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Non-native and native organisms moving into high elevation and high latitude ecosystems in an era of climate change: new challenges for ecology and conservation

Cold environments at high elevation and high latitude are often viewed as resistant to biological invasions. However, climate warming, land use change and associated increased connectivity all increase the risk of biological invasions in these environments. Here we present a summary of the key discussions of the workshop ‘Biosecurity in Mountains and Northern Ecosystems: Current Status and Future Challenges’ (Flen, Sweden, 1–3 June 2015). The aims of the workshop were to (1) increase awareness about the growing importance of species expansion—both non-native and native—at high elevation and high latitude with climate change, (2) review existing knowledge about invasion risks in these areas, and (3) encourage more research on how species will move and interact in cold environments, the consequences for biodiversity, and animal and human health and wellbeing. The diversity of potential and actual invaders reported at the workshop and the likely interactions between them create major challenges for managers of cold environments. However, since these cold environments have experienced fewer invasions when compared with many warmer, more populated environments, prevention has a real chance of success, especially if it is coupled with prioritisation schemes for targeting invaders likely to have greatest impact. Communication and co-operation between cold environment regions will facilitate rapid response, and maximise the use of limited research and management resources.

Biological Invasions

Divergent effects of land-use, propagule pressure, and climate on woody riparian invasion

Landscape-scale analyses of biological invasion are needed to understand the relative importance of environmental drivers that vary at larger scales, such as climate, propagule pressure, resource availability, and human disturbance. One poorly understood landscape-scale question is, how does human land-use influence riparian plant invasion? To evaluate the relative importance of land-use, climate, propagule pressure, and water availability in riparian invasion, we examined tamarisk ( Tamarix ramosissima, T. chinensis , hybrids), Russian olive ( Elaeagnus angustifolia ), and Siberian elm ( Ulmus pumila ) occurrence, abundance, and dominance in 238 riparian sites in developed, cultivated, and undeveloped areas of four western USA river basins (281,946 km 2 ). Temperature and propagule pressure from individuals planted nearby largely drove invasive species occurrence, whereas factors likely to affect resource availability (e.g., land-use, precipitation, streamflow intermittency) were more important to abundance and dominance, supporting the argument that species distribution models based on occurrence alone may fail to identify conditions where invasive species have the greatest impact. The role of land-use varied among taxa: urban and suburban land-use increased Siberian elm occurrence, abundance, and dominance, and urban land-use increased Russian olive occurrence, whereas suburban land-use reduced tamarisk dominance. Surprisingly, Siberian elm, which has received scant prior scientific and management attention, occurred as or more frequently than tamarisk and Russian olive (except in undeveloped areas of the Colorado River headwaters) and had higher density and dominance than tamarisk and Russian olive in developed areas. More research is needed to understand the impacts of this largely unrecognized invader on riparian ecosystem services, particularly in urban and suburban areas.

Colorado, New Mexico

Solutions in microbiome engineering: Prioritizing barriers to organism establishment

Microbiome engineering is increasingly being employed as a solution to challenges in health, agriculture, and climate. Often manipulation involves inoculation of new microbes designed to improve function into a preexisting microbial community. Despite, increased efforts in microbiome engineering inoculants frequently fail to establish and/or confer long-lasting modifications on ecosystem function. We posit that one underlying cause of these shortfalls is the failure to consider barriers to organism establishment. This is a key challenge and focus of macroecology research, specifically invasion biology and restoration ecology. We adopt a framework from invasion biology that summarizes establishment barriers in three categories: (1) propagule pressure, (2) environmental filtering, and (3) biotic interactions factors. We suggest that biotic interactions is the most neglected factor in microbiome engineering research, and we recommend a number of actions to accelerate engineering solutions.

