ALBERT

Description: Author Posting. © The Author(s), 2007. This is the author's version of the work. It is posted here by permission of Ecological Society of America for personal use, not for redistribution. The definitive version was published in Ecological Applications 17, Suppl. (2007): S42–S63, doi:10.1890/06-0452.1.

Description: The sustainability of coastal ecosystems in the face of widespread environmental change is an issue of pressing concern throughout the world (Emeis et al. 2001). Coastal ecosystems form a dynamic interface between terrestrial and oceanic systems and are one of the most productive ecosystems in the world. Coastal systems probably serve more human uses than any other ecosystem and they have always been valued for their rich bounty of fish and shellfish. Coastal areas are also the sites of the nation’s and the world’s most intense commercial activity and population growth; worldwide, approximately 75% of the human population now lives in coastal regions (Emeis et al. 2001). Over the past three decades nutrient enrichment of coastal and estuarine waters has become the premier issue for both scientists and managers (National Research Council 2000). Our understanding of coastal eutrophication has been developed principally through monitoring of estuaries, with a focus on pelagic or subtidal habitats (National Research Council 2000, Cloern 2001). Because estuarine systems are usually nitrogen limited, NO3- is the most common nutrient responsible for cultural nutrient enrichment (Cloern 2001). Increased nitrogen delivery to pelagic habitats of estuaries produces the classic response of ecosystems to stress (altered primary producers and nutrient cycles and loss of secondary producer species and production; Nixon 1995, Rapport and Whitford 1999, Deegan et al. 2002). Salt marsh ecosystems have been thought of as not susceptible to nitrogen over-loading because early studies found added nitrogen increased marsh grass production (primarily Spartina spp., cordgrass) and concluded that salt marshes can adsorb excess nutrients in plants and salt marsh plant-derived organic matter as peat (Verhoeven et al. 2006). Detritus from Spartina is important in food webs (Deegan et al. 2000) and in creating peat that forms the physical structure of the marsh platform (Freidrichs and Perry 2001). However, the accumulation of peat and inputs of sediments and loss of peat through decomposition and sediment through erosion may be altered under high nutrient regimes and threaten the long-term stability of marsh systems. Nitrogen addition may lead to either net gain or loss of the marsh depending on the balance between increased marsh plant production and increased decomposition. Absolute change in marsh surface elevation is determined by marsh plant species composition, production and allocation to above- and belowground biomass, microbial decomposition, sedimentation, erosion and compaction (Friedrichs and Perry 2001). Levine et al. (1998) suggested that competitive dynamics among plants might be affected by nutrient enrichment, potentially altering relative abundance patterns favoring species with less belowground storage and thus lowering rates of peat formation. When combined with the observation that nutrient additions may also stimulate microbial respiration and decomposition (Morris and Bradley 1999), the net effect on the salt marsh under conditions of chronic nitrogen loading is a critical unknown. Although most research treats nutrient enrichment as a stand-alone stress, it never occurs in isolation from other perturbations. The effect of nutrient loading on species composition (both plants and animals) and the resultant structure and function of wetlands has been largely ignored when considering their ability to adsorb nutrients (Verhoeven et al. 2006). Recent studies suggest the response of estuaries to stress may depend on animal species composition (Silliman et al. 2005). Animal species composition may alter the balance between marsh gain and loss as animals may increase or decrease primary production, decomposition or N recycling (Pennings and Bertness 2001). Failure to understand interactions between nutrient loading and change in species composition may lead to underestimating the impacts of these stresses. The 'bottom up or top down' theory originated from the observation that nutrient availability (bottom up)sets the quantity of primary productivity, while other studies have shown that species composition (top down), particularly of top consumers, has a marked and cascading effect on ecosystems, including controlling species composition and nutrient cycling (Matson and Price 1992, Pace et al. 1999). Most examples of trophic cascades are in aquatic ecosystems with fairly simple, algal grazing pelagic food webs (Strong 1992). The rarity of trophic cascades in terrestrial systems has been attributed to the importance of detrital food webs (Polis 1999). Detritus-based aquatic ecosystems, such as salt marshes, bogs, and swamps, have classically been considered bottom-up or physically controlled ecosystems. Recent experiments, however, suggest that salt marshes may exhibit top-down control at several trophic levels (Silliman and Zeiman. 2001, Silliman and Bertness 2002, Quiñones-Rivera and Fleeger 2005). One abundant, ubiquitous predator, a small (〈10 cm total length) killifish (Fundulus heteroclitus, mummichog) has been suggested to control benthic algal through a trophic cascade because they prey on the invertebrates that graze on the benthic algae (Kneib 1997, Sarda et al. 1998). In late summer, killifish are capable of consuming 3-10 times the creek meiofauna production and meiofauna in the absence of predators appear capable of grazing over 60% of the microalgal community per day (Carman et al. 1997). Strong top-down control by grazers is considered a moderating influence on the negative effects of elevated nutrients on algae (Worm et al. 2000). Small-scale nutrient additions and predator community exclusion experiments have demonstrated bottom-up and top-down control of macroinfauna in mudflats associated with salt marsh creeks (Posey et al. 1999, Posey et al. 2002). Together, these observations suggest mummichogs are at the top of a trophic cascade that controls benthic algae (Sarda et al. 1998). Mummichogs are also omnivorous and ingest algae, bulk detritus and the attached microbial community (D’Avanzo and Valiela 1990). As a result, marsh decomposition rates may be limited by top-down controls through trophic pathways or by release from competition with algae for nutrients. Whole-ecosystem experiments