Practical Guide to Measuring Wetland Carbon Pools and Fluxes.

Wetlands cover a small portion of the world, but have disproportionate influence on global carbon (C) sequestration, carbon dioxide and methane emissions, and aquatic C fluxes. However, the underlying biogeochemical processes that affect wetland C pools and fluxes are complex and dynamic, making measurements of wetland C challenging. Over decades of research, many observational, experimental, and analytical approaches have been developed to understand and quantify pools and fluxes of wetland C. Sampling approaches range in their representation of wetland C from short to long timeframes and local to landscape spatial scales. This review summarizes common and cutting-edge methodological approaches for quantifying wetland C pools and fluxes. We first define each of the major C pools and fluxes and provide rationale for their importance to wetland C dynamics. For each approach, we clarify what component of wetland C is measured and its spatial and temporal representativeness and constraints. We describe practical considerations for each approach, such as where and when an approach is typically used, who can conduct the measurements (expertise, training requirements), and how approaches are conducted, including considerations on equipment complexity and costs. Finally, we review key covariates and ancillary measurements that enhance the interpretation of findings and facilitate model development. The protocols that we describe to measure soil, water, vegetation, and gases are also relevant for related disciplines such as ecology. Improved quality and consistency of data collection and reporting across studies will help reduce global uncertainties and develop management strategies to use wetlands as nature-based climate solutions. Supplementary Information: The online version contains supplementary material available at 10.1007/s13157-023-01722-2.

The impacts of mangrove range expansion on wetland ecosystem services in the southeastern United States: Current understanding, knowledge gaps, and emerging research needs.

Climate change is transforming ecosystems and affecting ecosystem goods and services. Along the Gulf of Mexico and Atlantic coasts of the southeastern United States, the frequency and intensity of extreme freeze events greatly influence whether coastal wetlands are dominated by freeze-sensitive woody plants (mangrove forests) or freeze-tolerant grass-like plants (salt marshes). In response to warming winters, mangroves have been expanding and displacing salt marshes at varying degrees of severity in parts of north Florida, Louisiana, and Texas. As winter warming accelerates, mangrove range expansion is expected to increasingly modify wetland ecosystem structure and function. Because there are differences in the ecological and societal benefits that salt marshes and mangroves provide, coastal environmental managers are challenged to anticipate the effects of mangrove expansion on critical wetland ecosystem services, including those related to carbon sequestration, wildlife habitat, storm protection, erosion reduction, water purification, fisheries support, and recreation. Mangrove range expansion may also affect wetland stability in the face of extreme climatic events and rising sea levels. Here, we review the current understanding of the effects of mangrove range expansion and displacement of salt marshes on wetland ecosystem services in the southeastern United States. We also identify critical knowledge gaps and emerging research needs regarding the ecological and societal implications of salt marsh displacement by expanding mangrove forests. One consistent theme throughout our review is that there are ecological trade-offs for consideration by coastal managers. Mangrove expansion and marsh displacement can produce beneficial changes in some ecosystem services, while simultaneously producing detrimental changes in other services. Thus, there can be local-scale differences in perceptions of the impacts of mangrove expansion into salt marshes. For very specific local reasons, some individuals may see mangrove expansion as a positive change to be embraced, while others may see mangrove expansion as a negative change to be constrained.

Coastal regime shifts: rapid responses of coastal wetlands to changes in mangrove cover.

Global changes are causing broad-scale shifts in vegetation communities worldwide, including coastal habitats where the borders between mangroves and salt marsh are in flux. Coastal habitats provide numerous ecosystem services of high economic value, but the consequences of variation in mangrove cover are poorly known. We experimentally manipulated mangrove cover in large plots to test a set of linked hypotheses regarding the effects of changes in mangrove cover. We found that changes in mangrove cover had strong effects on microclimate, plant community, sediment accretion, soil organic content, and bird abundance within 2 yr. At higher mangrove cover, wind speed declined and light interception by vegetation increased. Air and soil temperatures had hump-shaped relationships with mangrove cover. The cover of salt marsh plants decreased at higher mangrove cover. Wrack cover, the distance that wrack was distributed from the water's edge, and sediment accretion decreased at higher mangrove cover. Soil organic content increased with mangrove cover. Wading bird abundance decreased at higher mangrove cover. Many of these relationships were non-linear, with the greatest effects when mangrove cover varied from zero to intermediate values, and lesser effects when mangrove cover varied from intermediate to high values. Temporal and spatial variation in measured variables often peaked at intermediate mangrove cover, with ecological consequences that are largely unexplored. Because different processes varied in different ways with mangrove cover, the "optimum" cover of mangroves from a societal point of view will depend on which ecosystem services are most desired.

