Biological invasion costs reveal insufficient proactive management worldwide.

The global increase in biological invasions is placing growing pressure on the management of ecological and economic systems. However, the effectiveness of current management expenditure is difficult to assess due to a lack of standardised measurement across spatial, taxonomic and temporal scales. Furthermore, there is no quantification of the spending difference between pre-invasion (e.g. prevention) and post-invasion (e.g. control) stages, although preventative measures are considered to be the most cost-effective. Here, we use a comprehensive database of invasive alien species economic costs (InvaCost) to synthesise and model the global management costs of biological invasions, in order to provide a better understanding of the stage at which these expenditures occur. Since 1960, reported management expenditures have totalled at least US$95.3 billion (in 2017 values), considering only highly reliable and actually observed costs - 12-times less than damage costs from invasions ($1130.6 billion). Pre-invasion management spending ($2.8 billion) was over 25-times lower than post-invasion expenditure ($72.7 billion). Management costs were heavily geographically skewed towards North America (54%) and Oceania (30%). The largest shares of expenditures were directed towards invasive alien invertebrates in terrestrial environments. Spending on invasive alien species management has grown by two orders of magnitude since 1960, reaching an estimated $4.2 billion per year globally (in 2017 values) in the 2010s, but remains 1-2 orders of magnitude lower than damages. National management spending increased with incurred damage costs, with management actions delayed on average by 11 years globally following damage reporting. These management delays on the global level have caused an additional invasion cost of approximately $1.2 trillion, compared to scenarios with immediate management. Our results indicate insufficient management - particularly pre-invasion - and urge better investment to prevent future invasions and to control established alien species. Recommendations to improve reported management cost comprehensiveness, resolution and terminology are also made.

Identifying economic costs and knowledge gaps of invasive aquatic crustaceans.

Despite voluminous literature identifying the impacts of invasive species, summaries of monetary costs for some taxonomic groups remain limited. Invasive alien crustaceans often have profound impacts on recipient ecosystems, but there may be great unknowns related to their economic costs. Using the InvaCost database, we quantify and analyse reported costs associated with invasive crustaceans globally across taxonomic, spatial, and temporal descriptors. Specifically, we quantify the costs of prominent aquatic crustaceans - crayfish, crabs, amphipods, and lobsters. Between 2000 and 2020, crayfish caused US$ 120.5 million in reported costs; the vast majority (99%) being attributed to representatives of Astacidae and Cambaridae. Crayfish-related costs were unevenly distributed across countries, with a strong bias towards European economies (US$ 116.4 million; mainly due to the signal crayfish in Sweden), followed by costs reported from North America and Asia. The costs were also largely predicted or extrapolated, and thus not based on empirical observations. Despite these limitations, the costs of invasive crayfish have increased considerably over the past two decades, averaging US$ 5.7 million per year. Invasive crabs have caused costs of US$ 150.2 million since 1960 and the ratios were again uneven (57% in North America and 42% in Europe). Damage-related costs dominated for both crayfish (80%) and crabs (99%), with management costs lacking or even more under-reported. Reported costs for invasive amphipods (US$ 178.8 thousand) and lobsters (US$ 44.6 thousand) were considerably lower, suggesting a lack of effort in reporting costs for these groups or effects that are largely non-monetised. Despite the well-known damage caused by invasive crustaceans, we identify data limitations that prevent a full accounting of the economic costs of these invasive groups, while highlighting the increasing costs at several scales based on the available literature. Further cost reports are needed to better assess the true magnitude of monetary costs caused by invasive aquatic crustaceans.

Knowledge gaps in economic costs of invasive alien fish worldwide.

Invasive alien fishes have had pernicious ecological and economic impacts on both aquatic ecosystems and human societies. However, a comprehensive and collective assessment of their monetary costs is still lacking. In this study, we collected and reviewed reported data on the economic impacts of invasive alien fishes using InvaCost, the most comprehensive global database of invasion costs. We analysed how total (i.e. both observed and potential/predicted) and observed (i.e. empirically incurred only) costs of fish invasions are distributed geographically and temporally and assessed which socioeconomic sectors are most affected. Fish invasions have potentially caused the economic loss of at least US$37.08 billion (US2017 value) globally, from just 27 reported species. North America reported the highest costs (>85% of the total economic loss), followed by Europe, Oceania and Asia, with no costs yet reported from Africa or South America. Only 6.6% of the total reported costs were from invasive alien marine fish. The costs that were observed amounted to US$2.28 billion (6.1% of total costs), indicating that the costs of damage caused by invasive alien fishes are often extrapolated and/or difficult to quantify. Most of the observed costs were related to damage and resource losses (89%). Observed costs mainly affected public and social welfare (63%), with the remainder borne by fisheries, authorities and stakeholders through management actions, environmental, and mixed sectors. Total costs related to fish invasions have increased significantly over time, from

High and rising economic costs of biological invasions worldwide.