have shown that responses to stress are often not predictable from studies of the individual components (Schindler 1998). Developing the information needed to predict the interacting impacts of nutrient loading and species composition change requires experiments with realistic alterations carried out at scales of space and time that include the complexities of real ecosystems. Whole ecosystem manipulation experiments have been used effectively in other ecosystems (Bormann and Likens 1979, Carpenter et al. 1995), but they are rare in coastal research. Experiments in salt marshes have traditionally been less than a few m2. Our understanding of the response of salt marsh plants to nutrient enrichment is from small (〈10 m2), plot-level additions where uniform levels of dry inorganic fertilizer (20 to 〉 1000 g N m-2 y-1) are sprinkled on the marsh surface at low tide. Dry fertilizer additions were usually made every two weeks or monthly and the duration of elevated nutrient levels after these additions was usually not determined. Tidal water is the primary vector for N delivery to coastal marshes, suggesting that dry fertilizer addition to the marsh surface may not be the best basis for determining if Spartina production responds to nutrient enrichment of tidal waters. Similarly, our understanding of top-down controls in salt marshes also relies on small (1 - 4 m2) exclusion experiments that use cages to isolate communities from top consumers. While the design of these cage experiments has improved, there are some remaining drawbacks. For example, it is impossible to selectively exclude single species using cages, and recruitment or size-selective movement into or out of the cages may obscure interpretations. In addition, while these small-scale experiments provide insight into controls on isolated ecosystem processes, they do not allow for interaction among different parts of the ecosystem which may buffer or alter the impacts and are not appropriate for determining the effects of populations of larger more motile animals on whole-ecosystems or the effects of ecosystem changes on populations. For example, interactions may be caused when a motile species alters its distribution among the habitats available to it because of an experimental treatment. Small-scale experiments generally do not allow such events to happen. Complex feedbacks among physical and biological processes can alter accumulation rates and affect marsh elevation relative to sea level rise making extrapolation of small plot level experiments to whole marsh ecosystems problematic. We are conducting an ecosystem-scale, multi-year field experiment including both nutrient and biotic manipulations to coastal salt marsh ecosystems. We are testing, for the first time at the ecosystem level, the hypothesis that nutrient enrichment and species composition change have interactive effects across multiple levels of biological organization and a range of biogeochemical processes. We altered whole salt marsh creek watersheds (~60,000 m2 of saltmarsh) by addition of nutrients (15x ambient) in flooding waters and by a 60% reduction of a key fish species, the mummichog. Small marsh creek watersheds provide an ideal experimental setting because they have the spatial complexity, species composition and processes characteristic of the larger salt marsh ecosystem, which are often hundreds of thousands of m2. Manipulating entire salt marsh creeksheds allowed us to examine effects on large motile animals and the interactive effects of motile species changes on ecosystem processes without cage artifacts. Because our manipulations were done on whole-marsh ecosystems, we are able to evaluate the integrated and interactive effects on all habitats (e.g., water column, tidal creeks and marsh) and on populations. These experiments are similar in many respects to the small watershed experiments carried out in forested catchments. Our nutrient enrichment is novel compared to past studies in two important ways. We added nutrients (N and P) directly to the flooding tidal creek waters to mimic the way in which anthropogenic nutrients reach marsh ecosystems. All previous experimental salt marsh nutrient enrichment studies used a dose-response design with spatially uniform dry fertilizer loading on small plots (〈10 m2). Nutrients carried in water will interact and reach parts of the ecosystem differently than dry fertilizer. Our enrichment method also creates a spatial gradient of nutrient loading across the landscape that is proportional to the frequency and depth of inundation in the marsh. Spatial gradients in loading within an ecosystem are typical in real world situations in many terrestrial and aquatic ecosystems. Because of our enrichment method, at any location in the ecosystem, nutrient load will be a function of the nutrient concentration in the water, the frequency and depth of tidal flooding and the reduction of nutrients from the flooding waters by other parts of the ecosystem. Uniform loading misses important aspects of the spatial complexity of ecosystem exposure and response. This work is organized around two questions that are central to understanding the long-term fate of coastal marshes: 1. Does chronic nutrient enrichment via flooding water increase primary production more than it stimulates microbial decomposition? 2. Do top-down controls change the response of the salt marsh ecosystem to nutrient enrichment? Here we present findings on the first 2 years of these experiments including 1) water chemistry, 2) standing stocks and species composition of benthic microalgae, 3) microbial production, 4) species composition and ecophysiology of macrophytes, 5) invertebrates, and 6) nekton. Because even highly eutrophic waters result in nutrient loading that is an order of magnitude less than most plot level experiments, we expected little stimulation of salt marsh vascular plant growth. However, moderate levels of nutrient enrichment in the water column were expected to increase benthic algal biomass and to stimulate bacterial activity and detrital decomposition throughout the ecosystem because of direct uptake of nitrogen from the water column and availability of more high quality organic matter from increased algal production. We predicted nutrient enrichment would increase invertebrate production because of an increase of high quality microalgal and microbial production at the base of the food web. Finally, we predicted that fish reduction would reduce predation on benthic invertebrates resulting in increased abundance of benthic invertebrates that would graze down the benthic algae.