Herbivore effects increase with latitude across the extent of a foundational seagrass.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse.

Negative outcomes of novel trophic interactions along mangrove range edges.

Tropicalization is a phenomenon that is changing the structure of ecosystems around the world. Mangrove encroachment is a particular form of tropicalization that may have cascading consequences for resident fauna in subtropical coastal wetlands. There is a knowledge gap regarding the extent of interactions between basal consumers and mangroves along mangrove range edges and the consequences of these novel interactions for consumers. This study focuses on the key coastal wetland consumers, Littoraria irrorata (marsh periwinkle) and Uca rapax (mudflat fiddler crabs), and their interactions with encroaching Avicennia germinans (black mangrove) in the Gulf of Mexico, USA. In food preference assays, Littoraria avoided consuming Avicennia and selectively ingested leaf tissue from a common marsh grass, Spartina alterniflora (smooth cordgrass), a preference that was also previously documented in Uca. The quality of Avicennia as a food source was determined by measuring the energy storage of consumers that had interacted with either Avicennia or marsh plants in the lab and the field. Littoraria and Uca both stored ~10% less energy when interacting with Avicennia, despite their different feeding behaviors and physiologies. The negative consequences of mangrove encroachment for these species at the individual level suggest that there may be negative population-level effects as encroachment continues. Many studies have documented shifts in floral and faunal communities following mangrove replacement of salt marsh vegetation, but this study is the first to identify physiological responses that may be contributing to these shifts.

A hurricane alters the relationship between mangrove cover and marine subsidies.

As global change alters the composition and productivity of ecosystems, the importance of subsidies from one habitat to another may change. We experimentally manipulated black mangrove (Avicennia germinans) cover in 10 large plots and over a 5-year period (2014-2019) quantifying the effects of mangrove cover on subsidies of floating organic material (wrack) into coastal wetlands. As mangrove cover increased from 0% to 100%, wrack cover and thickness decreased by ~60%, the distance that wrack penetrated into the plots decreased by ~70%, and the percentage of the wrack trapped in the first 6 m of the plot tripled. These patterns observed during 4 "normal" years disappeared in a fifth year following Hurricane Harvey (2017), when large quantities of wrack were pushed far into the interior of all the plots, regardless of mangrove cover. Prior to the storm, the abundance of animals collected in grab samples increased with wrack biomass. Wrack composition did not affect animal abundance or composition. Experimental outplants of two types of wrack (red algae and seagrass) revealed that animal abundance and species composition varied between the fringe and interior of the plots, and between microhabitats dominated by salt marsh versus mangrove vegetation. The importance of wrack to overall carbon stocks varied as a function of autochthonous productivity: wrack inputs (per m2 ) based on survey data were greater than aboveground plant biomass in the plots (42 × 24 m) dominated by salt-marsh vegetation, but decreased to 5% of the total aboveground biomass in plots dominated by mangroves. Our results illustrate that increasing mangrove cover decreases the relative importance of marine subsidies into the intertidal at the plot level, but concentrates subsidies at the front edge of the mangrove stand. Storms, however, may temporarily override mangrove attenuation of wrack inputs. Our results highlight the importance of understanding how changes in plant species composition due to global change will impact marine subsidies and exchanges among ecosystems, and foster a broader understanding of the functional interdependence of adjacent habitats within coastal ecosystems.

Effects of mangrove cover on coastal erosion during a hurricane in Texas, USA.

We tested the hypothesis that mangroves provide better coastal protection than salt marsh vegetation using 10 1,008-m2 plots in which we manipulated mangrove cover from 0 to 100%. Hurricane Harvey passed over the plots in 2017. Data from erosion stakes indicated up to 26 cm of vertical and 970 cm of horizontal erosion over 70 months in the plot with 0% mangrove cover, but relatively little erosion in other plots. The hurricane did not increase erosion, and erosion decreased after the hurricane passed. Data from drone images indicated 196 m2 of erosion in the 0% mangrove plot, relatively little erosion in other plots, and little ongoing erosion after the hurricane. Transects through the plots indicated that the levee (near the front of the plot) and the bank (the front edge of the plot) retreated up to 9 m as a continuous function of decreasing mangrove cover. Soil strength was greater in areas vegetated with mangroves than in areas vegetated by marsh plants, or nonvegetated areas, and increased as a function of plot-level mangrove cover. Mangroves prevented erosion better than marsh plants did, but this service was nonlinear, with low mangrove cover providing most of the benefits.

