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1.  Thresholds in marsh resilience to the Deepwater Horizon oil spill 
Scientific Reports  2016;6:32520.
Ecosystem boundary retreat due to human-induced pressure is a generally observed phenomenon. However, studies that document thresholds beyond which internal resistance mechanisms are overwhelmed are uncommon. Following the Deepwater Horizon (DWH) oil spill, field studies from a few sites suggested that oiling of salt marshes could lead to a biogeomorphic feedback where plant death resulted in increased marsh erosion. We tested for spatial generality of and thresholds in this effect across 103 salt marsh sites spanning ~430 kilometers of shoreline in coastal Louisiana, Alabama, and Mississippi, using data collected as part of the natural resource damage assessment (NRDA). Our analyses revealed a threshold for oil impacts on marsh edge erosion, with higher erosion rates occurring for ~1–2 years after the spill at sites with the highest amounts of plant stem oiling (90–100%). These results provide compelling evidence showing large-scale ecosystem loss following the Deepwater Horizon oil spill. More broadly, these findings provide rare empirical evidence identifying a geomorphologic threshold in the resistance of an ecosystem to increasing intensity of human-induced disturbance.
PMCID: PMC5040145  PMID: 27679956
2.  A keystone mutualism underpins resilience of a coastal ecosystem to drought 
Nature Communications  2016;7:12473.
Droughts are increasing in severity and frequency, yet the mechanisms that strengthen ecosystem resilience to this stress remain poorly understood. Here, we test whether positive interactions in the form of a mutualism between mussels and dominant cordgrass in salt marshes enhance ecosystem resistance to and recovery from drought. Surveys spanning 250 km of southeastern US coastline reveal spatially dispersed mussel mounds increased cordgrass survival during severe drought by 5- to 25-times. Surveys and mussel addition experiments indicate this positive effect of mussels on cordgrass was due to mounds enhancing water storage and reducing soil salinity stress. Observations and models then demonstrate that surviving cordgrass patches associated with mussels function as nuclei for vegetative re-growth and, despite covering only 0.1–12% of die-offs, markedly shorten marsh recovery periods. These results indicate that mutualisms, in supporting stress-resistant patches, can play a disproportionately large, keystone role in enhancing ecosystem resilience to climatic extremes.
Intensifying drought has caused massive die-offs in ecosystems worldwide. Here, Angelini et al. use observations, experiments, and models in US salt marshes to show that a key mutualism increases ecosystem resilience by maintaining stress-resistant habitat patches that aid post-drought recovery.
PMCID: PMC4992128  PMID: 27534803
3.  Foundation species' overlap enhances biodiversity and multifunctionality from the patch to landscape scale in southeastern United States salt marshes 
Although there is mounting evidence that biodiversity is an important and widespread driver of ecosystem multifunctionality, much of this research has focused on small-scale biodiversity manipulations. Hence, which mechanisms maintain patches of enhanced biodiversity in natural systems and if these patches elevate ecosystem multifunctionality at both local and landscape scales remain outstanding questions. In a 17 month experiment conducted within southeastern United States salt marshes, we found that patches of enhanced biodiversity and multifunctionality arise only where habitat-forming foundation species overlap—i.e. where aggregations of ribbed mussels (Geukensia demissa) form around cordgrass (Spartina alterniflora) stems. By empirically scaling up our experimental results to the marsh platform at 12 sites, we further show that mussels—despite covering only approximately 1% of the marsh surface—strongly enhance five distinct ecosystem functions, including decomposition, primary production and water infiltration rate, at the landscape scale. Thus, mussels create conditions that support the co-occurrence of high densities of functionally distinct organisms within cordgrass and, in doing so, elevate salt marsh multifunctionality from the patch to landscape scale. Collectively, these findings suggest that patterns in foundation species' overlap drive variation in biodiversity and ecosystem functioning within and across natural ecosystems. We therefore argue that foundation species should be integrated in our conceptual understanding of forces that moderate biodiversity–ecosystem functioning relationships, approaches for conserving species diversity and strategies to improve the multifunctionality of degraded ecosystems.
