Temporal dynamics of Grime's CSR strategies in plant communities during 60 years of succession.

Grime's competitive, stress-tolerant, ruderal (CSR) theory predicts a shift in plant communities from ruderal to stress-tolerant strategies during secondary succession. However, this fundamental tenet lacks empirical validation using long-term continuous successional data. Utilizing a 60-year longitudinal data of old-field succession, we investigated the community-level dynamics of plant strategies over time. Our findings reveal that while plant communities generally transitioned from ruderal to stress-tolerant strategies during succession, initial abandonment conditions crucially shaped early successional strategies, leading to varied strategy trajectories across different fields. Furthermore, we found a notable divergence in the CSR strategies of alien and native species over succession. Initially, alien and native species exhibited similar ruderal strategies, but in later stages, alien species exhibited higher ruderal and lower stress tolerance compared to native species. Overall, our findings underscore the applicability of Grime's predictions regarding temporal shifts in CSR strategies depending on both initial community conditions and species origin.

Genetic relatedness can alter the strength of plant-soil interactions.

PREMISE: Intraspecific variation may play a key role in shaping the relationships between plants and their interactions with soil microbial communities. The soil microbes of individual plants can generate intraspecific variation in the responsiveness of the plant offspring, yet have been much less studied. To address this need, we explored how the relatedness of seedlings from established clones of Solidago altissima altered the plant-soil interactions of the seedlings. METHODS: Seedlings of known parentage were generated from a series of 24 clones grown in a common garden. Seedlings from these crosses were inoculated with soils from maternal, paternal, or unrelated clones and their performance compared to sterilized control inocula. RESULTS: We found that soil inocula influenced by S. altissima clones had an overall negative effect on seedling biomass. Furthermore, seedlings inoculated with maternal or paternal soils tended to experience larger negative effects than seedlings inoculated with unrelated soils. However, there was much variation among individual crosses, with not all responding to relatedness. CONCLUSIONS: Our data argue that genetic relatedness to the plant from which the soil microbial inoculum was obtained may cause differential impacts on establishing seedlings, encouraging the regeneration of non-kin adjacent to established clones. Such intraspecific variation represents a potentially important source of heterogeneity in plant-soil microbe interactions with implications for maintaining population genetic diversity.

(-)-Loliolide is a general signal of plant stress that activates jasmonate-related responses.

The production of defensive metabolites in plants can be induced by signaling chemicals released by neighboring plants. Induction is mainly known from volatile aboveground signals, with belowground signals and their underlying mechanisms largely unknown. We demonstrate that (-)-loliolide triggers defensive metabolite responses to competitors, herbivores, and pathogens in seven plant species. We further explore the transcriptional responses of defensive pathways to verify the signaling role of (-)-loliolide in wheat and rice models with well-known defensive metabolites and gene systems. In response to biotic and abiotic stressors, (-)-loliolide is produced and secreted by roots. This, in turn, induces the production of defensive compounds including phenolic acids, flavonoids, terpenoids, alkaloids, benzoxazinoids, and cyanogenic glycosides, regardless of plant species. (-)-Loliolide also triggers the expression of defense-related genes, accompanied by an increase in the concentration of jasmonic acid and hydrogen peroxide (H2 O2 ). Transcriptome profiling and inhibitor incubation indicate that (-)-loliolide-induced defense responses are regulated through pathways mediated by jasmonic acid, H2 O2 , and Ca 2+ . These findings argue that (-)-loliolide functions as a common belowground signal mediating chemical defense in plants. Such perception-dependent plant chemical defenses will yield critical insights into belowground signaling interactions.

Root placement patterns in allelopathic plant-plant interactions.

