Woody invaders are more highly colonized by arbuscular mycorrhizal fungi than congeneric native species.

PREMISE: Invasive species tend to possess acquisitive plant traits that support fast growth and strong competitive ability. However, the relevance of symbioses with arbuscular mycorrhizal fungi (AMF) to the fast growing, acquisitive strategy of invasive species is still unclear. METHODS: We measured AMF colonization in roots of five congeneric pairs of invasive and native eastern North American woody species (10 species total; 4 lianas, 6 shrubs) that were grown in a monoculture common garden experiment in Syracuse, NY. We then examined the relationships of AMF colonization to above and belowground traits of these species. RESULTS: Total AMF colonization and arbuscule colonization were greater in invasive compared to native woody species, a pattern that was more distinct in congeneric shrubs than congeneric lianas. The level of AMF colonization was also positively correlated with traits indicative of rapid plant growth and nutrient uptake. CONCLUSIONS: The concordance of a resource-acquisitive strategy with higher AMF colonization suggests that symbioses with AMF may be part of the strategy by which invasive woody plants of eastern North America are able to maintain fast growth rates and outcompete their native counterparts.

Fast but steady: An integrated leaf-stem-root trait syndrome for woody forest invaders.

Successful control and prevention of biological invasions depend on identifying traits of non-native species that promote fitness advantages in competition with native species. Here, we show that, among 76 native and non-native woody plants of deciduous forests of North America, invaders express a unique functional syndrome that combines high metabolic rate with robust leaves of longer lifespan and a greater duration of annual carbon gain, behaviours enabled by seasonally plastic xylem structure and rapid production of thin roots. This trait combination was absent in all native species examined and suggests the success of forest invaders is driven by a novel resource-use strategy. Furthermore, two traits alone-annual leaf duration and nuclear DNA content-separated native and invasive species with 93% accuracy, supporting the use of functional traits in invader risk assessments. A trait syndrome reflecting both fast growth capacity and understorey persistence may be a key driver of forest invasions.

Impacts of experimental defoliation on native and invasive saplings: are native species more resilient to canopy disturbance?

Many non-native, invasive woody species in mesic forests of North America are both shade tolerant and more productive than their native counterparts, but their ability to tolerate disturbances remains unclear. In particular, complete defoliation associated with herbivory and extreme weather events may have larger impacts on invaders if natives maintain greater resource reserves to support regrowth. On the other hand, invaders may be more resilient to partial defoliation by means of upregulation of photosynthesis or may be better able to take advantage of canopy gaps to support refoliation. Across a light gradient, we measured radial growth, new leaf production, non-structural carbohydrates (NSCs), chlorophyll content and survival in response to varying levels of defoliation in saplings of two native and two invasive species that commonly co-occur in deciduous forests of Eastern North America. Individuals were subjected to one of the four leaf removal treatments: no-defoliation controls, 50% defoliation over three growing seasons, 100% defoliation over one growing season and 100% defoliation over two growing seasons. Contrary to our hypothesis, native and invasive species generally did not differ in defoliation responses, although invasive species experienced more pronounced decreases in leaf chlorophyll following full defoliation and native species' survival was more dependent on light availability. Radial growth progressively decreased with increasing defoliation intensity, and refoliation mass was largely a function of sapling size. Survival rates for half-defoliated saplings did not differ from controls (90% of saplings survived), but survival rates in fully defoliated individuals over one and two growing seasons were reduced to 45 and 15%, respectively. Surviving defoliated saplings generally maintained control NSC concentrations. Under high light, chlorophyll concentrations were higher in half-defoliated saplings compared with controls, which may suggest photosynthetic upregulation. Our results indicate that native and invasive species respond similarly to defoliation, despite the generally faster growth strategy of invaders.

Functional shifts in leaves of woody invaders of deciduous forests between their home and away ranges.

Temperate forests are widely invaded by shade-tolerant shrubs and trees, including those of Eastern North America (ENA). However, it remains unknown whether these invaders are 'preadapted' for success in their new ranges due to unique aspects of their evolutionary history or whether selection due to enemy release or other postintroduction processes have driven rapid evolution in the invaded range. We sampled leaf traits of populations of woody understory invaders across light gradients in their native range in Japan and in their invaded ENA range to examine potential phenotypic shifts related to carbon gain and nitrogen use between ranges. We also measured leaf traits in three co-occurring ENA native shrub species. In their invaded range, invaders invested significantly less in leaf chlorophyll content (both per unit leaf mass and area) compared with native range populations of the same species, yet maintained similar rates of photosynthesis in low light. In addition, compared with ENA natives, ENA invaders displayed greater trait variation in response to increasing light availability (forest edges, gaps), giving them a potential advantage over ENA natives in a variety of light conditions. We conclude that, for this group of species, newly evolved phenotypes in the invaded range are more important than preadaptation for their success as shade-tolerant forest invaders.

