Policy and management responses to earthworm invasions in North America

The introduction, establishment and spread of non-native earthworm species in North America have been ongoing for centuries. These introductions have occurred across the continent and in some ecosystems have resulted in considerable modifications to ecosystem processes and functions associated with above- and belowground foodwebs. However, many areas of North America have either never been colonized by introduced earthworms, or have soils that are still inhabited exclusively by native earthworm fauna. Although several modes of transport and subsequent proliferation of non-native earthworms have been identified, little effort has been made to interrupt the flow of new species into new areas. Examples of major avenues for introduction of earthworms are the fish-bait, horticulture, and vermicomposting industries. In this paper we examine land management practices that influence the establishment of introduced species in several ecosystem types, and identify situations where land management may be useful in limiting the spread of introduced earthworm species. Finally, we discuss methods to regulate the importation of earthworms and earthworm-containing media so that introduction of new exotic species can be minimized or avoided. Although our focus in this paper is necessarily North American, many of the management and policy options presented here could be applicable to the problem of earthworm invasions in other parts of the world.     

Local-scale correlates of native and non-native earthworm distributions in juniper-encroached tallgrass prairie

European and Asian earthworms have invaded much of North America with profound impacts to soils, plant communities, and animal populations. However, few studies have assessed local-scale correlates of earthworm distributions, and most invasive earthworm research has occurred in northern forests. Additionally, despite several studies showing facilitative relationships between invasive earthworms and invasive plants, no research has assessed a potential facilitative interaction between earthworms and woody plants encroaching into prairies. We conducted the first assessment of factors influencing local-scale distributions of native and non-native earthworms for the U.S. Great Plains in a tallgrass prairie-woodland mosaic experiencing eastern redcedar (Juniperus virginiana) encroachment. We documented both native and non-native earthworms, including non-native species from Eurasia (Aporrectodea spp.) and South America (Family Ocnerodrilidae). Native and non-native earthworm distributions were strongly correlated, yet local-scale predictors of distribution also differed between the groups. Native earthworms were more likely to occur near roads and in areas with moist soils. Contrary to expectation, we found no evidence that non-native earthworms occurred more frequently in areas with eastern redcedar-encroachment; instead, non-native earthworms were most likely to occur in tallgrass prairie. Our results suggest that, within prairies and woodlands of the Great Plains, native and non-native earthworms occur most frequently near roadways and in locations with moist soil. Because the few approaches for controlling invasive earthworms are only likely to be feasible on a small scale, findings from such local-scale studies are important for directing management to reduce earthworm impacts on biodiversity and ecosystem services.     

Ecosystem effects of non-native earthworms in Mid-Atlantic deciduous forests

In many mid-Atlantic forests where both native and non-native earthworms exist, it is the non-native species that are the dominant component of the soil macrofauna. Few earthworm ecology studies, however, focus attention on these forest systems in order to determine the relative ecological roles and potential interactions of the native and non-native earthworms. In a series of field samplings and experimental manipulations we collected data on the effects of earthworms on below-and aboveground ecosystem processes. Earthworm abundance and the ecological processes measured were dynamic in space and time across the range of study sites. Leaf litter decay rates doubled at sites that had abundant non-native earthworms. Earthworms also altered the abundance of soil fungi, the activity of extracellular enzymes, soil respiration, and the growth of tree seedlings but the effects varied among sites depending on differences in land-use history and forest age. Red oak seedling growth was less at sites that had abundant earthworms but tulip poplar and red maple seedlings grew equally well with and without abundant earthworms. These preliminary results suggest that non-native earthworms have significant ecosystem effects, even in forests where native earthworms still occur. Land use history, however, plays an important role in determining what those effects will be, and these effects are likely to be dynamic, depending on the abundance of non-native earthworms.     

