Thermal acclimation of leaf respiration is consistent in tropical and subtropical populations of two mangrove species.

Populations from different climates often show unique growth responses to temperature, reflecting temperature adaptation. Yet, whether populations from different climates differ in physiological temperature acclimation remains unclear. Here, we test whether populations from differing thermal environments exhibit different growth responses to temperature and differences in temperature acclimation of leaf respiration. We grew tropical and subtropical populations of two mangrove species (Avicennia germinans and Rhizophora mangle) under ambient and experimentally warmed conditions in a common garden at the species' northern range limit. We quantified growth and temperature responses of leaf respiration (R) at seven time points over ~10 months. Warming increased productivity of tropical populations more than subtropical populations, reflecting a higher temperature optimum for growth. In both species, R measured at 25 °C declined as seasonal temperatures increased, demonstrating thermal acclimation. Contrary to our expectations, acclimation of R was consistent across populations and temperature treatments. However, populations differed in adjusting the temperature sensitivity of R (Q10) to seasonal temperatures. Following a freeze event, tropical Avicennia showed greater freeze damage than subtropical Avicennia, while both Rhizophora populations appeared equally susceptible. We found evidence of temperature adaptation at the whole-plant scale but little evidence for population differences in thermal acclimation of leaf physiology. Studies that examine potential costs and benefits of thermal acclimation in an evolutionary context may provide new insights into limits of thermal acclimation.

Climate-driven regime shifts in a mangrove-salt marsh ecotone over the past 250 years.

Climate change is driving the tropicalization of temperate ecosystems by shifting the range edges of numerous species poleward. Over the past few decades, mangroves have rapidly displaced salt marshes near multiple poleward mangrove range limits, including in northeast Florida. It is uncertain whether such mangrove expansions are due to anthropogenic climate change or natural climate variability. We combined historical accounts from books, personal journals, scientific articles, logbooks, photographs, and maps with climate data to show that the current ecotone between mangroves and salt marshes in northeast Florida has shifted between mangrove and salt marsh dominance at least 6 times between the late 1700s and 2017 due to decadal-scale fluctuations in the frequency and intensity of extreme cold events. Model projections of daily minimum temperature from 2000 through 2100 indicate an increase in annual minimum temperature by 0.5 °C/decade. Thus, although recent mangrove range expansion should indeed be placed into a broader historical context of an oscillating system, climate projections suggest that the recent trend may represent a more permanent regime shift due to the effects of climate change.

Is the central-marginal hypothesis a general rule? Evidence from three distributions of an expanding mangrove species, Avicennia germinans (L.) L.

The central-marginal hypothesis (CMH) posits that range margins exhibit less genetic diversity and greater inter-population genetic differentiation compared to range cores. CMH predictions are based on long-held "abundant-centre" assumptions of a decline in ecological conditions and abundances towards range margins. Although much empirical research has confirmed CMH, exceptions remain almost as common. We contend that mangroves provide a model system to test CMH that alleviates common confounding factors and may help clarify this lack of consensus. Here, we document changes in black mangrove (Avicennia germinans) population genetics with 12 nuclear microsatellite loci along three replicate coastlines in the United States (only two of three conform to underlying "abundant-centre" assumptions). We then test an implicit prediction of CMH (reduced genetic diversity may constrain adaptation at range margins) by measuring functional traits of leaves associated with cold tolerance, the climatic factor that controls these mangrove distributional limits. CMH predictions were confirmed only along the coastlines that conform to "abundant-centre" assumptions and, in contrast to theory, range margin A. germinans exhibited functional traits consistent with greater cold tolerance compared to range cores. These findings support previous accounts that CMH may not be a general rule across species and that reduced neutral genetic diversity at range margins may not be a constraint to shifts in functional trait variation along climatic gradients.

Hurricanes overcome migration lag and shape intraspecific genetic variation beyond a poleward mangrove range limit.

