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.

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.

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.

Mangroves give cause for conservation optimism, for now.

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

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.

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.

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.

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.

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.

Mangrove dieback during fluctuating sea levels.

Recent evidence indicates that climate change and intensification of the El Niño Southern Oscillation (ENSO) has increased variation in sea level. Although widespread impacts on intertidal ecosystems are anticipated to arise from the sea level seesaw associated with climate change, none have yet been demonstrated. Intertidal ecosystems, including mangrove forests are among those ecosystems that are highly vulnerable to sea level rise, but they may also be vulnerable to sea level variability and extreme low sea level events. During 16 years of monitoring of a mangrove forest in Mangrove Bay in north Western Australia, we documented two forest dieback events, the most recent one being coincident with the large-scale dieback of mangroves in the Gulf of Carpentaria in northern Australia. Diebacks in Mangrove Bay were coincident with periods of very low sea level, which were associated with increased soil salinization of 20-30% above pre-event levels, leading to canopy loss, reduced Normalized Difference Vegetation Index (NDVI) and reduced recruitment. Our study indicates that an intensification of ENSO will have negative effects on some mangrove forests in parts of the Indo-Pacific that will exacerbate other pressures.

Precocious reproduction increases at the leading edge of a mangrove range expansion.

Climate change-driven shifts in species ranges are ongoing and expected to increase. However, life-history traits may interact with climate to influence species ranges, potentially accelerating or slowing range shifts in response to climate change. Tropical mangroves have expanded their ranges poleward in the last three decades. Here, we report on a shift at the range edge in life-history traits related to reproduction and dispersal. With a common garden experiment and field observations, we show that Rhizophora mangle individuals from northern populations reproduce at a younger age than those from southern populations. In a common garden at the northern range limit, 38% of individuals from the northernmost population were reproductive by age 2, but less than 10% of individuals from the southernmost population were reproductive by the same age, with intermediate amounts of reproduction from intermediate latitudes. Field observations show a similar pattern of younger reproductive individuals toward the northern range limit. We also demonstrate a shift toward larger propagule size in populations at the leading range edge, which may aid seedling growth. The substantial increase in precocious reproduction at the leading edge of the R. mangle range could accelerate population growth and hasten the expansion of mangroves into salt marshes.

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.

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.

Effects of nutrient enrichment on mangrove leaf litter decomposition.

Nutrient enrichment of mangroves, a common phenomenon along densely populated coastlines, may negatively affect mangrove ecosystems by modifying internal carbon and nutrient cycling. The decomposition of litter exerts a strong influence on these processes and is potentially modified by eutrophication. This study describes effects of N and P enrichment on litter decomposition rate and mineralisation/immobilisation patterns. By making use of reciprocal litter transplantation experiments among fertiliser treatments, it was tested if nutrient addition primarily acts on the primary producers (i.e. changes in litter quantity and quality) or on the microbial decomposers (i.e. changes in nutrient limitation for decomposition). Measurements were done in two mangrove forests where primary production was either limited by N or by P, which had been subject to at least 5 years of experimental N and P fertilisation. Results of this study indicated that decomposers were always N-limited regardless of the limitation of the primary producers. This leads to a differential nutrient limitation between decomposers and primary producers in sites where mangrove production was P-limited. In these sites, fertilisation with P caused litter quality to change, resulting in a higher decomposition rate. This study shows that direct effects of fertilisation on decomposition through an effect on decomposer nutrient availability might be non-significant, while the indirect effects through modifying litter quality might be quite substantial in mangroves. Our results show no indication that eutrophication increases decomposition without stimulating primary production. Therefore we do not expect a decline in carbon sequestration as a result of eutrophication of mangrove 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.