Weeds,worms, and deer: positive relationships among common forest understory stressors

Biotic global change agents, such as non-native plants (‘weeds’), non-native earthworms (‘worms’), and overabundant herbivores (white-tailed ‘deer’), can be major stressors in the forest understory. The status and relationships among these global change stressors across large spatial extents and under naturally varying conditions are poorly understood. Here, through an observational study using a network of U.S. National Park Service forest health monitoring plots (n = 350) from eight parks in seven northeastern states, we modeled causal pathways among global change stressors through model selection in a structural equation (SEM) framework. Weeds, worms, and, deer were common across all parks in the study—46% of plots had non-native plants, 42% of plots had evidence of earthworms, and all parks had plots with high deer browse damage. All biotic global change stressors were significantly and positively correlated with one another (all Spearman rank correlations ≥ 0.44). Consequently, 28% of plots had a combination of earthworms absent, low deer browse, and no non-native plants, and 29% of plots included earthworms, non-native plants, and moderate or greater browse damage. Through SEM, we found strong support for pathways among global change stressors, e.g., deer browse positively influenced earthworm presence and both deer and earthworms promoted non-native plants. Warmer air temperatures and higher soil pH also facilitated non-natives. This research highlights the tremendous multipronged management challenge for areas already experiencing the combined effects of weeds, worms, and deer and the future vulnerability of other areas as temperatures warm and conditions become more amenable to biotic global change stressors.     

Non-native earthworms alter the assembly of a meadow plant community

Non-native earthworms can alter ecosystems by modifying soil structure, depredating seeds and seedlings, and consuming soil organic matter, yet the initial responses of plant communities to earthworm invasions remain poorly understood. We assessed the effect of non-native earthworms on seedling survival during germination and after establishment using six native and six non-native plant species grown from seed in single- and multi-species experimental mesocosms. We examined the extent to which earthworms (1) influenced seedling survival, (2) selectively depredated native versus non-native plants, (3) impacted establishment based on seed size and/or root morphology, and (4) shaped community assembly. The effect of earthworms on seedling survival varied temporally and among species but inconsistently with respect to species origin. Differences in seed/seedling survival translated to changes in community assembly. Earthworms tended to reduce species abundance, richness, evenness, and diversity in multi-species mesocosms and led to the divergence of communities by treatment. In general, species with large seeds and fibrous roots dominated communities with earthworms present, whereas species with small seeds and taproots only persisted in multi-species mesocosms without earthworms. Our findings suggest that earthworms act as ecological filters in the early stages of invasion to shape community composition based on plant morphological traits.

     

Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms

Population genetic studies can help to determine whether invasive species are established via single vs. multiple introduction events and also to distinguish among various colonization scenarios. We used this approach to investigate the introduction of Dendrobaena octaedra , a non-native earthworm species, to the boreal forest of northern Alberta. The spread of non-native earthworms in forested systems is not well understood, although bait abandonment and vehicular transport are believed to be important. Mitochondrial DNA sequencing revealed that multiple introductions of this species have occurred in northern Alberta, although individual populations may have been established by either single or multiple invaders introduced on one or more occasions. There was no relationship between genetic distances and either geographical distances or distances along road networks, suggesting that human-mediated jump dispersal is more common than diffusive spread via road networks or via active dispersal. As well, genetic diversity was significantly greater at boat launches than roads, indicating that multiple introductions may be more likely to occur at those locations. Focusing management efforts on areas where multiple introductions are likely to occur may help to reduce invasive species' potential for adaptive evolution and subsequent rapid spread.     

Invasive earthworms in a Northern Great Plains prairie fragment

Although ample research exists on the ecological impacts of earthworm invasion in the Great Lakes region and northern hardwood forests, little data is available on the presence, distribution, and impact of earthworms in the prairies of the Northern Tallgrass Prairie. Sampling in a Northern Tallgrass Prairie fragment yielded three species of invasive earthworms occupying three different functional groups: surface and litter dwellers (epigeic), subsurface horizontal burrowers (endogeic), and deep vertical bore inhabitants (anecic). This research note illustrates the presence of non-native and potentially invasive earthworms in Northern Tallgrass Prairie.     