The ISME Journal: Multidisciplinary Journal of Mic

Alien invasions in aquatic ecosystems: Toward an understanding of brook trout invasions and potential impacts on inland cutthroat trout in western North America

Experience from case studies of biological invasions in aquatic ecosystems has motivated a set of proposed empirical “rules” for understanding patterns of invasion and impacts on native species. Further evidence is needed to better understand these patterns, and perhaps contribute to a useful predictive theory of invasions. We reviewed the case of brook trout ( Salvelinus fontinalis )invasions in the western United States and their impacts on native cutthroat trout ( Oncorhynchus clarki ). Unlike many biological invasions, a considerable body of empirical research on brook trout and cutthroat trout is available. We reviewed life histories of each species, brook trout invasions, their impacts on cutthroat trout, and patterns and causes of segregation between brook trout and cutthroat trout. We considered four stages of the invasion process: transport, establishment, spread, and impacts to native species. Most of the research we found focused on impacts. Interspecific interactions, especially competition, were commonly investigated and cited as impacts of brook trout. In many cases it is not clear if brook trout invasions have a measurable impact. Studies of species distributions in the field and a variety of experiments suggest invasion success of brook trout is associated with environmental factors, including temperature, landscape structure, habitat size, stream flow, and human influences. Research on earlier stages of brook trout invasions (transport, establishment, and spread) is relatively limited, but has provided promising insights. Management alternatives for controlling brook trout invasions are limited, and actions to control brook trout focus on direct removal, which is variably successful and can have adverse effects on native species. The management applicability of research has been confounded by the complexity of the problem and by a focus on understanding processes at smaller scales, but not on predicting patterns at larger scales. In the short-term, an improved predictive understanding of brook trout invasions could prove to be most useful, even if processes are incompletely understood. A stronger connection between research and management is needed to identify more effective alternatives for controlling brook trout invasions and for identifying management priorities.

western United States

Patterns of recent brook trout invasion in bull trout streams in relation to habitat, source connectivity, biotic resistance, and disturbance

Knowledge of which habitats are at risk of invasion by nonnative species is essential to conservation, but a changing climate often complicates assessments of where future invasions may occur. Nonnative brook trout Salvelinus fontinalis threaten cold-adapted native salmonids throughout western North America, and the extent of future invasions in coldwater streams is recognized as an area of uncertainty with important consequences. We addressed this uncertainty using spatial-stream-network (SSN) modeling to develop a species distribution model (SDM) for brook trout in Idaho, creating high-resolution prediction maps of suitable (i.e., invadable) habitat under baseline (1990–2015) and future (2080s) climate scenarios, and querying predictions within natal bull trout S. confluentus habitat patches (stream–subwatershed scale) for each scenario. Results indicated that brook trout will experience a net loss of suitable habitat in Idaho, but a large increase of suitable habitat in cold streams. The total proportion of bull trout habitat invadable by brook trout increased from 0.33 during the baseline scenario to 0.44 during the future scenario—a result of upstream expansions of brook trout habitat that were partially offset by contractions in bull trout habitat. Changes in the proportion of invadable habitat varied widely among bull trout patches. Between scenarios, the largest increases in suitable habitat occurred in small, low-gradient, unconfined streams with mean August water temperatures of 7–9 °C during the baseline period. A relatively small proportion of patches contained the majority of invadable habitat in both scenarios, particularly patches in “U-shaped” glacial valleys. A changing climate will broadly increase the threat that brook trout pose to bull trout, but the degree of change experienced by individual populations will vary with local context. The high-resolution prediction maps created by our SSN model will help conservation planners identify and prioritize control efforts on the small proportion of brook trout populations that most threaten bull trout.

Idaho

Plant migration due to winter climate change: Range expansion of tropical invasive plants in response to warming winters

Warming winters due to climate change can facilitate the range expansion of invasive non-native species. In the southeastern United States, the frequency and intensity of extreme winter temperatures determines the northern range limits of many tropical organisms including many species of invasive non-native plants. However, the effects of winter climate change on invasive species’ range limits have been understudied. Here, we used temperature and species occurrence data to examine the sensitivity of invasive tropical plant species to freezing temperatures. We also examined the potential for northward range expansion of these species due to winter climate change. From an initial group of 81 invasive plant species selected due to their ability to transform native plant communities, our analyses identify and quantify species-specific temperature thresholds for 40 tropical, cold sensitive species. Future winter warming scenarios indicate that these tropical invasive plant species have the potential for northward range expansion across the southeastern United States in response to small changes in the severity of winter cold temperature extremes. The potential for range expansion is greatest in coastal areas, which typically have warmer temperatures than inland counterparts. Thus, coastal regions are likely to serve as biological invasion hotspots from which invasive species expand into inland areas. The state of Florida has become a global hotspot for biological invasions, with tens of millions of dollars (US) spent annually to control the ecological and societal impacts of invasive plants on publicly held conservation lands. Collectively, our results underscore the need to better anticipate and prepare for the northward range expansion of invasive plants from Florida into the southeastern United States in response to winter climate change.