Quantifying how changing mangrove cover affects ecosystem carbon storage in coastal wetlands.

Despite overall global declines, mangroves are expanding into and within many subtropical wetlands, leading to heterogeneous cover of marsh-mangrove coastal vegetation communities near the poleward edge of mangroves' ranges. Coastal wetlands are globally important carbon sinks, yet the effects of shifts in mangrove cover on organic-carbon (OC) storage remains uncertain. We experimentally maintained black mangrove (Avicennia germinans) or marsh vegetation in patches (n = 1,120, 3 × 3 m) along a gradient in mangrove cover (0-100%) within coastal wetland plots (n = 10, 24 × 42 m) and measured changes in OC stocks and fluxes. Within patches, above and belowground biomass (OC) was 1,630% and 61% greater for mangroves than for recolonized marshes, and soil OC was 30% greater beneath mangrove than marsh vegetation. At the plot scale, above and belowground biomass increased linearly with mangrove cover but soil OC was highly variable and unrelated to mangrove cover. Root ingrowth was not different in mangrove or marsh patches, nor did it change with mangrove cover. After 11 months, surface OC accretion was negatively related to plot-scale mangrove cover following a high-wrack deposition period. However, after 22 months, accretion was 54% higher in mangrove patches, and there was no relationship to plot-scale mangrove cover. Marsh (Batis maritima) leaf and root litter had 1,000% and 35% faster breakdown rates (k) than mangrove (A. germinans) leaf and root litter. Soil temperatures beneath mangroves were 1.4°C lower, decreasing aboveground k of fast- (cellulose) and slow-decomposing (wood) standard substrates. Wood k in shallow soil (0-15 cm) was higher in mangrove than marsh patches, but vegetation identity did not impact k in deeper soil (15-30 cm). We found that mangrove cover enhanced OC storage by increasing biomass, creating more recalcitrant organic matter and reducing k on the soil surface by altering microclimate, despite increasing wood k belowground and decreasing allochthonous OC subsidies. Our results illustrate the importance of mangroves in maintaining coastal OC storage, but also indicate that the impacts of vegetation change on OC storage may vary based on ecosystem conditions, organic-matter sources, and the relative spatiotemporal scales of mangrove vegetation change.

Nutrient enrichment shifts mangrove height distribution: Implications for coastal woody encroachment.

Global changes, such as increased temperatures and elevated CO2, are driving shifts in plant species distribution and dominance, like woody plant encroachment into grasslands. Local factors within these ecotones can influence the rate of regime shifts. Woody encroachment is occurring worldwide, though there has been limited research within coastal systems, where mangrove (woody shrub/tree) stands are expanding into salt marsh areas. Because coastal systems are exposed to various degrees of nutrient input, we investigated how nutrient enrichment may locally impact mangrove stand expansion and salt marsh displacement over time. We fertilized naturally co-occurring Avicennia germinans (black mangrove) and Spartina alterniflora (smooth cordgrass) stands in Port Aransas, TX, an area experiencing mangrove encroachment within the Northern Gulf of Mexico mangrove-marsh ecotone. After four growing seasons (2010-2013) of continuous fertilization, Avicennia was more positively influenced by nutrient enrichment than Spartina. Most notably, fertilized plots had a higher density of taller (> 0.5 m) mangroves and mangrove maximum height was 46% taller than in control plots. Fertilization may promote an increase in mangrove stand expansion within the mangrove-marsh ecotone by shifting Avicennia height distribution. Avicennia individuals, which reach certain species-specific height thresholds, have reduced negative neighbor effects and have higher resilience to freezing temperatures, which may increase mangrove competitive advantage over marsh grass. Therefore, we propose that nutrient enrichment, which augments mangrove height, could act locally as a positive feedback to mangrove encroachment, by reducing mangrove growth suppression factors, thereby accelerating the rates of increased mangrove coverage and subsequent marsh displacement. Areas within the mangrove-marsh ecotone with high anthropogenic nutrient input may be at increased risk of a regime shift from grass to woody dominated ecosystems.

The contribution of mangrove expansion to salt marsh loss on the Texas Gulf Coast.

