The EICAT+ framework enables classification of positive impacts of alien taxa on native biodiversity.

Species introduced through human-related activities beyond their native range, termed alien species, have various impacts worldwide. The IUCN Environmental Impact Classification for Alien Taxa (EICAT) is a global standard to assess negative impacts of alien species on native biodiversity. Alien species can also positively affect biodiversity (for instance, through food and habitat provisioning or dispersal facilitation) but there is currently no standardized and evidence-based system to classify positive impacts. We fill this gap by proposing EICAT+, which uses 5 semiquantitative scenarios to categorize the magnitude of positive impacts, and describes underlying mechanisms. EICAT+ can be applied to all alien taxa at different spatial and organizational scales. The application of EICAT+ expands our understanding of the consequences of biological invasions and can inform conservation decisions.

Global environmental changes more frequently offset than intensify detrimental effects of biological invasions.

Human-induced abiotic global environmental changes (GECs) and the spread of nonnative invasive species are rapidly altering ecosystems. Understanding the relative and interactive effects of invasion and GECs is critical for informing ecosystem adaptation and management, but this information has not been synthesized. We conducted a meta-analysis to investigate effects of invasions, GECs, and their combined influences on native ecosystems. We found 458 cases from 95 published studies that reported individual and combined effects of invasions and a GEC stressor, which was most commonly warming, drought, or nitrogen addition. We calculated standardized effect sizes (Hedges' d) for individual and combined treatments and classified interactions as additive (sum of individual treatment effects), antagonistic (smaller than expected), or synergistic (outside the expected range). The ecological effects of GECs varied, with detrimental effects more likely with drought than the other GECs. Invasions were more strongly detrimental, on average, than GECs. Invasion and GEC interactions were mostly antagonistic, but synergistic interactions occurred in >25% of cases and mostly led to more detrimental outcomes for ecosystems. While interactive effects were most often smaller than expected from individual invasion and GEC effects, synergisms were not rare and occurred across ecological responses from the individual to the ecosystem scale. Overall, interactions between invasions and GECs were typically no worse than the effects of invasions alone, highlighting the importance of managing invasions locally as a crucial step toward reducing harm from multiple global changes.

Combining local, landscape, and regional geographies to assess plant community vulnerability to invasion impact.

Invasive species science has focused heavily on the invasive agent. However, management to protect native species also requires a proactive approach focused on resident communities and the features affecting their vulnerability to invasion impacts. Vulnerability is likely the result of factors acting across spatial scales, from local to regional, and it is the combined effects of these factors that will determine the magnitude of vulnerability. Here, we introduce an analytical framework that quantifies the scale-dependent impact of biological invasions on native richness from the shape of the native species-area relationship (SAR). We leveraged newly available, biogeographically extensive vegetation data from the U.S. National Ecological Observatory Network to assess plant community vulnerability to invasion impact as a function of factors acting across scales. We analyzed more than 1000 SARs widely distributed across the USA along environmental gradients and under different levels of non-native plant cover. Decreases in native richness were consistently associated with non-native species cover, but native richness was compromised only at relatively high levels of non-native cover. After accounting for variation in baseline ecosystem diversity, net primary productivity, and human modification, ecoregions that were colder and wetter were most vulnerable to losses of native plant species at the local level, while warmer and wetter areas were most susceptible at the landscape level. We also document how the combined effects of cross-scale factors result in a heterogeneous spatial pattern of vulnerability. This pattern could not be predicted by analyses at any single scale, underscoring the importance of accounting for factors acting across scales. Simultaneously assessing differences in vulnerability between distinct plant communities at local, landscape, and regional scales provided outputs that can be used to inform policy and management aimed at reducing vulnerability to the impact of plant invasions.

Dynamic species interactions associated with the range-shifting marine gastropod Mexacanthina lugubris.

