Caitlin M. Crain

Interactive and cumulative effects of multiple human stressors in marine systems

Humans impact natural systems in a multitude of ways, yet the cumulative effect of multiple stressors on ecological communities remains largely unknown. Here we synthesized 171 studies that manipulated two or more stressors in marine and coastal systems and found that cumulative effects in individual studies were additive (26%), synergistic (36%), and antagonistic (38%). The overall interaction effect across all studies was synergistic, but interaction type varied by response level (community: antagonistic, population: synergistic), trophic level (autotrophs: antagonistic, heterotrophs: synergistic), and specific stressor pair (seven pairs additive, three pairs each synergistic and antagonistic). Addition of a third stressor changed interaction effects significantly in two-thirds of all cases and doubled the number of synergistic interactions. Given that most studies were performed in laboratories where stressor effects can be carefully isolated, these three-stressor results suggest that synergies may be quite common in nature where more than two stressors almost always coexist. While significant gaps exist in multiple stressor research, our results suggest an immediate need to account for stressor interactions in ecological studies and conservation planning.

Guiding ecological principles for marine spatial planning

The declining health of marine ecosystems around the world is evidence that current piecemeal governance is inadequate to successfully support healthy coastal and ocean ecosystems and sustain human uses of the ocean. One proposed solution to this problem is ecosystem-based marine spatial planning (MSP), which is a process that informs the spatial distribution of activities in the ocean so that existing and emerging uses can be maintained, use conflicts reduced, and ecosystem health and services protected and sustained for future generations. Because a key goal of ecosystem-based MSP is to maintain the delivery of ecosystem services that humans want and need, it must be based on ecological principles that articulate the scientifically recognized attributes of healthy, functioning ecosystems. These principles should be incorporated into a decision-making framework with clearly defined targets for these ecological attributes. This paper identifies ecological principles for MSP based on a synthesis of previously suggested and/or operationalized principles, along with recommendations generated by a group of twenty ecologists and marine scientists with diverse backgrounds and perspectives on MSP. The proposed four main ecological principles to guide MSP--maintaining or restoring: native species diversity, habitat diversity and heterogeneity, key species, and connectivity--and two additional guidelines, the need to account for context and uncertainty, must be explicitly taken into account in the planning process. When applied in concert with social, economic, and governance principles, these ecological principles can inform the designation and siting of ocean uses and the management of activities in the ocean to maintain or restore healthy ecosystems, allow delivery of marine ecosystem services, and ensure sustainable economic and social benefits.

PHYSICAL AND BIOTIC DRIVERS OF PLANT DISTRIBUTION ACROSS ESTUARINE SALINITY GRADIENTS

Although it has long been recognized that marsh plant community composition shifts across estuarine salinity gradients, the mechanisms responsible for this species zonation have never been experimentally examined. In southern New England marshes of the United States, we investigated the relative importance of physical and biotic factors in generating estuarine species distribution patterns. Greenhouse studies revealed that all of the common plants in this system grow better in fresh water than in full-strength salt water. To test the hypothesis that the spatial segregation of these plants is driven by differential tolerance to salt stress and plant competition, we performed transplant experiments with 10 common plants in the system. When freshwater marsh plants were transplanted to salt marshes, they did poorly and generally died with or without neighbors present. In contrast, when saltmarsh plants were transplanted to freshwater marshes, they thrived in the absence of neighbors, growing better than they did in salt marshes, but when neighbors were present, they were strongly suppressed. These results suggest that the spatial segregation of plants across estuarine salinity gradients is driven by competitively superior freshwater marsh plants displacing salt-tolerant plants to physically harsh saltmarsh habitats, whereas freshwater marsh plants are limited from living in salt marshes by physical factors (e.g., high salinities). These results contribute to our understanding of the organization and assembly of tidal marsh plant communities and have important implications for understanding how marsh plant communities will respond to human modification of estuarine hydrology and climate change.

Ecosystem Engineering across Environmental Gradients: Implications for Conservation and Management

Abstract Ecosystem engineers are organisms whose presence or activity alters their physical surroundings or changes the flow of resources, thereby creating or modifying habitats. Because ecosystem engineers affect communities through environmentally mediated interactions, their impact and importance are likely to shift across environmental stress gradients. We hypothesize that in extreme physical environments, ecosystem engineers that ameliorate physical stress are essential for ecosystem function, whereas in physically benign environments where competitor and consumer pressure is typically high, engineers support ecosystem processes by providing competitor- or predator-free space. Important ecosystem engineers alleviate limiting abiotic and biotic stresses, expanding distributional limits for numerous species, and often form the foundation for community development. Because managing important engineers can protect numerous associated species and functions, we advocate using these organisms as conservation targets, harnessing the benefits of ecosystem engineers in various environments. Developing a predictive understanding of engineering across environmental gradients is important for furthering our conceptual understanding of ecosystem structure and function, and could aid in directing limited management resources to critical ecosystem engineers.