Florida, Georgia, South Carolina

SPCIS: Standardized Plant Community with Introduced Status database

The movement of plant species across the globe exposes native communities to new species introductions. While introductions are pervasive, two aspects of variability underlie patterns and processes of biological invasions at macroecological scales. First, only a portion of introduced species become invaders capable of substantially impacting ecosystems. Second, species that do become invasive at one location may not be invasive in others; impacts depend on invader abundance and recipient species and conditions. Accounting for these phenomena is essential to accurately understand the patterns of plant invasion and explain the idiosyncratic results reflected in the literature on biological invasions. The lack of community-level richness and the abundance of data spanning broad scales and environmental conditions have until now hindered our understanding of invasions at a macroecological scale. To address this limitation, we leveraged quantitative surveys of plant communities in the USA and integrated and harmonized nine datasets into the Standardized Plant Community with Introduced Status (SPCIS) database. The database contains 14,056 unique taxa identified within 83,391 sampling units, of which 52.6% have at least one introduced species. The SPCIS database includes comparable information on plant species occurrence, abundance, and native status across the 50 U.S. States and Puerto Rico. SPCIS can be used to answer macro-scale questions about native plant communities and interactions with invasive plants. There are no copyright restrictions on the data, and we ask the users of this dataset to cite this paper, the respective paper(s) corresponding to the dataset sampling design (all references are provided in Data S1: Metadata S1: Class II-B-2), and the references described in Data S1: Metadata S1: Class III-B-4 as applicable to the dataset being utilized.

Ecology

INVASIVESNET towards an International Association for Open Knowledge on Invasive Alien Species

In a world where invasive alien species (IAS) are recognised as one of the major threats to biodiversity, leading scientists from five continents have come together to propose the concept of developing an international association for open knowledge and open data on IAS—termed “INVASIVESNET”. This new association will facilitate greater understanding and improved management of invasive alien species (IAS) and biological invasions globally, by developing a sustainable network of networks for effective knowledge exchange. In addition to their inclusion in the CBD Strategic Plan for Biodiversity, the increasing ecological, social, cultural and economic impacts associated with IAS have driven the development of multiple legal instruments and policies. This increases the need for greater co-ordination, co-operation, and information exchange among scientists, management, the community of practice and the public. INVASIVESNET will be formed by linking new and existing networks of interested stakeholders including international and national expert working groups and initiatives, individual scientists, database managers, thematic open access journals, environmental agencies, practitioners, managers, industry, non-government organisations, citizens and educational bodies. The association will develop technical tools and cyberinfrastructure for the collection, management and dissemination of data and information on IAS; create an effective communication platform for global stakeholders; and promote coordination and collaboration through international meetings, workshops, education, training and outreach. To date, the sustainability of many strategic national and international initiatives on IAS have unfortunately been hampered by time-limited grants or funding cycles. Recognising that IAS initiatives need to be globally coordinated and ongoing, we aim to develop a sustainable knowledge sharing association to connect the outputs of IAS research and to inform the consequential management and societal challenges arising from IAS introductions. INVASIVESNET will provide a dynamic and enduring network of networks to ensure the continuity of connections among the IAS community of practice, science and management.

Management of Biological Invasions

Reproductive biology of invasive grass carp (Ctenopharyngodon idella) in two North American systems

