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, but 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.

Ecological effects of low-level phosphorus additions on two plant communities in a neotropical freshwater wetland ecosystem

We conducted a low-level phosphorus (P) enrichment study in two oligotrophic freshwater wetland communities (wet prairies [WP] and sawgrass marsh [SAW]) of the neotropical Florida Everglades. The experiment included three P addition levels (0, 3.33, and 33.3 mg P m−2 month−1), added over 2 years, and used in situ mesocosms located in northeastern Everglades National Park, Fla., USA. The calcareous periphyton mat in both communities degraded quickly and was replaced by green algae. In the WP community, we observed significant increases in net aboveground primary production (NAPP) and belowground biomass. Aboveground live standing crop (ALSC) did not show a treatment effect, though, because stem turnover rates of Eleocharis spp., the dominant emergent macrophyte in this community, increased significantly. Eleocharis spp. leaf tissue P content decreased with P additions, causing higher C:P and N:P ratios in enriched versus unenriched plots. In the SAW community, NAPP, ALSC, and belowground biomass all increased significantly in response to P additions. Cladium jamaicense leaf turnover rates and tissue nutrient content did not show treatment effects. The two oligotrophic communities responded differentially to P enrichment. Periphyton which was more abundant in the WP community, appeared to act as a P buffer that delayed the response of other ecosystem components until after the periphyton mat had disappeared. Periphyton played a smaller role in controlling ecosystem dynamics and community structure in the SAW community. Our data suggested a reduced reliance on internal stores of P by emergent macrophytes in the WP that were exposed to P enrichment. Eleocharis spp. rapidly recycled P through more rapid aboveground turnover. In contrast, C. jamaicense stored added P by initially investing in belowground biomass, then shifting growth allocation to aboveground tissue without increasing leaf turnover rates. Our results suggest that calcareous wetland systems throughout the Caribbean, and oligotrophic ecosystems in general, respond rapidly to low-level additions of their limiting nutrient.

Temporally dependent C, N, and P dynamics associated with the decay of Rhizophora mangle L. leaf litter in oligotrophic mangrove wetlands of the Southern Everglades

We performed two litter decomposition experiments using nearly-senesced red mangrove (Rhizophora mangle L.) leaves collected from an Everglades dwarf mangrove wetland to understand the short-term (3 weeks) and long-term (1 year) changes in mass, as well as C-, N-, and P-content of decomposing leaf litter. We expected that leaves decomposing in this oligotrophic environment would be short-term sources of C, N, and P, but potential long-term sinks for N and P. In May 1998, we conducted a 3-week leaching experiment, incubating fresh, individual leaves in seawater for up to 21 days. From May 1997 to May 1998, leaf litter in mesh bags decomposed on the forest floor at two dwarf mangrove sites. Leaching accounted for about 33% loss of dry mass from R. mangle leaves after 3 weeks. Leaching losses were rapid, peaking by day 2, and large, with leachate concentrations of total organic carbon (TOC) and total phosphorus (TP) increasing by more than an order of magnitude after 3 weeks. Mean leaf C:N increased from 105 to 115 and N:P increased from a mean of 74 to 95 after 21 days, reflecting the relatively large leaching losses of N and P. Loss of mass in the litterbags leveled off after 4 months, with roughly 60%dry mass remaining (DMR) after nearly 1 year of decomposition. The mass of carbon in each litterbag declined significantly after 361 days, but the mass of nitrogen and phosphorus doubled, indicating long-term accumulation of these constituents into the detritus. Subsequently, the leaf C:N ratio dropped significantly from 90 to 34 after 361 days. Following an initial 44-day increase, leaf N:P decreased from 222 to 144, reflecting high accumulation of P relative to N. A review of several estuarine macrophyte decomposition studies reveals a trend in nitrogen accumulation through time regardless of site, but suggests no clear pattern for C and P. We believe that the increase in litter P observed in this study was indicative of the P-limited status of the greater Everglades ecosystem and that decomposing mangrove litter may represent a substantial phosphorus pool in the system.