Biological invasions are responsible for substantial biodiversity declines as well as high economic losses to society and monetary expenditures associated with the management of these invasions1,2. The InvaCost database has enabled the generation of a reliable, comprehensive, standardized and easily updatable synthesis of the monetary costs of biological invasions worldwide3. Here we found that the total reported costs of invasions reached a minimum of US$1.288 trillion (2017 US dollars) over the past few decades (1970-2017), with an annual mean cost of US$26.8 billion. Moreover, we estimate that the annual mean cost could reach US$162.7 billion in 2017. These costs remain strongly underestimated and do not show any sign of slowing down, exhibiting a consistent threefold increase per decade. We show that the documented costs are widely distributed and have strong gaps at regional and taxonomic scales, with damage costs being an order of magnitude higher than management expenditures. Research approaches that document the costs of biological invasions need to be further improved. Nonetheless, our findings call for the implementation of consistent management actions and international policy agreements that aim to reduce the burden of invasive alien species.

Global economic costs of aquatic invasive alien species.

Much research effort has been invested in understanding ecological impacts of invasive alien species (IAS) across ecosystems and taxonomic groups, but empirical studies about economic effects lack synthesis. Using a comprehensive global database, we determine patterns and trends in economic costs of aquatic IAS by examining: (i) the distribution of these costs across taxa, geographic regions and cost types; (ii) the temporal dynamics of global costs; and (iii) knowledge gaps, especially compared to terrestrial IAS. Based on the costs recorded from the existing literature, the global cost of aquatic IAS conservatively summed to US$345 billion, with the majority attributed to invertebrates (62%), followed by vertebrates (28%), then plants (6%). The largest costs were reported in North America (48%) and Asia (13%), and were principally a result of resource damages (74%); only 6% of recorded costs were from management. The magnitude and number of reported costs were highest in the United States of America and for semi-aquatic taxa. Many countries and known aquatic alien species had no reported costs, especially in Africa and Asia. Accordingly, a network analysis revealed limited connectivity among countries, indicating disparate cost reporting. Aquatic IAS costs have increased in recent decades by several orders of magnitude, reaching at least US$23 billion in 2020. Costs are likely considerably underrepresented compared to terrestrial IAS; only 5% of reported costs were from aquatic species, despite 26% of known invaders being aquatic. Additionally, only 1% of aquatic invasion costs were from marine species. Costs of aquatic IAS are thus substantial, but likely underreported. Costs have increased over time and are expected to continue rising with future invasions. We urge increased and improved cost reporting by managers, practitioners and researchers to reduce knowledge gaps. Few costs are proactive investments; increased management spending is urgently needed to prevent and limit current and future aquatic IAS damages.

Aquaculture at the crossroads of global warming and antimicrobial resistance.

In many developing countries, aquaculture is key to ensuring food security for millions of people. It is thus important to measure the full implications of environmental changes on the sustainability of aquaculture. We conduct a double meta-analysis (460 articles) to explore how global warming and antimicrobial resistance (AMR) impact aquaculture. We calculate a Multi-Antibiotic Resistance index (MAR) of aquaculture-related bacteria (11,274 isolates) for 40 countries, of which mostly low- and middle-income countries present high AMR levels. Here we show that aquaculture MAR indices correlate with MAR indices from human clinical bacteria, temperature and countries' climate vulnerability. We also find that infected aquatic animals present higher mortalities at warmer temperatures. Countries most vulnerable to climate change will probably face the highest AMR risks, impacting human health beyond the aquaculture sector, highlighting the need for urgent action. Sustainable solutions to minimise antibiotic use and increase system resilience are therefore needed.

Patterns of fish communities and water quality in impounded lakes of China's south-to-north water diversion project.