Plants actively respond to their neighbors by altering root placement patterns. Neighbor-modulated root responses involve root detection and interactions mediated by root-secreted functional metabolites. However, chemically mediated root placement patterns and their underlying mechanisms remain elusive. We used an allelopathic wheat model system challenged with 60 target species to identify root placement responses in window rhizobox experiments. We then tested root responses and their biochemical mechanisms in incubation experiments involving the addition of activated carbon and functional metabolites with amyloplast staining and auxin localization in roots. Wheat and each target species demonstrated intrusive, avoidant or unresponsive root placement, resulting in a total of nine combined patterns. Root placement patterns were mediated by wheat allelochemicals and (-)-loliolide signaling of neighbor species. In particular, (-)-loliolide triggered wheat allelochemical production that altered root growth and placement, degraded starch grains in the root cap and induced uneven distribution of auxin in target species roots. Root placement patterns in wheat-neighbor interactions were perception dependent and species dependent. Signaling (-)-loliolide induced the production and release of wheat allelochemicals that modulated root placement patterns. Therefore, root placement patterns are generated by both signaling chemicals and allelochemicals in allelopathic plant-plant interactions.

Root-secreted (-)-loliolide modulates both belowground defense and aboveground flowering in Arabidopsis and tobacco.

Plant defense, growth, and reproduction can be modulated by chemicals emitted from neighboring plants, mainly via volatile aboveground signals. However, belowground signals and their underlying control mechanisms are largely unknown. Here, we experimentally demonstrate that the root-secreted carotenoid (-)-loliolide mediates both defensive and reproductive responses in wild-type Arabidopsis, a carotenoid-deficient Arabidopsis mutant (szl1-1), and tobacco (Nicotiana benthamiana). Wild-type Arabidopsis plants flower later than szl1-1, and they secrete (-)-loliolide into the soil, whereas szl1-1 roots do not. When Arabidopsis and tobacco occur together, wild-type Arabidopsis induces nicotine production and defense-related gene expression in tobacco, whereas szl1-1 impairs this induction but accelerates tobacco flowering. Furthermore, nicotine production and the expression of the key genes involved in nicotine biosynthesis (QPT, PMT1), plant defense (CAT1, SOD1, PR-2a, PI-II, TPI), and flowering (AP1, LFY, SOC1, FT3, FLC) are differently regulated by incubation with wild-type Arabidopsis and szl1-1 root exudates or (-)-loliolide. In particular, (-)-loliolide up-regulated flowering suppressors (FT3 and FLC) and transiently down-regulated flowering stimulators (AP1 and SOC1), delaying tobacco flowering. Therefore, root-secreted (-)-loliolide modulates plant belowground defense and aboveground flowering, yielding critical insights into plant-plant signaling interactions.

Positive interactions of native species melt invasional meltdown over long-term plant succession.

Positive interactions have been hypothesised to influence plant community dynamics and species invasions. However, their prevalence and importance relative to negative interactions remain unclear to understand community change and invasibility. We examined pairwise biotic interactions using over 50 years of successional data to assess the prevalence of positive interactions and their effects on each focal species (either native or exotic). We found that positive interactions were widespread and the relative frequency of positive and negative interactions varied with establishment stage and between native and exotic species. Specifically, positive interactions were more frequent during early establishment and less frequent at later stages. Positive interactions involving native species were more frequent and stronger than those between exotic species, reducing the importance of invasional meltdown on succession. Our study highlights the role of positive native interactions in shielding communities from biological invasion and enhancing the potential for long-term resilience.

Root exudate signals in plant-plant interactions.