Phenological mismatch with trees reduces wildflower carbon budgets.

Interacting species can respond differently to climate change, causing unexpected consequences. Many understorey wildflowers in deciduous forests leaf out and flower in the spring when light availability is the highest before overstorey canopy closure. Therefore, different phenological responses by understorey and overstorey species to increased spring temperature could have significant ecological implications. Pairing contemporary data with historical observations initiated by Henry David Thoreau (1850s), we found that overstorey tree leaf out is more responsive to increased spring temperature than understorey wildflower phenology, resulting in shorter periods of high light in the understorey before wildflowers are shaded by tree canopies. Because of this overstorey-understorey mismatch, we estimate that wildflower spring carbon budgets in the northeastern United States were 12-26% larger during Thoreau's era and project a 10-48% reduction during this century. This underappreciated phenomenon may have already reduced wildflower fitness and could lead to future population declines in these ecologically important species.

Carbon gain phenologies of spring-flowering perennials in a deciduous forest indicate a novel niche for a widespread invader.

Strategies of herbaceous species in deciduous forests are often characterized by the timing of life history phases (e.g. emergence, flowering, leaf senescence) relative to overstory tree canopy closure. Although springtime photosynthesis is assumed to account for the majority of their annual carbon budgets, the 12-month photosynthetic trajectories of forest herbs have not been quantified. We measured the temporal dynamics of carbon assimilation for seven native herbaceous perennials and the biennial Alliaria petiolata, a widespread invader in eastern North American forests. We assessed the relative importance of spring, summer, and autumn to species-level annual carbon budgets. Spring-emerging species showed significant variation in carbon assimilation patterns. High spring irradiance before canopy closure accounted for 39-100% of species-level annual carbon assimilation, but summer and autumn accounted for large proportions of some species' carbon budgets (up to 58% and 19%, respectively). Alliaria was phenologically unique, taking advantage both autumn and spring irradiance. Although spring-emerging understory species are often expected to rely on early-season irradiance, our results highlight interspecific differences and the importance of mid-late season carbon gain. Phenological strategies of forest herbs are a continuum rather than discrete categories, and invasive species may follow strategies that are underrepresented in the native flora.

To spend or to save? Assessing energetic growth-storage tradeoffs in native and invasive woody plants.

Many non-native woody plants invade low-light forest understories but differ from native species in leaf phenology and seasonality of photosynthesis. It is unknown whether such differences in assimilation patterns are due to contrasting strategies of energy allocation. In a group of native and invasive species in Eastern North America, we hypothesized that invaders employ a grow-first strategy, prioritizing allocation to new structural biomass over carbon storage compared to native congeners. We also hypothesized that species producing a single spring leaf flush exhibit a more conservative carbon storage strategy than species with continuous leaf production. We measured sugar and starch concentrations (non-structural carbohydrates; NSCs) in spring and fall in the stems and roots of 39 species of native and non-native shrubs in a common garden, and compared these to patterns of leaf production across species. Native species had higher soluble sugar concentrations than invaders, but invaders tended to store more root starch in spring. We found no difference in leaf production between natives and invaders. Determinate species had more soluble sugars than indeterminate species but had lower root starch. We found no relationship between aboveground productivity and carbon storage. Our results suggest that closely related species with contrasting evolutionary histories have different carbon storage strategies, although not necessarily in relation to their growth potential. The higher soluble sugar concentrations of native species may reflect their evolutionary response to historical disturbances, or different interactions with soil microbes, while increased spring root starch in invaders may support fine root or fruit production.

Temperature accelerates the rate fields become forests.

