Ilka C. Feller

Nitrogen vs. phosphorus limitation across an ecotonal gradient in a mangrove forest

Mangrove forests are characterized by distinctive tree-height gradientsthat reflect complex spatial, within-stand differences in environmentalfactors,including nutrient dynamics, salinity, and tidal inundation, across narrowgradients. To determine patterns of nutrient limitation and the effects ofnutrient availability on plant growth and within-stand nutrient dynamics, weused a factorial experiment with three nutrient treatment levels (control, N,P)and three zones along a tree-height gradient (fringe, transition, dwarf) onoffshore islands in Belize. Transects were laid out perpendicular to theshoreline across a mangrove forest from a fringe stand along the seaward edge,through a stand of intermediate height, into a dwarf stand in the interior ofthe island. At three sites, three trees were fertilized per zone for 2yr. Although there was spatial variability in response, growth byR. mangle was generally nitrogen (N) -limited in thefringe zone;phosphorus (P) -limited in the dwarf zone; and, N- and/or P-limited in thetransition zone. Phosphorus-resorption efficiency decreased in all three zones,and N-resorption efficiency increased in the dwarf zone in response to Penrichment. The addition of N had no effect on either P or N resorptionefficiencies. Belowground decomposition was increased by P enrichment in allzones, whereas N enrichment had no effect. This study demonstrated thatessential nutrients are not uniformly distributed within mangrove ecosystems;that soil fertility can switch from conditions of N to P limitation acrossnarrow ecotonal gradients; and, that not all ecological processes respondsimilarly to, or are limited by, the same nutrient.

MANGROVE ISOTOPIC (δ15N AND δ13C) FRACTIONATION ACROSS A NITROGEN VS. PHOSPHORUS LIMITATION GRADIENT

Mangrove islands in Belize are characterized by a unique switching from nitrogen (N) to phosphorus (P) limitation to tree growth from shoreline to interior. Fertilization has previously shown that Rhizophora mangle (red mangrove) fringe trees (5–6 m tall) growing along the shoreline are N limited; dwarf trees (≤1.5 m tall) in the forest interior are P limited; and transition trees (2–4 m tall) are co-limited by both N and P. Growth patterns paralleled a landward decrease in soil flushing by tides and an increase in bioavailable N, but P availability remained consistently low across the gradient. Stable isotopic composition was measured in R. mangle leaves to aid in explaining this nutrient switching pattern and growth variation. Along control transects, leaf δ15N decreased from +0.10‰ (fringe) to −5.38‰ (dwarf). The δ15N of N-fertilized trees also varied spatially, but the values were consistently more negative (by ∼3‰) compared to control trees. Spatial variation in δ15N values disappeared when the trees were fertilized with P, and values averaged +0.12‰, similar to that in control fringe trees. Neither variation in source inputs nor microbial fractionation could fully account for the observed patterns in δ15N. The results instead suggest that the lower δ15N values in transition and dwarf control trees were due to plant fractionation as a consequence of slower growth and lower N demand. P fertilization increased N demand and decreased fractionation. Although leaf δ13C was unaffected by fertilization, values increased from fringe (−28.6‰) to transition (−27.9‰) to dwarf (−26.4‰) zones, indicating spatial variation in environmental stresses affecting stomatal conductance or carboxylation. The results thus suggest an interaction of external supply, internal demand, and plant ability to acquire nutrients under different hydro-edaphic conditions that vary across this tree-height gradient. The findings not only aid in understanding mangrove discrimination of nitrogen and carbon isotopes, but also have implications for identifying nutrient loading and other stress conditions in coastal systems dominated by mangroves.

Nutrition of mangroves.

Mangrove forests dominate the worlds tropical and subtropical coastlines. Similar to other plant communities, nutrient availability is one of the major factors influencing mangrove forest structure and productivity. Many mangrove soils have extremely low nutrient availability, although nutrient availability can vary greatly among and within mangrove forests. Nutrient-conserving processes in mangroves are well developed and include evergreeness, resorption of nutrients prior to leaf fall, the immobilization of nutrients in leaf litter during decomposition, high root/shoot ratios and the repeated use of old root channels. Both nitrogen-use efficiency and nutrient resorption efficiencies in mangroves are amongst the highest recorded for angiosperms. A complex range of interacting abiotic and biotic factors controls the availability of nutrients to mangrove trees, and mangroves are characteristically plastic in their ability to opportunistically utilize nutrients when these become available. Nitrogen and phosphorus have been implicated as the nutrients most likely to limit growth in mangroves. Ammonium is the primary form of nitrogen in mangrove soils, in part as a result of anoxic soil conditions, and tree growth is supported mainly by ammonium uptake. Nutrient enrichment is a major threat to marine ecosystems. Although mangroves have been proposed to protect the marine environment from land-derived nutrient pollution, nutrient enrichment can have negative consequences for mangrove forests and their capacity for retention of nutrients may be limited.

Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events

Significance Coastal mangrove forests support a diverse array of associated species and provide ecosystem services to human communities. Mangroves cannot tolerate extreme freezing temperatures and so are generally limited to tropical environments. However, climate change in the form of increasing temperatures has the potential to facilitate increases in mangrove abundance near tropical–temperate transition zones. Here, we use 28 y of satellite imagery to demonstrate that increases in mangrove area have already occurred along the northeast coast of Florida. These increases correspond to decreases in the frequency of extreme cold events in this region. We also identify a temperature-related ecological threshold of −4°C. These results suggest that landscape-scale increases in mangrove area may occur in other regions where this threshold is crossed. Regional warming associated with climate change is linked with altered range and abundance of species and ecosystems worldwide. However, the ecological impacts of changes in the frequency of extreme events have not been as well documented, especially for coastal and marine environments. We used 28 y of satellite imagery to demonstrate that the area of mangrove forests has doubled at the northern end of their historic range on the east coast of Florida. This expansion is associated with a reduction in the frequency of “extreme” cold events (days colder than −4 °C), but uncorrelated with changes in mean annual temperature, mean annual precipitation, and land use. Our analyses provide evidence for a threshold response, with declining frequency of severe cold winter events allowing for poleward expansion of mangroves. Future warming may result in increases in mangrove cover beyond current latitudinal limits of mangrove forests, thereby altering the structure and function of these important coastal ecosystems.

EFFECTS OF NUTRIENT ENRICHMENT ON WITHIN-STAND CYCLING IN A MANGROVE FOREST

Within-stand nutrient cycling is dependent on many factors, including pri- mary productivity, nutrient-use efficiency, nutrient resorption, sclerophylly, decomposition, nutritional quality of plant tissue, and allocation to defense. The efficiency of these plant- mediated processes depends on nutrient availability in the environment and inherent func- tional properties of plants. However, little is known about how nutrient availability will affect these processes in forested wetlands in the tropics. In a factorial experiment we fertilized 48 dwarfed Rhizophora mangle (red mangrove) trees along tidal-elevation and water-depth gradients at Twin Cays, a range of intertidal, peat-based offshore mangrove islands in Belize, Central America. Initial results indicated that phosphorus (P) deficiency is a major factor limiting primary productivity. Phosphorus-fertilized trees had a significant decrease in P-use efficiency and P-resorption efficiency, but a significant increase in nitrogen (N)-use efficiency and N-resorption efficiency in their leaves compared with controls and N-fertilized trees. Sclerophylly decreased dramatically in P-fertilized trees, while the nu- tritional quality of the plant tissue increased. Phosphorus fertilization did not affect P leaching from green leaves. We found no fertilizer effect on the decomposition rates of leaf tissue, possibly due to higher phenolic concentrations in the P-fertilized trees compared with controls and N-fertilized trees. However, belowground decomposition of cotton strips increased in the substrate associated with P-fertilized trees. Environmental conditions re- lated to position along a tidal gradient may be as important as nutrients in controlling belowground decomposition.

Mangrove growth in New Zealand estuaries: the role of nutrient enrichment at sites with contrasting rates of sedimentation

Mangrove forest coverage is increasing in the estuaries of the North Island of New Zealand, causing changes in estuarine ecosystem structure and function. Sedimentation and associated nutrient enrichment have been proposed to be factors leading to increases in mangrove cover, but the relative importance of each of these factors is unknown. We conducted a fertilization study in estuaries with different sedimentation histories in order to determine the role of nutrient enrichment in stimulating mangrove growth and forest development. We expected that if mangroves were nutrient-limited, nutrient enrichment would lead to increases in mangrove growth and forest structure and that nutrient enrichment of trees in our site with low sedimentation would give rise to trees and sediments that converged in terms of functional characteristics on control sites in our high sedimentation site. The effects of fertilizing with nitrogen (N) varied among sites and across the intertidal zone, with enhancements in growth, photosynthetic carbon gain, N resorption prior to leaf senescence and the leaf area index of canopies being significantly greater at the high sedimentation sites than at the low sedimentation sites, and in landward dwarf trees compared to seaward fringing trees. Sediment respiration (CO2 efflux) was higher at the high sedimentation site than at the low one sedimentation site, but it was not significantly affected by fertilization, suggesting that the high sedimentation site supported greater bacterial mineralization of sediment carbon. Nutrient enrichment of the coastal zone has a role in facilitating the expansion of mangroves in estuaries of the North Island of New Zealand, but this effect is secondary to that of sedimentation, which increases habitat area and stimulates growth. In estuaries with high sediment loads, enrichment with N will cause greater mangrove growth and further changes in ecosystem function.