Plant-to-plant signalling is a key mediator of interactions among plant species. Plants can perceive and respond to chemical cues emitted from their neighbours, altering survival and performance, impacting plant coexistence and community assembly. An increasing number of studies indicate root exudates as key players in plant-to-plant signalling. Root exudates mediate root detection and behaviour, kin recognition, flowering and production, driving inter- and intra-specific facilitation in cropping systems and mixed-species plantations. Altered interactions may be attributed to the signalling components within root exudates. Root ethylene, strigolactones, jasmonic acid, (-)-loliolide and allantoin are signalling chemicals that convey information on local conditions in plant-plant interactions. These root-secreted signalling chemicals appear ubiquitous in plants and trigger a series of belowground responses inter- and intra-specifically, involving molecular events in biosynthesis, secretion and action. The secretion of root signals, mainly mediated by ATP-binding cassette transporters, is critical. Root-secreted signalling chemicals and their molecular mechanisms are rapidly revealing a multitude of fascinating plant-plant interactions. However, many root signals, particularly species-specific signals and their underlying mechanisms, remain to be uncovered due to methodological limitations and root-soil interactions. A thorough understanding of root-secreted chemical signals and their mechanisms will offer many ecological implications and potential applications for sustainable agriculture.

Intra-specific kin recognition contributes to inter-specific allelopathy: A case study of allelopathic rice interference with paddy weeds.

Species interactions and mechanisms affect plant coexistence and community assembly. Despite increasing knowledge of kin recognition and allelopathy in regulating inter-specific and intra-specific interactions among plants, little is known about whether kin recognition mediates allelopathic interference. We used allelopathic rice cultivars with the ability for kin recognition grown in kin versus non-kin mixtures to determine their impacts on paddy weeds in field trials and a series of controlled experiments. We experimentally tested potential mechanisms of the interaction via altered root behaviour, allelochemical production and resource partitioning in the dominant weed competitor, as well as soil microbial communities. We consistently found that the establishment and growth of paddy weeds were more inhibited by kin mixtures compared to non-kin mixtures. The effect was driven by kin recognition that induced changes in root placement, altered weed carbon and nitrogen partitioning, but was associated with similar soil microbial communities. Importantly, genetic relatedness enhanced the production of intrusive roots towards weeds and reduced the production of rice allelochemicals. These findings suggest that relatedness allows allelopathic plants to discriminate their neighbouring collaborators (kin) or competitors and adjust their growth, competitiveness and chemical defense accordingly.

Fine-root traits are linked to species dynamics in a successional plant community.

Despite the importance of fine roots for the acquisition of soil resources such as nitrogen and water, the study of linkages between traits and both population and community dynamics remains focused on aboveground traits. We address this gap by investigating associations between belowground traits and metrics of species dynamics. Our analysis included 85 species from a long-term data set on the transition from old field to forest in eastern North America (the Buell-Small Succession Study) and the new Fine-Root Ecology Database. Given the prominent roles of life form (woody vs. non-woody) and species origin (native vs. exotic) in defining functional relationships, we also assessed whether traits or their relationships with species dynamics differed for these groups. Species that reached their peak abundance early in succession had fine-root traits corresponding to resource acquisitive strategies (i.e., they were thinner, less dense, and had higher nitrogen concentrations) while species that peaked progressively later had increasingly conservative strategies. In addition to having more acquisitive root traits than native species, exotics diverged from the above successional trend, having consistently thinner fine roots regardless of the community context. Species with more acquisitive fine-root morphologies typically had faster rates of abundance increase and achieved their maximal rates in fewer years. Decreasing soil nutrient availability and increasing belowground competition may become increasingly strong filters in successional communities, acting on root traits to promote a transition from acquisitive to conservative foraging. However, disturbances that increase light and soil resource availability at local scales may allow acquisitive species, especially invasive exotics, to continue colonizing late into the community transition to forest.

Infection patterns and molecular data reveal host and tissue specificity of Posthodiplostomum species in centrarchid hosts.

