Erin K. Cameron

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.

Human-facilitated invasion of exotic earthworms into northern boreal forests.

Abstract Recreational and industrial development is rapidly expanding in the boreal forest of western Canada. Concerns exist that such activity is facilitating the introduction and spread of non-native species such as exotic earthworms. The mechanisms by which earthworms are introduced and spread in forested systems are not well understood. Given the poor intrinsic dispersal abilities of earthworms, we propose 4 major introduction mechanisms: 1) abandonment of worms brought as fishing bait; 2) dispersal via vehicles; 3) dispersal via vertebrate predators; or 4) dispersal via waterways. To test these hypotheses, we sampled earthworms in forest stands near boat launches, roads, seismic lines, forest interiors, and remote shorelines of lakes in the boreal forest of northern Alberta, Canada. Boat launches and roads had a significantly higher probability of earthworm occurrence (54% of plots occupied) compared with the other locations (13% of plots occupied). Species commonly used as fishing bait occurred more often near boat launches (18% of plots occupied) than near roads alone (1% of plots occupied). These results suggest that vehicle transport and bait abandonment may both be mechanisms of earthworm introduction. The consequences of these introductions remain unclear but suggest that reduced road construction and regulations prohibiting the discarding of bait need to be considered to slow earthworm invasions.

Higher predation risk for insect prey at low latitudes and elevations

Risky in the tropics It is well known that diversity increases toward the tropics. Whether this increase translates into differences in interaction rates among species, however, remains unclear. To simplify the problem, Roslin et al. tested for predation rates by using a single approach involving model caterpillars across six continents. Predator attack rates were higher toward the equator, but only for arthropod predators. Science, this issue p. 742 Like diversity, predation rates among insects increase toward the equator and at lower altitudes. Biotic interactions underlie ecosystem structure and function, but predicting interaction outcomes is difficult. We tested the hypothesis that biotic interaction strength increases toward the equator, using a global experiment with model caterpillars to measure predation risk. Across an 11,660-kilometer latitudinal gradient spanning six continents, we found increasing predation toward the equator, with a parallel pattern of increasing predation toward lower elevations. Patterns across both latitude and elevation were driven by arthropod predators, with no systematic trend in attack rates by birds or mammals. These matching gradients at global and regional scales suggest consistent drivers of biotic interaction strength, a finding that needs to be integrated into general theories of herbivory, community organization, and life-history evolution.

The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta-analysis).

Abstract Globally, biological invasions can have strong impacts on biodiversity as well as ecosystem functioning. While less conspicuous than introduced aboveground organisms, introduced belowground organisms may have similarly strong effects. Here, we synthesize for the first time the impacts of introduced earthworms on plant diversity and community composition in North American forests. We conducted a meta‐analysis using a total of 645 observations to quantify mean effect sizes of associations between introduced earthworm communities and plant diversity, cover of plant functional groups, and cover of native and non‐native plants. We found that plant diversity significantly declined with increasing richness of introduced earthworm ecological groups. While plant species richness or evenness did not change with earthworm invasion, our results indicate clear changes in plant community composition: cover of graminoids and non‐native plant species significantly increased, and cover of native plant species (of all functional groups) tended to decrease, with increasing earthworm biomass. Overall, these findings support the hypothesis that introduced earthworms facilitate particular plant species adapted to the abiotic conditions of earthworm‐invaded forests. Further, our study provides evidence that introduced earthworms are associated with declines in plant diversity in North American forests. Changing plant functional composition in these forests may have long‐lasting effects on ecosystem functioning.

Non-Native Earthworm Influences on Ectomycorrhizal Colonization and Growth of White Spruce

Abstract: Exotic earthworms are entering previously uninhabited soils of boreal forests, their invasion largely facilitated through human activities. As ecosystem engineers, earthworms are capable of causing dramatic changes in above- and belowground forest composition, but whether they have the same effects in all forests remains unclear. Forest compositional changes caused by earthworms may be mediated by interactions between earthworms and mycorrhizal fungi. Specifically, tree seedling growth may be altered by the presence of exotic earthworms and their subsequent impact on mycorrhizal fungi. In this study, we investigate the effects of exotic earthworms on ectomycorrhizal colonization and seedling growth of the conifer Picea glauca (white spruce) in gray luvisolic soils from the Boreal Plains. Anecic Lumbricus terrestris and epigeic Dendrobaena octaedra earthworms were added to mesocosms each containing a white spruce seedling in a greenhouse experiment. Impacts on the composition of ectomycorrhizal fungi in the mesocosms were determined using a combination of morphological and molecular techniques, and effects on seedling growth were assessed through above- and belowground measurements. The proportion of ectomycorrhizal root tips and ectomycorrhizal community composition did not vary as a function of earthworm species or density. Similarly, exotic earthworms had no significant effect on spruce seedling growth or survival.