The Role of Tourism and Recreation in the Spread of Non-Native Species: A Systematic Review and Meta-Analysis

Managing the pathways by which non-native species are introduced and spread is considered the most effective way of preventing species invasions. Tourism and outdoor recreation involve the frequent congregation of people, vehicles and vessels from geographically diverse areas. They are therefore perceived to be major pathways for the movement of non-native species, and ones that will become increasingly important with the continued growth of these sectors. However, a global assessment of the relationship between tourism activities and the introduction of non-native species–particularly in freshwater and marine environments–is lacking. We conducted a systematic review and meta-analysis to determine the impact of tourism and outdoor recreation on non-native species in terrestrial, marine and freshwater environments. Our results provide quantitative evidence that the abundance and richness of non-native species are significantly higher in sites where tourist activities take place than in control sites. The pattern was consistent across terrestrial, freshwater and marine environments; across a variety of vectors (e.g. horses, hikers, yachts); and across a range of taxonomic groups. These results highlight the need for widespread biosecurity interventions to prevent the inadvertent introduction of invasive non-native species (INNS) as the tourism and outdoor recreation sectors grow.     

Settlements as a source for the spread of non-native plants into Central European suburban forests

Urbanization is considered as a major driver for biotic homogenization. Urbanization also promotes the dispersal of non-native species. This study examined the roles of suburban settlements and of the surrounding landscape composition for the spread of non-native plant species into adjacent mixed deciduous forests in Southern and Northwestern Switzerland. The number and abundance of native and non-native vascular plant species in both the ground vegetation and shrub layer were recorded in 15 forest sites situated adjacent to settlements and 15 control sites far from settlements. Various site and landscape characteristics were assessed in the surroundings (100 m radius) of the study sites. In both regions we found a higher number and larger abundance of non-native plant species in forest sites adjacent to settlements than in control forest sites. Furthermore, non-native plants were more frequently recorded close to roads and in sites surrounded by a large percentage cover of garden. All these effects were more pronounced in Southern Switzerland, a region with milder winter climate, than in Northwestern Switzerland. Our study showed that settlements are a source for the spread of non-native plant species into Central European suburban forests, and that the composition of the surrounding landscape matrix (e.g. traffic infrastructure, percentage cover of gardens) also affects the establishment of non-native plants.     

Minerals in the rhizosphere: overlooked mediators of soil nitrogen availability to plants and microbes

Non-native earthworms are a continued source of environmental change in the northeastern United States that may affect trace metals in the plant-soil system, with largely unknown effects. We assessed earthworm impacts on exchangeable and strong acid extractable (total) concentrations and pools of Al, Fe, Cu, Zn, Mo, Pb in non-point source polluted, forest soil horizons (Organic, A, and B) and foliar metals concentrations in young (<?3 years) Acer saccharum and Polystichum acrostichoides at four proximal forests in the Finger Lakes Region of New York. We observed decreasing total trace metal Organic horizon pools and increasing total trace metal A horizon concentrations as a function of increasing earthworm biomass. Earthworms had limited effects on exchangeable concentrations in A and B horizons and total metal concentrations in the B horizon. Foliar trace metal concentrations in Acer were better explained by earthworm biomass than soil concentrations but foliar concentrations for Polystichum were poorly predicted by both earthworm biomass and soil metal concentrations. Our results suggest that earthworms can affect trace metal uptake by some plants, but not by increasing soil trace metal exchangeability or from changing soil properties (pH, %SOM, or cation exchange capacity). Instead, non-native earthworms may indirectly alter understory plant uptake of trace metals.     

Application of environmental DNA methods for the detection and abundance estimation of invasive aquatic plant Egeria densa in lotic habitats

Limnology - Estimating the presence and abundance of non-native species in the early stage of invasion is important to prevent further spread of non-native species in aquatic systems. Environmental...     

