lakes, Lake Atitlán did not show a relationship between total phosphorus (TP) and chlorophyll a (Chl-a) concentrations. Average molar ratios of total nitrogen (TN) to TP decreased from 16.4 to 4.5 between stratified and mixing conditions. During our monitoring period, Tropical Storm Agatha landed on Guatemala, washing in sediment from the watershed, and concentrations of P temporarily increased in the lake by >60%. Initial experimental bioassays indicated phytoplankton growth was colimited by N and P prior to the storm, whereas post-storm assays suggested limitation by P and trace elements. Compared to previous years, Limnoraphis robusta, an N-fixing cyanobacterium, increased in abundance earlier in the year; however, there was no bloom event during our sampling period. Experimental studies indicated that nitrogenase activity was limited by P and iron availability while light was secondarily limiting of overall phytoplankton growth. This study illustrates the potential for baseline nutrient and phytoplankton growth dynamics to substantially differ for tropical lake systems from conventionally studied temperate lakes and the potential for “pulse” events (e.g., tropical storms) to alter those dynamics.

Life on a Stoichiometric Knife Edge: Biogeochemical Interactions and Trophic Interactions in Stromatolites in Rio Mesquites

One of the unique features of CCB is its diverse and abundant microbialites (“stromatolites”). For example, in Rio Mesquites there are abundant spheroid or “oncoid” microbialites (akin to fossil stromatolites). These microbial communities form layers of CaCO3 when photosynthesis raises pH and precipitates CaCO3. We hypothesized that CaCO3 precipitation accentuates P limitation in CCB as carbonate deposition can trap phosphate in inorganic and organic forms in the growing matrix. A series of field experiments tested these ideas. In the first, investigators determined the balance of calcification on oncoid stromatolites with and without snails. In the next series of experiments, oncoid stromatolites were fertilized with P, and responses of biomass C:N:P ratios, microbial communities, and performance of snails were assessed. Stromatolite C:P and N:P ratios were high but decreased under P fertilization. Surprisingly, P fertilization stimulated snail performance when C:P was reduced moderately but inhibited growth and increased mortality when C:P was strongly reduced, leading us to propose a “stoichiometric knife edge” for snails, with both high and low C:P being detrimental. Finally, studies in Rio Mesquites explored the process of calcification and supported the concept of an active “competition” for P between calcification and biotic P uptake. We emerge with a view that CCB’s intense P limitation is at least in part a result of widespread CaCO3 precipitation and that this P limitation imposes a strong stoichiometric limitation on herbivore growth and thus is likely a strong selective factor for consumers.

Influence of soil temperature and moisture on the dissolved carbon, nitrogen, and phosphorus in organic matter entering lake ecosystems

Concentrations of terrestrially derived dissolved organic matter (DOM) have been increasing in many north temperate and boreal lakes for over two decades. The concentration of DOM in lakes is influenced by a number of environmental factors, but there is still considerable debate about how the availability of terrestrial DOM, and associated dissolved nitrogen and phosphorus, may be affected by drivers of climatic change. Using experimental and observational methods, we considered how changes in soil temperature and moisture affected the composition of carbon, nitrogen, and phosphorus entering freshwater lakes. In our experiment, organic soil cores were collected from the wetland shoreline of a darkly-stained seepage lake in northern Wisconsin, USA and manipulated in laboratory with temperature and moisture treatments. During the 28-day study, soil leachate was sampled and analyzed for optical properties of DOM via UV/Vis absorbance, as well as concentrations of dissolved organic carbon (DOC), total dissolved nitrogen, and total dissolved phosphorus (TDP). DOM optical properties were particularly sensitive to moisture, with drier scenarios resulting in DOM of lower molecular weight and aromaticity. Warmer temperatures led to lower DOC and TDP concentrations. To consider long-term relationships between climate and lake chemical properties, we analyzed long-term water chemistry data from two additional Wisconsin lakes from the long term ecological research (LTER) project in a cross correlation analysis with Palmer drought severity index data. Analysis of the LTER data supported our experimental results that soil moisture has a significant effect on the quality of DOM entering lakes and that climate may significantly affect lake chemical properties. Although unexpected in terms of DOM loading for climate change scenarios, these results are consistent with patterns of decomposition in organic soils and may be attributed to an increase in soil DOM processing.

Caught between a Rock and a Hard Mineral Encrustation: Long-Lived Aquatic Insects Accumulate Calcium Carbonate Deposits in a Montane Desert Stream

Abstract. Aquatic ecosystems overlying regions of limestone bedrock can feature active deposition of calcium carbonate in the form of travertine or tufa. Although most travertine deposits form a cement-like layer on stream substrates, mineral deposits can also form on benthic invertebrates. However, little is known about which taxa may be prone to calcium carbonate encrustation and which life history traits may make taxa more susceptible to becoming encrusted. Here we report the presence of calcium carbonate deposits on live insects collected from a montane stream in the Madrean Sky Islands (Huachuca Mountains) of Arizona between 2011 and 2013. Life history differences are examined between taxa with and without travertine deposits. Thirteen genera of aquatic insects were found with calcium carbonate deposits on the exoskeleton as well as 22 other genera, also encountered in the study stream, that have not previously been found with such deposits. Taxa with calcium carbonate encrustation had significantly longer-lived aquatic stages than those without encrustation. Furthermore, encrustation presence did not differ among aerial dispersal modes. These results suggest that the extent of calcium carbonate deposition on aquatic insects is primarily related to the length of time they are in the stream. Since mineral encrustation may reduce predation pressure and mobility, changes in patterns of travertine formation in these systems may have profound effects on ecological interactions.