Landscape-level shifts in plant species distribution and abundance can fundamentally change the ecology of an ecosystem. Such shifts are occurring within mangrove-marsh ecotones, where over the last few decades, relatively mild winters have led to mangrove expansion into areas previously occupied by salt marsh plants. On the Texas (USA) coast of the western Gulf of Mexico, most cases of mangrove expansion have been documented within specific bays or watersheds. Based on this body of relatively small-scale work and broader global patterns of mangrove expansion, we hypothesized that there has been a recent regional-level displacement of salt marshes by mangroves. We classified Landsat-5 Thematic Mapper images using artificial neural networks to quantify black mangrove (Avicennia germinans) expansion and salt marsh (Spartina alterniflora and other grass and forb species) loss over 20 years across the entire Texas coast. Between 1990 and 2010, mangrove area grew by 16.1 km(2), a 74% increase. Concurrently, salt marsh area decreased by 77.8 km(2), a 24% net loss. Only 6% of that loss was attributable to mangrove expansion; most salt marsh was lost due to conversion to tidal flats or water, likely a result of relative sea level rise. Our research confirmed that mangroves are expanding and, in some instances, displacing salt marshes at certain locations. However, this shift is not widespread when analyzed at a larger, regional level. Rather, local, relative sea level rise was indirectly implicated as another important driver causing regional-level salt marsh loss. Climate change is expected to accelerate both sea level rise and mangrove expansion; these mechanisms are likely to interact synergistically and contribute to salt marsh loss.

Avicennia germinans (black mangrove) vessel architecture is linked to chilling and salinity tolerance in the Gulf of Mexico.

Over the last several decades, the distribution of the black mangrove Avicennia germinans in the Gulf of Mexico has expanded, in part because it can survive the occasional freeze events and high soil salinities characteristic of the area. Vessel architecture may influence mangrove chilling and salinity tolerance. We surveyed populations of A. germinans throughout the Gulf to determine if vessel architecture was linked to field environmental conditions. We measured vessel density, hydraulically weighted vessel diameter, potential conductance capacity, and maximum tensile fracture stress. At each sampling site we recorded mangrove canopy height and soil salinity, and determined average minimum winter temperature from archived weather records. At a subset of sites, we measured carbon fixation rates using a LI-COR 6400XT Portable Photosynthesis System. Populations of A. germinans from cooler areas (Texas and Louisiana) had narrower vessels, likely reducing the risk of freeze-induced embolisms but also decreasing water conductance capacity. Vessels were also narrower in regions with high soil salinity, including Texas, USA and tidal flats in Veracruz, Mexico. Vessel density did not consistently vary with temperature or soil salinity. In abiotically stressful areas, A. germinans had a safe hydraulic architecture with narrower vessels that may increase local survival. This safe architecture appears to come at a substantial physiological cost in terms of reduction in conductance capacity and carbon fixation potential, likely contributing to lower canopy heights. The current distribution of A. germinans in the Gulf is influenced by the complex interplay between temperature, salinity, and vessel architecture. Given the plasticity of A. germinans vessel characters, it is likely that this mangrove species will be able to adapt to a wide range of potential future environmental conditions, and continue its expansion in the Gulf of Mexico in response to near-term climate change.

The interactive effects of pulsed grazing disturbance and patch size vary among wetland arthropod guilds.

Pulse disturbances and habitat patch size can determine community composition independently or in concert, and may be particularly influential on small spatial scales for organisms with low mobility. In a field experiment, we investigated whether the effects of a pulsed disturbance that simulated a grazing event varied with habitat patch size. We focused on the short-term responses of multiple co-occurring emergent salt marsh arthropods with differing levels of mobility and dispersal potential. As part of a marsh restoration project, two types of emergent marsh structures were created: small circular mounds (0.5 m diameter) separated by several meters of aquatic habitat, and larger, elongated terraces (>50 m long). Study plots (0.25 m(2)) were established on both structures; in a subset of plots, we simulated a pulsed grazing disturbance event by clipping the aboveground tissue of emergent plants, primarily Spartina alterniflora. At the end of the two-month recovery period, Ischnodemus (Hemiptera: Blissidae) density was over 50% lower in disturbed treatments within both large (terrace) and small (mound) patches. Predatory spider treatment responses were similar to Ischnodemus responses, suggesting a trophic relationship between those two arthropod groups. Alternatively, spiders may have been directly affected by the loss of shelter in the disturbed plots. Prokelisia (Homoptera: Delphacidae), which are generally more mobile than Ischnodemus, were not affected by disturbance treatment or by patch size, suggesting the potential for rapid recolonization following disturbance. Larval stem borers decreased by an order of magnitude in disturbed plots, but only in the large patches. In general, the disturbance effects of vegetation removal on arthropod density and community composition were stronger than patch size effects, and there were few interactions between pulsed disturbance and patch size. Rather, emergent marsh arthropod responses to disturbance and habitat area treatments were linked to the dispersal potential and mobility of each individual taxon.