Transdimensional approximate Bayesian computation for inference on invasive species models with latent variables of unknown dimension

Accurate information on patterns of introduction and spread of non-native species is essential for making predictions and management decisions. In many cases, estimating unknown rates of introduction and spread from observed data requires evaluating intractable variable-dimensional integrals. In general, inference on the large class of models containing latent variables of large or variable dimension precludes the use of exact sampling techniques. Approximate Bayesian computation (ABC) methods provide an alternative to exact sampling but rely on inefficient conditional simulation of the latent variables. To accomplish this task efficiently, a new transdimensional Monte Carlo sampler is developed for approximate Bayesian model inference and used to estimate rates of introduction and spread for the non-native earthworm species Dendrobaena octaedra (Savigny) along roads in the boreal forest of northern Alberta. Using low and high estimates of introduction and spread rates, the extent of earthworm invasions in northeastern Alberta is simulated to project the proportion of suitable habitat invaded in the year following data collection.

Effects of an ecosystem engineer on belowground movement of microarthropods.

Ecosystem engineers affect other species by changing physical environments. Such changes may influence movement of organisms, particularly belowground where soil permeability can restrict dispersal. We investigated whether earthworms, iconic ecosystem engineers, influence microarthropod movement. Our experiment tested whether movement is affected by tunnels (i.e., burrows), earthworm excreta (mucus, castings), or earthworms themselves. Earthworm burrows form tunnel networks that may facilitate movement. This effect may be enhanced by excreta, which could provide resources for microarthropods moving along the network. Earthworms may also promote movement via phoresy. Conversely, negative effects could occur if earthworms alter predator-prey relationships or change competitive interactions between microarthropods. We used microcosms consisting of a box connecting a “source” container in which microarthropods were present and a “destination” container filled with autoclaved soil. Treatments were set up within the boxes, which also contained autoclaved soil, as follows: 1) control with no burrows; 2) artificial burrows with no excreta; 3) abandoned burrows with excreta but no earthworms; and 4) earthworms (Lumbricus rubellus) present in burrows. Half of the replicates were sampled once after eight days, while the other half were sampled repeatedly to examine movement over time. Rather than performing classical pairwise comparisons to test our hypotheses, we used AICc to assess support for three competing models (presence of tunnels, excreta, and earthworms). More individuals of Collembola, Mesostigmata, and all microarthropods together dispersed when tunnels were present. Models that included excreta and earthworms were less well supported. Total numbers of dispersing Oribatida and Prostigmata+Astigmata were not well explained by any models tested. Further research is needed to examine the impact of soil structure and ecosystem engineering on movement belowground, as the substantial increase in movement of some microarthropods when corridors were present suggests these factors can strongly affect colonization and community assembly.

Red list of a black box

To the Editor — It has recently been announced that for the first time the Federal Agency for Nature Conservation (BfN) Red List (a regional red list of threatened species in Germany) includes groups of soil invertebrates, namely earthworms, millipedes and centipedes1. Although these taxa already appear in very small numbers on other regional red lists (http://www.nationalredlist.org/) and the global IUCN Red List (http:// www.iucnredlist.org/), the taxonomic bias towards more charismatic species means that these understudied soil invertebrates are under-represented2 (Fig. 1). However, more worrying is the lack of information regarding the threats faced by these species. Of the 47 earthworm species assessed for the BfN Red List based on occurrence data, the most common status was Least Concern (22; although 14 of the 47 earthworm species were assessed as Extremely Rare); however, there are virtually no data on longor short-term population trends or risks faced1. For example, very little is known about the effects of human impacts, such as land-use change and climate change, on below-ground communities3, especially compared with above-ground organisms, highlighting the urgent need for more information. The lack of available soil biodiversity data results in under-representation in many biodiversity databases and synthesis analyses4,5. Existing databases often (1) have few data on soil organisms (for example, the PREDICTS database contains just under 1% of all described annelids6, whereas BioTIME4 contains no soil invertebrate time-series data); (2) are not global7; or (3) concentrate on a small subset of soil taxa8. We strongly advocate for data-mobilization initiatives focused on soil biodiversity, in order to address large-scale questions9. Such synthetic analyses can be useful in answering key questions as to how soil biodiversity might respond to anthropogenic impacts2,3, and if the response differs from those seen in above-ground biodiversity10. Given the importance of local biodiversity for ecosystem services and function, determining whether local biodiversity is declining (a hotly debated topic11), both aboveand below-ground2, is crucial in sustaining human well-being12. Mobilizing the necessary information and data on the ‘black box’ of soil biodiversity will require large collaborative initiatives. In addition, increasing the representation of the hidden biota on national and global red lists will help raise the awareness of policymakers as well as the general public, ideally resulting in increased funding for assessments and research in order to better understand changes in this underexplored biodiversity that is so critical for human well-being. ❐

