Invasive earthworms reduce chemical defense and increase herbivory and pathogen infection in native trees.

Plant monocultures growing for extended periods face severe losses of productivity. This phenomenon, known as ‘yield decline', is often caused by the accumulation of above‐ and below‐ground plant antagonists. The effectiveness of plant defences against antagonists might help explain differences in yield decline among species. Using a trait‐based approach, we studied the role of 20 physical and chemical defence traits of leaves and fine roots on yield decline of 4‐ and 18‐year‐old monocultures of 27 grassland species. We hypothesized that yield decline is lower for species with high defences, that root defences are better predictors of yield decline than leaf defences, and that in roots, physical defences better predict yield decline than chemical defences, while the reverse is true for leaves. We additionally hypothesized that the relationship between defences and yield decline increases with time and that species increasing the expression of defence traits after long‐term monoculture growth would suffer less yield decline. We summarized leaf and fine root defence traits using principal component analyses and analysed the relationship between the most informative components along with their temporal changes and monoculture yield decline. The significant predictors of yield decline were traits related to the so‐called collaboration gradient of the root economics space (specific root length and root diameter) as well as their temporal changes and traits related to the leaf physical vs chemical defence tradeoff (leaf dry matter, silicon and cellulose content, toughness and phytochemical diversity). We were unable to unequivocally identify the mechanisms relating the effect of those traits to yield decline as they could mediate plant responses to several stressors such as antagonist accumulation, nutrient depletion or drought. Further studies are needed to differentiate between these alternative mechanisms and to gain a comprehensive understanding of the drivers of yield decline in relation to root and leaf defence traits.

Indirect and direct effects of exotic earthworms on soil nutrient and carbon pools in North American temperate forests

Differences in soil nutrients beneath different tree species are often attributed to the impacts of species-level patterns of nutrient uptake and litter chemistry. However, in naturally established forests it is difficult to isolate tree species' influence on soil development from differences in underlying soil properties that can affect tree species establishment. To discern the impacts of tree species on soil properties, we investigated how Norway spruce (Picea abies (L.) H. Karst.), red oak (Quercus rubra L.), and sugar maple (Acer saccharum Marshall) influence the distribution of carbon, nitrogen, and calcium in a 67-year-old common garden. We expected these species would produce foliar litter with contrasting chemistry, resulting in corresponding variation in organic matter (OM) turnover and nutrient accumulation in soils. Instead, we found that forest floor mean residence time correlated negatively with earthworm density and did not correlate with any measurement of litter chemistry. Red oak exhibited the fastest OM turnover and highest earthworm densities and Norway spruce showed the greatest OM accumulation and fewest earthworms. These findings suggest that future changes in earthworm invasion and forest tree species composition may have strong implications for ecosystem nutrient cycling and retention.

Recent studies have shown that invasive earthworms can dramatically reduce native biodiversity, both above and below the ground. However, we still lack a synthetic understanding of the underlying mechanisms behind these changes, such as whether earthworm effects on soil chemical properties drive such relationships. Here, we investigated the effects of invasive earthworms on soil chemical properties (pH, water content, and the stocks and fluxes of carbon, nitrogen, and phosphorus) by conducting a meta-analysis. Invasive earthworms generally increased soil pH, indicating that the removal of organic layers and the upward transport of more base-rich mineral soil caused a shift in soil pH. Moreover, earthworms significantly decreased soil water content, suggesting that the burrowing activities of earthworms may have increased water infiltration of and/or increased evapotranspiration from soil. Notably, invasive earthworms had opposing effects on organic and mineral soil for carbon and nitrogen stocks, with decreases in organic, and increases in mineral soil. Nitrogen fluxes were higher in mineral soil, whereas fluxes in organic soil were not significantly affected by the presence of invasive earthworms, indicating that earthworms mobilize and redistribute nutrients among soil layers and increase overall nitrogen loss from the soil. Invasive earthworm effects on element stocks increased with ecological group richness only in organic soil. Earthworms further decreased ammonium stocks with negligible effects on nitrate stocks in organic soil, whereas they increased nitrate stocks but not ammonium stocks in mineral soil. Notably, all of these results were consistent across forest and grassland ecosystems underlining the generality of our findings. However, we found some significant differences between studies that were conducted in the field (observational and experimental settings) and in the lab, such as that the effects on soil pH decreased from field to lab settings, calling for a careful interpretation of lab findings. Our meta-analysis provides strong empirical evidence that earthworm invasion may lead to substantial changes in soil chemical properties and element cycling in soil. Furthermore, our results can help explain the dramatic effects of invasive earthworms on native biodiversity, for example, shifts towards the dominance of grass species over herbaceous ones, as shown by recent meta-analyses.