Posthodiplostomum minimum utilizes a three-host life cycle with multiple developmental stages. The metacercarial stage, commonly known as 'white grub', infects the visceral organs of many freshwater fishes and was historically considered a host generalist due to its limited morphological variation among a wide range of hosts. In this study, infection data and molecular techniques were used to evaluate the host and tissue specificity of Posthodiplostomum metacercariae in centrarchid fishes. Eleven centrarchid species from three genera were collected from the Illinois portion of the Ohio River drainage and necropsied. Posthodiplostomum infection levels differed significantly by host age, host genera and infection locality. Three Posthodiplostomum spp. were identified by DNA sequencing, two of which were relatively common within centrarchid hosts. Both common species were host specialists at the genus level, with one species restricted to Micropterus hosts and the other preferentially infecting Lepomis. Host specificity is likely dictated by physiological compatibility and deviations from Lepomis host specificity may be related to host hybridization. Posthodiplostomum species also differed in their utilization of host tissues. Neither common species displayed strong genetic structure over the scale of this study, likely due to their utilization of bird definitive hosts.

Nutrient foraging strategies are associated with productivity and population growth in forest shrubs.

Background and Aims: Temperate deciduous forest understoreys are experiencing widespread changes in community composition, concurrent with increases in rates of nitrogen supply. These shifts in plant abundance may be driven by interspecific differences in nutrient foraging (i.e. conservative vs. acquisitive strategies) and, thus, adaptation to contemporary nutrient loading conditions. This study sought to determine if interspecific differences in nutrient foraging could help explain patterns of shrub success and decline in eastern North American forests. Methods: Using plants grown in a common garden, fine root traits associated with nutrient foraging were measured for six shrub species. Traits included the mean and skewness of the root diameter distribution, specific root length (SRL), C:N ratio, root tissue density, arbuscular mycorrhizal colonization and foraging precision. Above- and below-ground productivity were also determined for the same plants, and population growth rates were estimated using data from a long-term study of community dynamics. Root traits were compared among species and associations among root traits, measures of productivity and rates of population growth were evaluated. Key Results: Species fell into groups having thick or thin root forms, which correspond to conservative vs. acquisitive nutrient foraging strategies. Interspecific variation in root morphology and tissue construction correlated with measures of productivity and rates of cover expansion. Of the four species with acquisitive traits, three were introduced species that have become invasive in recent decades, and the fourth was a weedy native. In contrast, the two species with conservative traits were historically dominant shrubs that have declined in abundance in eastern North American forests. Conclusions: In forest understoreys of eastern North America, elevated nutrient availability may impose a filter on species success in addition to above-ground processes such as herbivory and overstorey canopy conditions. Shrubs that have root traits associated with rapid uptake of soil nutrients may be more likely to increase in abundance, while species without such traits may be less likely to keep pace with more productive species.

Soil microbial communities alter leaf chemistry and influence allelopathic potential among coexisting plant species.

While both plant-soil feedbacks and allelochemical interactions are key drivers of plant community dynamics, the potential for these two drivers to interact with each other remains largely unexplored. If soil microbes influence allelochemical production, this would represent a novel dimension of heterogeneity in plant-soil feedbacks. To explore the linkage between soil microbial communities and plant chemistry, we experimentally generated soil microbial communities and evaluated their impact on leaf chemical composition and allelopathic potential. Four native perennial old-field species (two each of Aster and Solidago) were grown in pairwise combination with each species' soil microbial community as well as a sterilized inoculum. We demonstrated unequivocally that variation in soil microbial communities altered leaf chemical fingerprints for all focal plant species and also changed their allelopathic potential. Soil microbes reduced allelopathic potential in bioassays by increasing germination 25-54% relative to sterile control soils in all four species. Plants grown with their own microbial communities had the lowest allelopathic potential, suggesting that allelochemical production may be lessened when growing with microbes from conspecifics. The allelopathic potential of plants grown in congener and confamilial soils was indistinguishable from each other, indicating an equivalent response to all non-conspecific microbial communities within these closely related genera. Our results clearly demonstrated that soil microbial communities cause changes in leaf tissue chemistry that altered their allelopathic properties. These findings represent a new mechanism of plant-soil feedbacks that may structure perennial plant communities over very small spatial scales that must be explored in much more detail.

Convergence and divergence in a long-term old-field succession: the importance of spatial scale and species abundance.