Root Foraging Influences Plant Growth Responses to Earthworm Foraging

Interactions among the foraging behaviours of co-occurring animal species can impact population and community dynamics; the consequences of interactions between plant and animal foraging behaviours have received less attention. In North American forests, invasions by European earthworms have led to substantial changes in plant community composition. Changes in leaf litter have been identified as a critical indirect mechanism driving earthworm impacts on plants. However, there has been limited examination of the direct effects of earthworm burrowing on plant growth. Here we show a novel second pathway exists, whereby earthworms (Lumbricus terrestris L.) impact plant root foraging. In a mini-rhizotron experiment, roots occurred more frequently in burrows and soil cracks than in the soil matrix. The roots of Achillea millefolium L. preferentially occupied earthworm burrows, where nutrient availability was presumably higher than in cracks due to earthworm excreta. In contrast, the roots of Campanula rotundifolia L. were less likely to occur in burrows. This shift in root behaviour was associated with a 30% decline in the overall biomass of C. rotundifolia when earthworms were present. Our results indicate earthworm impacts on plant foraging can occur indirectly via physical and chemical changes to the soil and directly via root consumption or abrasion and thus may be one factor influencing plant growth and community change following earthworm invasion. More generally, this work demonstrates the potential for interactions to occur between the foraging behaviours of plants and soil animals and emphasizes the importance of integrating behavioural understanding in foraging studies involving plants.

Global gaps in soil biodiversity data

To the Editor — Soil biodiversity represents a major terrestrial biodiversity pool, supports key ecosystem services and is under pressure from human activities1. Yet soil biodiversity has been neglected from many global biodiversity assessments and policies. This omission is undoubtedly related to the paucity of comprehensive information on soil biodiversity, particularly on larger spatial scales. Information on belowground species distributions, population trends, endemism and threats to belowground diversity is important for conservation prioritization, but is practically non-existent. As a consequence, much of our understanding of global macroecological patterns in biodiversity, as well as mapping of global biodiversity hotspots, has been based on aboveground taxa (such as plants2) and has not considered the functionally vital, but less visible, biodiversity found in soil. We mapped the study sites from existing global datasets on soil biodiversity (soil macrofauna3, fungi4 and bacteria5) to examine key data gaps (Fig. 1). Our map indicates significant gaps in soil biodiversity data across northern latitudes, including most of Russia and Canada. Data are also lacking from much of central Asia and central Africa (for example, the Sahara Desert), as well as many tropical regions. The higher density of soil biodiversity sampling sites in Europe and the United States is similar to patterns observed for data on terrestrial bird, mammal and amphibian species6, as well as plants7. Yet, in such aboveground datasets, the gaps in understudied regions are much less pronounced than in the soil biodiversity datasets shown here. The comparative lack of soil biodiversity data across these regions limits our ability to examine global macroecological patterns and to quantify potential mismatches between aboveground and soil biodiversity. The potential for such mismatches (areas with high aboveground diversity, but low soil biodiversity, or vice versa) may be substantial, as evidence suggests that plant species richness declines more rapidly towards the North Pole than fungal species richness, which reaches a plateau4. Soil ecologists are increasingly conducting their own large-scale assessments (such as the African Soil Microbiology Project8) and additional databases on soil biodiversity are beginning to be developed9, in part through the Global Soil Biodiversity Initiative. However, increased efforts to fill these gaps and to compile additional global datasets on other soil taxa (for example, mesofauna) are needed to allow more detailed analyses of soil biodiversity on broad spatial scales. Of major concern is the lack of a global consensus on sampling strategies and methodological approaches to assess soil biodiversity, which in many cases makes it challenging to compare datasets directly. Furthermore, greater cooperation with conservation biologists and policymakers is needed to better integrate soil biodiversity into global policies. For instance, soil biodiversity should be more explicitly considered in the post-2020 global biodiversity framework10 that will follow the Strategic Plan for Biodiversity 2011–2020 and in future assessments of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services11. These evident gaps in soil biodiversity data restrict our ability to develop policies to protect soil biodiversity. We argue that addressing these data gaps will ultimately benefit human well-being1 and provide an impetus for increased policy-relevant research on soil biodiversity. ❐