Andrew H. Altieri

Global shifts towards positive species interactions with increasing environmental stress

The study of positive species interactions is a rapidly evolving field in ecology. Despite decades of research, controversy has emerged as to whether positive and negative interactions predictably shift with increasing environmental stress as hypothesised by the stress-gradient hypothesis (SGH). Here, we provide a synthesis of 727 tests of the SGH in plant communities across the globe to examine its generality across a variety of ecological factors. Our results show that plant interactions change with stress through an outright shift to facilitation (survival) or a reduction in competition (growth and reproduction). In a limited number of cases, plant interactions do not respond to stress, but they never shift towards competition with stress. These findings are consistent across stress types, plant growth forms, life histories, origins (invasive vs. native), climates, ecosystems and methodologies, though the magnitude of the shifts towards facilitation with stress is dependent on these factors. We suggest that future studies should employ standardised definitions and protocols to test the SGH, take a multi-factorial approach that considers variables such as plant traits in addition to stress, and apply the SGH to better understand how species and communities will respond to environmental change.

Habitat Cascades: The Conceptual Context and Global Relevance of Facilitation Cascades via Habitat Formation and Modification

The importance of positive interactions is increasingly acknowledged in contemporary ecology. Most research has focused on direct positive effects of one species on another. However, there is recent evidence that indirect positive effects in the form of facilitation cascades can also structure species abundances and biodiversity. Here we conceptualize a specific type of facilitation cascade-the habitat cascade. The habitat cascade is defined as indirect positive effects on focal organisms mediated by successive facilitation in the form of biogenic formation or modification of habitat. Based on a literature review, we demonstrate that habitat cascades are a general phenomenon that enhances species abundance and diversity in forests, salt marshes, seagrass meadows, and seaweed beds. Habitat cascades are characterized by a hierarchy of facilitative interactions in which a basal habitat former (typically a large primary producer, e.g., a tree) creates living space for an intermediate habitat former (e.g., an epiphyte) that in turn creates living space for the focal organisms (e.g., spiders, beetles, and mites). We then present new data on a habitat cascade common to soft-bottom estuaries in which a relatively small invertebrate provides basal habitat for larger intermediate seaweeds that, in turn, generate habitat for focal invertebrates and epiphytes. We propose that indirect positive effects on focal organisms will be strongest when the intermediate habitat former is larger and different in form and function from the basal habitat former. We also discuss how humans create, modify, and destroy habitat cascades via global habitat destruction, climatic change, over-harvesting, pollution, or transfer of invasive species. Finally, we outline future directions for research that will lead to a better understanding of habitat cascades.

Hierarchical Organization via a Facilitation Cascade in Intertidal Cordgrass Bed Communities

It has recently been proposed that many communities are structured by a hierarchy of interactions in which facilitation by foundation species is of primary importance. We conducted the first explicit experimental test of this hypothesis by investigating the organization of positive interactions on New England cobblestone beaches. In this midintertidal community, wave‐generated substrate instability and solar stress largely limit marine organisms to the shelter of cordgrass beds. Cordgrass, which can establish and persist without the aid of other foundation species, facilitates a dense assemblage of inhabitants (e.g., mussels, snails, seaweeds) with roots/rhizomes that stabilize substrate and a dense canopy that baffles waves and provides shade. Within the cordgrass bed community, ribbed mussels further enhance physical conditions and densities of other species (e.g., amphipods, barnacles) by providing crevice space and hard substrate. We conclude that cordgrass bed communities are hierarchically organized: secondary interactions (e.g., facilitation by ribbed mussels) play a key role within an assemblage dependent on primary facilitation by the independently successful foundation species cordgrass. Our results identify emergent indirect positive interactions in the form of facilitation cascades, have broad implications for conservation, and help unify existing models of community organization that were developed without considering the fundamental role of positive interactions.

Facilitation cascade drives positive relationship between native biodiversity and invasion success.

