Winter climate change and coastal wetland foundation species: salt marshes vs. mangrove forests in the southeastern United States

We live in an era of unprecedented ecological change in which ecologists and natural resource managers are increasingly challenged to anticipate and prepare for the ecological effects of future global change. In this study, we investigated the potential effect of winter climate change upon salt marsh and mangrove forest foundation species in the southeastern United States. Our research addresses the following three questions: (1) What is the relationship between winter climate and the presence and abundance of mangrove forests relative to salt marshes; (2) How vulnerable are salt marshes to winter climate change‐induced mangrove forest range expansion; and (3) What is the potential future distribution and relative abundance of mangrove forests under alternative winter climate change scenarios? We developed simple winter climate‐based models to predict mangrove forest distribution and relative abundance using observed winter temperature data (1970–2000) and mangrove forest and salt marsh habitat data. Our results identify winter climate thresholds for salt marsh–mangrove forest interactions and highlight coastal areas in the southeastern United States (e.g., Texas, Louisiana, and parts of Florida) where relatively small changes in the intensity and frequency of extreme winter events could cause relatively dramatic landscape‐scale ecosystem structural and functional change in the form of poleward mangrove forest migration and salt marsh displacement. The ecological implications of these marsh‐to‐mangrove forest conversions are poorly understood, but would likely include changes for associated fish and wildlife populations and for the supply of some ecosystem goods and services.     

Development of six microsatellite loci for black mangrove (Avicennia germinans)

We developed six new microsatellite loci for the black mangrove (Avicennia germinans), an important member of wetland communities worldwide. Loci showed moderate to high polymorphism and a survey of four locations [Puerto Rico (Jobos Bay and Luquillo), Mexico, French Guyana] revealed clear regional (and local) population structure. All populations were genetically distinct and the two continental populations showed much higher diversity than the two insular Puerto Rican locations. These loci complement those recently published by Nettel et al. (2005 ) and promise to be valuable for characterizing local and regional population dynamics in the black mangrove.     

Biotic interactions influence the projected distribution of a specialist mammal under climate change

Aim

To measure the effects of including biotic interactions on climate‐based species distribution models (SDMs) used to predict distribution shifts under climate change. We evaluated the performance of distribution models for an endangered marsupial, the northern bettong (Bettongia tropica), comparing models that used only climate variables with models that also took into account biotic interactions.

Location

North‐east Queensland, Australia.

Methods

We developed separate climate‐based distribution models for the northern bettong, its two main resources and a competitor species. We then constructed models for the northern bettong by including climate suitability estimates for the resources and competitor as additional predictor variables to make climate + resource and climate + resource + competition models. We projected these models onto seven future climate scenarios and compared predictions of northern bettong distribution made by these differently structured models, using a ‘global’ metric, the I similarity statistic, to measure overlap in distribution and a ‘local’ metric to identify where predictions differed significantly.

Results

Inclusion of food resource biotic interactions improved model performance. Over moderate climate changes, up to 3.0 °C of warming, the climate‐only model for the northern bettong gave similar predictions of distribution to the more complex models including interactions, with differences only at the margins of predicted distributions. For climate changes beyond 3.0 °C, model predictions diverged significantly. The interactive model predicted less contraction of distribution than the simpler climate‐only model.

Main conclusions

Distribution models that account for interactions with other species, in particular direct resources, improve model predictions in the present‐day climate. For larger climate changes, shifts in distribution of interacting species cause predictions of interactive models to diverge from climate‐only models. Incorporating interactions with other species in SDMs may be needed for long‐term prediction of changes in distribution of species under climate change, particularly for specialized species strongly dependent on a small number of biotic interactions.     

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.     