Grass carp ( Ctenopharyngodon idella ) are nonnative, herbivorous freshwater fish that represent an ecological threat in North American waters. However, data are limited on reproductive biology specific to wild populations in midwestern North America, despite recent concern for grass carp establishment within the Great Lakes. Basic information on reproductive traits could be useful to determine reproductive potential, inform future population modelling and provide information to aid control efforts. Our objectives were to evaluate grass carp age-at-maturity, spawning season timing, fecundity type, developmental timing and spawning strategy. Additionally, we evaluated the reliability of the gonadosomatic index (GSI) as a proxy for identifying mature grass carp and compared body condition across study areas. We sampled grass carp in portions of the Mississippi River watershed within the state of Missouri and within the Lake Erie basin. Based on gonad histological samples ( n = 274), grass carp are batch spawners with indeterminate fecundity and asynchronous ovarian developmental timing. This allows flexibility in their spawning, exemplified by a protracted spawning season in Lake Erie (April to November) in temperatures ranging from 12.3 to 27.3°C. Minimum observed age-at-maturity for females in Missouri and for both males and females in the Lake Erie population was age-3 and age-2 for males in Missouri. Accuracy of GSI as a measure of maturity during the spawning season was 89.7% and 87.5%, for females and males, respectively. Compared to Missouri, grass carp in Lake Erie had a significantly higher body condition, and females ready to spawn had significantly higher GSI values, suggesting that the grass carp in Lake Erie are healthier and more fecund relative to Missouri and, if left uncontrolled, potentially have a high probability of establishment within the Great Lakes. The results of this study will allow managers to identify the reproductive status of grass carp in the field and more accurately estimate populations and reproductive potential.

Michigan, Missouri, Ohio

Climate-smart invasive species management for 21st century global change challenges

Addressing the global challenges of climate change and biotic invasions requires understanding their interactions and implications for natural resource management. To facilitate and support invasive species management in a changing climate, we review how climate change and invasions interact to impact the planning, action, and outcomes of invasive species management. Climate change is affecting which species natural resource managers need to assess, monitor, and target by facilitating the introduction of new potential invasive species and altering pathways of introduction and spread. Climate-driven shifts in seasonal conditions and phenological events disrupt and require more flexible management timelines. Climate change may reduce the efficacy and feasibility of current treatment methods and create a need to shift management goals as native ecosystems become more vulnerable to disturbance. Additionally, extreme climate events can compound the spread and impacts of biological invasions, making invasive species management a necessary part of extreme event preparation and response planning. As a solution to these challenges, we propose climate-smart invasive species management, which we define as the approaches that managers and decision-makers can take to address the interactive effects of climate change and invasions. Climate-smart invasive species management includes considering shifts in species ranges, abundance, and impacts to inform monitoring, treatment, and regulation of potential and new invaders at multiple scales. Managers can also adjust the timing of and approach to treatment as efficacy and feasibility change, promote resilient ecosystems through climate-smart restoration, and consider the effects of climate change when setting management goals. Furthermore, climate adaptation funds could expand avenues of funding and support for invasive species management. Explicitly considering the interactions of climate change and biological invasions within organizational decision-making and policy will lead to more effective management and can promote more resilient landscapes.

Global Change Biology

The influence of interspecific interactions on species range expansion rates

Ongoing and predicted global change makes understanding and predicting species’ range shifts an urgent scientific priority. Here, we provide a synthetic perspective on the so far poorly understood effects of interspecific interactions on range expansion rates. We present theoretical foundations for how interspecific interactions may modulate range expansion rates, consider examples from empirical studies of biological invasions and natural range expansions as well as process-based simulations, and discuss how interspecific interactions can be more broadly represented in process-based, spatiotemporally explicit range forecasts. Theory tells us that interspecific interactions affect expansion rates via alteration of local population growth rates and spatial displacement rates, but also via effects on other demographic parameters. The best empirical evidence for interspecific effects on expansion rates comes from studies of biological invasions. Notably, invasion studies indicate that competitive dominance and release from specialized enemies can enhance expansion rates. Studies of natural range expansions especially point to the potential for competition from resident species to reduce expansion rates. Overall, it is clear that interspecific interactions may have important consequences for range dynamics, but also that their effects have received too little attention to robustly generalize on their importance. We then discuss how interspecific interactions effects can be more widely incorporated in dynamic modeling of range expansions. Importantly, models must describe spatiotemporal variation in both local population dynamics and dispersal. Finally, we derive the following guidelines for when it is particularly important to explicitly represent interspecific interactions in dynamic range expansion forecasts: if most interacting species show correlated spatial or temporal trends in their effects on the target species, if the number of interacting species is low, and if the abundance of one or more strongly interacting species is not closely linked to the abundance of the target species.