Understanding the ecological impacts of large-scale hydraulic projects is critical for maintaining ecosystem health while meeting human water needs. It is, however, currently hindered by a lack of direct evidence on ecological impacts associated with this type of project particularly on water quality and fish communities. Here, we characterized patterns and variations of fish communities and water quality in five impounded lakes of the Chinese South-to-North Water Diversion Project (SNWDP), with the aim of better understanding potential ecological impacts of inter-basin water transfers. We found that 1) the impacts of water transfer on water quality in the impounded lakes was generally characterized by hydrological parameters (e.g. total suspended solids, turbidity, transparency, chlorophyll a, dissolved oxygen, conductivity and total hardness) in an upstream-downstream direction; 2) increased hydrological connectivity may have favored biological invasion (e.g. Tridentiger bifasciatus) and promoted a potential biotic homogenization among the impounded lakes; and 3) there was a pattern of decreased fish abundance and biomass from the upstream to downstream lakes with fish communities strongly driven by changing water quality patterns across the impounded lakes. These findings improve our understanding of ecological impacts of large-scale hydraulic projects and provide a significant basis for water agencies with similar water transfer systems to optimize their water transfer management in order to minimize ecological impacts.

Overlapping niches between two co-occurring invasive fish: the topmouth gudgeon Pseudorasbora parva and the common bleak Alburnus alburnus.

Invasive fish species impact aquatic ecosystems and modify native communities, often leading to a decline in local species. These ecological impacts include the transmission of pathogens, predation, competition as well as hybridization. Two invasive fish species, the common bleak Alburnus alburnus and the topmouth gudgeon Pseudorabora parva, have both been recently found co-occurring in several regions of southern Europe, such as the Italian Arno River. Nonetheless, the trophic relationships among invasive fish species, especially cyprinids, remain poorly understood, and no studies have reported the trophic interaction between these two species. This study compared length-weight relationship and used stomach content and stable isotope analysis of two co-occurring populations in the Arno River to characterize the growth and overlap of potential trophic niches. It also found similar allometric growth in both species, a wider generalist trophic niche for P. parva and a more specialized niche for A. alburnus. A considerable niche overlap was found, suggesting that feeding competition can occur if resources were to be limited. Moreover, the niche of P. parva was more likely to overlap with that of A. alburnus than vice versa, suggesting that P. parva can be considered as a potential over competitor. Nonetheless, the authors found in the overlapping populations no evidence of realized competition, probably avoided through a combination of fine-scale mechanisms. They also highlighted that these two invasive species can co-exist and share resources, at least in an open ecosystem like a river, thus potentially doubling up their trophic impact on local communities.

Genomic footprints of a biological invasion: Introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva).

Facilitated by the intensification of global trading, the introduction and dispersal of species to areas in which they are historically non-native is nowadays common. From an evolutionary standpoint, invasions are paradoxical: not only non-native environments could be different from native ones for which introduced individuals would be ill-adapted, but also small founding population size should be associated with reduced adaptive potential. As such, biological invasions are considered valuable real-time evolutionary experiments. Here, we investigated the population structure and adaptive potential of the highly invasive topmouth gudgeon (Pseudorasbora parva) across Europe and East Asia. We RAD-sequenced 301 specimens from sixteen populations and three distinct within-catchment invaded regions as well as two locations in the native range. With 13,785 single nucleotide polymorphisms, we provide conclusive evidence for a genome-wide signature of two distinct invasion events, in Slovakia and Turkey, each originating from a specific area in the native range. A third invaded area, in France, appears to be the result of dispersal within the invasive range. Few loci showed signs of selection, the vast majority of which being identified in the Slovakian region. Functional annotation suggests that faster early stage development, resistance to pollution and immunocompetence contribute to the invasion success of the local habitats. By showing that populations in the invasive range have different evolutionary histories, our study reinforces the idea that populations, rather than species, are the units to consider in invasion biology.

Origin and invasion of the emerging infectious pathogen Sphaerothecum destruens.

Non-native species are often linked to the introduction of novel pathogens with detrimental effects on native biodiversity. Since Sphaerothecum destruens was first discovered as a fish pathogen in the United Kingdom, it has been identified as a potential threat to European fish biodiversity. Despite this parasite's emergence and associated disease risk, there is still a poor understanding of its origin in Europe. Here, we provide the first evidence to support the hypothesis that S. destruens was accidentally introduced to Europe from China along with its reservoir host Pseudorasbora parva via the aquaculture trade. This is the first study to confirm the presence of S. destruens in China, and it has expanded the confirmed range of S. destruens to additional locations in Europe. The demographic analysis of S. destruens and its host P. parva in their native and invasive range further supported the close association of both species. This research has direct significance and management implications for S. destruens in Europe as a non-native parasite.

Deforestation-driven food-web collapse linked to emerging tropical infectious disease, Mycobacterium ulcerans.

