Jennifer L. Bowen

Mangrove Forests: One of the World's Threatened Major Tropical Environments

he mass media and scientific press have widely reported losses of tropical environments, such as fellingof rain forests and bleaching of coral reefs.This well-meritedattention has created a worldwide constituency that supportsconservation and restoration efforts in both of these threat-ened ecosystems. The remarkable degree of public aware-ness and support has been manifested in benefit rock concertsat Carnegie Hall and in the designation of ice cream flavorsafter rain forest products. Mangrove forests are another im-portant tropical environment,but these have received muchless publicity.Concern about the magnitude of losses of man-grove forests has been voiced mainly in the specialized liter-ature (Saenger et al. 1983, Spalding et al. 1997).Mangrove trees grow ubiquitously as a relatively narrowfringe between land and sea, between latitudes 25°N and30°S.They form forests of salt-tolerant species,with complexfood webs and ecosystem dynamics (Macnae 1968,Lugo andSnedaker 1974, Tomlinson 1986).Destruction of mangrove forests is occurring globally.Global changes such as an increased sea level may affect man-groves (Ellison 1993,Field 1995),although accretion rates inmangrove forests may be large enough to compensate for thepresent-day rise in sea level (Field 1995).More important,itis human alterations created by conversion of mangroves tomariculture,agriculture,and urbanization,as well as forestryuses and the effects of warfare, that have led to the remark-able recent losses of mangrove habitats (Saenger et al. 1983,Fortes 1988, Marshall 1994, Primavera 1995, Twilley 1998).New data on the magnitude of mangrove area and changesin it have become more readily available, especially with theadvent of satellite imagery and the Internet. Moreover, in-formation about the function of mangrove swamps, theirimportance in the sustainability of the coastal zone, and theeffects of human uses of mangrove forests is growing. Somepublished regional assessments have viewed anthropogenicthreats to mangrove forests with alarm (Ong 1982,Fortes 1988,Ellison and Farnsworth 1996),but reviews at the global scaleare dated (Linden and Jernelov 1980, Saenger et al. 1983).We collated and revised published information to reviewthe status of mangrove swamps worldwide.To assess the sta-tus of this major coastal environment, we compiled and ex-amined available data to quantify the extent of mangroveforest areas in different parts of the world,the losses of man-grove forest area recorded during recent decades, and therelative contributions by various human activities to theselosses.We first assessed current mangrove forest area in tropicalcountries of the world.It is difficult to judge the quality of thesedata in the published literature, because in many cases themethods used to obtain them were insufficiently described andthe associated uncertainty was not indicated. Much infor-mation based on satellite imagery is summarized in the

SUSCEPTIBILITY OF SALT MARSHES TO NUTRIENT ENRICHMENT AND PREDATOR REMOVAL

Salt marsh ecosystems have been considered not susceptible to nitrogen overloading because early studies suggested that salt marshes adsorbed excess nutrients in plant growth. However, the possible effect of nutrient loading on species composition, and the combined effects of nutrients and altered species composition on structure and function, was largely ignored. Failure to understand interactions between nutrient loading and species composition may lead to severe underestimates of the impacts of stresses. We altered whole salt marsh ecosystems (;60 000 m 2 /treatment) by addition of nutrients in flooding waters and by reduction of a key predatory fish, the mummichog. We added nutrients (N and P; 15-fold increase over ambient conditions) directly to the flooding tide to mimic the way anthropogenic nutrients are delivered to marsh ecosystems. Despite the high concentrations (70 mmol N/L) achieved in the water column, our annual N loadings (15-60 g Nm � 2 � yr � 1 ) were an order of magnitude less than most plot-level fertilization experiments, yet we detected responses at several trophic levels. Preliminary calculations suggest that 30-40% of the added N was removed by the marsh during each tidal cycle. Creek bank Spartina alterniflora and high marsh S. patens production increased, but not stunted high marsh S. alterniflora. Microbial production increased in the fertilized creek bank S. alterniflora habitat where benthic microalgae also increased. We found top-down control of benthic microalgae by killifish, but only under nutrient addition and in the opposite direction (increase) than that predicted by a fish-invertebrate-microalgae trophic cascade. Surprisingly, infauna declined in abundance during the first season of fertilization and with fish removal. Our results demonstrate ecological effects of both nutrient addition and mummichog reduction at the whole-system level, including evidence for synergistic interactions.

Microbial community composition in sediments resists perturbation by nutrient enrichment

Functional redundancy in bacterial communities is expected to allow microbial assemblages to survive perturbation by allowing continuity in function despite compositional changes in communities. Recent evidence suggests, however, that microbial communities change both composition and function as a result of disturbance. We present evidence for a third response: resistance. We examined microbial community response to perturbation caused by nutrient enrichment in salt marsh sediments using deep pyrosequencing of 16S rRNA and functional gene microarrays targeting the nirS gene. Composition of the microbial community, as demonstrated by both genes, was unaffected by significant variations in external nutrient supply in our sampling locations, despite demonstrable and diverse nutrient-induced changes in many aspects of marsh ecology. The lack of response to external forcing demonstrates a remarkable uncoupling between microbial composition and ecosystem-level biogeochemical processes and suggests that sediment microbial communities are able to resist some forms of perturbation.