Long-term trends in seasonal plankton dynamics in Lake Mead (Nevada-Arizona,USA) and implications for climate change

Where biodiversity conservation and environmental preservation are significant concerns, rapid assessment and monitoring of the colonization and spread of non-native species are essential for timely decision-making and response. We developed and evaluated the adequacy of a rapid assessment protocol (RAP) for detecting non-native fish species in 74 Eastern Brazilian lakes. The RAP consists of a single field day employing two surveyors to conduct interviews with local sport fishers, visual surveys of fish, angling with lures, and gillnetting. We compared our results with those from separate, intense, large sampling effort (LSE) field surveys. Despite requiring less than 1/100th of the field effort, the RAP was able to detect the presence of most non-native fish species that were reported in the same lakes by LSE surveys. Information from local sport fishers was invaluable, particularly for detecting species that were in low abundance, but was not available for lakes within a forest preserve area. Non-native introductions commonly lead to rapid and widespread invasion and adverse effects on native biota. Our results strongly suggest that the RAP could function as a cost-effective tool for efficiently assessing the presence of non-native fishes in lakes and monitoring their colonization and spread over large geographic areas.     

Human-mediated introduction of geoengineering earthworms in the Fennoscandian arctic

It is now well established that European earthworms are re-shaping formerly glaciated forests in North America with dramatic ecological consequences. However, few have considered the potential invasiveness of this species assemblage in the European arctic. Here we argue that some earthworm species (Lumbricus rubellus, Lumbricus terrestris and Aporrectodea sp.) with great geomorphological impact (geoengineering species) are non-native and invasive in the Fennoscandian arctic birch forests, where they have been introduced by agrarian settlers and most recently through recreational fishing and gardening. Our exploratory surveys indicate no obvious historical dispersal mechanism that can explain early arrival of these earthworms into the Fennoscandian arctic: that is, these species do not appear to establish naturally along coastlines mimicking conditions following deglaciation in Fennoscandia, nor were they spread by early native (Sami) cultures. The importance of anthropogenic sources and the invasive characteristics of L. rubellus and Aporrectodea sp. in the arctic is evident from their radiation outwards from abandoned farms and modern cabin lawns into adjacent arctic birch forests. They appear to outcompete previously established litter-dwelling earthworm species (i.e. Dendrobaena octaedra) that likely colonized the Fennoscandian landscape rapidly following deglaciation via hydrochory and/or dispersal by early Sami settlements. The high geoengineering earthworm biomasses, their recognized ecological impact in other formerly glaciated environments, and their persistence once established leads us to suggest that geoengineering earthworms may pose a potent threat to some of the most remote and protected arctic environments in northern Europe.     

Non-native and native shrubs have differing impacts on species diversity and composition of associated plant communities

The spread of non-native plants has been depicted as a serious threat to biodiversity. However, it remains unclear whether the indigenousness of the invading plant plays a marked role for the ecological consequences of an invasion as few studies have compared the ecological impacts of non-native shrubs with structurally or functionally comparable native shrubs. We studied patches of introduced and native shrubs to assess whether there are general differences in plant species composition or biomass between patches formed by non-native versus native shrubs. The indigenousness of the shrub (non-native vs. native) did not explain the variation in soil nutrients, neither the production of shoot biomass or allocation of growth to different parts of the shoot. The amount of light reaching ground level did not differ between patches of a non-native and a native shrub. However, species richness and biomass of herbaceous plants were lower in patches of non-native than native shrubs and the amount of litter was higher below non-native than native shrubs. Our results suggest that the indigenousness of the patch-forming plant may be an important factor for the diversity and composition of associated herbaceous vegetation. Based on our results, resource availability (light and nutrients) is not a sufficient explanation for the negative effects of non-native shrubs on plant communities. Further research is needed to investigate whether alternative explanations, such as the novelty of the toxic compounds produced by non-native plants, can explain the differences we observed.     