Globally, species are undergoing range shifts in response to climate change. However, the potential impacts of climate-driven range shifts are not well understood. In southern California, the predatory whelk Mexacanthina lugubris has undergone a northward range shift of more than 100 km in the past four decades. We traced the history of the whelk's range shift and assessed potential effects using an integrated approach, consisting of field surveys, as well as feeding and thermotolerance experiments. We found that at sites where Mexacanthina and native species co-occurred, native whelks distributions peaked lower in the intertidal. In laboratory experiments, we found that the presence of Mexacanthina led to reduced growth in native whelks (Acanthinucella spirata). Additionally, the range-shifting whelk was able to tolerate higher temperatures than common native species (A. spirata and Nucella emarginata), suggesting further impacts as a result of climate warming. Many species are likely to undergo range shifts as a coping mechanism for changing climatic conditions. However, communities are unlikely to shift as a whole due to species-specific responses. By studying the impacts of range-shifting species, like Mexacanthina, we can better understand how climate change will alter existing community structure and composition.

Disentangling the abundance-impact relationship for invasive species.

To predict the threat of biological invasions to native species, it is critical that we understand how increasing abundance of invasive alien species (IAS) affects native populations and communities. The form of this relationship across taxa and ecosystems is unknown, but is expected to depend strongly on the trophic position of the IAS relative to the native species. Using a global metaanalysis based on 1,258 empirical studies presented in 201 scientific publications, we assessed the shape, direction, and strength of native responses to increasing invader abundance. We also tested how native responses varied with relative trophic position and for responses at the population vs. community levels. As IAS abundance increased, native populations declined nonlinearly by 20%, on average, and community metrics declined linearly by 25%. When at higher trophic levels, invaders tended to cause a strong, nonlinear decline in native populations and communities, with the greatest impacts occurring at low invader abundance. In contrast, invaders at the same trophic level tended to cause a linear decline in native populations and communities, while invaders at lower trophic levels had no consistent impacts. At the community level, increasing invader abundance had significantly larger effects on species evenness and diversity than on species richness. Our results show that native responses to invasion depend critically on invasive species' abundance and trophic position. Further, these general abundance-impact relationships reveal how IAS impacts are likely to develop during the invasion process and when to best manage them.

Going with the flow: the role of ocean circulation in global marine ecosystems under a changing climate.

Ocean warming, acidification, deoxygenation and reduced productivity are widely considered to be the major stressors to ocean ecosystems induced by emissions of CO2 . However, an overlooked stressor is the change in ocean circulation in response to climate change. Strong changes in the intensity and position of the western boundary currents have already been observed, and the consequences of such changes for ecosystems are beginning to emerge. In this study, we address climatically induced changes in ocean circulation on a global scale but relevant to propagule dispersal for species inhabiting global shelf ecosystems, using a high-resolution global ocean model run under the IPCC RCP 8.5 scenario. The » degree model resolution allows improved regional realism of the ocean circulation beyond that of available CMIP5-class models. We use a Lagrangian approach forced by modelled ocean circulation to simulate the circulation pathways that disperse planktonic life stages. Based on trajectory backtracking, we identify present-day coastal retention, dominant flow and dispersal range for coastal regions at the global scale. Projecting into the future, we identify areas of the strongest projected circulation change and present regional examples with the most significant modifications in their dominant pathways. Climatically induced changes in ocean circulation should be considered as an additional stressor of marine ecosystems in a similar way to ocean warming or acidification.

Long-term declines in an intertidal foundation species parallel shifts in community composition.