Coastal groundwater discharge – an additional source of phosphorus for the oligotrophic wetlands of the Everglades

In this manuscript we define a new term we call coastal groundwater discharge (CGD), which is related to submarine groundwater discharge (SGD), but occurs when seawater intrudes inland to force brackish groundwater to discharge to the coastal wetlands. A hydrologic and geochemical investigation of both the groundwater and surface water in the southern Everglades was conducted to investigate the occurrence of CGD associated with seawater intrusion. During the wet season, the surface water chemistry remained fresh. Enhanced chloride, sodium, and calcium concentrations, indicative of brackish groundwater discharge, were observed in the surface water during the dry season. Brackish groundwaters of the southern Everglades contain 1–2.3μM concentrations of total phosphorus (TP). These concentrations exceed the expected values predicted by conservative mixing of local fresh groundwater and intruding seawater, which both have TPμM. The additional source of TP may be from seawater sediments or from the aquifer matrix as a result of water–rock interactions (such as carbonate mineral dissolution and ion exchange reactions) induced by mixing fresh groundwater with intruding seawater. We hypothesize that CGD maybe an additional source of phosphorus (a limiting nutrient) to the coastal wetlands of the southern Everglades.

Nutrient content of the seagrass Thalassia testudinum reveals regional patterns of relative availability of nitrogen and phosphorus in the Florida Keys USA

Between 1992 and 2000, we sampled 504 randomly chosen locations in theFlorida Keys, Florida, USA, for the elemental content of green leaves of theseagrass Thalassia testudinum. Carbon content ranged from29.4–43.3% (dry weight), nitrogen content from 0.88–3.96%, andphosphorus content from 0.048–0.243%. N and P content of the samples werenot correlated, suggesting that the relative availability of N and P variedacross the sampling region. Spatial pattern in C:N indicated a decrease in Navailability from inshore waters to the reef tract 10 km offshore;in contrast, the pattern in C:P indicated an increase in P availability frominshore waters to the reef tract. The spatial pattern in N:P was used to definea P-limited region of seagrass beds in Florida Bay and near shore, and anN-limited region of seagrass beds offshore. The close juxtaposition ofN–and P-limited regions allows the possibility that N loading from thesuburban Florida Keys could influence the offshore, N-limited seagrass bedswithout impacting the more nearshore, P-limited seagrass beds. Carbonate - Nutrient lim

Responses of seagrass communities to fertilization along a gradient of relative availability of nitrogen and phosphorus in a carbonate environment

Patterns of relative nutrient availability in south Florida suggest spatial differences regarding the importance of nitrogen (N) and phosphorus (P) to benthic primary producers. We did a 14-month in situ fertilization experiment to test predictions of N and P limitation in the subtropical nearshore marine waters of the upper Florida Keys. Six sites were divided into two groups (nearshore, offshore) representing the endpoints of an N: P stoichiometric gradient. Twenty-four plots were established at each site with six replicates of each treatment (1N, 1P, 1N1P, control), for a total of 144 experimental plots. The responses of benthic communities to N and P enrichment varied appreciably between nearshore and offshore habitats. Offshore seagrass beds were strongly limited by nitrogen, and nearshore beds were affected by nitrogen and phosphorus. Nutrient addition at offshore sites increased the length and aboveground standing crop of the two seagrasses, Thalassia testudinum and Syringodium filiforme, and growth rates of T. testudinum. Nutrient addition at nearshore sites increased the relative abundance of macroalgae, epiphytes, and sediment microalgae. N limitation of seagrass in this carbonate system was clearly demonstrated. However, added phosphorus was retained in the system more effectively than N, suggesting that phosphorus might have important long-term effects on these benthic communities. The observed species-specific responses to nutrient enrichment underscores the need to monitor all primary producers when addressing questions of nutrient limitation and eutrophication in seagrass communities.