Description: The National Science Foundation (Grant DEB 0213767, OCE 9726921, and OCE 0423565) supported this work. Additional funding was provided by the National Science Foundation postdoctoral fellowship in Microbial Biology (DBI-0400819), the NOAA Coastal Intern grant (NA04NOS4780182), the Office of Environmental Education of Louisiana, Middlebury College and Connecticut College.

Description: Author Posting. © The Author(s), 2007. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Journal of Experimental Marine Biology and Ecology 357 (2008): 20-34, doi:10.1016/j.jembe.2007.12.003.

Description: Responses of infaunal saltmarsh benthic invertebrates to whole-ecosystem fertilization and predator removal were quantified in Plum Island Estuary, Massachusetts, USA. Throughout a growing season, we enriched an experimental creek on each flooding tide to 70 mM NO3 - and 4 mM PO4 -3 (a 10 x increase in loading above background), and we reduced Fundulus heteroclitus density by 60% in a branch of the fertilized and a reference creek. Macroinfauna and meiofauna were sampled in creek (mudflat and creek wall), marsh edge (tall form Spartina alterniflora) and marsh platform (Spartina patens and stunted S. alterniflora) habitats before and after treatments were begun; responses were tested with BACI-design statistics. Treatment effects were most common in the mid-range of the inundation gradient. Most fertilization effects were on creek wall where ostracod abundance increased, indices of copepod reproduction increased and copepod and annelid communities were altered. These taxa may use epiphytes (that respond rapidly to fertilization) of filamentous algae as a food source. Killifish reduction effects on meiobenthic copepod abundance were detected at the marsh edge and suggest predator limitation. Fish reduction effects on annelids did not suggest top-down regulation in any habitat; however, fish reduction may have stimulated an increased predation rate on annelids by grass shrimp. Interactions between fertilization and fish reduction occurred under S. patens canopy where indirect predator reduction effects on annelids were indicated. No effects were observed in mudflat or stunted S. alterniflora habitats. Although the responses of infauna to fertilization and predator removal were largely independent and of similar mild intensity, our data suggests that the effects of ecological stressors vary across the marsh landscape.

Description: This research was supported by the National Science Foundation under Grants No. 0213767 and 9726921.

Description: Author Posting. © The Author(s), 2013. This is the author's version of the work. It is posted here by permission of Inter-Research for personal use, not for redistribution. The definitive version was published in Marine Ecology Progress Series 474 (2013): 27-41, doi:10.3354/meps10090.