Ecography

Economic costs of invasive carps in the United States: Case study and management implications

Biological invasions can have far-reaching impacts and incur enormous monetary costs. Economic considerations play an important role in management decision-making. We used the invasion of U.S. waterways by silver ( Hypophthalmichthys molitrix ) and bighead ( H. nobilis ) carp as a case study of the costs of aquatic invasive species. Although these carps are well-known invaders, published reports on their economic costs are lacking. Our study included market values for commercial fisheries, non-market values for recreational fisheries, and management costs. Our results showed that by 2020, U.S. federal and state agencies had spent nearly $592 million in cumulative management costs. A difference-in-difference model testing for the effect of invasive carp on commercial harvest in invaded versus uninvaded reaches of the Mississippi and Illinois Rivers showed no statistical significance. A benefit transfer analysis of invasion effects on total economic value of recreational fishing, an important ecosystem service, in a heavily invaded section of the Illinois River estimated a total loss of more than $10 million over 10 years. While there are other known impacts on ecosystem services, including alteration of aquatic food webs, plankton communities, and native fish communities, these could not be quantified in economic terms in our analysis.

conterminous United States

Strategic planning of prevention and surveillance for emerging diseases and invasive species

Emerging infectious diseases and biological invasions pose increasing threats to public and ecosystems health. Proactive measures—such as prevention and surveillance taken before initial detection of the pathogen or species—are essential to ensure minimal spread prior to first detection. We developed an optimization model to determine where, when, and how much effort should be allocated to prevention versus surveillance. The model accounts for imperfect detection, system dynamics, spatial heterogeneity in risk and costs and is scalable to large landscapes. We found that the most cost-effective strategy is to maintain the prevention and surveillance efforts at stable equilibrium for the majority of the time, with deviations occurring only initially to steer the system toward the equilibrium. The equilibrium effort is jointly determined by the introduction risk, management costs, and total budget. Application of this model to chronic wasting disease in New York State suggests that the optimal strategy could reduce the cumulative disease cases before initial detection by an average of 22% compared to current practice. The optimal surveillance strategy could detect the disease on average over 8 mo earlier than the current strategy.

PNAS

Invasion-mediated mutualism disruption is evident across heterogeneous environmental conditions and varying invasion intensities

The impact of a biological invasion on native communities is expected to be uneven across invaded landscapes due to differences in local abiotic conditions, invader abundance, and traits and composition of the native community. One way to improve predictive ability about the impact of an invasive species given variable conditions is to exploit known mechanisms driving invasive species' success. Invasive plants frequently exhibit allelopathic traits, which can be directly toxic to plants or indirectly impact them via disruption of root symbionts, including mycorrhizal fungi. The indirect mechanism – mutualism disruption – is predicted to impact plants that rely on mycorrhizas but not affect non-mycorrhizal plant species. To assess whether invader-driven mutualism disruption explains observed changes in native plant communities, we analyzed long-term (1998–2018) plant cover data from forest plots across the state of Illinois. We evaluated native plant communities experiencing a range of abundance of invasive allelopathic garlic mustard Alliaria petiolata and varying environmental conditions. Consistent with the mutualism disruption hypothesis, we showed that as garlic mustard abundance increased over time in 0.25 m 2 sampling quadrats, the abundance of mycorrhizal plant species decreased, but non-mycorrhizal plant species did not. Over space and time, garlic mustard abundance predicted plant abundances and diversity at the quadrat level, but this relationship was not present at a larger scale when quadrats were aggregated within sites. Garlic mustard's impact on the plant community was highly localized, yet it was as important as abiotic variables for predicting local plant diversity. We showed that garlic mustard abundance was a key predictor of patterns of plant diversity across invasion intensity and environmental heterogeneity in a way that is consistent with mutualism disruption. Our work indicates that the mutualism disruption hypothesis can provide generalizable predictions of the impacts of allelopathic invasive plants that are evident at a broad spatial scale.