Phosphorus Availability and Salinity Control Productivity and Demography of the Seagrass Thalassia testudinum in Florida Bay

Biomass, net primary productivity (NPP), foliar elemental content, and demography of Thalassia testudinum were monitored in populations from five sites across Florida Bay beginning in January 2001. Sites were selected to take advantage of the spatial variability in phosphorus (P) availability and salinity climates across the bay. Aboveground biomass and NPP of T. testudinum were determined five to six times annually. Short-shoot demography, belowground biomass, and belowground NPP were assessed from a single destructive harvest at each site and short-shoot cohorts were estimated from leaf scar counts multiplied by site-specific leaf production rates. Biomass, relative growth rate (RGR), and overall NPP were positively correlated with P availability. Additionally, a positive correlation between P availability and the ratio of photosynthetic to non-photosynthetic biomass suggests that T. testudinum increases allocation to aboveground biomass as P availability increases. Population turnover increased with P availability, evident in positive correlations of recruitment and mortality rates with P availability. Departures from seasonally modeled estimates of RGR were found to be influenced by salinity, which depressed RGR when below 20 psu or above 40 psu. Freshwater management in the headwaters of Florida Bay will alter salinity and nutrient climates. It is becoming clear that such changes will affect T. testudinum, with likely feedbacks on ecosystem structure, function, and habitat quality.

Recent and Historic Drivers of Landscape Change in the Everglades Ridge, Slough, and Tree Island Mosaic

More than half of the original Everglades extent formed a patterned peat mosaic of elevated ridges, lower and more open sloughs, and tree islands aligned parallel to the dominant flow direction. This ecologically important landscape structure remained in a dynamic equilibrium for millennia prior to rapid degradation over the past century in response to human manipulation of the hydrologic system. Restoration of the patterned landscape structure is one of the primary objectives of the Everglades restoration effort. Recent research has revealed that three main drivers regulated feedbacks that initiated and maintained landscape structure: the spatial and temporal distribution of surface water depths, surface and subsurface flow, and phosphorus supply. Causes of recent degradation include but are not limited to perturbations to these historically important controls; shifts in mineral and sulfate supply may have also contributed to degradation. Restoring predrainage hydrologic conditions will likely preserve remaining landscape pattern structure, provided a sufficient supply of surface water with low nutrient and low total dissolved solids content exists to maintain a rainfall-driven water chemistry. However, because of hysteresis in landscape evolution trajectories, restoration of areas with a fully degraded landscape could require additional human intervention.

Phosphorus cycling and partitioning in an oligotrophic Everglades wetland ecosystem: a radioisotope tracing study

1. Our goal was to quantify short-term phosphorus (P) partitioning and identify the ecosystem components important to P cycling in wetland ecosystems. To do this, we added P radiotracer to oligotrophic, P-limited Everglades marshes. 32PO4 was added to the water column in six 1-m2 enclosed mesocosms located in long-hydroperiod marshes of Shark River Slough, Everglades National Park. Ecosystem components were then repeatedly sampled over 18 days. 2. Water column particulates (>0.45 μm) incorporated radiotracer within the first minute after dosing and stored 95–99% of total water column 32P activity throughout the study. Soluble (<0.45 μm) 32P in the water column, in contrast, was always <5% of the 32P in surface water. Periphyton, both floating and attached to emergent macrophytes, had the highest specific activity of 32P (Bq g−131P) among the different ecosystem components. Fish and aquatic macroinvertebrates also had high affinity for P, whereas emergent macrophytes, soil and flocculent detrital organic matter (floc) had the lowest specific activities of radiotracer. 3. Within the calcareous, floating periphyton mats, 81% of the initial 32P uptake was associated with Ca, but most of this 32P entered and remained within the organic pool (Ca-associated = 14% of total) after 1 day. In the floc layer, 32P rapidly entered the microbial pool and the labile fraction was negligible for most of the study. 4. Budgeting of the radiotracer indicated that 32P moved from particulates in the water column to periphyton and floc and then to the floc and soil over the course of the 18 day incubations. Floc (35% of total) and soil (27%) dominated 32P storage after 18 days, with floating periphyton (12%) and surface water (10%) holding smaller proportions of total ecosystem 32P. 5. To summarise, oligotrophic Everglades marshes exhibited rapid uptake and retention of labile 32P. Components dominated by microbes appear to control short-term P cycling in this oligotrophic ecosystem.