Expansion of many tree species lags behind climate change projections. Extreme storms can rapidly overcome this lag, especially for coastal species, but how will storm-driven expansion shape intraspecific genetic variation? Do storms provide recruits only from the nearest sources, or from more distant sources? Answers to these questions have ecological and evolutionary implications, but empirical evidence is absent from the literature. In 2017, Hurricane Irma provided an opportunity to address this knowledge gap at the northern range limit of the neotropical black mangrove (Avicennia germinans) on the Atlantic coast of Florida, USA. We observed massive post-hurricane increases in beach-stranded A. germinans propagules at, and past, this species' present day range margin when compared to a previously surveyed nonhurricane year. Yet, propagule dispersal does not guarantee subsequent establishment and reproductive success (i.e., effective dispersal). We also evaluated prior effective dispersal along this coastline with isolated A. germinans trees identified beyond the most northern established population. We used 12 nuclear microsatellite loci to genotype 896 hurricane-driven drift propagules from nine sites and 10 isolated trees from four sites, determined their sources of origin, and estimated dispersal distances. Almost all drift propagules and all isolated trees came from the nearest sources. This research suggests that hurricanes are a prerequisite for poleward range expansion of a coastal tree species and that storms can shape the expanding gene pool by providing almost exclusively range-margin genotypes. These insights and empirical estimates of hurricane-driven dispersal distances should improve our ability to forecast distributional shifts of coastal species.

Mangrove microclimates alter seedling dynamics at the range edge.

Recent climate warming has led to asynchronous species migrations, with major consequences for ecosystems worldwide. In woody communities, localized microclimates have the potential to create feedback mechanisms that can alter the rate of species range shifts attributed to macroclimate drivers alone. Mangrove encroachment into saltmarsh in many areas is driven by a reduction in freeze events, and this encroachment can further modify local climate, but the subsequent impacts on mangrove seedling dynamics are unknown. We monitored microclimate conditions beneath mangrove canopies and adjacent open saltmarsh at a freeze-sensitive mangrove-saltmarsh ecotone and assessed survival of experimentally transplanted mangrove seedlings. Mangrove canopies buffered night time cooling during the winter, leading to interspecific differences in freeze damage on mangrove seedlings. However, mangrove canopies also altered biotic interactions. Herbivore damage was higher under canopies, leading to greater mangrove seedling mortality beneath canopies relative to saltmarsh. While warming-induced expansion of mangroves can lead to positive microclimate feedbacks, simultaneous fluctuations in biotic drivers can also alter seedling dynamics. Thus, climate change can drive divergent feedback mechanisms through both abiotic and biotic channels, highlighting the importance of vegetation-microclimate interactions as important moderators of climate driven range shifts.

Review of the ecosystem service implications of mangrove encroachment into salt marshes.

Salt marsh and mangrove have been recognized as being among the most valuable ecosystem types globally in terms of their supply of ecosystem services and support for human livelihoods. These coastal ecosystems are also susceptible to the impacts of climate change and rising sea levels, with evidence of global shifts in the distribution of mangroves, including encroachment into salt marshes. The encroachment of woody mangrove shrubs and trees into herbaceous salt marshes may represent a substantial change in ecosystem structure, although resulting impacts on ecosystem functions and service provisions are largely unknown. In this review, we assess changes in ecosystem services associated with mangrove encroachment. While there is quantitative evidence to suggest that mangrove encroachment may enhance carbon storage and the capacity of a wetland to increase surface elevation in response to sea-level rise, for most services there has been no direct assessment of encroachment impact. On the basis of current understanding of ecosystem structure and function, we theorize that mangrove encroachment may increase nutrient storage and improve storm protection, but cause declines in habitat availability for fauna requiring open vegetation structure (such as migratory birds and foraging bats) as well as the recreational and cultural activities associated with this fauna (e.g., birdwatching and/or hunting). Changes to provisional services such as fisheries productivity and cultural services are likely to be site specific and dependent on the species involved. We discuss the need for explicit experimental testing of the effects of encroachment on ecosystem services in order to address key knowledge gaps, and present an overview of the options available to coastal resource managers during a time of environmental change.

