Quantifying co-extinctions and ecosystem service vulnerability in coastal ecosystems experiencing climate warming.

Climate change is negatively impacting ecosystems and their contributions to human well-being, known as ecosystem services. Previous research has mainly focused on the direct effects of climate change on species and ecosystem services, leaving a gap in understanding the indirect impacts resulting from changes in species interactions within complex ecosystems. This knowledge gap is significant because the loss of a species in a food web can lead to additional species losses or "co-extinctions," particularly when the species most impacted by climate change are also the species that play critical roles in food web persistence or provide ecosystem services. Here, we present a framework to investigate the relationships among species vulnerability to climate change, their roles within the food web, their contributions to ecosystem services, and the overall persistence of these systems and services in the face of climate-induced species losses. To do this, we assess the robustness of food webs and their associated ecosystem services to climate-driven species extinctions in eight empirical rocky intertidal food webs. Across food webs, we find that highly connected species are not the most vulnerable to climate change. However, we find species that directly provide ecosystem services are more vulnerable to climate change and more connected than species that do not directly provide services, which results in ecosystem service provision collapsing before food webs. Overall, we find that food webs are more robust to climate change than the ecosystem services they provide and show that combining species roles in food webs and services with their vulnerability to climate change offer predictions about the impacts of co-extinctions for future food web and ecosystem service persistence. However, these conclusions are limited by data availability and quality, underscoring the need for more comprehensive data collection on linking species roles in interaction networks and their vulnerabilities to climate change.

Merging theory and experiments to predict and understand coextinctions.

In an era of mass extinction, predicting the consequences of species loss has become a priority for ecologists. Extinction of one species can trigger the loss of dependent species, sometimes leading to cascades of extinctions. Simulations predict that cascading extinctions should be commonplace, but empirical observations of extinction cascades rarely match those predicted by simulation. By contrast, species-removal field experiments have yielded surprises, such as novel interactions following removals. Thus, given this mismatch, the true predictive value of extinction simulation studies is unknown. We explore the value of validating extinction simulations with observational and experimental studies. We propose a new framework that unites both approaches to studying extinction cascades, and which reveals new opportunities to couple theory and data.

An ecological network approach to predict ecosystem service vulnerability to species losses.

Human-driven threats are changing biodiversity, impacting ecosystem services. The loss of one species can trigger secondary extinctions of additional species, because species interact-yet the consequences of these secondary extinctions for services remain underexplored. Herein, we compare robustness of food webs and the ecosystem services (hereafter 'services') they provide; and investigate factors determining service responses to secondary extinctions. Simulating twelve extinction scenarios for estuarine food webs with seven services, we find that food web and service robustness are highly correlated, but that robustness varies across services depending on their trophic level and redundancy. Further, we find that species providing services do not play a critical role in stabilizing food webs - whereas species playing supporting roles in services through interactions are critical to the robustness of both food webs and services. Together, our results reveal indirect risks to services through secondary species losses and predictable differences in vulnerability across services.

Quantifying the relative importance of variation in predation and the environment for species coexistence.

Coexistence and food web theory are two cornerstones of the long-standing effort to understand how species coexist. Although competition and predation are known to act simultaneously in communities, theory and empirical study of these processes continue to be developed largely independently. Here, we integrate modern coexistence theory and food web theory to simultaneously quantify the relative importance of predation and environmental fluctuations for species coexistence. We first examine coexistence in a theoretical, multitrophic model, adding complexity to the food web using machine learning approaches. We then apply our framework to a stochastic model of the rocky intertidal food web, partitioning empirical coexistence dynamics. We find the main effects of both environmental fluctuations and variation in predator abundances contribute substantially to species coexistence. Unexpectedly, their interaction tends to destabilise coexistence, leading to new insights about the role of bottom-up vs. top-down forces in both theory and the rocky intertidal ecosystem.

Generality in multispecies responses to ocean acidification revealed through multiple hypothesis testing.

Decades of research have demonstrated that many calcifying species are negatively affected by ocean acidification, a major anthropogenic threat in marine ecosystems. However, even closely related species may exhibit different responses to ocean acidification and less is known about the drivers that shape such variation in different species. Here, we examine the drivers of physiological performance under ocean acidification in a group of five species of turf-forming coralline algae. Specifically, quantitating the relative weight of evidence for each of ten hypotheses, we show that variation in coralline calcification and photosynthesis was best explained by allometric traits. Across ocean acidification conditions, larger individuals (measured as noncalcified mass) had higher net calcification and photosynthesis rates. Importantly, our approach was able to not only identify the aspect of size that drove the performance of coralline algae, but also determined that responses to ocean acidification were not dependent on species identity, evolutionary relatedness, habitat, shape, or structural composition. In fact, we found that failure to test multiple, alternative hypotheses would underestimate the generality of physiological performances, leading to the conclusion that each species had different baseline performance under ocean acidification. Testing among alternative hypotheses is an essential step toward determining the generalizability of experiments across taxa and identifying common drivers of species responses to global change.

Fundamental contradictions among observational and experimental estimates of non-trophic species interactions.