Generalist microorganisms are the agents of many emerging infectious diseases (EIDs), but their natural life cycles are difficult to predict due to the multiplicity of potential hosts and environmental reservoirs. Among 250 known human EIDs, many have been traced to tropical rain forests and specifically freshwater aquatic systems, which act as an interface between microbe-rich sediments or substrates and terrestrial habitats. Along with the rapid urbanization of developing countries, population encroachment, deforestation, and land-use modifications are expected to increase the risk of EID outbreaks. We show that the freshwater food-web collapse driven by land-use change has a nonlinear effect on the abundance of preferential hosts of a generalist bacterial pathogen, Mycobacterium ulcerans. This leads to an increase of the pathogen within systems at certain levels of environmental disturbance. The complex link between aquatic, terrestrial, and EID processes highlights the potential importance of species community composition and structure and species life history traits in disease risk estimation and mapping. Mechanisms such as the one shown here are also central in predicting how human-induced environmental change, for example, deforestation and changes in land use, may drive emergence.

Functional Diversity as a New Framework for Understanding the Ecology of an Emerging Generalist Pathogen.

Emerging infectious disease outbreaks are increasingly suspected to be a consequence of human pressures exerted on natural ecosystems. Previously, host taxonomic communities have been used as indicators of infectious disease emergence, and the loss of their diversity has been implicated as a driver of increased presence. The mechanistic details in how such pathogen-host systems function, however, may not always be explained by taxonomic variation or loss. Here we used machine learning and methods based on Gower's dissimilarity to quantify metrics of invertebrate functional diversity, in addition to functional groups and their taxonomic diversity at sites endemic and non-endemic for the model generalist pathogen Mycobacterium ulcerans, the causative agent of Buruli ulcer. Changes in these metrics allowed the rapid categorisation of the ecological niche of the mycobacterium's hosts and the ability to relate specific host traits to its presence in aquatic ecosystems. We found that taxonomic diversity of hosts and overall functional diversity loss and evenness had no bearing on the mycobacterium's presence, or whether the site was in an endemic area. These findings, however, provide strong evidence that generalist environmentally persistent bacteria such as M. ulcerans can be associated with specific functional traits rather than taxonomic groups of organisms, increasing our understanding of emerging disease ecology and origin.

Allometric scaling of intraspecific space use.

Allometric scaling relationships enable exploration of animal space-use patterns, yet interspecific studies cannot address many of the underlying mechanisms. We present the first intraspecific study of home range (HR) allometry relative to energetic requirements over several orders of magnitude of body mass, using as a model the predatory fish, pike Esox lucius. Analogous with interspecific studies, we show that space use increases more rapidly with mass (exponent = 1.08) than metabolic scaling theories predict. Our results support a theory that suggests increasing HR overlap with body mass explains many of these differences in allometric scaling of HR size. We conclude that, on a population scale, HR size and energetic requirement scale allometrically, but with different exponents.

The alternate role of direct and environmental transmission in fungal infectious disease in wildlife: threats for biodiversity conservation.

Emerging fungal pathogens have substantial consequences for infected hosts, as revealed by the global decline of amphibian species from the chytrid fungus. According to the "curse of the Pharaoh" hypothesis, free-living infectious stages typical of fungal pathogens lengthen the timespan of transmission. Free-living infectious stages whose lifespan exceeds the infection time of their hosts are not constrained by virulence, enabling them to persist at high levels and continue transmitting to further sensitive hosts. Using the only Mesomycetozoea fungal species that can be cultured, Sphaerothecum destruens, we obtained tractable data on infectivity and pathogen life cycle for the first time. Here, based on the outcomes of a set of infectious trials and combined with an epidemiological model, we show a high level of dependence on direct transmission in crowded, confined environments and establish that incubation rate and length of infection dictate the epidemic dynamics of fungal disease. The spread of Mesomycetozoea in the wild raise ecological concerns for a range of susceptible species including birds, amphibians and mammals. Our results shed light on the risks associated with farming conditions and highlight the additional risk posed by invasive species that are highly abundant and can act as infectious reservoir hosts.

Maintaining economic value of ecosystem services whilst reducing environmental cost: a way to achieve freshwater restoration in China.