Whether plant communities in a given region converge towards a particular stable state during succession has long been debated, but rarely tested at a sufficiently long time scale. By analysing a 50-year continuous study of post-agricultural secondary succession in New Jersey, USA, we show that the extent of community convergence varies with the spatial scale and species abundance classes. At the larger field scale, abundance-based dissimilarities among communities decreased over time, indicating convergence of dominant species, whereas incidence-based dissimilarities showed little temporal tend, indicating no sign of convergence. In contrast, plots within each field diverged in both species composition and abundance. Abundance-based successional rates decreased over time, whereas rare species and herbaceous plants showed little change in temporal turnover rates. Initial abandonment conditions only influenced community structure early in succession. Overall, our findings provide strong evidence for scale and abundance dependence of stochastic and deterministic processes over old-field succession.

Species colonisation, not competitive exclusion, drives community overdispersion over long-term succession.

Ecological communities often transition from phylogenetic and functional clustering to overdispersion over succession as judged by space-for-time substitution studies. Such a pattern has been generally attributed to the increase in competitive exclusion of closely related species with similar traits through time, although colonisation and extinction have rarely been examined. Using 44 years of uninterrupted old-field succession in New Jersey, USA, we confirmed that phylogenetic and functional clustering decreased as succession unfolded, but the transition was largely driven by colonisation. Early colonists were closely related and functionally similar to residents, while later colonists became less similar to the species present. Extirpated species were generally more distantly related to residents than by chance, or exhibited random phylogenetic/functional patterns, and their relatedness to residents was not associated with time. These results provide direct evidence that the colonisation of distant relatives, rather than extinction of close relatives, drives phylogenetic and functional overdispersion over succession.

The effects of phylogenetic relatedness on invasion success and impact: deconstructing Darwin's naturalisation conundrum.

Darwin's naturalisation conundrum describes the paradox that the relatedness of exotic species to native residents could either promote or hinder their success through opposing mechanisms: niche pre-adaptation or competitive interactions. Previous studies focusing on single snapshots of invasion patterns have provided support to both sides of the conundrum. Here, by examining invasion dynamics of 480 plots over 40 years, we show that exotic species more closely related to native species were more likely to enter, establish and dominate the resident communities, and that native residents more closely related to these successful exotics were more likely to go locally extinct. Therefore, non-random displacement of natives during invasion could weaken or even reverse the negative effects of exotic-native phylogenetic distances on invasion success. The scenario that exotics more closely related to native residents are more successful, but tend to eliminate their closely related natives, may help to reconcile the 150-year-old conundrum.

Scale-dependent changes in ecosystem temporal stability over six decades of succession.

A widely assumed, but largely untested, tenet in ecology is that ecosystem stability tends to increase over succession. We rigorously test this idea using 60-year continuous data of old field succession across 480 plots nested within 10 fields. We found that ecosystem temporal stability increased over succession at the larger field scale (γ stability) but not at the local plot scale (α stability). Increased spatial asynchrony among plots within fields increased γ stability, while temporal increases in species stability and decreases in species asynchrony offset each other, resulting in no increase in α stability at the local scale. Furthermore, we found a notable positive diversity-stability relationship at the larger but not local scale, with the increased γ stability at the larger scale associated with increasing functional diversity later in succession. Our results emphasize the importance of spatial scale in assessing ecosystem stability over time and how it relates to biodiversity.

Spatiotemporal dynamics of lianas during 50 years of succession to temperate forest.