Indirect effects of ecosystem engineering combine with consumer behaviour to determine the spatial distribution of herbivory.

Ecosystem engineers alter environments by creating, modifying or destroying habitats. The indirect impacts of ecosystem engineering on trophic interactions should depend on the combination of the spatial distribution of engineered structures and the foraging behaviour of consumers that use these structures as refuges. In this study, we assessed the indirect effects of ecosystem engineering by a wood-boring beetle in a neotropical mangrove forest system. We identified herbivory patterns in a dwarf mangrove forest on the archipelago of Twin Cays, Belize. Past wood-boring activity impacted more than one-third of trees through the creation of tree holes that are now used, presumably as predation or thermal refuge, by the herbivorous mangrove tree crab Aratus pisonii. The presence of these refuges had a significant impact on plant-animal interactions; herbivory was more than fivefold higher on trees influenced by tree holes relative to those that were completely isolated from these refuges. Additionally, herbivory decreased exponentially with increasing distance from tree holes. We use individual-based simulation modelling to demonstrate that the creation of these herbivory patterns depends on a combination of the use of engineered tree holes for refuge by tree crabs, and the use of two behaviour patterns in this species-site fidelity to a "home tree," and more frequent foraging near their home tree. We demonstrate that understanding the spatial distribution of herbivory in this system depends on combining both the use of ecosystem engineering structures with individual behavioural patterns of herbivores.

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

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.

Nutrient enrichment intensifies hurricane impact in scrub mangrove ecosystems in the Indian River Lagoon, Florida, USA.

Mangroves are an ecological assemblage of trees and shrubs adapted to grow in intertidal environments along tropical, subtropical, and warm temperate coasts. Despite repeated demonstrations of their ecologic and economic value, multiple stressors including nutrient over-enrichment threaten these and other coastal wetlands globally. These ecosystems will be further stressed if tropical storm intensity and frequency increase in response to global climate changes. These stressors will likely interact, but the outcome of that interaction is uncertain. Here, we examined potential interaction between nutrient over-enrichment and the September 2004 hurricanes. Hurricanes Frances and Jeanne made landfall along Florida's Indian River Lagoon and caused extensive damage to a long-term fertilization experiment in a mangrove forest, which previously revealed that productivity was nitrogen (N) limited across the forest and, in particular, that N enrichment dramatically increased growth rates and aboveground biomass of stunted Avicennia germinans trees in the interior scrub zone. During the hurricanes, these trees experienced significant defoliation with three to four times greater reduction in leaf area index (LAI) than control trees. Over the long-term, the +N scrub trees took four years to recover compared to two years for controls. In the adjacent fringe and transition zones, LAI was reduced by > 70%, but with no differences based on zone or fertilization treatment. Despite continued delayed mortality for at least five years after the storms, LAI in the fringe and transition returned to pre-hurricane conditions in two years. Thus, nutrient over-enrichment of the coastal zone will increase the productivity of scrub mangroves, which dominate much of the mangrove landscape in Florida and the Caribbean; however, that benefit is offset by a decrease in their resistance and resilience to hurricane damage that has the potential to destabilize the system.

Integrating physiological threshold experiments with climate modeling to project mangrove species' range expansion.

Predictions of climate-related shifts in species ranges have largely been based on correlative models. Due to limitations of these models, there is a need for more integration of experimental approaches when studying impacts of climate change on species distributions. Here, we used controlled experiments to identify physiological thresholds that control poleward range limits of three species of mangroves found in North America. We found that all three species exhibited a threshold response to extreme cold, but freeze tolerance thresholds varied among species. From these experiments, we developed a climate metric, freeze degree days (FDD), which incorporates both the intensity and the frequency of freezes. When included in distribution models, FDD accurately predicted mangrove presence/absence. Using 28 years of satellite imagery, we linked FDD to observed changes in mangrove abundance in Florida, further exemplifying the importance of extreme cold. We then used downscaled climate projections of FDD to project that these range limits will move northward by 2.2-3.2 km yr(-1) over the next 50 years.