Short-term changes in phosphorus storage in an oligotrophic Everglades wetland ecosystem receiving experimental nutrient enrichment

Natural, unenriched Evergladeswetlands are known to be limited by phosphorus(P) and responsive to P enrichment. However,whole-ecosystem evaluations of experimental Padditions are rare in Everglades or otherwetlands. We tested the response of theEverglades wetland ecosystem to continuous,low-level additions of P (0, 5, 15, and30 μg L−1 above ambient) in replicate,100 m flow-through flumes located in unenrichedEverglades National Park. After the first sixmonths of dosing, the concentration andstanding stock of phosphorus increased in thesurface water, periphyton, and flocculentdetrital layer, but not in the soil or macrophytes. Of the ecosystem components measured, total P concentration increased the most in the floating periphyton mat (30 μg L−1: mean = 1916 μg P g−1, control: mean =149 μg P g−1), while the flocculentdetrital layer stored most of the accumulated P(30 μg L−1: mean = 1.732 g P m−2,control: mean = 0.769 g P m−2). Significant short-term responsesof P concentration and standing stock wereobserved primarily in the high dose (30 μgL−1 above ambient) treatment. Inaddition, the biomass and estimated P standingstock of aquatic consumers increased in the 30and 5 μg L−1 treatments. Alterationsin P concentration and standing stock occurredonly at the upstream ends of the flumes nearestto the point source of added nutrient. Thetotal amount of P stored by the ecosystemwithin the flume increased with P dosing,although the ecosystem in the flumes retainedonly a small proportion of the P added over thefirst six months. These results indicate thatoligotrophic Everglades wetlands respondrapidly to short-term, low-level P enrichment,and the initial response is most noticeable inthe periphyton and flocculent detrital layer.

Phosphorus budgets in Everglades wetland ecosystems: the effects of hydrology and nutrient enrichment

The Florida Everglades is a naturally oligotrophic hydroscape that has experienced large changes in ecosystem structure and function as the result of increased anthropogenic phosphorus (P) loading and hydrologic changes. We present whole-ecosystem models of P cycling for Everglades wetlands with differing hydrology and P enrichment with the goal of synthesizing existing information into ecosystem P budgets. Budgets were developed for deeper water oligotrophic wet prairie/slough (‘Slough’), shallower water oligotrophic Cladium jamaicense (‘Cladium’), partially enriched C. jamaicense/Typha spp. mixture (‘Cladium/Typha’), and enriched Typha spp. (‘Typha’) marshes. The majority of ecosystem P was stored in the soil in all four ecosystem types, with the flocculent detrital organic matter (floc) layer at the bottom of the water column storing the next largest proportion of ecosystem P pools. However, most P cycling involved ecosystem components in the water column (periphyton, floc, and consumers) in deeper water, oligotrophic Slough marsh. Fluxes of P associated with macrophytes were more important in the shallower water, oligotrophic Cladium marsh. The two oligotrophic ecosystem types had similar total ecosystem P stocks and cycling rates, and low rates of P cycling associated with soils. Phosphorus flux rates cannot be estimated for ecosystem components residing in the water column in Cladium/Typha or Typha marshes due to insufficient data. Enrichment caused a large increase in the importance of macrophytes to P cycling in Everglades wetlands. The flux of P from soil to the water column, via roots to live aboveground tissues to macrophyte detritus, increased from 0.03 and 0.2 g P m−2 yr−1 in oligotrophic Slough and Cladium marsh, respectively, to 1.1 g P m−2 yr−1 in partially enriched Cladium/Typha, and 1.6 g P m−2 yr−1 in enriched Typha marsh. This macrophyte translocation P flux represents a large source of internal eutrophication to surface waters in P-enriched areas of the Everglades.

Phosphorus Biogeochemistry and the Impact of Phosphorus Enrichment: Why Is the Everglades so Unique?