Assessment of models for estimation of land-derived nitrogen loads to shallow estuaries

The performance of several models used to estimate land-derived N loads to shallow receiving estuaries are compared. Models included in the comparison differed in complexity and approach, and predicted either loads or concentrations in estuary water. In all cases, model predictions were compared to measured loads or concentrations, as appropriate. Measured N loads to 9 estuaries on Cape Cod, MA, were obtained as the product of mean concentrations in groundwater about to seep into estuaries multiplied by the annual recharge of groundwater. Measured annual mean N concentrations in estuaries were obtained by extensive sampling surveys. The validity of this procedure to measure loads was verified by comparison against seepage meter data. Responsiveness of model predictions was generally good: predictions increased significantly as measured values increased in 8 of the 10 models evaluated. Precision of predictions was significant for all models. Three models provided highly accurate predictions; correction terms were calculated that could be applied to predictions from the other models to improve accuracy. Four of the models provided reasonable predictive ability. Simulations were run with somewhat different versions of two of the models; in both cases, the modified versions yielded improved predictions. The more complex models tended to be more responsive and precise, but not necessarily more accurate or predictive. Simpler models are attractive because they demand less information for use, but models with more comprehensive formulations, and emphasis on processes tended to perform better. Different models predicted widely different partitioning of land-derived N loads from wastewater, fertilizers, and atmospheric deposition. This is of concern, because mitigation options would be based on such partitioning of predictions. Choice of model to be used in management decisions or for research purposes therefore is not a trivial decision.

Salt marsh sediment diversity : a test of the variability of the rare biosphere among environmental replicates

Much of the phylogenetic diversity in microbial systems arises from rare taxa that comprise the long tail of taxon rank distribution curves. This vast diversity presents a challenge to testing hypotheses about the effects of perturbations on microbial community composition because variability of rare taxa among environmental replicates may be sufficiently large that it would require a prohibitive degree of sequencing to discern differences between samples. In this study we used pyrosequencing of 16S rRNA tags to examine the diversity and within-site variability of salt marsh sediment bacteria. Our goal was to determine whether pyrosequencing could produce similar patterns in community composition among replicate environmental samples from the same location. We hypothesized that repeated sampling from the same location would produce different snapshots of the rare community due to incomplete sequencing of the taxonomically rich rare biosphere. We demonstrate that the salt marsh sediments we sampled contain a remarkably diverse array of bacterial taxa and, in contrast to our hypothesis, repeated sampling from within the same site produces reliably similar patterns in bacterial community composition, even among rare organisms. These results demonstrate that deep sequencing of 16s tags is well suited to distinguish site-specific similarities and differences among rare taxa and is a valuable tool for hypothesis testing in microbial ecology.

Salt marsh sediment bacteria: their distribution and response to external nutrient inputs

A primary focus among microbial ecologists in recent years has been to understand controls on the distribution of microorganisms in various habitats. Much less attention has been paid to the way that environmental disturbance interacts with processes that regulate bacterial community composition. We determined how human disturbance affected the distribution and community structure of salt marsh sediment bacteria by using denaturing gradient gel electrophoresis of 16S rRNA in five different habitats in each of four salt marshes located in northeastern Massachusetts, USA. Two of the four marsh creeks were experimentally enriched 15 × above background by the addition of nitrogen and phosphorus fertilizers for two or more growing seasons. Our results indicate that extrinsic factors acting at broad scales do not influence the distribution of salt marsh sediment bacteria. Intrinsic factors, controlled by local-scale environmental heterogeneity, do play a role in structuring these sediment microbial communities, although nutrient enrichment did not have a consequential effect on the microbial community in most marsh habitats. Only in one habitat, a region of the marsh creek wall that is heavily colonized by filamentous algae, did we see any effect of fertilization on the microbial community structure. When similar habitats were compared among marshes, there was considerable convergence in the microbial community composition during the growing season. Environmental factors that correlated best with microbial community composition varied with habitat, suggesting that habitat-specific intrinsic forces are primarily responsible for maintaining microbial diversity in salt marsh sediments.

Shifts in Winter Distribution in Birds: Effects of Global Warming and Local Habitat Change

Abstract As global warming intensified toward the end of the 20th century, there was a northward shift in winter ranges of bird species in Cape Cod, Massachusetts, USA. These pole-ward shifts were correlated to local increases in minimum winter temperatures and global temperature anomalies. This evidence, plus other recent results, suggests that during the last two decades global warming has led to massive and widespread biogeographic shifts with potentially major ecological and human consequences. Local habitat changes associated with urban sprawl affected mainly forest birds with more northern winter distributions. In Cape Cod, the effects of warming on bird distributions are more substantial at the start of the 21st century, than those of habitat alteration, but as urban sprawl continues its importance may rival that of global warming.