The earth is in the midst of a biodiversity crisis, and projections indicate continuing and accelerating rates of global changes. Future alterations in communities and ecosystems may be precipitated by changes in the abundance of strongly interacting species, whose disappearance can lead to profound changes in abundance of other species, including an increase in extinction rate for some. Nearshore coastal communities are often dependent on the habitat and food resources provided by foundational plant (e.g., kelp) and animal (e.g., shellfish) species. We quantified changes in the abundance of the blue mussel (Mytilus edulis), a foundation species known to influence diversity and productivity of intertidal habitats, over the past 40 years in the Gulf of Maine, USA, one of the fastest warming regions in the global ocean. Using consistent survey methods, we compared contemporary population sizes to historical data from sites spanning >400 km. The results of these comparisons showed that blue mussels have declined in the Gulf of Maine by >60% (range: 29-100%) at the site level since the earliest benchmarks in the 1970s. At the same time as mussels declined, community composition shifted: at the four sites with historical community data, the sessile community became increasingly algal dominated. Contemporary (2013-2014) surveys across 20 sites showed that sessile species richness was positively correlated to mussel abundance in mid to high intertidal zones. These results suggest that declines in a critical foundation species may have already impacted the intertidal community. To inform future conservation efforts, we provide a database of historical and contemporary baselines of mussel population abundance and dynamics in the Gulf of Maine. Our results underscore the importance of anticipating not only changes in diversity but also changes in the abundance and identity of component species, as strong interactors like foundation species have the potential to drive cascading community shifts.

Integrated assessment of biological invasions.

As the main witnesses of the ecological and economic impacts of invasions on ecosystems around the world, ecologists seek to provide the relevant science that informs managers about the potential for invasion of specific organisms in their region(s) of interest. Yet, the assorted literature that could inform such forecasts is rarely integrated to do so, and further, the diverse nature of the data available complicates synthesis and quantitative prediction. Here we present a set of analytical tools for synthesizing different levels of distributional and/or demographic data to produce meaningful assessments of invasion potential that can guide management at multiple phases of ongoing invasions, from dispersal to colonization to proliferation. We illustrate the utility of data-synthesis and data-model assimilation approaches with case studies of three well-known invasive species--a vine, a marine mussel, and a freshwater crayfish--under current and projected future climatic conditions. Results from the integrated assessments reflect the complexity of the invasion process and show that the most relevant climatic variables can have contrasting effects or operate at different intensities across habitat types. As a consequence, for two of the study species climate trends will increase the likelihood of invasion in some habitats and decrease it in others. Our results identified and quantified both bottlenecks and windows of opportunity for invasion, mainly related to the role of human uses of the landscape or to disruption of the flow of resources. The approach we describe has a high potential to enhance model realism, explanatory insight, and predictive capability, generating information that can inform management decisions and optimize phase-specific prevention and control efforts for a wide range of biological invasions.

Poised to prosper? A cross-system comparison of climate change effects on native and non-native species performance.

Climate change and biological invasions are primary threats to global biodiversity that may interact in the future. To date, the hypothesis that climate change will favour non-native species has been examined exclusively through local comparisons of single or few species. Here, we take a meta-analytical approach to broadly evaluate whether non-native species are poised to respond more positively than native species to future climatic conditions. We compiled a database of studies in aquatic and terrestrial ecosystems that reported performance measures of non-native (157 species) and co-occurring native species (204 species) under different temperature, CO(2) and precipitation conditions. Our analyses revealed that in terrestrial (primarily plant) systems, native and non-native species responded similarly to environmental changes. By contrast, in aquatic (primarily animal) systems, increases in temperature and CO(2) largely inhibited native species. There was a general trend towards stronger responses among non-native species, including enhanced positive responses to more favourable conditions and stronger negative responses to less favourable conditions. As climate change proceeds, aquatic systems may be particularly vulnerable to invasion. Across systems, there could be a higher risk of invasion at sites becoming more climatically hospitable, whereas sites shifting towards harsher conditions may become more resistant to invasions.

Competitive and demographic leverage points of community shifts under climate warming.

Accelerating rates of climate change and a paucity of whole-community studies of climate impacts limit our ability to forecast shifts in ecosystem structure and dynamics, particularly because climate change can lead to idiosyncratic responses via both demographic effects and altered species interactions. We used a multispecies model to predict which processes and species' responses are likely to drive shifts in the composition of a space-limited benthic marine community. Our model was parametrized from experimental manipulations of the community. Model simulations indicated shifts in species dominance patterns as temperatures increase, with projected shifts in composition primarily owing to the temperature dependence of growth, mortality and competition for three critical species. By contrast, warming impacts on two other species (rendering them weaker competitors for space) and recruitment rates of all species were of lesser importance in determining projected community changes. Our analysis reveals the importance of temperature-dependent competitive interactions for predicting effects of changing climate on such communities. Furthermore, by identifying processes and species that could disproportionately leverage shifts in community composition, our results contribute to a mechanistic understanding of climate change impacts, thereby allowing more insightful predictions of future biodiversity patterns.