PMCID: PMC4528541  PMID: 26136442
decomposition; ecosystem function; facilitation; primary production; salt marsh; Spartina alterniflora
4.  Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas 
Marine protected areas (MPAs) are key tools for combatting the global overexploitation of endangered species. The prevailing paradigm is that MPAs are beneficial in helping to restore ecosystems to more ‘natural’ conditions. However, MPAs may have unintended negative effects when increasing densities of protected species exert destructive effects on their habitat. Here, we report on severe seagrass degradation in a decade-old MPA where hyper-abundant green turtles adopted a previously undescribed below-ground foraging strategy. By digging for and consuming rhizomes and roots, turtles create abundant bare gaps, thereby enhancing erosion and reducing seagrass regrowth. A fully parametrized model reveals that the ecosystem is approaching a tipping point, where consumption overwhelms regrowth, which could potentially lead to complete collapse of the seagrass habitat. Seagrass recovery will not ensue unless turtle density is reduced to nearly zero, eliminating the MPA's value as a turtle reserve. Our results reveal an unrecognized, yet imminent threat to MPAs, as sea turtle densities are increasing at major nesting sites and the decline of seagrass habitat forces turtles to concentrate on the remaining meadows inside reserves. This emphasizes the need for policy and management approaches that consider the interactions of protected species with their habitat.
PMCID: PMC3896025  PMID: 24403341
marine reserves; plant–herbivore interactions; alternate stable states
5.  Correction: Population Genetics of a Trochid Gastropod Broadens Picture of Caribbean Sea Connectivity 
PLoS ONE  2010;5(9):10.1371/annotation/57fcda53-c9ef-486f-a87c-3cb3673cea70.
PMCID: PMC2947706
6.  Livestock as a potential biological control agent for an invasive wetland plant 
PeerJ  2014;2:e567.
Invasive species threaten biodiversity and incur costs exceeding billions of US$. Eradication efforts, however, are nearly always unsuccessful. Throughout much of North America, land managers have used expensive, and ultimately ineffective, techniques to combat invasive Phragmites australis in marshes. Here, we reveal that Phragmites may potentially be controlled by employing an affordable measure from its native European range: livestock grazing. Experimental field tests demonstrate that rotational goat grazing (where goats have no choice but to graze Phragmites) can reduce Phragmites cover from 100 to 20% and that cows and horses also readily consume this plant. These results, combined with the fact that Europeans have suppressed Phragmites through seasonal livestock grazing for 6,000 years, suggest Phragmites management can shift to include more economical and effective top-down control strategies. More generally, these findings support an emerging paradigm shift in conservation from high-cost eradication to economically sustainable control of dominant invasive species.
PMCID: PMC4178463  PMID: 25276502
Top-down control; Salt marshes; Invasive species; Biocontrol
7.  Animal-Borne Imaging Reveals Novel Insights into the Foraging Behaviors and Diel Activity of a Large-Bodied Apex Predator, the American Alligator (Alligator mississippiensis) 
PLoS ONE  2014;9(1):e83953.
Large-bodied, top- and apex predators (e.g., crocodilians, sharks, wolves, killer whales) can exert strong top-down effects within ecological communities through their interactions with prey. Due to inherent difficulties while studying the behavior of these often dangerous predatory species, relatively little is known regarding their feeding behaviors and activity patterns, information that is essential to understanding their role in regulating food web dynamics and ecological processes. Here we use animal-borne imaging systems (Crittercam) to study the foraging behavior and activity patterns of a cryptic, large-bodied predator, the American alligator (Alligator mississippiensis) in two estuaries of coastal Florida, USA. Using retrieved video data we examine the variation in foraging behaviors and activity patterns due to abiotic factors. We found the frequency of prey-attacks (mean = 0.49 prey attacks/hour) as well as the probability of prey-capture success (mean = 0.52 per attack) were significantly affected by time of day. Alligators attempted to capture prey most frequently during the night. Probability of prey-capture success per attack was highest during morning hours and sequentially lower during day, night, and sunset, respectively. Position in the water column also significantly affected prey-capture success, as individuals’ experienced two-fold greater success when attacking prey while submerged. These estimates are the first for wild adult American alligators and one of the few examples for any crocodilian species worldwide. More broadly, these results reveal that our understandings of crocodilian foraging behaviors are biased due to previous studies containing limited observations of cryptic and nocturnal foraging interactions. Our results can be used to inform greater understanding regarding the top-down effects of American alligators in estuarine food webs. Additionally, our results highlight the importance and power of using animal-borne imaging when studying the behavior of elusive large-bodied, apex predators, as it provides critical insights into their trophic and behavioral interactions.