Environmental tolerances of rare and common mangroves along light and salinity gradients.

Although mangroves possess a variety of morphological and physiological adaptations for life in a stressful habitat, interspecific differences in survival and growth under different environmental conditions can shape their local and geographic distributions. Soil salinity and light are known to affect mangrove performance, often in an interactive fashion. It has also been hypothesized that mangroves are intrinsically shade intolerant due to the high physiological cost of coping with saline flooded soils. To evaluate the relationship between stress tolerance and species distributions, we compared responses of seedlings of three widespread mangrove species and one narrow endemic mangrove species in a factorial array of light levels and soil salinities in an outdoor laboratory experiment. The more narrowly distributed species was expected to exhibit a lower tolerance of potentially stressful conditions. Two of the widespread species, Avicennia germinans and Lumnitzera racemosa, survived and grew well at low-medium salinity, regardless of light level, but performed poorly at high salinity, particularly under high light. The third widespread species, Rhizophora mangle, responded less to variation in light and salinity. However, at high salinity, its relative growth rate was low at every light level and none of these plants flushed leaves. As predicted, the rare species, Pelliciera rhizophorae, was the most sensitive to environmental stressors, suffering especially high mortality and reduced growth and quantum yield under the combined conditions of high light and medium-high salinity. That it only thrives under shaded conditions represents an important exception to the prevailing belief that halophytes are intrinsically constrained to be shade intolerant.

Belize Blue Carbon: Establishing a national carbon stock estimate for mangrove ecosystems.

Mangrove ecosystems are among the most economically and ecologically valuable marine environments in the world. Mangroves are effective at long-term carbon storage within their sediments and are estimated to hold 12 billion metric tons of carbon worldwide. These ecosystems are therefore vitally important for carbon sequestration and, by extension, climate change mitigation. As part of the Paris Agreement, participating countries agree to provide plans to reduce their carbon emissions, or nationally determined contributions (NDCs). However, despite mangroves being recognized as important nature-based solutions, many countries still lack national data on carbon stocks and must use global or regional averages, which may not be sufficiently accurate. Here, we present the national carbon stock estimate of mangrove ecosystems for the NDC of Belize, acquired through a collaborative approach involving government agencies and NGOs. We conducted a comprehensive sampling of mangroves across the country, including a range of mangrove ecotypes. The mean total ecosystem carbon stock (TECS) for the nation was 444.1 ± 21.0 Mg C ha-1, with 74.4 ± 6.2 Mg C ha-1 in biomass stocks, and 369.7 ± 17.7 Mg C ha-1 in sediment stocks. Combining these data with a recent mapping effort, we provide the first national comprehensive mangrove carbon stock estimate of 25.7 Tg C. The national mean from this study varies from previous global analyses, which can under- or overestimate TECS by as much as 0.6 Tg C and 16.5 Tg C, respectively, depending on the study. These data supported the NDC update of Belize, and can be used to inform the country's mangrove protection and restoration commitments. The collaborative approach of this work should serve as a blueprint for other countries seeking to conserve natural blue carbon sinks as a strategy to achieve their climate targets.

Insectivorous birds reduce herbivory but do not increase mangrove growth across productivity zones.