The pervasive impact of invasive species has motivated considerable research to understand how characteristics of invaded communities, such as native species diversity, affect the establishment of invasive species. Efforts to identify general mechanisms that limit invasion success, however, have been frustrated by disagreement between landscape-scale observations that generally find a positive relationship between native diversity and invasibility and smaller-scale experiments that consistently reveal competitive interactions that generate the opposite relationship. Here we experimentally elucidate the mechanism explaining the large-scale positive associations between invasion success and native intertidal diversity revealed in our landscape-scale surveys of New England shorelines. Experimental manipulations revealed this large-scale pattern is driven by a facilitation cascade where ecosystem-engineering species interact nonlinearly to enhance native diversity and invasion success by alleviating thermal stress and substrate instability. Our findings reveal that large-scale diversity-invasion relationships can be explained by small-scale positive interactions that commonly occur across multiple trophic levels and functional groups. We argue that facilitation has played an important but unrecognized role in the invasion of other well studied systems, and will be of increasing importance with anticipated climate change.

A trophic cascade triggers collapse of a salt‐marsh ecosystem with intensive recreational fishing

Overexploitation of predators has been linked to the collapse of a growing number of shallow-water marine ecosystems. However, salt-marsh ecosystems are often viewed and managed as systems controlled by physical processes, despite recent evidence for herbivore-driven die-off of marsh vegetation. Here we use field observations, experiments, and historical records at 14 sites to examine whether the recently reported die-off of northwestern Atlantic salt marshes is associated with the cascading effects of predator dynamics and intensive recreational fishing activity. We found that the localized depletion of top predators at sites accessible to recreational anglers has triggered the proliferation of herbivorous crabs, which in turn results in runaway consumption of marsh vegetation. This suggests that overfishing may be a general mechanism underlying the consumer-driven die-off of salt marshes spreading throughout the western Atlantic. Our findings support the emerging realization that consumers play a dominant role in regulating marine plant communities and can lead to ecosystem collapse when their impacts are amplified by human activities, including recreational fishing.

Role of Crab Herbivory in Die-Off of New England Salt Marshes

Die-offs of cordgrass are pervasive throughout western Atlantic salt marshes, yet understanding of the mechanisms precipitating these events is limited. We tested whether herbivory by the native crab, Sesarma reticulatum, is generating die-offs of cordgrass that are currently occurring on Cape Cod, Massachusetts (U.S.A.), by manipulating crab access to cordgrass transplanted into die-off areas and healthy vegetation. We surveyed 12 Cape Cod marshes to investigate whether the extent of cordgrass die-off on creek banks, where die-offs are concentrated, was related to local Sesarma grazing intensity and crab density. We then used archived aerial images to examine whether creek bank die-off areas have expanded over the past 2 decades and tested the hypothesis that release from predation, leading to elevated Sesarma densities, is triggering cordgrass die-offs by tethering crabs where die-offs are pervasive and where die-offs have not yet been reported. Intensity of crab grazing on transplanted cordgrass was an order of magnitude higher in die-off areas than in adjacent vegetation. Surveys revealed that Sesarma herbivory has denuded nearly half the creek banks in Cape Cod marshes, and differences in crab-grazing intensity among marshes explained >80% of variation in the extent of the die-offs. Moreover, the rate of die-off expansion and area of marsh affected have more than doubled since 2000. Crab-tethering experiments suggest that release from predation has triggered elevated crab densities that are driving these die-offs, indicating that disruption of predator-prey interactions may be generating the collapse of marsh ecosystems previously thought to be exclusively under bottom-up control.

Economic development and coastal ecosystem change in China

Despite their value, coastal ecosystems are globally threatened by anthropogenic impacts, yet how these impacts are driven by economic development is not well understood. We compiled a multifaceted dataset to quantify coastal trends and examine the role of economic growth in Chinas coastal degradation since the 1950s. Although Chinas coastal population growth did not change following the 1978 economic reforms, its coastal economy increased by orders of magnitude. All 15 coastal human impacts examined increased over time, especially after the reforms. Econometric analysis revealed positive relationships between most impacts and GDP across temporal and spatial scales, often lacking dropping thresholds. These relationships generally held when influences of population growth were addressed by analyzing per capita impacts, and when population density was included as explanatory variables. Historical trends in physical and biotic indicators showed that Chinas coastal ecosystems changed little or slowly between the 1950s and 1978, but have degraded at accelerated rates since 1978. Thus economic growth has been the cause of accelerating human damage to Chinas coastal ecosystems. Chinas GDP per capita remains very low. Without strict conservation efforts, continuing economic growth will further degrade Chinas coastal ecosystems.

Local extinction of a foundation species in a hypoxic estuary: integrating individuals to ecosystem.