The Protective Role of Coastal Marshes: A Systematic Review and Meta-analysis

Background Salt marshes lie between many human communities and the coast and have been presumed to protect these communities from coastal hazards by providing important ecosystem services. However, previous characterizations of these ecosystem services have typically been based on a small number of historical studies, and the consistency and extent to which marshes provide these services has not been investigated. Here, we review the current evidence for the specific processes of wave attenuation, shoreline stabilization and floodwater attenuation to determine if and under what conditions salt marshes offer these coastal protection services. Methodology/Principal Findings We conducted a thorough search and synthesis of the literature with reference to these processes. Seventy-five publications met our selection criteria, and we conducted meta-analyses for publications with sufficient data available for quantitative analysis. We found that combined across all studies (n = 7), salt marsh vegetation had a significant positive effect on wave attenuation as measured by reductions in wave height per unit distance across marsh vegetation. Salt marsh vegetation also had a significant positive effect on shoreline stabilization as measured by accretion, lateral erosion reduction, and marsh surface elevation change (n = 30). Salt marsh characteristics that were positively correlated to both wave attenuation and shoreline stabilization were vegetation density, biomass production, and marsh size. Although we could not find studies quantitatively evaluating floodwater attenuation within salt marshes, there are several studies noting the negative effects of wetland alteration on water quantity regulation within coastal areas. Conclusions/Significance Our results show that salt marshes have value for coastal hazard mitigation and climate change adaptation. Because we do not yet fully understand the magnitude of this value, we propose that decision makers employ natural systems to maximize the benefits and ecosystem services provided by salt marshes and exercise caution when making decisions that erode these services.

Understanding and Managing Human Threats to the Coastal Marine Environment

Coastal marine habitats at the interface of land and sea are subject to threats from human activities in both realms. Researchers have attempted to quantify how these various threats impact different coastal ecosystems, and more recently have focused on understanding the cumulative impact from multiple threats. Here, the top threats to coastal marine ecosystems and recent efforts to understand their relative importance, ecosystem‐level impacts, cumulative effects, and how they can best be managed and mitigated, are briefly reviewed. Results of threat analysis and rankings will differ depending on the conservation target (e.g., vulnerable species, pristine ecosystems, mitigatable threats), scale of interest (local, regional, or global), whether externalities are considered, and the types of management tools available (e.g., marine‐protected areas versus ecosystem‐based management). Considering the cumulative effect of multiple threats has only just begun and depends on spatial analysis to predict overlapping threats and a better understanding of multiple‐stressor effects and interactions. Emerging conservation practices that hold substantial promise for protecting coastal marine systems include multisector approaches, such as ecosystem‐based management (EBM), that account for ecosystem service valuation; comprehensive spatial management, such as ocean zoning; and regulatory mechanisms that encourage or require cross‐sector goal setting and evaluation. In all cases, these efforts require a combination of public and private initiatives for success. The state of our ecological understanding, public awareness, and policy initiatives make the time ripe for advancing coastal marine management and improving our stewardship of coastal and marine ecosystems.

Using expert judgment to estimate marine ecosystem vulnerability in the California Current.

As resource management and conservation efforts move toward multi-sector, ecosystem-based approaches, we need methods for comparing the varying responses of ecosystems to the impacts of human activities in order to prioritize management efforts, allocate limited resources, and understand cumulative effects. Given the number and variety of human activities affecting ecosystems, relatively few empirical studies are adequately comprehensive to inform these decisions. Consequently, management often turns to expert judgment for information. Drawing on methods from decision science, we offer a method for eliciting expert judgment to (1) quantitatively estimate the relative vulnerability of ecosystems to stressors, (2) help prioritize the management of stressors across multiple ecosystems, (3) evaluate how experts give weight to different criteria to characterize vulnerability of ecosystems to anthropogenic stressors, and (4) identify key knowledge gaps. We applied this method to the California Current region in order to evaluate the relative vulnerability of 19 marine ecosystems to 53 stressors associated with human activities, based on surveys from 107 experts. When judging the relative vulnerability of ecosystems to stressors, we found that experts primarily considered two criteria: the ecosystems resistance to the stressor and the number of species or trophic levels affected. Four intertidal ecosystems (mudflat, beach, salt marsh, and rocky intertidal) were judged most vulnerable to the suite of human activities evaluated here. The highest vulnerability rankings for coastal ecosystems were invasive species, ocean acidification, sea temperature change, sea level rise, and habitat alteration from coastal engineering, while offshore ecosystems were assessed to be most vulnerable to ocean acidification, demersal destructive fishing, and shipwrecks. These results provide a quantitative, transparent, and repeatable assessment of relative vulnerability across ecosystems to any ongoing or emerging human activity. Combining these results with data on the spatial distribution and intensity of human activities provides a systematic foundation for ecosystem-based management.