Mangrove expansion and salt marsh decline at mangrove poleward limits

Mangroves are species of halophytic intertidal trees and shrubs derived from tropical genera and are likely delimited in latitudinal range by varying sensitivity to cold. There is now sufficient evidence that mangrove species have proliferated at or near their poleward limits on at least five continents over the past half century, at the expense of salt marsh. Avicennia is the most cold‐tolerant genus worldwide, and is the subject of most of the observed changes. Avicennia germinans has extended in range along the USA Atlantic coast and expanded into salt marsh as a consequence of lower frost frequency and intensity in the southern USA. The genus has also expanded into salt marsh at its southern limit in Peru, and on the Pacific coast of Mexico. Mangroves of several species have expanded in extent and replaced salt marsh where protected within mangrove reserves in Guangdong Province, China. In south‐eastern Australia, the expansion of Avicennia marina into salt marshes is now well documented, and Rhizophora stylosa has extended its range southward, while showing strong population growth within estuaries along its southern limits in northern New South Wales. Avicennia marina has extended its range southwards in South Africa. The changes are consistent with the poleward extension of temperature thresholds coincident with sea‐level rise, although the specific mechanism of range extension might be complicated by limitations on dispersal or other factors. The shift from salt marsh to mangrove dominance on subtropical and temperate shorelines has important implications for ecological structure, function, and global change adaptation.     

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.     

Mutualism influences species distribution predictions for a bromeliad‐breeding anuran under climate change

Ecological niche models, or species distribution models, have been widely used to identify potentially suitable areas for species in future climate change scenarios. However, there are inherent errors to these models due to their inability to evaluate species occurrence influenced by non‐climatic factors. With the intuit to improve the modelling predictions for a bromeliad‐breeding treefrog (Phyllodytes melanomystax, Hylidae), we investigate how the climatic suitability of bromeliads influences the distribution model for the treefrog in the context of baseline and 2050 climate change scenarios. We used point occurrence data on the frog and the bromeliad (Vriesea procera, Bromeliaceae) to generate their predicted distributions based on baseline and 2050 climates. Using a consensus of five algorithms, we compared the accuracy of the models and the geographic predictions for the frog generated from two modelling procedures: (i) a climate‐only model for P. melanomystax and V. procera; and (ii) a climate‐biotic model for P. melanomystax, in which the climatic suitability of the bromeliad was jointly considered with the climatic variables. Both modelling approaches generated strong and similar predictive power for P. melanomystax, yet climate‐biotic modelling generated more concise predictions, particularly for the year 2050. Specifically, because the predicted area of the bromeliad overlaps with the predictions for the treefrog in the baseline climate, both modelling approaches produce reasonable similar predicted areas for the anuran. Alternatively, due to the predicted loss of northern climatically suitable areas for the bromeliad by 2050, only the climate‐biotic models provide evidence that northern populations of P. melanomystax will likely be negatively affected by 2050.     

Amphibian breeding phenology trends under climate change: predicting the past to forecast the future

Global climate warming is predicted to hasten the onset of spring breeding by anuran amphibians in seasonal environments. Previous data had indicated that the breeding phenology of a population of Fowler's Toads (Anaxyrus fowleri) at their northern range limit had been progressively later in spring, contrary to generally observed trends in other species. Although these animals are known to respond to environmental temperature and the lunar cycle to commence breeding, the timing of breeding should also be influenced by the onset of overwintering animals’ prior upward movement through the soil column from beneath the frost line as winter becomes spring. I used recorded weather data to identify four factors of temperature, rainfall and snowfall in late winter and early spring that correlated with the toads’ eventual date of emergence aboveground. Estimated dates of spring emergence of the toads calculated using a predictive model based on these factors, as well as the illumination of the moon, were highly correlated with observed dates of emergence over 24 consecutive years. Using the model to estimate of past dates of spring breeding (i.e. retrodiction) indicated that even three decades of data were insufficient to discern any appreciable phenological trend in these toads. However, by employing weather data dating back to 1876, I detected a significant trend over 140 years towards earlier spring emergence by the toads by less than half a day/decade, while, over the same period of time, average annual air temperature and annual precipitation had both increased. Changes in the springtime breeding phenology for late‐breeding species, such as Fowler's Toads, therefore may conform to expectations of earlier breeding under global warming. Improved understanding of the environmental cues that bring organisms out of winter dormancy will enable better interpretation of long‐term phenological trends.     