We integrated across individual, population, community, and ecosystem levels to understand the impact of environmental stress by tracking the foundation species Mytilus edulis in the hypoxic estuary Narragansett Bay, Rhode Island, USA. Our initial surveys revealed that the mussels occurred in nine extensive (2-28 ha) dense (814-9943 individuals/m2) subtidal reefs that attracted a diverse suite of predators (sea stars, crabs, gastropods). Hypoxia occurred in the summer of 2001, and a mussel transplant experiment revealed overall reduced growth rates of individuals, and higher mortality rates among larger mussels. At the population level, large decreases in densities and cover of mussels were correlated with dissolved oxygen concentrations, leading to extinction at one site and reductions of over an order of magnitude at others. Within one year, seven of the eight remaining populations were edged to extinction, and the previously extinct population was recolonized. At the community level, a predator exclusion experiment indicated that predation was an unimportant source of mussel mortality during the hypoxic period, in part due to the emigration of sea stars, as predicted by the Consumer Stress Model. However, mussels were too intolerant to hypoxia to have a net benefit from the predation refuge. The seasonal (summer) occurrence of hypoxia allowed sea stars to return following a lag, as predicted by a stress return time model, and the resumption of predation contributed to the subsequent extinction of mussel populations. At the ecosystem level, the initial filtration rate of the mussel reefs was estimated at 134.6 x 10(6) m3/d, equivalent to filtering the volume of the bay 1.3 times during the 26-d average residence time. That function was reduced by >75% following hypoxia. The effect of hypoxia on each level of organization had consequences at others. For example, size-specific mortality and decreased growth of individuals, and reduced filtration capacity of reefs, indicated a loss of the ability of mussels to entrain planktonic productivity and potential to control future eutrophication and hypoxia. Our study quantified patterns of loss and identified pathways within an integrative framework of feedbacks, summarized in a conceptual model that is applicable to similar foundation species subjected to environmental stress.

DEAD ZONES ENHANCE KEY FISHERIES SPECIES BY PROVIDING PREDATION REFUGE

Natural stress gradients can reduce predation intensity and increase prey abundances. Whether the harsh conditions of anthropogenic habitat degradation can similarly reduce predation intensity and structure community dynamics remains largely unexplored. Oxygen depletion in coastal waters (hypoxia) is a form of degradation that has recently emerged as one of the greatest threats to coastal ecosystems worldwide due to increased rates of eutrophication and climate change. I conducted field experiments and surveys to test whether relaxed predation could explain the paradoxically high abundance of clams that have sustained a fishery in a degraded estuary with chronic hypoxic conditions. Hypoxia reduced predation on all experimental species but enhanced the long-term survivorship of only sufficiently hypoxia-tolerant prey due to periodic extreme conditions. As a consequence, only the harvested quahog clam (Mercenaria mercenaria) thrived in hypoxic areas that were otherwise rendered dead zones with depauperate diversity and low abundances of other species. This suggests that enhanced populations of some key species may be part of a predictable nonlinear community response that sustains ecosystem services and masks overall downward trends of habitat degradation.

Whole-Community Facilitation Regulates Biodiversity on Patagonian Rocky Shores

Background Understanding the factors that generate and maintain biodiversity is a central goal in ecology. While positive species interactions (i.e., facilitation) have historically been underemphasized in ecological research, they are increasingly recognized as playing important roles in the evolution and maintenance of biodiversity. Dominant habitat-forming species (foundation species) buffer environmental conditions and can therefore facilitate myriad associated species. Theory predicts that facilitation will be the dominant community-structuring force under harsh environmental conditions, where organisms depend on shelter for survival and predation is diminished. Wind-swept, arid Patagonian rocky shores are one of the most desiccating intertidal rocky shores ever studied, providing an opportunity to test this theory and elucidate the context-dependency of facilitation. Methodology/Principal Findings Surveys across 2100 km of southern Argentinean coastline and experimental manipulations both supported theoretical predictions, with 43 out of 46 species in the animal assemblage obligated to living within the matrices of mussels for protection from potentially lethal desiccation stress and predators having no detectable impact on diversity. Conclusions/Significance These results provide the first experimental support of long-standing theoretical predictions and reveal that in extreme climates, maintenance of whole-community diversity can be maintained by positive interactions that ameliorate physical stress. These findings have important conservation implications and emphasize that preserving foundation species should be a priority in remediating the biodiversity consequences of global climate change.