Urban riparian systems function as corridors for both native and invasive plant species

Riparian areas are often the only green areas left in urban and suburban landscapes, providing opportunities for conservation and connectivity of both aquatic and terrestrial organisms. While city planners and land managers often tout the importance of riparian networks for these uses, it is not well established if urban riparian plant communities are actually functioning as connected assemblages. Furthermore, urban riparian zones are well known to be highly invaded by non-native plant species and may be functioning to increase the spread of non-native species across the landscape. Here we examine connectivity of plant assemblages in riparian networks within an extensively urbanized landscape. We sampled riparian plant communities at 13 sites along three second-order streams of the Rahway River watershed, New Jersey. We also characterized propagule dispersal at each site by sampling litter packs on the river banks five times between March–October 2011 and identifying germinants from litter packs after cold stratification. Species turnover of both riparian and litter vegetation was more strongly associated with flow distance, particularly for native species, indicating that riverine systems are important for promoting connectivity of native plant assemblages in urban landscapes. However, non-native germinants significantly dominated propagule dispersal along the stream reaches, particularly early in the growing season, suggesting spread utilizing the river system and preemption may be an important mechanism for invasion success in this system. Our data show that management of invasive species should be planned and implemented at the watershed scale to reduce spread via the river system.     

Dispersal of non-native plants by introduced bison in an island ecosystem

An understanding of the mechanisms of seed dispersal is critical to effectively managing populations of non-native plants. We investigated whether introduced bison on Santa Catalina Island, California, have the potential to spread non-native plants through the shedding of clumps of seed-laden hair and/or ingesting and later excreting seeds. We collected clumps of hair shaved from bison during a roundup and dislodged by wallowing activity. Greenhouse and field trials were used to test for seed viability and persistence of hair clumps in wallows. In addition to trials with bison hair, we collected samples of bison dung and tested for seed germination in a greenhouse. The majority of seeds extracted from bison hair clumps were of non-native forbs. There was a significant positive relationship between the size of hair clumps and the number of seeds extracted from the clumps, suggesting that managing the introduced bison population at a lower level will help minimize the spread of non-native plants by the species. Seeds of non-native plants were capable of germinating under conditions similar to those on Santa Catalina Island. Clumps of bison hair persisted in wallows, but did not remain intact and lost nearly 40% of their original mass. The number of germinable seeds contained in bison dung was low: 18 seeds germinated from 6 of 18 dung samples. Introduced bison appear to facilitate the dispersal of non-native plants over native plants on Santa Catalina Island. Our study suggests that a comprehensive strategy to control non-native plants must involve the management of the animal agents of plant dispersal.     

Assessing the importance of disturbance, site conditions, and the biotic barrier for dandelion invasion in an Alpine habitat

Several factors have been identified as relevant in determining the abundance of non-native invasive species. Nevertheless, the relative importance of these factors will vary depending on the invaded habitat and the characteristics of the invasive species. Due to their harsh environmental conditions and remoteness, high-alpine habitats are often considered to be at low risk of plant invasion. However, an increasing number of reports have shown the presence and spread of non-native plant species in alpine habitats; thus, it is important to study which factors control the invasion process in these harsh habitats. In this study, we assessed the role of disturbance, soil characteristics, biotic resistance and seed rain in the establishment and abundance of the non-native invasive species Taraxacum officinale (dandelion) in the Andes of central Chile. By focusing on human-disturbed patches, naturally disturbed patches, and undisturbed patches, we did not find that disturbance per se, or its origin, affected the establishment and abundance of T. officinale. The abundance of this non-native invasive species was not negatively related to the diversity of native species at local scales, indicating no biotic resistance to invasion; instead, some positive relationships were found. Our results indicate that propagule pressure (assessed by the seed rain) and the abiotic soil characteristics are the main factors related to the abundance of this non-native invasive species. Hence, in contrast to what has been found for more benign habitats, disturbance and biotic resistance have little influence on the invasibility of T. officinale in this high-alpine habitat.     