The Florida Everglades is extremely oligotrophic and sensitive to small increases in phosphorus (P) concentrations. P enrichment is one of the dominant anthropogenic impacts on the ecosystem and is therefore a main focus of restoration efforts. In this review, we synthesize research on P biogeochemistry and the impact of P enrichment on ecosystem structure and function in the Florida Everglades. There are clear patterns of increased P concentrations and altered structure and processes along nutrient-enrichment gradients in the water, periphyton, soils, macrophytes, and consumers. Periphyton, an assemblage of algae, bacteria, and associated microfauna, is abundant and has a large influence on phosphorus cycling in the Everglades. The oligotrophic Everglades is P-starved, has lower P concentrations and higher nitrogen–phosphorus (N:P) ratios, and has oxidized to only slightly reduced soil profiles compared to other freshwater wetland ecosystems. Possible general causes and indications of P limitation in the Everglades and other wetlands include geology, hydrology, and dominance of oxidative microbial nutrient cycling. The Everglades may be unique with respect to P biogeochemistry because of the multiple causes of P limitation and the resulting high degree of limitation.

Changes in mass and nutrient content of wood during decomposition in a south Florida mangrove forest

1. Large pools of dead wood in mangrove forests following disturbances such as hurricanes may influence nutrient fluxes. We hypothesized that decomposition of wood of mangroves from Florida, USA (Avicennia germinans, Laguncularia racemosa and Rhizophora mangle), and the consequent nutrient dynamics, would depend on species, location in the forest relative to freshwater and marine influences and whether the wood was standing, lying on the sediment surface or buried. 2. Wood disks (8–10 cm diameter, 1 cm thick) from each species were set to decompose at sites along the Shark River, either buried in the sediment, on the soil surface or in the air (above both the soil surface and high tide elevation). 3. A simple exponential model described the decay of wood in the air, and neither species nor site had any effect on the decay coefficient during the first 13 months of decomposition. 4. Over 28 months of decomposition, buried and surface disks decomposed following a two-component model, with labile and refractory components. Avicennia germinans had the largest labile component (18 ± 2% of dry weight), while Laguncularia racemosa had the lowest (10 ± 2%). Labile components decayed at rates of 0.37–23.71% month−1, while refractory components decayed at rates of 0.001–0.033% month−1. Disks decomposing on the soil surface had higher decay rates than buried disks, but both were higher than disks in the air. All species had similar decay rates of the labile and refractory components, but A. germinans exhibited faster overall decay because of a higher proportion of labile components. 5. Nitrogen content generally increased in buried and surface disks, but there was little change in N content of disks in the air over the 2-year study. Between 17% and 68% of total phosphorus in wood leached out during the first 2 months of decomposition, with buried disks having the greater losses, P remaining constant or increasing slightly thereafter. 6. Newly deposited wood from living trees was a short-term source of N for the ecosystem but, by the end of 2 years, had become a net sink. Wood, however, remained a source of P for the ecosystem. 7. As in other forested ecosystems, coarse woody debris can have a significant impact on carbon and nutrient dynamics in mangrove forests. The prevalence of disturbances, such as hurricanes, that can deposit large amounts of wood on the forest floor accentuates the importance of downed wood in these forests.

Patterns of phosphorus, nitrogen and δ15N along a peat development gradient in a coastal mire, Panama

Differentiation of limiting nutrients within small spatial scales has been observed in coastal mangrove forests, but research on other tropical peatlands suggests it is a more widespread phenomenon. In the Changuinola mire of coastal Panama, oligotrophy was hypothesized to increase along a gradient of peat development (peat doming). Nutrient and carbon concentration of leaf tissue, soil, and soil porewater were characterised over a successive sequence of plant communities along the gradient. Soil phosphorus (P) and nitrogen (N) concentrations decreased from 1200 μg P g−1 and 27 mg N g−1 to 377 μg P g−1 and 22 mg N g−1 within 2.7 km into the mire interior. These changes coincided with an increase in soil and average leaf N:P molar ratios from 52–128 and 24–41, respectively. Soil P was strongly related to leaf P and soil N:P to foliar N:P. There was a wide range in δ15N values for canopy (4.0 to −9.4‰), Campnosperma panamense (4.0 to −7.8‰) and understorey (4.8 to −3.1‰) species. Foliar δ15N values of canopy species were strongly related to soil N:P, soil P and leaf P. The depleted foliar δ15N values appeared to be an effect of both the N atmospheric source and P limitation. Here, P limitation is likely associated with ombrotrophic conditions that developed as hydrologic inputs became dominated by precipitation.