Andrea Dávalos

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-consumptive Effects of Native Deer on Introduced Earthworm Abundance

Chronic ungulate herbivory impacts are well documented, consistently showing changes in plant community dynamics. In contrast, indirect ungulate effects on soil biota and processes are less well understood and idiosyncratic. Evidence suggests that increased deer abundance in northeastern North American forests may facilitate invasions by non-native earthworms and non-native plants through indirect non-consumptive processes. We sampled earthworm abundance using paired open and fenced plots (experimentally excluding deer) from 2008 to 2011 at 12 sites at West Point, NY and in 2013 at 21 additional sites across four states that varied in exclosure size and age since establishment. Fencing decreased earthworm abundance at West Point and in regional surveys. At West Point, negative effects of fencing on earthworm abundance decreased with soil pH and were stronger at sites dominated by native than non-native understory vegetation. Sites dominated by native vegetation had more acidic soils and lower earthworm abundance compared to sites dominated by non-native vegetation. In the regional survey, negative effects of fencing on earthworm abundance increased with time since fences were established, but effects were not affected by exclosure size or site location. We show unforeseen indirect effects of deer exclusion on earthworm populations. Results illustrate the need to account for complex interactive effects among co-occurring stressors, such as deer, earthworms, and non-native plants. Failures to account for these interactions will result in hidden treatments, will complicate interpretation of ecological experiments, and will create difficulties in designing appropriate management strategies aimed at reducing stressor effects.

Unexpected earthworm effects on forest understory plants

BackgroundIntroduced earthworms are widespread in forests of North America creating significant negative impacts on forest understory communities. However, much of the reported evidence for negative earthworm effects comes from field investigations either comparing invaded and non-invaded forests or across invasion fronts. While important, such work is rarely able to capture the true effect of earthworms on individual plant species because most forests in North America simultaneously face multiple stressors which may confound earthworm impacts.We used a mesocosm experiment to isolate effects of the anecic introduced earthworm, Lumbricus terrestris L. on seedlings of 14 native plant species representing different life form groups (perennial herb, graminoid, and tree).ResultsEarthworm presence did not affect survival, fertility or biomass of any of the seedling plant species tested over a 17-week period. However, L. terrestris presence significantly decreased growth of two sedges (Carex retroflexa Muhl. ex Willd. and Carex radiata (Wahlenb.) Small) by decreasing the number of culms.ConclusionsOur mesocosm results with seedlings contrast with field reports indicating extensive and significant negative effects of introduced earthworms on many mature native forbs, and positive effects on sedges. We suggest that earthworm impacts are context- and age-specific and that generalizations about their impacts are potentially misleading without considering and manipulating other associated factors.

The effects of flooding, plant traits, and predation on purple loosestrife leaf-beetles

Classical biological weed control is based on the premise that introducing specialized natural enemies from the native range re‐establishes herbivore control of plant invaders, ultimately leading to negative population growth rates. Evidence from past biocontrol programs suggests that herbivores are not solely responsible for shaping plant demography. Diverse environmental conditions in the introduced range may not only affect demography, but also influence top‐down control of target plants. We investigated how flooding affects impacts of predators (top‐down) and plant quality (bottom‐up) on performance of two leaf‐beetles, Galerucella calmariensis L. and Galerucella pusilla Duftschmid (Coleoptera: Chrysomelidae: Galerucini), released in North America as biocontrol agents of purple loosestrife, Lythrum salicaria L. (Lythraceae). Predation and flooding regime have been linked to low leaf‐beetle recruitment at sites where insects failed to attain outbreak populations. Predator exclusion experiments at adjacent flooded and non‐flooded sites indicated a positive effect of flooding on leaf‐beetle survival for all developmental stages, whereas predator exposure had little effect. There was no difference in predation rates at sites with successful or failed purple loosestrife control, questioning the importance of predation in limiting growth and impact of these biocontrol agents’ populations. Effect of flooding on purple loosestrife quality was evaluated in a common garden study where plants were grown under different flooding treatments. Plants grown in flooded soil had higher water content and lower tannic acid concentration than plants grown in well‐drained soil. Consistent with field observations, leaf‐beetle oviposition rate and survival were higher on flooded plants. Results indicate that both bottom‐up and top‐down forces operate on Galerucella populations, yet their relative strength is mediated by flooding regime. Ignoring intricacies of plant‐herbivore and trophic interactions in the introduced range appears to be a major handicap for the improvement of weed biocontrol programs.

An indicator approach to capture impacts of white-tailed deer and other ungulates in the presence of multiple associated stressors

We developed a standardized metric to measure impacts of high white-tailed deer populations using red oak (Quercus rubra) seedlings. Our “sentinel approach” showed that deer browse reduced oak seedling survival and growth far more than invasive plants or invasive earthworms. Our approach can be used in areas devoid of vegetation but under heavy deer browse pressure, and the method can be implemented by non-specialists.

Assessing plant community composition fails to capture impacts of white-tailed deer on native and invasive plant species

Excessive herbivory by native deer can reduce abundance of native vegetation and increase non-native vegetation, but how does the forest recover when deer are excluded or numbers are reduced? The expectation is that understory vegetation will return to a previously diverse condition, but this is not always the case. We found that community-level monitoring captured both change and lack of change in vegetation cover, height, species richness, and response of common species, but failed to capture response of uncommon species. In contrast, monitoring of target species favored by deer indicated increased plant size and reproduction when deer were reduced or excluded. We conclude that measuring individual plants (growth, flowering and reproductive success) provides a sensitive and powerful assessment of forest understory responses to deer management.