Decoupling of nutrient and grazer impacts on a benthic estuarine diatom assemblage.

Strong interactions between top-down (consumptive) and bottom-up (resource supply) trophic factors occur in many aquatic communities, but these forces can act independently in some microphytobenthic communities. Within benthic estuarine diatom assemblages, the dynamics of these interactions and how they vary with abiotic environmental conditions are not well understood. We conducted a field experiment at two sites with varying habitat characteristics to investigate the interactive effects of grazers and nutrients on benthic estuarine diatoms. We crossed snail (Cerithidea californica) and nutrient (nitrogen and phosphorus) addition treatments in enclosures on a restored tidal sandflat and a reference tidal mudflat in Mugu Lagoon, southern California. We repeated the study in summer 2000 and spring 2001 to assess temporal variation in the interactions. Snails caused a large decrease in diatom relative abundance and biomass (estimated as surface area); nutrients increased diatom abundance but did not alter diatom biomass. Snails and nutrients both reduced average diatom length, although the nutrient effect was weaker and temporally variable, occurring in the reference mudflat in the spring. There were few interactions between snail and nutrient addition treatments, suggesting that links between top-down and bottom-up forces on the diatom community were weak. There were no consistent differences in diatom assemblage characteristics between the two study sites, despite marked differences in sediment grain size and other abiotic characteristics between the sites. The strong diatom response to herbivores and weaker responses to enrichment differed from the previous studies where cyanobacteria increased in response to nutrient enrichment, further dissolving the "black box" perception of microphytobenthic communities.

NUTRIENT EFFECTS ON SEAGRASS EPIPHYTE COMMUNITY STRUCTURE IN FLORIDA BAY(1).

A field experiment was employed in Florida Bay investigating the response of seagrass epiphyte communities to nitrogen (N) and phosphorus (P) additions. While most of the variability in epiphyte community structure was related to uncontrolled temporal and spatial environmental heterogeneity, P additions increased the relative abundance of the red algae-cyanobacterial complex and green algae, with a concomitant decrease in diatoms. When N was added along with P, the observed changes to the diatoms and the red algae-cyanobacterial complex were in the same direction as P-only treatments, but the responses were decreased in magnitude. Within the diatom community, species relative abundances, species richness, and diversity responded weakly to nutrient addition. P additions produced changes in diatom community structure that were limited to summer and were stronger in eastern Florida Bay than in the western bay. These changes were consistent with well-established temporal and spatial patterns of P limitation. Despite the significant change in community structure resulting from P addition, diatom communities from the same site and time, regardless of nutrient treatment, remained more similar to one another than to the diatom communities subject to identical nutrient treatments from different sites and times. Overall, epiphyte communities exhibited responses to P addition that were most evident at the division level.

Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response.

We evaluated the effects of nutrient addition on interactions between the benthic microalgal community and a dominant herbivorous gastropod, Cerithidea californica (California horn snail), on tidal flats in Mugu Lagoon, southern California, USA. We crossed snail and nutrient (N and P) addition treatments in enclosures on two tidal flats varying from 71 to 92% sand content in a temporally replicated experiment (summer 2000, fall 2000, spring 2001). Diatom biomass increased slightly (approximately 30%) in response to nutrient treatments but was not affected by snails. Blooms of cyanobacteria (up to 200%) and purple sulfur bacteria (up to 400%) occurred in response to nutrient enrichment, particularly in the sandier site, but only cyanobacterial biomass decreased in response to snail grazing. Snail mortality was 2-5 times higher in response to nutrient addition, especially in the sandier site, corresponding to a relative increase in cyanobacterial biomass. Nutrient-related snail mortality occurred only in the spring and summer, when the snails were most actively feeding on the microalgal community. Inactive snails in the fall showed no response to nutrient-induced cyanobacterial growths. This study demonstrated strongly negative upward cascading effects of nutrient enrichment through the food chain. The strength of this upward cascade was closely linked to sediment type and microalgal community composition.