Although belowground invasive species are probably equally widespread and as important as their aboveground counterparts, they remain understudied, and their impacts are likely to be stronger when these invaders act as ecosystem engineers and differ functionally from native species. This is the case in regions historically devoid of native earthworms, such as parts of northern North America, which are now experiencing an invasion by European earthworms. Although invasive earthworms have been reported to have multiple consequences for native communities and ecosystem functioning, this knowledge is mostly based on observational studies, and the mechanisms underlying their cascading impacts need to be investigated. Here, we thus investigated the sequence of events, i.e., ecological cascades following earthworm invasion, that have rarely been studied before, in a two-year field experiment. We expected that the changes in soil abiotic properties observed following invasion would coincide with changes in plant community diversity and community trait composition, as well as in alterations in above- and belowground ecosystem functions. To test these hypotheses, we set up a field experiment that ran for two years in a forest in Alberta (Canada) to investigate soil properties and understory plant community composition in response to invasive earthworms. Our study shows that invasive European earthworms alter several soil abiotic properties (i.e., soil nutrient content, and pH) after two years of experiment. Invasive earthworm effects varied with soil depth for some soil properties (i.e., soil pH, water-stable aggregates, nitrogen, and microbial basal respiration), but we did not find any significant earthworm effect on soil water content, bulk density, or the total soil microbial biomass independently of the soil layer. Moreover, invasive earthworms did not affect plant community composition and only slightly affected community diversity in this short-term experiment. The minor changes observed in plant functional group composition are thus potentially the first signs of invasive-earthworm effects on plant communities. Our research provides experimental evidence that previously reported observational effects of invasive earthworms on soil properties are indeed causal and already significant after two years of invasion. These changes in soil properties are likely to have cascading effects on plant community composition, functional diversity, and ecosystem functioning, but such effects may take longer than two years to materialize.

Induced anti‐herbivore defences in plants can shape ecosystem structure and functions. Since these are known to be highly variable, quantifying their sources of variation remains important to understand their eco‐evolutionary roles. We conducted meta‐analysis of 647 experiments (paired control and treatment) from 192 studies to address sources of variation in induced anti‐herbivore defensive traits. This covered different agents of herbivory (insect, mammal and clipping), studies in greenhouse and in field settings, and covered 24 types of defence traits in 163 species from 50 families across 24 angiosperm orders. We used meta‐regression models—multi‐level random‐effects (MLREs) and robust variance estimators (RVEs)—to quantify variation due to study setting, herbivore type, chemical identity, angiosperm order, volatility, fertilization, and publication year as moderator variables. There were strong indications for publication bias in favour of large effect sizes, and studies with adequate sample size and precision were rare. Strength of induction was distributed uniformly over the phylogeny of 24 angiosperm orders. Stronger effects were reported from greenhouses than in field conditions, and induction was uninfluenced by herbivore type. Volatiles showed stronger response than non‐volatiles in greenhouses for insects. Biosynthetic precursors (e.g. jasmonates) and many defensive chemicals were induced in the greenhouse, but when measured in field conditions, they were unresponsive to herbivory and appear to be constitutive. Similar to constitutive response, induced responses were also unaffected by fertilization. Direction and magnitude of induction differ greatly from previous assessments as these have also changed over time, representing natural epistemological growth. A third of the variability was explained by moderators (marginal R 2 : chemical identity, angiosperm order, study setting, herbivore type and publication year); another third (conditional R 2 ) was attributed to the identity of individual studies and observations. Synthesis . Manipulative experiments reveal many intrinsic differences among defensive chemicals and traits. They suggest plants in greenhouses may respond very differently to herbivores from those in field conditions. Although biosynthetic pathways of chemical responses, their modes of action and their effects on herbivores are well‐understood, studies with greater statistical power under ecologically relevant settings are needed to discern induced and constitutive defences in how plants respond to their natural enemies

Recent studies document North American earthworm invasions and their profound effects on the structure of the soil profile, which is the habitat for soil microorganisms (mainly fungi and bacteria). Dramatic alterations made to these layers during earthworm invasion significantly change microbial community structure and therefore microbial activities such as C transformations. Understanding the impacts of earthworm invasion on the microbes themselves will give insight into earthworm effects on microbial activities. Bacterial and actinomycete communities in earthworm guts and casts have not been studied in environments recently invaded by earthworms. Earthworm invasion tended to decrease fungal species density and fungal species diversity and richness. The presence of earthworms decreased zygomycete species abundance probably due to disruption of fungal hyphae. Physical disruption of hyphae may also explain decreased mycorrhizal colonization rates, decreased mycorrhizal abundance and altered mycorrhizal morphology in the presence of earthworms. Mixing of organic layers into mineral soil during earthworm invasion tended to decrease microbial biomass in forest floor materials while increasing it in mineral soil. In newly invaded forest soils, microbial respiration and the metabolic quotient tended to decline. In forests where either the microbial community has had time to adapt to earthworm activities, or where the destruction of the forest floor is complete, as in invasions by the Asian Amynthas hawayanus, the presence of earthworms tends to increase the metabolic quotient indicating a shift to a smaller, more active microbial community.