Ecography

Genomic structural variation rescues a classic biological invader from a population bottleneck

Invasion genetics presents a classic paradox: how do species successfully spread despite severe population bottlenecks? The brown treesnake ( Boiga irregularis ) in Guam represents a striking example of this phenomenon, having been introduced with only a handful of individuals. We show that the population endured an extreme bottleneck, with roughly half of the genome exhibiting runs of homozygosity, comparable to species of conservation concern. Despite this, we uncovered extensive diversity in the form of nearly 19,000 genomic structural variants, which affect almost eight times more of the genome than single-nucleotide variants and provide material for ‘rescuing’ the population from inbreeding-driven declines. Structural variant density was highest in gene promoters, where recombination and DNA repair often occur, providing a mechanism for rapid evolution of gene-linked diversity. This diversity is enriched in genes vital for adaptive immunity and olfaction, suggesting genomic diversity in key chromosomal regions can rescue populations from inbreeding. This work has critical implications for invasion biology and conservation genetics practitioners.

BioRxiv

Comparative genomics reveals potential mechanisms of invasion in Phragmites australis (common reed)

Biological invasions are transforming ecosystems worldwide, yet the genomic bases enabling certain species to dominate new environments remain poorly understood. Phragmites australis , a widespread wetland grass with invasive and native subspecies co-occurring in North America, provides a powerful system to investigate genomic mechanisms of invasiveness. We generated independent chromosome-scale genome assemblies for invasive P. australis ssp. australis and co-occurring native ssp. americanus and used comparative genomic and transcriptomic analyses to identify lineage-specific innovations associated with invasive success. The invasive subspecies exhibits genomic novelties through functionally-biased single-copy orthologs, intronless genes, and subgenome expression asymmetry, along with a stress-ready basal transcriptome relative to the native subspecies. Following the removal of aboveground shoots (“cutback”), which measures the ability to recover from damage, the invasive subspecies undergoes stronger transcriptional reprogramming, increased shoot production, and higher biomass accumulation compared to the native. It also displays expansion of gene families and coordinately expressed gene modules that support resource mobilization, growth responses to light, and stress tolerance. Beyond Phragmites , comparative analyses across multiple grass genomes, including eight invasive species with related non-invasive species, revealed repeated expansion of gene families associated with abiotic stress tolerance and developmental regulation, suggesting convergent adaptive strategies in the grass family for invasive success. Together, these results demonstrate genomic architecture linked to invasion success and highlight potential targets for managing invasive grasses.

BioRxiv

Introduced species: A significant component of human-caused global change

Biological invasions are a widespread and significant component of human-caused global environmental change. The extent of invasions of oceanic islands, and their consequences for native biological diversity, have long been recognized. However, invasions of continental regions also are substantial. For example, more than 2,000 species of alien plants are established in the continental United States. These invasions represent a human-caused breakdown of the regional distinctiveness of Earth's flora and fauna—a substantial global change in and of itself. Moreover, there are well- documented examples of invading species that degrade human health and wealth, alter the structure and functioning of otherwise undisturbed ecosystems, and/or threaten native biological diversity. Invasions also interact synergistically with other components of global change. notably land use change. People and institutions working to understand, prevent, and control invasions are carrying out some of the most important—and potentially most effective—work on global environmental change.

New Zealand Journal of Ecology

Habitat and co-occurrence of native and invasive crayfish in the Pacific Northwest, USA

Biological invasions can have dramatic effects on freshwater ecosystems and introduced crayfish can be particularly impacting. We document crayfish distribution in three large hydrographic basins (Rogue, Umpqua, Willamette/Columbia) in the Pacific Northwest USA. We used occupancy analyses to investigate habitat relationships and evidence for displacement of native Pacifastacus leniusculus (Dana, 1852) by two invaders. We found invasive Procambarus clarkii (Girard, 1852), in 51 of 283 sites and in all three hydrographic basins. We found invasive Orconectes n. neglectus (Faxon, 1885) at 68% of sites in the Rogue basin and provide first documentation of their broad distribution in the Umpqua basin. We found P. clarkii in both lentic and lotic habitats, and it was positively associated with manmade sites. P. leniusculus was positively associated with lotic habitats and negatively related to manmade sites. In the Rogue and Umpqua basins, O. n. neglectus and P. leniusculus were similar in their habitat associations. We did not find a negative relationship in site occupancy between O. n. neglectus and P. leniusculus. Our data suggest that P. clarkii has potential to locally displace P. leniusculus. There is still time for preventive measures to limit the spread of the invasive crayfish in this region.

Aquatic Invasions