Photosynthetic performance and resource utilization of two mangrove species coexisting in a hypersaline scrub forest

In a hypersaline mangrove scrub forest in northern Florida, coexisting trees of Laguncularia racemosa and Avicennia germinans were either fertilized with nitrogen or phosphorus, or not fertilized (controls). We aimed to test whether nutrient additions differentially altered photosynthetic performance and resource utilization in these two species. In control trees, photosynthetic rates were higher in L. racemosa than A. germinans. However, leaf nitrogen concentrations were higher in A. germinans than L. racemosa. Avicennia germinans responded to fertilization with nitrogen by increasing leaf nitrogen concentrations and rates of photosynthesis such that they were equivalent to photosynthesis in L. racemosa. Laguncularia racemosa did not show a response to nitrogen additions. Neither species showed strong responses to phosphorus fertilization. Avicennia germinans had high photosynthetic water-use efficiency (photosynthesis/transpiration), but low photosynthetic nitrogen-use efficiency (photosynthesis/leaf nitrogen). In contrast, L. racemosa had comparatively low photosynthetic water use efficiency and high photosynthetic nitrogen use efficiency. Leaf level characteristics lead us to hypothesize that coexistence of A. germinans and L. racemosa should occur where nitrogen levels are low and salinity is moderate, or at least moderate for some period of the year.

Nutrient Enrichment Increases Mortality of Mangroves

Nutrient enrichment of the coastal zone places intense pressure on marine communities. Previous studies have shown that growth of intertidal mangrove forests is accelerated with enhanced nutrient availability. However, nutrient enrichment favours growth of shoots relative to roots, thus enhancing growth rates but increasing vulnerability to environmental stresses that adversely affect plant water relations. Two such stresses are high salinity and low humidity, both of which require greater investment in roots to meet the demands for water by the shoots. Here we present data from a global network of sites that documents enhanced mortality of mangroves with experimental nutrient enrichment at sites where high sediment salinity was coincident with low rainfall and low humidity. Thus the benefits of increased mangrove growth in response to coastal eutrophication is offset by the costs of decreased resilience due to mortality during drought, with mortality increasing with soil water salinity along climatic gradients.

CO2 Efflux from cleared mangrove peat

Background CO2 emissions from cleared mangrove areas may be substantial, increasing the costs of continued losses of these ecosystems, particularly in mangroves that have highly organic soils. Methodology/Principal Findings We measured CO2 efflux from mangrove soils that had been cleared for up to 20 years on the islands of Twin Cays, Belize. We also disturbed these cleared peat soils to assess what disturbance of soils after clearing may have on CO2 efflux. CO2 efflux from soils declines from time of clearing from ∼10 600 tonnes km−2 year−1 in the first year to 3000 tonnes km2 year−1 after 20 years since clearing. Disturbing peat leads to short term increases in CO2 efflux (27 umol m−2 s−1), but this had returned to baseline levels within 2 days. Conclusions/Significance Deforesting mangroves that grow on peat soils results in CO2 emissions that are comparable to rates estimated for peat collapse in other tropical ecosystems. Preventing deforestation presents an opportunity for countries to benefit from carbon payments for preservation of threatened carbon stocks.

Nutrient Addition Differentially Affects Ecological Processes of Avicennia germinans in Nitrogen versus Phosphorus Limited Mangrove Ecosystems

Nutrient over-enrichment is a major threat to marine environments, but system-specific attributes of coastal ecosystems may result in differences in their sensitivity and susceptibility to eutrophication. We used fertilization experiments in nitrogen (N)- and phosphorus (P)-limited mangrove forests to test the hypothesis that alleviating different kinds of nutrient limitation may have different effects on ecosystem structure and function in natural systems. We compared a broad range of ecological processes to determine if these systems have different thresholds where shifts might occur in nutrient limitation. Growth responses indicated N limitation in Avicennia germinans (black mangrove) forests in the Indian River Lagoon (IRL), Florida, and P limitation at Twin Cays, Belize. When nutrient deficiency was relieved, A. germinans grew out of its stunted form by increasing wood relative to leaf biomass and shoot length relative to lateral growth. At the P-limited site, P enrichment (+P) increased specific leaf area, N resorption, and P uptake, but had no effect on P resorption. At the N-limited site, +N increased both N and P resorption, but did not alter biomass allocation. Herbivory was greater at the P-limited site and was unaffected by +P, whereas +N led to increased herbivory at the N-limited site. The responses to nutrient enrichment depended on the ecological process and limiting nutrient and suggested that N- versus P-limited mangroves do have different thresholds. +P had a greater effect on more ecological processes at Twin Cays than did +N at the IRL, which indicated that the P-limited site was more sensitive to nutrient loading. Because of this sensitivity, eutrophication is more likely to cause a shift in nutrient limitation at P-limited Twin Cays than N-limited IRL.