Secondary succession, the postdisturbance transition of herbaceous to woody-dominated ecosystems, occurs faster at lower latitudes with important ramifications for ecosystem processes. This pattern could be driven by the direct effect of temperature on tree growth; however, an alternative mechanism is tree-herb competition, which may be more intense in more fertile northern soils. We manipulated soil fertility and herbaceous species composition in identical experiments at six sites spanning the Eastern United States (30-43° N) and monitored the growth and survival of four early successional trees. Tree seedling mass 2 years after sowing was strongly associated with site differences in mean growing season temperature, regardless of species or soil treatment. The effect of temperature was twofold: seedlings grew faster in response to warmer site temperatures, but also due to the reduction of competitive interference from the herbaceous community, which was inhibited in warmer sites. Our results suggest that increasing temperatures will promote a faster transition of fields to forests in temperate ecosystems.

Spring predictability explains different leaf-out strategies in the woody floras of North America, Europe and East Asia.

Intuitively, interannual spring temperature variability (STV) should influence the leaf-out strategies of temperate zone woody species, with high winter chilling requirements in species from regions where spring warming varies greatly among years. We tested this hypothesis using experiments in 215 species and leaf-out monitoring in 1585 species from East Asia (EA), Europe (EU) and North America (NA). The results reveal that species from regions with high STV indeed have higher winter chilling requirements, and, when grown under the same conditions, leaf out later than related species from regions with lower STV. Since 1900, STV has been consistently higher in NA than in EU and EA, and under experimentally short winter conditions NA species required 84% more spring warming for bud break, EU ones 49% and EA ones only 1%. These previously unknown continental-scale differences in phenological strategies underscore the need for considering regional climate histories in global change models.

Links between soil microbial communities and plant traits in a species-rich grassland under long-term climate change.

Climate change can influence soil microorganisms directly by altering their growth and activity but also indirectly via effects on the vegetation, which modifies the availability of resources. Direct impacts of climate change on soil microorganisms can occur rapidly, whereas indirect effects mediated by shifts in plant community composition are not immediately apparent and likely to increase over time. We used molecular fingerprinting of bacterial and fungal communities in the soil to investigate the effects of 17 years of temperature and rainfall manipulations in a species-rich grassland near Buxton, UK. We compared shifts in microbial community structure to changes in plant species composition and key plant traits across 78 microsites within plots subjected to winter heating, rainfall supplementation, or summer drought. We observed marked shifts in soil fungal and bacterial community structure in response to chronic summer drought. Importantly, although dominant microbial taxa were largely unaffected by drought, there were substantial changes in the abundances of subordinate fungal and bacterial taxa. In contrast to short-term studies that report high resistance of soil fungi to drought, we observed substantial losses of fungal taxa in the summer drought treatments. There was moderate concordance between soil microbial communities and plant species composition within microsites. Vector fitting of community-weighted mean plant traits to ordinations of soil bacterial and fungal communities showed that shifts in soil microbial community structure were related to plant traits representing the quality of resources available to soil microorganisms: the construction cost of leaf material, foliar carbon-to-nitrogen ratios, and leaf dry matter content. Thus, our study provides evidence that climate change could affect soil microbial communities indirectly via changes in plant inputs and highlights the importance of considering long-term climate change effects, especially in nutrient-poor systems with slow-growing vegetation.

Invaders do not require high resource levels to maintain physiological advantages in a temperate deciduous forest.

Non-native, invasive plants are commonly typified by trait strategies associated with high resource demands and plant invasions are often thought to be dependent upon site resource availability or disturbance. However, the invasion of shade-tolerant woody species into deciduous forests of the Eastern United States seems to contradict such generalization, as growth in this ecosystem is strongly constrained by light and, secondarily, nutrient stress. In a factorial manipulation of light and soil nitrogen availability, we established an experimental resource gradient in a secondary deciduous forest to test whether three common, woody, invasive species displayed increased metabolic performance and biomass production compared to six co-occurring woody native species, and whether these predicted differences depend upon resource supply. Using hierarchical Bayesian models of photosynthesis that included leaf trait effects, we found that invasive species exhibited functional strategies associated with higher rates of carbon gain. Further, invader metabolic and growth-related attributes were more responsive to increasing light availability than those of natives, but did not fall below average native responses even in low light. Surprisingly, neither group showed direct trait or growth responses to soil N additions. However, invasive species showed increased photosynthetic nitrogen use efficiencies with decreasing N availability, while that of natives remained constant. Although invader advantage over natives was amplified in higher resource conditions in this forest, our results indicate that some invasive species can maintain physiological advantages over co-occurring natives regardless of resource conditions.

More of the same? In situ leaf and root decomposition rates do not vary between 80 native and nonnative deciduous forest species.

