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.

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.

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.

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.

Extended leaf phenology and the autumn niche in deciduous forest invasions.

The phenology of growth in temperate deciduous forests, including the timing of leaf emergence and senescence, has strong control over ecosystem properties such as productivity and nutrient cycling, and has an important role in the carbon economy of understory plants. Extended leaf phenology, whereby understory species assimilate carbon in early spring before canopy closure or in late autumn after canopy fall, has been identified as a key feature of many forest species invasions, but it remains unclear whether there are systematic differences in the growth phenology of native and invasive forest species or whether invaders are more responsive to warming trends that have lengthened the duration of spring or autumn growth. Here, in a 3-year monitoring study of 43 native and 30 non-native shrub and liana species common to deciduous forests in the eastern United States, I show that extended autumn leaf phenology is a common attribute of eastern US forest invasions, where non-native species are extending the autumn growing season by an average of 4 weeks compared with natives. In contrast, there was no consistent evidence that non-natives as a group show earlier spring growth phenology, and non-natives were not better able to track interannual variation in spring temperatures. Seasonal leaf production and photosynthetic data suggest that most non-native species capture a significant proportion of their annual carbon assimilate after canopy leaf fall, a behaviour that was virtually absent in natives and consistent across five phylogenetic groups. Pronounced differences in how native and non-native understory species use pre- and post-canopy environments suggest eastern US invaders are driving a seasonal redistribution of forest productivity that may rival climate change in its impact on forest processes.

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.

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.

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.

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.

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.

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.

Resource-use strategies of native and invasive plants in Eastern North American forests.

Studies in disturbed, resource-rich environments often show that invasive plants are more productive than co-occurring natives, but with similar physiological tradeoffs. However, in resource-limited habitats, it is unclear whether native and invasive plants have similar metabolic constraints or if invasive plants are more productive per unit resource cost - that is, use resources more efficiently. Using a common garden to control for environment, we compared leaf physiological traits relating to resource investments, carbon returns, and resource-use efficiencies in 14 native and 18 nonnative invasive species of common genera found in Eastern North American (ENA) deciduous forest understories, where growth is constrained by light and nutrient limitation. Despite greater leaf construction and nitrogen costs, invaders exhibited greater instantaneous photosynthetic energy-use efficiency (PEUE) and marginally greater photosynthetic nitrogen-use efficiency (PNUE). When integrated over leaf lifespan (LL), these differences were magnified. Differences in efficiency were driven by greater productivity per unit leaf investment, as invaders exhibited both greater photosynthetic abilities and longer LL. Our results indicate that woody understory invaders in ENA forests are not constrained to the same degree by leaf-based metabolic tradeoffs as the native understory flora. These strategy differences could be attributable to pre-adaptation in the native range, although other explanations are possible.

Drivers of secondary succession rates across temperate latitudes of the Eastern USA: climate, soils, and species pools.

Climate change is widely expected to induce large shifts in the geographic distribution of plant communities, but early successional ecosystems may be less sensitive to broad-scale climatic trends because they are driven by interactions between species that are only indirectly related to temperature and rainfall. Building on a biogeographic analysis of secondary succession rates across the Eastern Deciduous Forest (EDF) of North America, we describe an experimental study designed to quantify the relative extent to which climate, soil properties, and geographic species pools drive variation in woody colonization rates of old fields across the EDF. Using a network of five sites of varying soil fertility spanning a latitudinal gradient from central New York to northern Florida, we added seeds of nine woody pioneer species to recently tilled old fields and monitored first-year growth and survivorship. Results suggest seedlings of southern woody pioneer species are better able to quickly establish in fields after abandonment, regardless of climate regime. Sites of lower soil fertility also exhibited faster rates of seedling growth, likely due to the slower development of the successional herbaceous community. We suggest that climate plays a relatively minor role in community dynamics at the onset of secondary succession, and that site edaphic conditions are a stronger determinant of the rate at which ecosystems develop to a woody-dominated state. More experimental research is necessary to determine the nature of the herbaceous-woody competitive interface and its sensitivity to environmental conditions.

Long-term resistance to simulated climate change in an infertile grassland.