Geographical range, heat tolerance and invasion success in aquatic species.

Species with broader geographical ranges are expected to be ecological generalists, while species with higher heat tolerances may be relatively competitive at more extreme and increasing temperatures. Thus, both traits are expected to relate to increased survival during transport to new regions of the globe, and once there, establishment and spread. Here, we explore these expectations using datasets of latitudinal range breadth and heat tolerance in freshwater and marine invertebrates and fishes. After accounting for the latitude and hemisphere of each species' native range, we find that species introduced to freshwater systems have broader geographical ranges in comparison to native species. Moreover, introduced species are more heat tolerant than related native species collected from the same habitats. We further test for differences in range breadth and heat tolerance in relation to invasion success by comparing species that have established geographically restricted versus extensive introduced distributions. We find that geographical range size is positively related to invasion success in freshwater species only. However, heat tolerance is implicated as a trait correlated to widespread occurrence of introduced populations in both freshwater and marine systems. Our results emphasize the importance of formal risk assessments before moving heat tolerant species to novel locations.

The functional effects of a dominant consumer are altered following the loss of a dominant producer.

Human impacts on ecosystems are resulting in unprecedented rates of biodiversity loss worldwide. The loss of species results in the loss of the multiple roles that each species plays or functions (i.e., "ecosystem multifunctionality") that it provides. A more comprehensive understanding of the effects of species on ecosystem multifunctionality is necessary for assessing the ecological impacts of species loss. We studied the effects of two dominant intertidal species, a primary producer (the seaweed Neorhodomela oregona) and a consumer (the shellfish Mytilus trossulus), on 12 ecosystem functions in a coastal ecosystem, both in undisturbed tide pools and following the removal of the dominant producer. We modified analytical methods used in biodiversity-multifunctionality studies to investigate the potential effects of individual dominant species on ecosystem function. The effects of the two dominant species from different trophic levels tended to differ in directionality (+/-) consistently (92% of the time) across the 12 individual functions considered. Using averaging and multiple threshold approaches, we found that the dominant consumer-but not the dominant producer-was associated with ecosystem multifunctionality. Additionally, the relationship between abundance and multifunctionality differed depending on whether the dominant producer was present, with a negative relationship between the dominant consumer and ecosystem function with the dominant producer present compared to a non-significant, positive trend where the producer had been removed. Our findings suggest that interactions among dominant species can drive ecosystem function. The results of this study highlight the utility of methods previously used in biodiversity-focused research for studying functional contributions of individual species, as well as the importance of species abundance and identity in driving ecosystem multifunctionality, in the context of species loss.

Biological modification of coastal pH depends on community composition and time.

Biological processes play important roles in determining how global changes manifest at local scales. Primary producers can absorb increased CO2 via daytime photosynthesis, modifying pH in aquatic ecosystems. Yet producers and consumers also increase CO2 via respiration. It is unclear whether biological modification of pH differs across the year, and, if so, what biotic and abiotic drivers underlie temporal differences. We addressed these questions using the intensive study of tide pool ecosystems in Alaska, USA, including quarterly surveys of 34 pools over 1 year and monthly surveys of five pools from spring to fall in a second year. We measured physical conditions, community composition, and changes in pH and dissolved oxygen during the day and night. We detected strong temporal patterns in pH dynamics. Our measurements indicate that pH modification varies spatially (between tide pools) and temporally (across months). This variation in pH dynamics mirrored changes in dissolved oxygen and was associated with community composition, including both relative abundance and diversity of benthic producers and consumers, whose role differed across the year, particularly at night. These results highlight the importance of the time of year when considering the ways that community composition influences pH conditions in aquatic ecosystems.

Negative carry-over effects on larval thermal tolerances across a natural thermal gradient.