Invaders often have greater rates of production and produce more labile litter than natives. The increased litter quantity and quality of invaders should increase nutrient cycling through faster litter decomposition. However, the limited number of invasive species that have been included in decomposition studies has hindered the ability to generalize their impacts on decomposition rates. Further, previous decomposition studies have neglected roots. We measured litter traits and decomposition rates of leaves for 42 native and 36 nonnative woody species, and those of fine roots for 23 native and 25 nonnative species that occur in temperate deciduous forests throughout the Eastern USA. Among the leaf and root traits that differed between native and invasive species, only leaf nitrogen was significantly associated with decomposition rate. However, native and nonnative species did not differ systematically in leaf and root decomposition rates. We found that among the parameters measured, litter decomposer activity was driven by litter chemical quality rather than tissue density and structure. Our results indicate that litter decomposition rate per se is not a pathway by which forest woody invasive species affect North American temperate forest soil carbon and nutrient processes.

Rapid genetic divergence in response to 15 years of simulated climate change.

Genetic diversity may play an important role in allowing individual species to resist climate change, by permitting evolutionary responses. Our understanding of the potential for such responses to climate change remains limited, and very few experimental tests have been carried out within intact ecosystems. Here, we use amplified fragment length polymorphism (AFLP) data to assess genetic divergence and test for signatures of evolutionary change driven by long-term simulated climate change applied to natural grassland at Buxton Climate Change Impacts Laboratory (BCCIL). Experimental climate treatments were applied to grassland plots for 15 years using a replicated and spatially blocked design and included warming, drought and precipitation treatments. We detected significant genetic differentiation between climate change treatments and control plots in two coexisting perennial plant study species (Festuca ovina and Plantago lanceolata). Outlier analyses revealed a consistent signature of selection associated with experimental climate treatments at individual AFLP loci in P. lanceolata, but not in F. ovina. Average background differentiation at putatively neutral AFLP loci was close to zero, and genomewide genetic structure was associated neither with species abundance changes (demography) nor with plant community-level responses to long-term climate treatments. Our results demonstrate genetic divergence in response to a suite of climatic environments in reproductively mature populations of two perennial plant species and are consistent with an evolutionary response to climatic selection in P. lanceolata. These genetic changes have occurred in parallel with impacts on plant community structure and may have contributed to the persistence of individual species through 15 years of simulated climate change at BCCIL.

Plant ecology. Worldwide evidence of a unimodal relationship between productivity and plant species richness.

The search for predictions of species diversity across environmental gradients has challenged ecologists for decades. The humped-back model (HBM) suggests that plant diversity peaks at intermediate productivity; at low productivity few species can tolerate the environmental stresses, and at high productivity a few highly competitive species dominate. Over time the HBM has become increasingly controversial, and recent studies claim to have refuted it. Here, by using data from coordinated surveys conducted throughout grasslands worldwide and comprising a wide range of site productivities, we provide evidence in support of the HBM pattern at both global and regional extents. The relationships described here provide a foundation for further research into the local, landscape, and historical factors that maintain biodiversity.

Fine-scale belowground species associations in temperate grassland.

Evaluating how belowground processes contribute to plant community dynamics is hampered by limited information on the spatial structure of root communities at the scale that plants interact belowground. In this study, roots were mapped to the nearest one mm and molecularly identified by species on vertical (0-15 cm deep) surfaces of soil blocks excavated from dry and mesic grasslands in Yellowstone National Park (YNP) to examine the spatial relationships among species at the scale that roots interact. Our results indicated that average interspecific root - root distances for the majority of species were within a distance (3 mm) that roots have been shown to compete for resources. Most species placed their roots at random, although low root numbers for many species probably led to overestimating the occurrence of random patterns. According to theory, we expected that most of the remaining species would segregate their root systems to avoid competition. Instead we found that more species aggregated than segregated from others. Based on previous investigations, we hypothesize that species aggregate to increase uptake of water, nitrogen and/or phosphorus made available by neighbouring roots, or as a consequence of a reduction in the pathogenicity of soil biota growing in multispecies mixtures. Our results indicate that YNP grassland root communities are organized as closely interdigitating networks of species that potentially can support strong interactions among many species combinations. Future root research should address the prevalence and functional consequences of species aggregation across plant communities.

Contrasting growth phenology of native and invasive forest shrubs mediated by genome size.