ELM, An Estuarine Nitrogen Loading Model: Formulation and Verification of Predicted Concentrations of Dissolved Inorganic Nitrogen

ELM is an Estuarine Loading Model that calculates mean annual concentration of dissolved inorganic nitrogen (DIN) available to producers in shallow estuaries by considering how different processes modify pools of nitrogen provided by inputs (streams, groundwater flow, atmospheric deposition, N2 fixation, and regeneration), and losses (burial and denitrification), within components of the estuarine system (bare sediments, seagrass meadows, salt marshes, water column). ELM also considers the effect of flushing rate within an estuary. Its formulation was constrained to minimize demands of data needed to run the model. In spite of simplifications such as the use of loss coefficients instead of functional formulations of processes, and uncertainties in all the terms included in ELM, predictions of mean annual DIN in water were not significantly different than field measurements done in estuaries in Cape Cod, Massachusetts, subject to different rates of nitrogen (N) loading. This verification suggests that, in spite of its simple formulation, ELM captures the functioning of nutrient dynamics within estuaries. ELM may therefore be a reasonable tool for use in basic studies in nutrient dynamics and land/estuary coupling. Because of its simplicity and comprehensiveness in inclusion of components and processes, ELM may also be useful in efforts to manage N loads to estuaries and related management issues.

Nitrogen loads to estuaries: Using loading models to assess the effectiveness of management options to restore estuarine water quality

Nitrogen (N) loading to estuaries has become a major concern for coastal planners. As urban development on coastal watershed continues, estuaries and bays are becoming more eutrophic, and cascading effects are being felt at every trophic level. Managers and stakeholders need to have a suite of effective management tools that can be applied to coastal watersheds to minimize the effects of eutrophication. We applied an N loading model and an estuarine loading model to examine the effectiveness of a suite of potential management options that could be implemented in Waquoit Bay, Cape Cod, Massachusetts. This estuarine system is a case study in which we can explore the relative potential effectiveness of decreasing inputs from wastewater and fertilizer-derived N, diverting nitrogenous runoff from impervious surfaces, altering zoning ordinances, preserving forested tracts of land as well as freshwater and saltwater wetlands, harvesting macroalgae, dredging estuary channels, and exterminating waterfowl. From a combination of simulation results, assessment of the magnitude of loads from different sources, and through different land covers, and the additional consideration of feasibility we identified management options with high, intermediate, and low potential effectiveness. Improvement of septic system performance, use of zoning regulations, preservation of forested tracts and freshwater bodies, and conservation of salt marshes emerged as the most promising avenues to manage N loads in our system. Installation of wastewater treatment plants, controlling fertilizer use, and harvesting macroalgae would potentially have intermediate success. Diversion of runoff from impervious surfaces, dredging, and extermination of waterfowl show little promise at reducing N loads. These conclusions potentially set priorities for decision-makers charged with the management of Waquoit Bay. The same procedures applied to another watershed-estuary system with different land covers and different estuarine features may differ. Evaluation studies like this need to be done for any particular site, since the watershed-estuary coupling and the loads delivered to the receiving estuary could differ. The Waquoit Bay case study provides an example of a protocol that leads to identification of the most promising management options.

Using δ15N to Assess Coupling between Watersheds and Estuaries in Temperate and Tropical Regions

Abstract Hydrological coupling between watersheds and estuaries is an important element in establishing eutrophic conditions in coastal waters. In coupled systems, nutrients derived on land enter estuaries through groundwater flow or stream runoff, resulting in increased rates of primary production. The extent of coupling is determined by precipitation, evapotransporation, and water use practices. We use stable nitrogen isotopes, salinity, and nutrient data to assess coupling in two temperate and two tropical ecosystems. In each region, we selected two estuaries, one pristine and one with considerable agricultural or urban development. In pristine systems freshwater entering estuaries had low nitrogen concentrations and low nitrogen isotopic signatures. In receiving waters of the pristine systems, there were similarly low nutrient concentrations, and the isotopic signatures in the estuary were similar to the signatures of incoming groundwater. In both disturbed sites freshwater on the watershed had high nitrogen concentrations and enriched nitrogen isotopic signatures. In the temperate system, the estuarine water had high nitrate concentrations and nitrogen isotopic signatures that were similar to that of the incoming freshwater, indicating that the watershed and estuary were tightly coupled. In contrast, in the disturbed tropical site the estuary had extremely low nitrogen concentrations, and the isotopic signatures were unrelated to the signatures found in freshwater on the adjoining watershed. These results demonstrate that under sufficiently dry conditions, watersheds and estuaries may be uncoupled.