The classical “low latitude–high defense” hypothesis is seldom supported by empirical evidence. In this context, we tested latitudinal patterns in the leaf defense traits of deciduous broadleaved (DB) and evergreen broadleaved (EGB) tree species, which are expected to affect herbivore diversity. We examined the co-occurrence of leaf defense traits (tannin and phenol content, leaf mechanical strength, leaf dry matter content, leaf mass per area, and leaf thickness) in 741 broadleaved tree species and their correlations with species geographical range in East Asian island flora. We discovered contrasting latitudinal defense strategy gradients in DB and EGB tree species. DB species employed chemical defenses (increasing tannin and phenol content) at higher latitudes and physical defenses (softer and thinner leaves) at lower latitudes, whereas EGB tree species exhibited opposite latitudinal defense patterns. The “low latitude high defense” hypothesis included a paradoxical aspect in chemical and physical defense traits across broadleaved tree species. To reconcile paradoxical defense strategies along the latitudinal gradient, we conclude that interactive correlations among leaf traits are controlled by leaf longevity, which differs between DB and EGB tree species.

Clarifying the functional consequences of intraspecific trait variability in response to interacting trophic levels would provide a significant improvement in our understanding of above‐ground–below‐ground linkages. In particular, the effects of grazing on plant traits may translate into altered litter quality, with potentially important consequences for litter‐feeding decomposers. Plant and litter variability in response to grazing is expected to depend on soil fertility levels, with tolerance and defensive strategies more commonly expressed on fertile and poorer soils, respectively. However, how grazing and fertility interactively alter litter quality and palatability to detritivores has not been explored yet. We conducted a cafeteria experiment with three common millipede (Diplopoda) species feeding on leaf litter from two plant species, the grass Bromopsis erecta and the forb Potentilla verna. Each millipede was offered a binary choice between litter types produced by the same plant species, but sampled in plots with distinct herbivory and fertilization status: litter originating from grazed areas or from 1‐year sheep exclosures, both in native areas and in adjacent paddocks that received chemical N and P fertilization, as well as litter from a 25‐year sheep exclosures in the native area. We found that fertilization and herbivore exclusion interactively affected Bromopsis litter quality and palatability, whereas Potentilla was much less affected. Bromopsis litter palatability was not affected by grazing when litter was collected in native plots, except for the long‐term exclosure which led to low palatability. In contrast, and in line with our expectations, herbivory was associated with much higher palatability in fertilized plots. The changes in palatability were associated with important alterations of litter quality. Overall, our study demonstrates that intraspecific variation in litter can have profound consequences for soil functioning. It emphasizes the role of grazing as a key, but plant species‐specific factor controlling litter intraspecific variability, and its complex interaction with soil fertility level. Moreover, our results advocate for a better understanding of the response of the different organisms involved in the decomposition process, in particular litter‐feeding macro‐detritivores. We encourage future studies aiming at disentangling the various and complex relationships between above‐ground processes such as herbivory and soil functioning.

Invasions of European earthworms into the forests of northern North America are causing dramatic changes in forest floor structure, vegetation communities, biogeochemical cycling, and site hydrology. However, long-term studies on the effects of invasive earthworms are limited because little data exist on the timing and rate of earthworm invasion at specific sites. We successfully used tree rings to identify the timing of earthworm invasions and the effects of earthworm activity on the Acer saccharum overstory of two recently invaded sites in northern Minnesota, thereby establishing a method to date earthworm invasions at other sites. In addition to identifying a tree-ring signature related to earthworm invasion, we found trees growing in invaded conditions were more sensitive to drought than trees growing in earthworm-free conditions. Increased drought sensitivity by A. saccharum has important implications for possible range shifts under climate change scenarios that include increasing drought frequency and severity.

We performed a comparative analysis of defensive and nutritional plant traits responsible for differential herbivory in a series of experimental feeding trials with generalist herbivores. We measured three defensive traits (leaf strength, leaf mass per unit area and endophytic fungal infection) and two nutritional traits (foliar nitrogen and water) for 26 native and eight non-native plant species from coastal California shrublands. Our feeding trials involved three species of generalist herbivore (beet armyworm, cabbage looper and the garden snail) in two types of laboratory feeding trial (single plant species and preference tests). All traits were significantly related to the amount of leaf area consumed, with foliar nitrogen followed by leaf strength explaining most of the variation in herbivore damage. Defensive and nutritional traits were tightly correlated with one another. These correlations were still apparent after incorporation of the phylogenetic relationships of species using independent contrasts, suggesting that there has been repeated selection for certain trait combinations. Non-native species had lower defensive traits and greater nutrient content and therefore experienced greater herbivory damage than natives. Poorly defended, nutrient-rich species (like most of the non-natives in our study) may be better suited for rapid growth and nutrient acquisition, thus reducing the cost of replenishing leaf material lost to herbivores.