PMCID: PMC3893291  PMID: 24454711
8.  Effects of selection and mutation on mitochondrial variation and inferences of historical population expansion in a Caribbean reef fish 
Mitochondrial sequence data has contributed to the understanding of historical demography through the application of neutrality tests and coalescent estimators of population growth rates. Characteristics of the mitochondrial genome, such as high mutation rate and lack of recombination, render it particularly suitable for these types of studies. However, selection can also affect patterns of mitochondrial variation. Furthermore, conclusions based on single mitochondrial loci can be sensitive to differences among mitochondrial genes in mutation rate and pattern and levels of homoplasy. We tested the contributions of these factors to patterns of mitochondrial variation in the Caribbean reef fish Halichoeres bivittatus using a multilocus sequence-based approach. Mitochondrial protein-coding loci deviated strongly from a neutral model of evolution and indicated high rates of estimated population growth. In contrast, the mitochondrial control region and a nuclear intron showed little or no deviation from neutrality and low estimated growth rates. The level of variation among loci is inconsistent with a demographic explanation and likely stems from the influence of mutation and selection on the mitochondrial genome. In H. bivittatus, a finding of high rates of population growth is likely an artifact of selection on mitochondrial proteins. This result suggests caution in the interpretation of variation at single mitochondrial loci, and highlights the importance of the use of unlinked nuclear loci to test demographic inferences made from mitochondrial DNA.
PMCID: PMC3737519  PMID: 20688179
Population genetics; Caribbean; Halichoeres; Mitochondrial; Selection; Multilocus
9.  Non-Linear Interactions between Consumers and Flow Determine the Probability of Plant Community Dominance on Maine Rocky Shores 
PLoS ONE  2013;8(8):e67625.
Although consumers can strongly influence community recovery from disturbance, few studies have explored the effects of consumer identity and density and how they may vary across abiotic gradients. On rocky shores in Maine, recent experiments suggest that recovery of plant- or animal- dominated community states is governed by rates of water movement and consumer pressure. To further elucidate the mechanisms of consumer control, we examined the species-specific and density-dependent effects of rocky shore consumers (crabs and snails) on community recovery under both high (mussel dominated) and low flow (plant dominated) conditions. By partitioning the direct impacts of predators (crabs) and grazers (snails) on community recovery across a flow gradient, we found that grazers, but not predators, are likely the primary agent of consumer control and that their impact is highly non-linear. Manipulating snail densities revealed that herbivorous and bull-dozing snails (Littorina littorea) alone can control recovery of high and low flow communities. After ∼1.5 years of recovery, snail density explained a significant amount of the variation in macroalgal coverage at low flow sites and also mussel recovery at high flow sites. These density-dependent grazer effects were were both non-linear and flow-dependent, with low abundance thresholds needed to suppress plant community recovery, and much higher levels needed to control mussel bed development. Our study suggests that consumer density and identity are key in regulating both plant and animal community recovery and that physical conditions can determine the functional forms of these consumer effects.
PMCID: PMC3734138  PMID: 23940510
10.  Top predators suppress rather than facilitate plants in a trait-mediated tri-trophic cascade 
Biology Letters  2011;7(5):710-713.