Examination of the significance of genome size to plant invasions has been largely restricted to its association with growth rate. We investigated the novel hypothesis that genome size is related to forest invasions through its association with growth phenology, as a result of the ability of large-genome species to grow more effectively through cell expansion at cool temperatures. We monitored the spring leaf phenology of 54 species of eastern USA deciduous forests, including native and invasive shrubs of six common genera. We used new measurements of genome size to evaluate its association with spring budbreak, cell size, summer leaf production rate, and photosynthetic capacity. In a phylogenetic hierarchical model that differentiated native and invasive species as a function of summer growth rate and spring budbreak timing, species with smaller genomes exhibited both faster growth and delayed budbreak compared with those with larger nuclear DNA content. Growth rate, but not budbreak timing, was associated with whether a species was native or invasive. Our results support genome size as a broad indicator of the growth behavior of woody species. Surprisingly, invaders of deciduous forests show the same small-genome tendencies of invaders of more open habitats, supporting genome size as a robust indicator of invasiveness.

Community functional responses to soil and climate at multiple spatial scales: when does intraspecific variation matter?

Despite increasing evidence of the importance of intraspecific trait variation in plant communities, its role in community trait responses to environmental variation, particularly along broad-scale climatic gradients, is poorly understood. We analyzed functional trait variation among early-successional herbaceous plant communities (old fields) across a 1200-km latitudinal extent in eastern North America, focusing on four traits: vegetative height, leaf area, specific leaf area (SLA), and leaf dry matter content (LDMC). We determined the contributions of species turnover and intraspecific variation to between-site functional dissimilarity at multiple spatial scales and community trait responses to edaphic and climatic factors. Among-site variation in community mean trait values and community trait responses to the environment were generated by a combination of species turnover and intraspecific variation, with species turnover making a greater contribution for all traits. The relative importance of intraspecific variation decreased with increasing geographic and environmental distance between sites for SLA and leaf area. Intraspecific variation was most important for responses of vegetative height and responses to edaphic compared to climatic factors. Individual species displayed strong trait responses to environmental factors in many cases, but these responses were highly variable among species and did not usually scale up to the community level. These findings provide new insights into the role of intraspecific trait variation in plant communities and the factors controlling its relative importance. The contribution of intraspecific variation to community trait responses was greatest at fine spatial scales and along edaphic gradients, while species turnover dominated at broad spatial scales and along climatic gradients.

Links between belowground and aboveground resource-related traits reveal species growth strategies that promote invasive advantages.

Belowground processes are rarely considered in comparison studies of native verses invasive species. We examined relationships between belowground fine root production and lifespan, leaf phenology, and seasonal nitrogen dynamics of Lonicera japonica (non-native) versus L. sempervirens (native) and Frangula alnus (non-native) versus Rhamnus alnifolia (native), over time. First and second order fine roots were monitored from 2010 to 2012 using minirhizotron technology and rhizotron windows. 15N uptake of fine roots was measured across spring and fall seasons. Significant differences in fine root production across seasons were seen between Lonicera species, but not between Frangula and Rhamnus, with both groups having notable asynchrony in regards to the timing of leaf production. Root order and the number of root neighbors at the time of root death were the strongest predictors of root lifespan of both species pairs. Seasonal 15N uptake was higher in spring than in the fall, which did not support the need for higher root activity to correspond with extended leaf phenology. We found higher spring 15N uptake in non-native L. japonica compared to native L. sempervirens, although there was no difference in 15N uptake between Frangula and Rhamnus species. Our findings indicate the potential for fast-growing non-native Lonicera japonica and Frangula alnus to outcompete native counterparts through differences in biomass allocation, root turnover, and nitrogen uptake, however evidence that this is a general strategy of invader dominance is limited.

Contrasting xylem vessel constraints on hydraulic conductivity between native and non-native woody understory species.

We examined the hydraulic properties of 82 native and non-native woody species common to forests of Eastern North America, including several congeneric groups, representing a range of anatomical wood types. We observed smaller conduit diameters with greater frequency in non-native species, corresponding to lower calculated potential vulnerability to cavitation index. Non-native species exhibited higher vessel-grouping in metaxylem compared with native species, however, solitary vessels were more prevalent in secondary xylem. Higher frequency of solitary vessels in secondary xylem was related to a lower potential vulnerability index. We found no relationship between anatomical characteristics of xylem, origin of species and hydraulic conductivity, indicating that non-native species did not exhibit advantageous hydraulic efficiency over native species. Our results confer anatomical advantages for non-native species under the potential for cavitation due to freezing, perhaps permitting extended growing seasons.