Top-down effects of predators and bottom-up effects of resources are important drivers of community structure and function in a wide array of ecosystems. Fertilization experiments impose variation in resource availability that can mediate the strength of predator impacts, but the prevalence of such interactions across natural productivity gradients is less clear. We studied the joint impacts of top-down and bottom-up factors in a tropical mangrove forest system, leveraging fine-grained patchiness in resource availability and primary productivity on coastal cays of Belize. We excluded birds from canopies of red mangrove (Rhizophoraceae: Rhizophora mangle) for 13 months in zones of phosphorus-limited, stunted dwarf mangroves, and in adjacent zones of vigorous mangroves that receive detrital subsidies. Birds decreased total arthropod densities by 62%, herbivore densities more than fivefold, and reduced rates of leaf and bud herbivory by 45% and 52%, respectively. Despite similar arthropod densities across both zones of productivity, leaf and bud damage were 2.0 and 4.3 times greater in productive stands. Detrital subsidies strongly impacted a suite of plant traits in productive stands, potentially making leaves more nutritious and vulnerable to damage. Despite consistently strong impacts on herbivory, we did not detect top-down forcing that impacted mangrove growth, which was similar with and without birds. Our results indicated that both top-down and bottom-up forces drive arthropod community dynamics, but attenuation at the plant-herbivore interface weakens top-down control by avian insectivores.

Mangrove growth response to experimental warming is greatest near the range limit in northeast Florida.

Shrubs are invading into grasslands around the world, but we don't yet know how these shrubs will fare in a warmer future. In ecotonal coastal wetland ecosystems, woody mangroves are encroaching into herbaceous salt marshes owing to changes in temperature, precipitation, and sediment dynamics. Increasing mangrove biomass in wetlands often increases carbon storage, which is high in these productive ecosystems, but little is known about how mangrove growth will change in response to warming. To address this knowledge gap, we deployed warming experiments at three coastal wetland sites along a latitudinal gradient in northeast Florida where Avicennia germinans, black mangroves, are encroaching into salt marshes. We achieved air temperature warming (+1.6°C during the day) at all three sites and measured stem elongation, canopy height and area changes, and leaf and node number. After 2 yr of warming, we found that mangrove growth rate in height increased due to warming. Warming increased stem elongation by 130% over unwarmed control plots after 1 yr at the northern site. Mangrove growth in canopy area did not respond to warming. Site differences in growth rate were pronounced, and mangrove growth in both height and area were lowest at the northern site, despite greater impacts of warming at that site. We also found that area-based relative growth rate was five times higher across all treatments than height-based relative growth rate, indicating that mangroves are growing wider rather than taller in these ecotonal environments. Our findings indicate that the growth effect of experimental warming depends on site characteristics and growth parameter measured. We also propose that differential mangrove growth across the three sites may be driven by biotic factors such as the identity of the salt marsh species into which mangroves are encroaching. Our results suggest that, as seen in other ecosystems, wetland plants may respond most strongly to warming at their poleward range edge.

Salinity has little effect on photosynthetic and respiratory responses to seasonal temperature changes in black mangrove (Avicennia germinans) seedlings.

Temperature and salinity are important regulators of mangrove range limits and productivity, but the physiological responses of mangroves to the interactive effects of temperature and salinity remain uncertain. We tested the hypothesis that salinity alters photosynthetic responses to seasonal changes in temperature and vapor pressure deficit (D), as well as thermal acclimation _of leaf respiration in black mangrove (Avicennia germinans). To test this hypothesis, we grew seedlings of A. germinans in an outdoor experiment for ~ 12 months under four treatments spanning 0 to 55 ppt porewater salinity. We repeatedly measured seedling growth and in situ rates of leaf net photosynthesis (Asat) and stomatal conductance to water vapor (gs) at prevailing leaf temperatures, along with estimated rates of Rubisco carboxylation (Vcmax) and electron transport for RuBP regeneration (Jmax), and measured rates of leaf respiration at 25 °C (Rarea25). We developed empirical models describing the seasonal response of leaf gas exchange and photosynthetic capacity to leaf temperature and D, and the response of Rarea25 to changes in mean daily air temperature. We tested the effect of salinity on model parameters. Over time, salinity had weak or inconsistent effects on Asat, gs and Rarea25. Salinity also had little effect on the biochemical parameters of photosynthesis (Vcmax, Jmax) and individual measurements of Asat, gs, Vcmax and Jmax showed a similar response to seasonal changes in temperature and D across all salinity treatments. Individual measurements of Rarea25 showed a similar inverse relationship with mean daily air temperature across all salinity treatments. We conclude that photosynthetic responses to seasonal changes in temperature and D, as well as seasonal temperature acclimation of leaf R, are largely consistent across a range of salinities in A. germinans. These results might simplify predictions of photosynthetic and respiratory responses to temperature in young mangroves.