Classical ecological theory states that in tri-trophic systems, predators indirectly facilitate plants by reducing herbivore densities through consumption, while more recent work has revealed that predators can generate the same positive effect on plants non-consumptively by inducing changes in herbivore traits (e.g. feeding rates). Based on observations in US salt marshes dominated by vast monocultures of cordgrass, we hypothesized that sit-and-wait substrate-dwelling predators (crabs) could actually strengthen per capita impacts of potent grazers (snails), by non-consumptively inducing a vertical habitat shift of snails to their predation refuge high on canopy leaves that are vulnerable to grazing. A two-month field experiment supported this hypothesis, revealing that predators non-consumptively increased the mean climbing height of snails on grasses, increased grazing damage per leaf and ultimately suppressed cordgrass biomass, relative to controls. While seemingly counterintuitive, our results can be explained by (i) the vulnerability of refuge resources to grazing, and (ii) universal traits that drove the vertical habitat shift—i.e. relative habitat domains of predator and prey, and the hunting mode of the top predator. These results underline the fact that not only should we continue to incorporate non-consumptive effects into our understanding of top-down predator impacts, but we should do so in a spatially explicit manner.
PMCID: PMC3169052  PMID: 21508017
non-consumptive; grazing; salt marsh
11.  Predator diversity stabilizes and strengthens trophic control of a keystone grazer 
Biology Letters  2010;7(1):79-82.
Despite the global vulnerability of predators to extinction, and the critical functional role they play in many ecosystems, there have been few realistic tests of the consequences of predator species deletion (conversely, predator diversity) in natural ecosystems. We performed a four-month field experiment in a southeastern United States salt marsh to test the role of predatory crab diversity in regulating populations of a keystone grazer that can decimate marsh vegetation at high densities. Our results revealed that a combination of this system's two resident predator species, in comparison to individual species, both stabilize and strengthen predation rates on the potent grazer. Monthly monitoring of predation rates from intense, hot summer months into the cooler autumn indicate this diversity benefit arises from predators responding differentially to changing environmental conditions across seasons. This study provides some of the first experimental field support for the insurance hypothesis from marine ecosystems, suggests that predator temporal complementarity may be more common than currently perceived, and argues for conservation of predator diversity to ensure reliable and effective control of potentially habitat-destroying grazers.
PMCID: PMC3030897  PMID: 20739314
biodiversity; insurance hypothesis; temporal complementarity
12.  A Meta-Analysis of Seaweed Impacts on Seagrasses: Generalities and Knowledge Gaps 
PLoS ONE  2012;7(1):e28595.
Seagrasses are important habitat-formers and ecosystem engineers that are under threat from bloom-forming seaweeds. These seaweeds have been suggested to outcompete the seagrasses, particularly when facilitated by eutrophication, causing regime shifts where green meadows and clear waters are replaced with unstable sediments, turbid waters, hypoxia, and poor habitat conditions for fishes and invertebrates. Understanding the situations under which seaweeds impact seagrasses on local patch scales can help proactive management and prevent losses at greater scales. Here, we provide a quantitative review of available published manipulative experiments (all conducted at the patch-scale), to test which attributes of seaweeds and seagrasses (e.g., their abundances, sizes, morphology, taxonomy, attachment type, or origin) influence impacts. Weighted and unweighted meta-analyses (Hedges d metric) of 59 experiments showed generally high variability in attribute-impact relationships. Our main significant findings were that (a) abundant seaweeds had stronger negative impacts on seagrasses than sparse seaweeds, (b) unattached and epiphytic seaweeds had stronger impacts than ‘rooted’ seaweeds, and (c) small seagrass species were more susceptible than larger species. Findings (a) and (c) were rather intuitive. It was more surprising that ‘rooted’ seaweeds had comparatively small impacts, particularly given that this category included the infamous invasive Caulerpa species. This result may reflect that seaweed biomass and/or shading and metabolic by-products like anoxia and sulphides could be lower for rooted seaweeds. In conclusion, our results represent simple and robust first-order generalities about seaweed impacts on seagrasses. This review also documented a limited number of primary studies. We therefore identified major knowledge gaps that need to be addressed before general predictive models on seaweed-seagrass interactions can be build, in order to effectively protect seagrass habitats from detrimental competition from seaweeds.
PMCID: PMC3254607  PMID: 22253693
13.  Whole-Community Facilitation Regulates Biodiversity on Patagonian Rocky Shores 
PLoS ONE  2011;6(10):e24502.
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.
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.
PMCID: PMC3192702  PMID: 22022356

Results 1-13 (13)