Under climate change, marine organisms will need to tolerate or adapt to increasing temperatures to persist. The ability of populations to cope with thermal stress may be influenced by conditions experienced by parents, by both genetic changes and transgenerational phenotypic plasticity through epigenetics or maternal provisioning. In organisms with complex life cycles, larval stages are particularly vulnerable to stress. Positive parental carry-over effects occur if more stressful parental environments yield more tolerant offspring while the opposite pattern leads to negative carry-over effects. This study evaluated the role of parental effects in determining larval thermal tolerances for the intertidal mussel, Mytilus californianus. We tested whether thermal environments across a natural gradient (shoreline elevation) impacted mussel temperature tolerances. Lethal thermal limits were compared for field-collected adults and their larvae. We observed parental effects across one generation, in which adult mussels exposed to warmer habitats yielded less tolerant offspring. Interestingly, although parental environments influenced offspring tolerances, we found no clear effects of habitat conditions on adult phenotypes (tolerances). We found indicators of trade-offs in energy investment, with higher reproductive condition and larger egg diameters in low stress environments. These results suggest that parental effects are negative, leading to possible adverse effects of thermal stress on the next generation.

Climate Change Amelioration by Marine Producers: Does Dominance Predict Impact?

AbstractClimate change threatens biodiversity worldwide, and assessing how those changes will impact communities will be critical for conservation. Dominant primary producers can alter local-scale environmental conditions, reducing temperature via shading and mitigating ocean acidification via photosynthesis, which could buffer communities from the impacts of climate change. We conducted two experiments on the coast of southeastern Alaska to assess the effects of a common seaweed species, Neorhodomela oregona, on temperature and pH in field tide pools and tide pool mesocosms. We found that N. oregona was numerically dominant in this system, covering >60% of habitable space in the pools and accounting for >40% of live cover. However, while N. oregona had a density-dependent effect on pH in isolated mesocosms, we did not find a consistent effect of N. oregona on either pH or water temperature in tide pools in the field. These results suggest that the amelioration of climate change impacts in immersed marine ecosystems by primary producers is not universal and likely depends on species' functional attributes, including photosynthetic rate and physical structure, in addition to abundance or dominance.

Accounting for variation in temperature and oxygen availability when quantifying marine ecosystem metabolism.

It is critical to understand how human modifications of Earth's ecosystems are influencing ecosystem functioning, including net and gross community production (NCP and GCP, respectively) and community respiration (CR). These responses are often estimated by measuring oxygen production in the light (NCP) and consumption in the dark (CR), which can then be combined to estimate GCP. However, the method used to create "dark" conditions-either experimental darkening during the day or taking measurements at night-could result in different estimates of respiration and production, potentially affecting our ability to make integrative predictions. We tested this possibility by measuring oxygen concentrations under daytime ambient light conditions, in darkened tide pools during the day, and during nighttime low tides. We made measurements every 1-3 months over one year in southeastern Alaska. Daytime respiration rates were substantially higher than those measured at night, associated with higher temperature and oxygen levels during the day and leading to major differences in estimates of GCP calculated using daytime versus nighttime measurements. Our results highlight the potential importance of measuring respiration rates during both day and night to account for effects of temperature and oxygen-especially in shallow-water, constrained systems-with implications for understanding the impacts of global change on ecosystem metabolism.

Ocean warming increases threat of invasive species in a marine fouling community.

We addressed the potential for climate change to facilitate invasions and precipitate shifts in community composition by testing effects of ocean warming on species in a marine fouling community in Bodega Harbor, Bodega Bay, California, USA. First, we determined that introduced species tolerated significantly higher temperatures than natives, suggesting that climate change will have a disproportionately negative impact on native species. Second, we assessed the temperature dependence of survival and growth by exposing juveniles to an ambient control temperature and increased temperatures predicted by ocean warming scenarios (+3 degrees C and +4.5 degrees C) in laboratory mesocosms. We found that responses differed between species, species origins, and demographic processes. Based on the temperature tolerance, survival, and growth results, we predict that, as ocean temperatures increase, native species will decrease in abundance, whereas introduced species are likely to increase in this system. Facilitation of invasions by climate change may already be underway; locally, invasive dominance has increased concurrent with ocean warming over the past approximately 40 years. We suggest that the effects of climate change on communities can occur via both direct impacts on the diversity and abundance of native species and indirect effects due to increased dominance of introduced species.