Description: We examined the responses of biota at or near the base of the benthic food web to nutrient enrichment in salt marsh mudflats in Plum Island estuary (Massachusetts, USA). To simulate eutrophication, nitrate and phosphate loading rates were increased 10- to 15-fold in creeks fertilized for 2 mo (i.e. short-term enrichment) or 6 yr (chronic enrichment). We found that benthic invertebrate community structure was not altered by nutrient enrichment, although the abundance of epifaunal, but not infaunal, grazers increased. Short-term enrichment had no effect on the food web, but significant changes were detected with chronic enrichment. Grazing experiments with 15N-enriched bacteria and 13C-enriched benthic algae revealed higher per capita ingestion rates of benthic microalgae by nematodes, copepods and hydrobiid snails in the creek with chronic nutrient enrichment where isotope composition also indicated that algae increased in dietary importance. The fraction of bacterial biomass grazed was not affected by nutrient enrichment; however, the fraction of benthic algal biomass grazed increased by 235% with chronic enrichment. This higher grazing pressure was partly the result of dietary changes (increases in per capita feeding rate or a change in selection) but was mostly due to an increased abundance of the grazing consumer with the highest biomass, the snail Nassarius obsoletus. This increased top-down control partially masked the bottom-up effects of nutrient enrichment on algal biomass and helps explain the slow and inconsistent response of microalgal biomass to chronic nutrient enrichment previously observed in this estuary. Our research shows that eutrophication may subtly affect benthic food webs before large, sustained increases in algal biomass are observed.

Description: Pierre-Yves Pascal conducted this research while being supported by a 563 postdoctoral fellowship funded by the Department of Energy Office of Biological and 564 Environmental Research Award DE-FG02-05ER64070 and the Louisiana State University 565 College of Science. This material is based upon work supported by the National Science 566 Foundation under Grant Nos. 0213767 and 9726921.

Description: Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Koninklijke Brill for personal use, not for redistribution. The definitive version was published in Journal of Crustacean Biology 34 (2014): 671-673, doi:10.1163/1937240X-00002268.

Description: A northern range extension is presented here for the marsh fiddler crab Uca pugnax. In summer 2014, adult crabs were found as far north as Hampton, New Hampshire (42.924428, -70.820517), which is 80 km north of its previously established northern limit determined in 2003. Thus, the mean annual northern movement of U. pugnax is currently 7.2 km y-1. I hypothesize that crabs recruited to the most northern sites during 2012 or 2013 when ocean temperatures were up to 1.3 C higher than the average of the previous decade. In a scenario of continued warming oceans associated with climate change, the range of U. pugnax is thus predicted to continue to extend northward. Given that fiddler crabs are ecosystem engineers affecting coastal wetland productivity, biogeochemistry and sediment structure, the introduction of this species into northern salt marshes may have consequences for marsh structure and function.

Description: This work was funded by NSF 1354494 and 1238212.

Description: Author Posting. © The Author(s), 2014. This is the author's version of the work. It is posted here by permission of Koninklijke Brill for personal use, not for redistribution. The definitive version was published in Journal of Crustacean Biology 35 (2015): 105-110, doi:10.1163/1937240X-00002293.

Description: Worldwide, climate-change is shifting species distributions poleward. Here I present recent (2012-2014) observations of the blue crab, Callinectes sapidus, in the Gulf of Maine (GoM), north of its historical range of Cape Cod, Massachusetts. To test the hypothesis of a climate-driven range expansion, I examined near-surface ocean temperatures. On average, ocean temperatures in the GoM in summer 2012 and 2013 were up to 1.3°C higher than the average of the previous decade, suggesting that warmer waters may have promoted the recruitment of C. sapidus to the GoM. Previous ephemeral populations of C. sapidus in the Gulf of Maine have been reported since the 1860's. Recent observations and continued warming in the northwest Atlantic may signal a permanent poleward expansion of C. sapidus into the GoM. If so, then a key goal for ecologists and managers will be to understand the effect of C. sapidus on GoM food-webs and fisheries.

Description: This work was funded by NSF Grants No. 1354494 and 1238212. Additional support from the Northeast Climate Science Center, Grant No. DOI G12AC00001.

Description: © The Author(s), 2015. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Ecosphere 6, no. 12 (2015): 1-14, doi:10.1890/ES15-00317.1.

Description: A major challenge in global change ecology is to predict the trajectory and magnitude of community change in response to global change drivers (GCDs). Here, we present a new framework that not only increases the predictive power of individual studies, but also allows for synthesis across GCD studies and ecosystems. First, we suggest that by quantifying community dissimilarity of replicates both among and within treatments, we can infer both the magnitude and predictability of community change, respectively. Second, we demonstrate the utility of integrating rank abundance curves with measures of community dissimilarity to understand the species-level dynamics driving community changes and propose a series of testable hypotheses linking changes in rank abundance curves with shifts in community dissimilarity. Finally, we review six case studies that demonstrate how our new conceptual framework can be applied. Overall, we present a new framework for holistically predicting community responses to GCDs that has broad applicability in this era of unprecedented global change and novel environmental conditions.