Nitrogen fertilization enhances water-use efficiency in a saline environment.

Effects of salinity and nutrients on carbon gain in relation to water use were studied in the grey mangrove, Avicennia marina, growing along a natural salinity gradient in south-eastern Australia. Tall trees characterized areas of seawater salinities (fringe zone) and stunted trees dominated landward hypersaline areas (scrub zone). Trees were fertilized with nitrogen (+N) or phosphorus (+P) or unfertilized. There was no significant effect of +P on shoot growth, whereas +N enhanced canopy development, particularly in scrub trees. Scrub trees maintained greater CO(2) assimilation per unit water transpired (water-use efficiency, WUE) and had lower nitrogen-use efficiency (NUE; CO(2) assimilation rate per unit leaf nitrogen) than fringe trees. The CO(2) assimilation rates of +N trees were similar to those in other treatments, but were achieved at lower transpiration rates, stomatal conductance and intercellular CO(2) concentrations. Maintaining comparable assimilation rates at lower stomatal conductance requires greater ribulose 1.5-bisphosphate carboxylase/oxygenase activity, consistent with greater N content per unit leaf area in +N trees. Hence, +N enhanced WUE at the expense of NUE. Instantaneous WUE estimates were supported by less negative foliar delta(13)C values for +N trees and scrub control trees. Thus, nutrient enrichment may alter the structure and function of mangrove forests along salinity gradients.

Nutrition of mangroves.

Mangrove forests dominate the world's 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.

Mangroves give cause for conservation optimism, for now.

Friess et al. discuss the results of conservation efforts for mangrove forests in recent years.

Mangrove recruitment after forest disturbance is facilitated by herbaceous species in the Caribbean.

Plant communities along tropical coastlines are often affected by natural and human disturbances, but little is known about factors influencing recovery. We focused on mangrove forests, which are among the most threatened ecosystems globally, to examine how facilitation by herbaceous vegetation might improve forest restoration after disturbance. We specifically investigated whether recovery of mangrove forests in harsh environments is accelerated by nurse plants and whether the beneficial effects are species-specific. Quantification of standardized effects allowed comparisons across performance parameters and over time for: (1) net effect of each herbaceous species on mangrove survival and growth, (2) effects of pre- and post-establishment factors associated with each herbaceous species, and (3) need for artificial planting to enhance growth or survival of mangrove seedlings. Mangrove recruitment in a clear-cut forest in Belize was accelerated by the presence of Sesuvium portulacastrum (succulent forb) and Distichlis spicata (grass), two coastal species common throughout the Caribbean region. The net effect of herbaceous vegetation was positive, but the magnitude of effects on mangrove survival and growth differed by species. Because of differences in their vegetative structure and other features, species effects on mangroves also varied by mechanism: (1) trapping of dispersing propagules (both species), (2) structural support of the seedling (Distichlis), and/or (3) promotion of survival (Sesuviumn) or growth (Distichlis) through amelioration of soil conditions (temperature, aeration). Artificial planting had a stronger positive effect on mangrove survival than did edaphic conditions, but planting enhanced mangrove growth more in Sesuvium than in Distichlis patches. Our study indicates that beneficial species might be selected based on features that provide multiple positive effects and that species comparisons may be improved using standardized effects. Our findings are not only relevant to the coastal environments found in the Caribbean region, but our assessment methods may be useful for developing site-specific information to restore disturbed mangrove forests worldwide, especially given the large pool of mangrove associates (>45 genera) available for screening.