Over the last century, nonnative earthworms have invaded forests of the Great Lakes region of North America. Although a growing body of scientific research has documented short-term changes associated with invasive earthworms, there is little research describing the effects of invasive earthworms over multiple decades. To investigate the long-term effects of invasive earthworms on forests, sites sampled in the past need to be classified as wormed or unwormed when originally sampled. However, this is often difficult to accomplish because field methods for sampling earthworms have only recently been developed, and the few historical permanent sites available for resampling largely do not have past information about earthworm presence or absence. Although historic sites lack data on invasive earthworm presence, many of these sites do have information about soil horizon thickness. Therefore, soil horizons can potentially be used as an indicator of the presence or absence of invasive earthworms. In this paper we developed a logistic regression generalized linear model to classify 40 sugar maple-basswood sites in the Chippewa National Forest of Northern Minnesota as wormed or unwormed (i.e., presence or relative absence of earthworms, respectively). A model using the thickness of the O horizon as a predictor variable correctly classified 93% of sites resampled in 2017 as wormed or unwormed. This result suggests we can predict which sugar maple-basswood stands in the Chippewa National Forest were wormed in the past. By comparing historic conditions to those present today, we can then analyze the long-term effects of invasive earthworms.

QuestionsHow did past land use and conifer plantation affect understorey plant communities? What plant traits explain understorey vegetation response to agricultural past land use and coniferous plantation?LocationForest of Orléans (50 000 ha), Loiret, north‐central France.MethodsCanopy cover, herb layer composition, litter and soil properties were measured in 80 100 m2 plots sampled in plantations of Pinus sylvestris or P. nigra vs natural regenerations of Quercus petraea and Q. robur along a gradient of forest continuity (using historical maps and aerial photos from 1840, 1949 and 2006). We related 15 plant traits to past land use and tree species using RLQ and fourth‐corner analyses.ResultsThe magnitude of past land use effect largely exceeded that of coniferous plantation. Post‐agricultural forests, even 150 yr after afforestation, differed from ancient forests in soil properties (thinner humus layer, higher P content, higher pH and lower C/N ratio) and plant traits. Ancient forests hosted more forest core species, stress‐tolerant, competitive species and bryophytes, but fewer ruderals, annuals/biennials, shrubs and trees and nutrient‐demanding species, and had lower SLA and higher LDMC. Conifer plantations had a thicker humus layer, lower pH and higher C/N ratio than deciduous forests, and hosted more light‐demanding species but less forest core species. Importantly, differences in soil and plant traits between conifer plantations and naturally regenerated deciduous stands were discernible in both recent and ancient forests, indicating that tree species lastingly influence ecosystem functioning.ConclusionsPast land use and coniferous plantation resulted in different understorey plant communities and traits under pine plantations and naturally regenerated oak stands. These differences were driven through soil acidification, litter decomposition rate, light conditions, canopy development, soil disturbance, stand management and dispersal and recruitment limitations. Coniferous plantations slowed down the recovery of post‐agricultural forests to ancient deciduous forest conditions. Applying natural regeneration and favouring native deciduous tree species thus helps recreate or maintain ancient forest plant communities.

Earthworm invasion shifts trophic niches of ground-dwelling invertebrates in a North American forest

As ecosystem engineers, invasive earthworms are one of the main drivers of plant community changes in North American forests previously devoid of earthworms. One explanation for these community changes is the effects of earthworms on the reproduction, recruitment, and development of plant species. However, few studies have investigated functional trait responses of native plants to earthworm invasion to explain the mechanisms underlying community changes. In a mesocosm (Ecotron) experiment, we set up a plant community composed of two herb and two grass species commonly found in northern North American forests under two earthworm treatments (presence vs. absence). We measured earthworm effects on above- and belowground plant biomass and functional traits after 3 months of experiment. Our results showed that earthworm presence did not significantly affect plant community biomass and cover. Furthermore, only four out of the fifteen above- and belowground traits measured were affected by earthworm presence. While some traits, such as the production of ramets, the carbon and nitrogen content of leaves, responded similarly between and within functional groups in the presence or absence of earthworms, we observed opposite responses for other traits, such as height, specific leaf area, and root length within some functional groups in the presence of earthworms. Plant trait responses were thus species-specific, although the two grass species showed a more pronounced response to earthworm presence with changes in their leaf traits than herb species. Overall, earthworms affected some functional traits related to resource uptake abilities of plants and thus could change plant competition outcomes over time, which could be an explanation of plant community changes observed in invaded ecosystems.