Morphological differences between native and non-native pumpkinseed in traits associated with locomotion

Adaptive strategies in morphology can significantly influence the successful invasion and establishment of non-native species. Since its introduction, the pumpkinseed (Lepomis gibbosus), a sunfish of North American origin, has spread throughout most of Europe, including the Iberian Peninsula. We hypothesized that 12 morphological traits, functionally significant for locomotion, would differ according to geographic origin (native/non-native) and habitat type (fluvial/lacustrine). Using flow-through raceways, we simultaneously reared F₁ young-of-the-year pumpkinseed from two native and two non-native populations, produced from adults kept in a common environment. Morphometric measurements were recorded at the beginning and end of the 90-day rearing period. Median-fin size and placement differed significantly between native and non-native populations, whereas paired fin size differed between fluvial and lacustrine populations. Other functionally significant traits, such as body width, also differed between native and non-native populations. Spanish populations were considered to have acquired these adaptive external morphologies through successive generations, following the species’ range expansion through the variable environments of the Iberian Peninsula.     

Invasion by a non‐native ecosystem engineer alters distribution of a native predator

Aim

Shifts in diet composition, abundance or distribution of native predators can occur as a result of exotic prey introductions. We examined effects of non‐native earthworms and anthropogenic landscape disturbance on habitat selection by the American robin (Turdus migratorius), a generalist predator, at landscape and local levels. We also investigated whether robins could act as vectors of spread for earthworm cocoons (egg cases).

Location

Boreal forest of Alberta, Canada.

Methods

We conducted robin and earthworm surveys at campgrounds, well pads, roads, pipelines, seismic lines and forest interiors across northern Alberta. At a subset of paired locations that had similar habitats and anthropogenic disturbance levels, we sampled both robins and earthworms.

Results

Both groups were most likely to occur at campgrounds, well pads and roads. Furthermore, robins were more likely to occur at locations where earthworms were present in our paired local‐level surveys. This correlation between robin and earthworm distributions could be due to robins acting as a vector for earthworm spread, rather than robins’ use of earthworms as prey. However, in tests using captive robins, earthworm cocoons did not survive digestion.

Main conclusions

Robin and earthworm distributions were correlated, likely due to robins’ use of earthworms as prey. These results suggest exotic prey can strongly influence native predators at both landscape and local levels, with shifts in native predator distributions occurring as a result of spatial variability in exotic prey distributions. Although the impacts of ecosystem engineering by earthworms have been previously demonstrated, our study provides evidence that effects of earthworms can also cascade upwards via trophic interactions.     

Geographic independence and phylogenetic diversity of red shiner introductions

Identifying areas at risk of invasion can be difficult when the distribution of a non-native species encompasses geographically disjunct regions. Understanding genealogical relationships among native and non-native populations can clarify the origins of fragmented distributions, which in turn can clarify how fast and far a non-native species may spread. We evaluated genetic variation across the native and invasive ranges of red shiner (Cyprinella lutrensis), a minnow known to displace and hybridize with native species, to reconstruct invasion pathways across the United States (USA). Examination of mitochondrial cytochrome-b variation found that native range populations of red shiner fall into four highly divergent lineages that likely warrant species recognition. Introduced red shiner populations in the eastern and western USA are derived from only two of these lineages. Western USA populations originate from the mid-western and western genetic lineages, whereas eastern introductions derive only from the mid-western lineage. Western USA invasive populations exhibit fewer, but more diverse haplotypes compared to eastern USA invasive populations. We also recovered an undescribed, divergent lineage of Cyprinella that has been cryptically introduced into the western USA, which raises the possibility that hybridization has proceeded following secondary contact between previously allopatric lineages. Approximate Bayesian Computation modeling suggests that the disjunct distribution of red shiner across North America is an agglomeration of independent regional invasions with distinct origins, rather than stepwise advance of an invasion front or secondary introductions across regions. Thus localized control may be effective in managing non-native red shiner, including further spread to areas of conservation concern.