Although they are important components of forest communities, the general ecology and spatiotemporal patterns of temperate lianas during forest regeneration are largely unknown. The dependence of lianas on other plants for physical support makes them a potentially important driver of community dynamics. We examined 50 years of vegetation data from an old-field succession study to determine the dynamics and community controls on liana expansion within the Piedmont region of New Jersey, USA. Four lianas, Lonicera japonica, Parthenocissus quinquefolia, Toxicodendron radicans, and Vitis spp., occurred in enough abundance for detailed analyses. In general, liana cover peaked during mid-succession (20-30 years post-abandonment) when community composition was mostly herbaceous with scattered trees and shrubs. Liana cover began to decrease as trees became dominant and the canopy closed. Temporal patterns of cover dynamics of abundant species indicated three early- and one late-successional liana species within the community. In contrast to cover, frequency of lianas increased throughout succession, indicating that liana populations persisted despite dramatic declines in cover for the three early-successional species. Temporal dynamics between native and nonnative lianas were similar but spatially distinct as cover of native species dispersed and expanded near the forest edge while the nonnative species preferentially grew far from the forest. These dynamics indicate that successional processes may ultimately lead to the decline of most lianas. However, the persistence of lianas as high numbers of suppressed individuals suggests that they may rebound quickly following canopy disturbance.

Inoculum handling alters the strength and direction of plant-microbe interactions.

The pooling of soil samples in plant-microbe interaction studies is commonly employed, but the impact of sample handling has rarely been explored experimentally. Concerns have been raised that sample pooling may reduce biological variation leading to inflated type I errors or may alter the magnitude of microbial effects observed, invalidating the results achieved. To assess the impact of inocula pooling on plant-microbe interactions, we examined the reciprocal influence of unpooled and pooled soil microbial inocula on growth of Solidago altissima and Schizachyrium scoparium, with and without inoculum sterilization. Soil pooling had no effect on the variance among replicates in either plant species. However, pooling dramatically altered the magnitude and direction of microbial impacts on plant performance. Pooling of Solidago altissima soil increased the antagonistic effects on growth of both target species. In contrast, pooling of Schizachyrium scoparium soil shifted impacts on Solidago altissima from effectively neutral to slightly positive. Pooling in this system altered both the strength and direction of plant-microbe interactions relative to unpooled soils. Therefore soil mixing should be avoided when the research goal is to determine naturally occurring interaction strengths, even within a single habitat.

Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals.

Plant neighbor detection and response strategies are important mediators of interactions among species. Despite increasing knowledge of neighbor detection and response involving plant volatiles, less is known about how soil-borne signaling chemicals may act belowground in plant-plant interactions. Here, we experimentally demonstrate neighbor detection and allelopathic responses between wheat and 100 other plant species via belowground signaling. Wheat can detect both conspecific and heterospecific neighbors and responds by increasing allelochemical production. Furthermore, we show that (-)-loliolide and jasmonic acid are present in root exudates from a diverse range of species and are able to trigger allelochemical production in wheat. These findings suggest that root-secreted (-)-loliolide and jasmonic acid are involved in plant neighbor detection and allelochemical response and may be widespread mediators of belowground plant-plant interactions.

Native and exotic plant species exhibit similar population dynamics during succession.

A growing body of literature has led to the debate in invasion biology whether exotic species perform within communities differently than native taxa due to inherent advantages. To address this issue, the population dynamics of native and exotic plant species were assessed from a 48-year record of permanent plot data from the Hutcheson Memorial Forest Center (New Jersey, USA) to determine rate of increase, lag time, maximum frequency, and the year of peak frequency. Overall, native and exotic species exhibited very similar population dynamics. Rates of increase and length of lag times were similar between native and exotic taxa but were strongly influenced by plant life form. Short-lived species were characterized by rapid population growth rates and short lag times. Growth rates decreased and lag times increased with species longevity. Overall, correlations between population metrics were the same in native and exotic taxa, suggesting similar trade-offs in life history patterns. The one difference observed was that, in native species, peak frequency was negatively associated with the year of peak frequency (i.e., early-successional species tended to become more abundant), while there was no relationship in exotic species. These analyses show that exotic species behave in essentially the same way as native taxa within dynamic communities. This suggests that abundant native and exotic plant species are exploiting the same range of ecological strategies resulting in similar roles within communities.