The difficulty of experimentally quantifying non-trophic species interactions has long troubled ecologists. Increasingly, a new application of the classic "checkerboard distribution" approach is used to infer interactions by examining the pairwise frequency at which species are found to spatially co-occur. However, the link between spatial associations, as estimated from observational co-occurrence, and species interactions has not been tested. Here we used nine common statistical methods to estimate associations from surveys of rocky intertidal communities in the Northeast Pacific Ocean. We compared those inferred associations with a new data set of experimentally determined net and direct species interactions. Although association methods generated networks with aggregate structure similar to previously published interaction networks, each method detected a different set of species associations from the same data set. Moreover, although association methods generally performed better than a random model, associations rarely matched empirical net or direct species interactions, with high rates of false positives and true positives, and many false negatives. Our findings cast doubt on studies that equate species co-occurrences to species interactions and highlight a persistent, unanswered question: how do we interpret spatial patterns in communities? We suggest future research directions to unify the observational and experimental study of species interactions, and discuss the need for community standards and best practices in association analysis.

Patterns and Variation in Benthic Biodiversity in a Large Marine Ecosystem.

While there is a persistent inverse relationship between latitude and species diversity across many taxa and ecosystems, deviations from this norm offer an opportunity to understand the conditions that contribute to large-scale diversity patterns. Marine systems, in particular, provide such an opportunity, as marine diversity does not always follow a strict latitudinal gradient, perhaps because several hypothesized drivers of the latitudinal diversity gradient are uncorrelated in marine systems. We used a large scale public monitoring dataset collected over an eight year period to examine benthic marine faunal biodiversity patterns for the continental shelf (55-183 m depth) and slope habitats (184-1280 m depth) off the US West Coast (47°20'N-32°40'N). We specifically asked whether marine biodiversity followed a strict latitudinal gradient, and if these latitudinal patterns varied across depth, in different benthic substrates, and over ecological time scales. Further, we subdivided our study area into three smaller regions to test whether coast-wide patterns of biodiversity held at regional scales, where local oceanographic processes tend to influence community structure and function. Overall, we found complex patterns of biodiversity on both the coast-wide and regional scales that differed by taxonomic group. Importantly, marine biodiversity was not always highest at low latitudes. We found that latitude, depth, substrate, and year were all important descriptors of fish and invertebrate diversity. Invertebrate richness and taxonomic diversity were highest at high latitudes and in deeper waters. Fish richness also increased with latitude, but exhibited a hump-shaped relationship with depth, increasing with depth up to the continental shelf break, ~200 m depth, and then decreasing in deeper waters. We found relationships between fish taxonomic and functional diversity and latitude, depth, substrate, and time at the regional scale, but not at the coast-wide scale, suggesting that coast-wide patterns can obscure important correlates at smaller scales. Our study provides insight into complex diversity patterns of the deep water soft substrate benthic ecosystems off the US West Coast.

Evaluating Temporal Consistency in Marine Biodiversity Hotspots.

With the ongoing crisis of biodiversity loss and limited resources for conservation, the concept of biodiversity hotspots has been useful in determining conservation priority areas. However, there has been limited research into how temporal variability in biodiversity may influence conservation area prioritization. To address this information gap, we present an approach to evaluate the temporal consistency of biodiversity hotspots in large marine ecosystems. Using a large scale, public monitoring dataset collected over an eight year period off the US Pacific Coast, we developed a methodological approach for avoiding biases associated with hotspot delineation. We aggregated benthic fish species data from research trawls and calculated mean hotspot thresholds for fish species richness and Shannon's diversity indices over the eight year dataset. We used a spatial frequency distribution method to assign hotspot designations to the grid cells annually. We found no areas containing consistently high biodiversity through the entire study period based on the mean thresholds, and no grid cell was designated as a hotspot for greater than 50% of the time-series. To test if our approach was sensitive to sampling effort and the geographic extent of the survey, we followed a similar routine for the northern region of the survey area. Our finding of low consistency in benthic fish biodiversity hotspots over time was upheld, regardless of biodiversity metric used, whether thresholds were calculated per year or across all years, or the spatial extent for which we calculated thresholds and identified hotspots. Our results suggest that static measures of benthic fish biodiversity off the US West Coast are insufficient for identification of hotspots and that long-term data are required to appropriately identify patterns of high temporal variability in biodiversity for these highly mobile taxa. Given that ecological communities are responding to a changing climate and other environmental perturbations, our work highlights the need for scientists and conservation managers to consider both spatial and temporal dynamics when designating biodiversity hotspots.

The mixed mating system of the sea palm kelp Postelsia palmaeformis: few costs to selfing.

Naturally isolated populations have conflicting selection pressures for successful reproduction and inbreeding avoidance. These species with limited seasonal reproductive opportunities may use selfing as a means of reproductive assurance. We quantified the frequency of selfing and the fitness consequences for inbred versus outcrossed progeny of an annual kelp, the sea palm (Postelsia palmaeformis). Using experimentally established populations and microsatellite markers to assess the extent of selfing in progeny from six founding parents, we found the frequency of selfing was higher than expected in every population, and few fitness costs were detected in selfed offspring. Despite a decline in heterozygosity of 30 per cent in the first generation of selfing, self-fertilization did not affect individual size or reproduction, and correlated only with a marginally significant decline in survival. Our results suggest both that purging of deleterious recessive alleles may have already occurred and that selfing may be key to reproductive assurance in this species with limited dispersal. Postelsia has an alteration of a free-living diploid and haploid stage, where the haploid stage may provide increased efficiency for purging the genetic load. This life history is shared by many seaweeds and may thus be an important component of mating system evolution in the sea.