A Hierarchical Mentoring Program Increases Confidence and Effectiveness in Data Analysis and Interpretation for Undergraduate Biology Students.

Science instructors are increasingly incorporating teaching techniques that help students develop core competencies such as critical-thinking and communication skills. These core competencies are pillars of career readiness that prepare undergraduate students to successfully transition to continuing education or the workplace, whatever the field. Course-based undergraduate research experiences that culminate in written research papers can be effective at developing critical-thinking and communication skills but are challenging to implement as class size (and student-to-instructor ratio) grows. We developed a hierarchical mentoring program in which graduate student mentors guided groups of four to five undergraduate students through the scientific process in an upper-level ecology course. Program effectiveness was evaluated by grading final research papers (including previous year papers, before the program was implemented) and surveys (comparing to a course that did not implement the program). Results indicated that primary benefits of hierarchical mentoring were improvements in perceived and demonstrated ability in data analysis and interpretation, leading to a median increase in paper score of ∼10% on a 100-point scale. Future directions indicated by our study were a need to incorporate more approaches (e.g., low-stakes writing exercises) and resources into a revised program to improve outcomes for students whose primary language is not English.

Biophysical feedbacks mediate carbonate chemistry in coastal ecosystems across spatiotemporal gradients.

Ocean acidification (OA) projections are primarily based on open ocean environments, despite the ecological importance of coastal systems in which carbonate dynamics are fundamentally different. Using temperate tide pools as a natural laboratory, we quantified the relative contribution of community composition, ecosystem metabolism, and physical attributes to spatiotemporal variability in carbonate chemistry. We found that biological processes were the primary drivers of local pH conditions. Specifically, non-encrusting producer-dominated systems had the highest and most variable pH environments and the highest production rates, patterns that were consistent across sites spanning 11° of latitude and encompassing multiple gradients of natural variability. Furthermore, we demonstrated a biophysical feedback loop in which net community production increased pH, leading to higher net ecosystem calcification. Extreme spatiotemporal variability in pH is, thus, both impacting and driven by biological processes, indicating that shifts in community composition and ecosystem metabolism are poised to locally buffer or intensify the effects of OA.

Primary producers may ameliorate impacts of daytime CO2 addition in a coastal marine ecosystem.

Predicting the impacts of ocean acidification in coastal habitats is complicated by bio-physical feedbacks between organisms and carbonate chemistry. Daily changes in pH and other carbonate parameters in coastal ecosystems, associated with processes such as photosynthesis and respiration, often greatly exceed global mean predicted changes over the next century. We assessed the strength of these feedbacks under projected elevated CO2 levels by conducting a field experiment in 10 macrophyte-dominated tide pools on the coast of California, USA. We evaluated changes in carbonate parameters over time and found that under ambient conditions, daytime changes in pH, pCO2, net ecosystem calcification (NEC), and O2 concentrations were strongly related to rates of net community production (NCP). CO2 was added to pools during daytime low tides, which should have reduced pH and enhanced pCO2. However, photosynthesis rapidly reduced pCO2 and increased pH, so effects of CO2 addition were not apparent unless we accounted for seaweed and surfgrass abundances. In the absence of macrophytes, CO2 addition caused pH to decline by ∼0.6 units and pCO2 to increase by ∼487 µatm over 6 hr during the daytime low tide. As macrophyte abundances increased, the impacts of CO2 addition declined because more CO2 was absorbed due to photosynthesis. Effects of CO2addition were, therefore, modified by feedbacks between NCP, pH, pCO2, and NEC. Our results underscore the potential importance of coastal macrophytes in ameliorating impacts of ocean acidification.