Freshwater fisheries are central to food security in China and this remains one of the most important priorities for the growing human population. Thus, combining ecosystem restoration with economics is pivotal in setting successful conservation in China. Here, we have developed a practical management model that combines fishery improvement with conservation. For six years, a ban on fertilizer and a reduction of planktivorous fish stocking along with the introduction of both mandarin fish Siniperca chuatsi and Chinese mitten crab Eriocheir sinensis was apparent in Wuhu Lake, a highly eutrophic lake located in the middle reaches of the Yangtze River. Annual fish yield decreased slightly after the change in management, whereas fisheries income increased 2.6 times. Mandarin fish and Chinese mitten crab accounted for only 16% of total fisheries production but for 48% of total fisheries income. During this six year period, water clarity increased significantly from 61 cm to 111 cm. Total nitrogen, total phosphorus and chlorophyll decreased significantly from 1.14 to 0.84 mg/L, 0.077 to 0.045 mg/L, and 21.45 to 11.59 µg/L respectively, and macrophyte coverage increased by about 30%. Our results showed that the ecological status of shallow lakes could be rapidly reversed from eutrophic to oligotrophic using simple biomanipulation, whilst maintaining fisheries economic value. It also offers a better approach to shallow fisheries lake management in Asia where traditionally the stocking of Chinese carp and use of fertilizers is still popular.

Topography and land cover of watersheds predicts the distribution of the environmental pathogen Mycobacterium ulcerans in aquatic insects.

BACKGROUND: An understanding of the factors driving the distribution of pathogens is useful in preventing disease. Often we achieve this understanding at a local microhabitat scale; however the larger scale processes are often neglected. This can result in misleading inferences about the distribution of the pathogen, inhibiting our ability to manage the disease. One such disease is Buruli ulcer, an emerging neglected tropical disease afflicting many thousands in Africa, caused by the environmental pathogen Mycobacterium ulcerans. Herein, we aim to describe the larger scale landscape process describing the distribution of M. ulcerans. METHODOLOGY: Following extensive sampling of the community of aquatic macroinvertebrates in Cameroon, we select the 5 dominant insect Orders, and conduct an ecological niche model to describe how the distribution of M. ulcerans positive insects changes according to land cover and topography. We then explore the generalizability of the results by testing them against an independent dataset collected in a second endemic region, French Guiana. PRINCIPAL FINDINGS: We find that the distribution of the bacterium in Cameroon is accurately described by the land cover and topography of the watershed, that there are notable seasonal differences in distribution, and that the Cameroon model does not predict the distribution of M. ulcerans in French Guiana. CONCLUSIONS/SIGNIFICANCE: Future studies of M. ulcerans would benefit from consideration of local structure of the local stream network in future sampling, and further work is needed on the reasons for notable differences in the distribution of this species from one region to another. This work represents a first step in the identification of large-scale environmental drivers of this species, for the purposes of disease risk mapping.

Current ecological understanding of fungal-like pathogens of fish: what lies beneath?

Despite increasingly sophisticated microbiological techniques, and long after the first discovery of microbes, basic knowledge is still lacking to fully appreciate the ecological importance of microbial parasites in fish. This is likely due to the nature of their habitats as many species of fish suffer from living beneath turbid water away from easy recording. However, fishes represent key ecosystem services for millions of people around the world and the absence of a functional ecological understanding of viruses, prokaryotes, and small eukaryotes in the maintenance of fish populations and of their diversity represents an inherent barrier to aquatic conservation and food security. Among recent emerging infectious diseases responsible for severe population declines in plant and animal taxa, fungal and fungal-like microbes have emerged as significant contributors. Here, we review the current knowledge gaps of fungal and fungal-like parasites and pathogens in fish and put them into an ecological perspective with direct implications for the monitoring of fungal fish pathogens in the wild, their phylogeography as well as their associated ecological impact on fish populations. With increasing fish movement around the world for farming, releases into the wild for sport fishing and human-driven habitat changes, it is expected, along with improved environmental monitoring of fungal and fungal-like infections, that the full extent of the impact of these pathogens on wild fish populations will soon emerge as a major threat to freshwater biodiversity.

Complex temporal climate signals drive the emergence of human water-borne disease.

Predominantly occurring in developing parts of the world, Buruli ulcer is a severely disabling mycobacterium infection which often leads to extensive necrosis of the skin. While the exact route of transmission remains uncertain, like many tropical diseases, associations with climate have been previously observed and could help identify the causative agent's ecological niche. In this paper, links between changes in rainfall and outbreaks of Buruli ulcer in French Guiana, an ultraperipheral European territory in the northeast of South America, were identified using a combination of statistical tests based on singular spectrum analysis, empirical mode decomposition and cross-wavelet coherence analysis. From this, it was possible to postulate for the first time that outbreaks of Buruli ulcer can be triggered by combinations of rainfall patterns occurring on a long (i.e., several years) and short (i.e., seasonal) temporal scale, in addition to stochastic events driven by the El Niño-Southern Oscillation that may disrupt or interact with these patterns. Long-term forecasting of rainfall trends further suggests the possibility of an upcoming outbreak of Buruli ulcer in French Guiana.