Contrasting responses to climate change at Himalayan treelines revealed by population demographics of two dominant species

1. Alpine treelines are expected to shift upward due to recent climate change. However, interpretation of changes in montane systems has been problematic because effects of climate change are frequently confounded with those of land use changes. The eastern Himalaya, particularly Langtang National Park, Central Nepal, has been relatively undisturbed for centuries and thus presents an opportunity for studying climate change impacts on alpine treeline uncontaminated by potential confounding factors.
2. We studied two dominant species, Abies spectabilis (AS) and Rhododendron campanulatum (RC), above and below the treeline on two mountains. We constructed 13 transects, each spanning up to 400 m in elevation, in which we recorded height and state (dead or alive) of all trees, as well as slope, aspect, canopy density, and measures of anthropogenic and animal disturbance.
3. All size classes of RC plants had lower mortality above treeline than below it, and young RC plants (<2 m tall) were at higher density above treeline than below. AS shows little evidence of a position change from the historic treeline, with a sudden extreme drop in density above treeline compared to below. Recruitment, as measured by size–class distribution, was greater above treeline than below for both species but AS is confined to ~25 m above treeline whereas RC is luxuriantly growing up to 200 m above treeline.
4. Synthesis. Evidence suggests that the elevational limits of RC have shifted upward both because (a) young plants above treeline benefited from facilitation of recruitment by surrounding vegetation, allowing upward expansion of recruitment, and (b) temperature amelioration to mature plants increased adult survival. We predict that the current pure stand of RC growing above treeline will be colonized by AS that will, in turn, outshade and eventually relegate RC to be a minor component of the community, as is the current situation below the treeline.

     

Contrasting demographic history and gene flow patterns of two mangrove species on either side of the Central American Isthmus

Comparative phylogeography offers a unique opportunity to understand the interplay between past environmental events and life‐history traits on diversification of unrelated but co‐distributed species. Here, we examined the effects of the quaternary climate fluctuations and palaeomarine currents and present‐day marine currents on the extant patterns of genetic diversity in the two most conspicuous mangrove species of the Neotropics. The black (Avicennia germinans, Avicenniaceae) and the red (Rhizophora mangle, Rhizophoraceae) mangroves have similar geographic ranges but are very distantly related and show striking differences on their life‐history traits. We sampled 18 Atlantic and 26 Pacific locations for A. germinans (N = 292) and R. mangle (N = 422). We performed coalescence simulations using microsatellite diversity to test for evidence of population change associated with quaternary climate fluctuations. In addition, we examined whether patterns of genetic variation were consistent with the directions of major marine (historical and present day) currents in the region. Our demographic analysis was grounded within a phylogeographic framework provided by the sequence analysis of two chloroplasts and one flanking microsatellite region in a subsample of individuals. The two mangrove species shared similar biogeographic histories including: (1) strong genetic breaks between Atlantic and Pacific ocean basins associated with the final closure of the Central American Isthmus (CAI), (2) evidence for simultaneous population declines between the mid‐Pleistocene and early Holocene, (3) asymmetric historical migration with higher gene flow from the Atlantic to the Pacific oceans following the direction of the palaeomarine current, and (4) contemporary gene flow between West Africa and South America following the major Atlantic Ocean currents. Despite the remarkable differences in life‐history traits of mangrove species, which should have had a strong influence on seed dispersal capability and, thus, population connectivity, we found that vicariant events, climate fluctuations and marine currents have shaped the distribution of genetic diversity in strikingly similar ways.     