THE COMMUNITY STRUCTURE OF WESTERN ATLANTIC PATAGONIAN ROCKY SHORES

We examined the structure of rocky intertidal communities on the central Patagonian coast of Argentina. Extensive beds of the mussel Perumytilus purpuratus cover wave-exposed headlands from the low to extreme high intertidal (>95%), and a diverse assemblage of diminutive mobile invertebrates including limpets, starfish, and crabs live exclusively in the mussel bed matrix to avoid physical stress. On nearby wave-protected rocky shores, the high intertidal habitat is dominated by bare space (>85%) with mussels restricted to tide pools and crevices. Mussel beds cover the middle intertidal, while the low intertidal habitat is dominated by the erect coralline alga Corallina officanalis. These patterns are driven overwhelmingly by variation in extreme physical conditions. Desiccation stress generated by the dry southern trade winds is harsher than in any previously studied rocky intertidal system, including the Gulf of Panama, by >30% and is more severe on wave-protected than wave-exposed shores. Transplant experiments suggest that on wave-protected shores desiccation stress limits the upper distribution of mussels in the high intertidal and Corallina in the mid-intertidal, but at low intertidal elevations Corallina outcompetes mussels, restricting mussel distribution to mid-intertidal elevations. Transplant experiments also demonstrated that the coralline alga is precluded from wave-exposed shores by wave stress. Recovery from disturbance is unusually slow, ostensibly due to extreme physical stress. Consumer pressure is weak, with no common predaceous crabs or snails, and grazing by limpets showed limited control of community development, mostly by regulating ephemeral algae. Patagonian rocky shore communities are exposed to unusually harsh physical conditions and consequently are more strongly organized by physical stress than previously studied rocky intertidal communities.

COMMUNITY IMPACTS OF A TUSSOCK SEDGE: IS ECOSYSTEM ENGINEERING IMPORTANT IN BENIGN HABITATS?

Ecosystem engineers impact other organisms through environmentally mediated indirect interactions, but the potential for the mechanisms and importance of engineering to vary predictably across environmental gradients has not been investigated. Previously, we investigated how hummock formation by Triglochin maritimum in physically stressful salt marsh pannes influences the plant community that grows only on hummock tops and found that species diversity was dependent on indirect positive effects of T. maritimum engineering. Here we examined how Carex stricta, the tussock sedge, drives superficially similar spatial patterning of plants in relatively benign tidal freshwater marshes at the opposite extreme of an estuarine salinity gradient. In C. stricta marshes, the entire vegetative community is located almost exclusively on top of tussocks while inter-tussock spaces are bare mud buried in C. stricta wrack. We manipulated tussock height, belowground substrate, and aboveground competition for light to investigate the mechanisms by which C. stricta influences the wetland plant community. We also conducted wrack-removal experiments and phytometer assays to examine the importance of wrack deposition in this community and to investigate the spatial distribution of herbivore pressure, respectively. Transplants of four common species performed well in all treatments, except natural inter-tussock spaces buried in wrack. Removal of wrack from inter-tussock spaces enabled substantial seedling emergence and vegetative cover within one growing season. C. stricta therefore drives plant distribution primarily through indirect negative impacts of wrack accumulation in inter-tussock spaces. Once tussocks are established, plants obtain a secondary benefit when growing on tussocks, as the inter-tussock spaces become runways for small mammalian herbivores that concentrate feeding in low protected areas. These results differ dramatically from nearby salt marshes where T. maritimum facilitates community diversity by alleviating physical stresses. The mechanisms and outcomes of hummock-forming engineers may thus vary predictably across estuarine salinity gradients where hummock formation has facilitative and important impacts in physically stressful environments, but negative and less essential impacts in physically benign environments.

Eutrophication and Consumer Control of New England Salt Marsh Primary Productivity

Although primary productivity in salt marshes is thought to be controlled by physical forces, recent evidence suggests that human disturbances can drive a switch to consumer control in these ecologically valuable ecosystems. We tested the hypothesis that nitrogen enrichment can trigger consumer control in salt marshes in Narragansett Bay, Rhode Island, with (1) a field experiment in which we manipulated nutrient availability (with nutrient additions) and insect herbivory (with insecticide application), (2) a survey of 20 salt marshes that examined the relationship between marsh nutrient status and herbivore pressure, and (3) insect herbivore removal at high and low nutrient input sites to directly test the hypothesis that nutrient enrichment is increasing insect herbivory in these marshes. Experimental nitrogen eutrophication initially increased plant productivity but eventually led to reduced plant biomass due to insect herbivory, and our surveys revealed that marsh nitrogen supply was a good predictor of herbivore damage to plants. Insects had minimal impacts on primary productivity in pristine marshes, but suppressed primary productivity in eutrophic salt marshes by 50-75%. Thus, eutrophication is currently triggering consumer suppression of primary productivity in New England salt marshes and may ultimately jeopardize the ecological and societal services these systems provide.