Climate shifts over this century are widely expected to alter the structure and functioning of temperate plant communities. However, long-term climate experiments in natural vegetation are rare and largely confined to systems with the capacity for rapid compositional change. In unproductive, grazed grassland at Buxton in northern England (U.K.), one of the longest running experimental manipulations of temperature and rainfall reveals vegetation highly resistant to climate shifts maintained over 13 yr. Here we document this resistance in the form of: (i) constancy in the relative abundance of growth forms and maintained dominance by long-lived, slow-growing grasses, sedges, and small forbs; (ii) immediate but minor shifts in the abundance of several species that have remained stable over the course of the experiment; (iii) no change in productivity in response to climate treatments with the exception of reduction from chronic summer drought; and (iv) only minor species losses in response to drought and winter heating. Overall, compositional changes induced by 13-yr exposure to climate regime change were less than short-term fluctuations in species abundances driven by interannual climate fluctuations. The lack of progressive compositional change, coupled with the long-term historical persistence of unproductive grasslands in northern England, suggests the community at Buxton possesses a stabilizing capacity that leads to long-term persistence of dominant species. Unproductive ecosystems provide a refuge for many threatened plants and animals and perform a diversity of ecosystem services. Our results support the view that changing land use and overexploitation rather than climate change per se constitute the primary threats to these fragile ecosystems.

Community and ecosystem effects of intraspecific genetic diversity in grassland microcosms of varying species diversity.

Studies of whether plant community structure and ecosystem properties depend on the genetic diversity of component populations have been largely restricted to species monocultures and have involved levels of genetic differentiation that do not necessarily correspond to that exhibited by neighboring mature individuals in the field. We established experimental communities of varying intraspecific genetic diversity, using genotypes of eight species propagated from clonal material of individuals derived from a small (100-m2) limestone grassland community, and tested whether genetic diversity (one, four, and eight genotypes per species) influenced community composition and annual aboveground productivity across communities of one, four, and eight species. Eight-species communities were represented by common grass, sedge, and forb species, and four- and one-species communities were represented by four graminoids and the dominant grass Festuca ovina, respectively. After three years of community development, there was a marginal increase of species diversity with increased genetic diversity in four- and eight-species communities, and genetic diversity altered the performance of genotypes in monospecific communities of F. ovina. However, shifts in composition from genetic diversity were not sufficient to alter patterns of community productivity. Neighborhood models describing pairwise interactions between species indicated that genetic diversity decreased the intensity of competition between species in four-species mixtures, thereby promoting competitive equivalency and enhancing species equitability. In F. ovina monocultures, neighborhood models revealed both synergistic and antagonistic interactions between genotypes that were reduced in intensity on more stressful shallow soils. Although the dependence of F. ovina genotype performance on neighborhood genetic composition did not influence total productivity, such dependence was sufficient to uncouple genotype performance in genetic mixtures and monocultures. Our results point to an important connection between local genetic diversity and species diversity in this species-rich ecosystem but suggest that such community-level dependence on genetic diversity may not feedback to ecosystem productivity.

Grassland root communities: species distributions and how they are linked to aboveground abundance.

There is little comprehensive information on the distribution of root systems among coexisting species, despite the expected importance of those distributions in determining the composition and diversity of plant communities. This gap in knowledge is particularly acute for grasslands, which possess large numbers of species with morphologically indistinguishable roots. In this study we adapted a molecular method, fluorescent fragment length polymorphism, to identify root fragments and determine species root distributions in two grasslands in Yellowstone National Park (YNP). Aboveground biomass was measured, and soil cores (2 cm in diameter) were collected to depths of 40 cm and 90 cm in an upland, dry grassland and a mesic, slope-bottom grassland, respectively, at peak foliar expansion. Cores were subdivided, and species that occurred in each 10-cm interval were identified. The results indicated that the average number of species in 10-cm intervals (31 cm3) throughout the sampled soil profile was 3.9 and 2.8 species at a dry grassland and a mesic grassland, respectively. By contrast, there was an average of 6.7 and 14.1 species per 0.5 m2, determined by the presence of shoot material, at dry and mesic sites, respectively. There was no relationship between soil depth and number of species per 10-cm interval in either grassland, despite the exponential decline of root biomass with soil depth at both sites. There also was no relationship between root frequency (i.e., the percentage of samples in which a species occurred) and soil depth for the vast majority of species at both sites. The preponderance of species were distributed throughout the soil profile at both sites. Assembly analyses indicated that species root occurrences were randomly assorted in all soil intervals at both sites, with the exception that Festuca idahoensis segregated from Artemisia tridentata and Pseudoroegnaria spicata in 10-20 cm soil at the dry grassland. Root frequency throughout the entire sampled soil profile was positively associated with shoot biomass among species. Together these results indicated the importance of large, well-proliferated root systems in establishing aboveground dominance. The findings suggest that spatial belowground segregation of species probably plays a minor role in fostering resource partitioning and species coexistence in these YNP grasslands.

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.