Description: We thank LTER Network Office for funding our working group and the National Socio-Environmental Synthesis Center for additional funding.

Description: Author Posting. © Ecological Society of America, 2016. This article is posted here by permission of Ecological Society of America for personal use, not for redistribution. The definitive version was published in Ecological Applications 26 (2016): 2647–2659, doi:10.1002/eap.1402.

Description: In saltmarsh plant communities, bottom-up pressure from nutrient enrichment is predicted to increase productivity, alter community structure, decrease biodiversity, and alter ecosystem functioning. Previous work supporting these predictions has been based largely on short-term, plot-level (e.g., 1–300 m2) studies, which may miss landscape-level phenomena that drive ecosystem-level responses. We implemented an ecosystem-scale, nine-year nutrient experiment to examine how saltmarsh plants respond to simulated conditions of coastal eutrophication. Our study differed from previous saltmarsh enrichment studies in that we applied realistic concentrations of nitrate (70–100 μM NO3−), the most common form of coastal nutrient enrichment, via tidal water at the ecosystem scale (~60,000 m2 creeksheds). Our enrichments added a total of 1,700 kg N·creek−1·yr−1, which increased N loading 10-fold vs. reference creeks (low-marsh, 171 g N·m−2·yr−1; high-marsh, 19 g N·m−2·yr−1). Nutrients increased the shoot mass and height of low marsh, tall Spartina alterniflora; however, declines in stem density resulted in no consistent increase in aboveground biomass. High-marsh plants S. patens and stunted S. alterniflora did not respond consistently to enrichment. Nutrient enrichment did not shift community structure, contrary to the prediction of nutrient-driven dominance of S. alterniflora and Distichlis spicata over S. patens. Our mild responses may differ from the results of previous studies for a number of reasons. First, the limited response of the high marsh may be explained by loading rates orders of magnitude lower than previous work. Low loading rates in the high marsh reflect infrequent inundation, arguing that inundation patterns must be considered when predicting responses to estuarine eutrophication. Additionally, we applied nitrate instead of the typically used ammonium, which is energetically favored over nitrate for plant uptake. Thus, the form of nitrogen enrichment used, not just N-load, may be important in predicting plant responses. Overall, our results suggest that when coastal eutrophication is dominated by nitrate and delivered via flooding tidal water, aboveground saltmarsh plant responses may be limited despite moderate-to-high water-column N concentrations. Furthermore, we argue that the methodological limitations of nutrient studies must be considered when using results to inform management decisions about wetlands.

Description: National Science Foundation Grant Numbers: DEB 0816963, DEB 0213767, DEB 1354494, OCE 0923689, OCE 0423565, OCE 0924287, OCE 1238212, OCE 1354124; Northeast Climate Science Center Grant Grant Number: DOI G12AC00001; Connecticut College through the Jean C. Tempel Professorship in Botany

Description: Author Posting. © The Author(s), 2010. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Deep Sea Research Part I: Oceanographic Research Papers 57 (2010): 696-707, doi:10.1016/j.dsr.2010.03.003.

Description: One proposed approach to ameliorate the effects of global warming is sequestration of the greenhouse gas CO2 in the deep sea. To evaluate the environmental impact of this approach, we exposed the sediment-dwelling fauna at the mouth of the Monterey Submarine Canyon (3262 m) and a site on the nearby continental rise (3607 m) to CO2- rich water. We measured meiobenthic nematode population and community metrics after ~30-day exposures along a distance gradient from the CO2 source and with sediment depth to infer the patterns of mortality. We also compared the nematode response with that of harpacticoid copepods. Nematode abundance, average sediment depth, tail-group composition, and length: width ratio did not vary with distance from the CO2 source. However, quantile regression showed that nematode length and diameter increased in close proximity to the CO2 source in both experiments. Further, the effects of CO2 exposure and sediment depth (nematodes became more slender at one site, but larger at the other, with increasing depth in the sediment) varied with body size. For example, the response of the longest nematodes differed from those of average length. We propose that nematode body length and diameter increases were induced by lethal exposure to CO2-rich water and that nematodes experienced a high rate of mortality in both experiments. In contrast, copepods experienced high mortality rates in only one experiment suggesting that CO2 sequestration effects are taxon specific.

Description: The Department of Energy Office of Biological and Environmental Research supported this research under award numbers DE‐FG02‐05ER64070 and DE‐FG03‐01ER63065 and the U.S. Department of Energy, Fossil Energy Group (award DE‐FC26‐00NT40929). We also appreciate significant support provided by the Monterey Bay Aquarium Research Institute (project 200002).