Quantitative analysis of oyster larval proteome provides new insights into the effects of multiple climate change stressors

The metamorphosis of planktonic larvae of the Pacific oyster (Crassostrea gigas) underpins their complex life‐history strategy by switching on the molecular machinery required for sessile life and building calcite shells. Metamorphosis becomes a survival bottleneck, which will be pressured by different anthropogenically induced climate change‐related variables. Therefore, it is important to understand how metamorphosing larvae interact with emerging climate change stressors. To predict how larvae might be affected in a future ocean, we examined changes in the proteome of metamorphosing larvae under multiple stressors: decreased pH (pH 7.4), increased temperature (30 °C), and reduced salinity (15 psu). Quantitative protein expression profiling using iTRAQ‐LC‐MS/MS identified more than 1300 proteins. Decreased pH had a negative effect on metamorphosis by down‐regulating several proteins involved in energy production, metabolism, and protein synthesis. However, warming switched on these down‐regulated pathways at pH 7.4. Under multiple stressors, cell signaling, energy production, growth, and developmental pathways were up‐regulated, although metamorphosis was still reduced. Despite the lack of lethal effects, significant physiological responses to both individual and interacting climate change related stressors were observed at proteome level. The metamorphosing larvae of the C. gigas population in the Yellow Sea appear to have adequate phenotypic plasticity at the proteome level to survive in future coastal oceans, but with developmental and physiological costs.     

Dramatic loss of seagrass habitat under projected climate change in the Mediterranean Sea

Although climate warming is affecting most marine ecosystems, the Mediterranean is showing earlier impacts. Foundation seagrasses are already experiencing a well‐documented regression in the Mediterranean which could be aggravated by climate change. Here, we forecast distributions of two seagrasses and contrast predicted loss with discrete regions identified on the basis of extant genetic diversity. Under the worst‐case scenario, Posidonia oceanica might lose 75% of suitable habitat by 2050 and is at risk of functional extinction by 2100, whereas Cymodocea nodosa would lose only 46.5% in that scenario as losses are compensated with gained and stable areas in the Atlantic. Besides, we predict that erosion of present genetic diversity and vicariant processes can happen, as all Mediterranean genetic regions could decrease considerably in extension in future warming scenarios. The functional extinction of Posidonia oceanica would have important ecological impacts and may also lead to the release of the massive carbon stocks these ecosystems stored over millennia.     

Changes in the range of the medicinal herb Eriocaulon buergerianum Körnicke. (Eriocaulaceae) under climate change

• Eriocaulon buergerianum Körnicke. (Eriocaulaceae) is one of the most common and least expensive herbal medicines for eye disease. This species is facing potential threats from climate change. Insufficient biogeographic knowledge of this plant species can hinder its effective management for long‐term population survival.
• We integrated ecological niche modelling (Biomod2) with 70 records of E. buergerianum and eight environmental variables to estimate changes in distribution over time. A core area Zonation algorithm was introduced to identify conservation priority areas.
• Our results indicate that the range of E. buergerianum will likely decrease in the future: the overall range change on average is ?44.36 ± 21.56% (?3.70% to ?77.73%); values of range loss and range gain are 45.79 ± 20.30% (9.29–78.19%) and 1.43 ± 1.53% (0.18–5.59%), respectively. According to conservation priority analysis, the mandatory reserve (top 5%), negotiable reserve (0.95–0.9) and partial reserve (0.9–0.8) areas are 19,799, 19,799 and 39,597 km², respectively. The areas identified as conservation priority are located in the southeast, especially in northern Taiwan and the Wuyi Mountains.
• Based on these results, we suggest a re‐evaluation of the threatened status of this species, with a potential upgrade to the vulnerable (VU) category. To overcome the adverse conditions faced by populations of E. buergerianum in China, we propose a multi‐faceted conservation strategy involving more complete resource assessment, a monitoring system, medical research focused on revealing medicinal components or substitutes, and a regional development plan that considers both wildlife and socio‐economic issues.