A trait-based framework linking the soil metabolome to plant-soil feedbacks.

By modifying the biotic and abiotic properties of the soil, plants create soil legacies that can affect vegetation dynamics through plant-soil feedbacks (PSF). PSF are generally attributed to reciprocal effects of plants and soil biota, but these interactions can also drive changes in the identity, diversity and abundance of soil metabolites, leading to more or less persistent soil chemical legacies whose role in mediating PSF has rarely been considered. These chemical legacies may interact with microbial or nutrient legacies to affect species coexistence. Given the ecological importance of chemical interactions between plants and other organisms, a better understanding of soil chemical legacies is needed in community ecology. In this Viewpoint, we aim to: highlight the importance of belowground chemical interactions for PSF; define and integrate soil chemical legacies into PSF research by clarifying how the soil metabolome can contribute to PSF; discuss how functional traits can help predict these plant-soil interactions; propose an experimental approach to quantify plant responses to the soil solution metabolome; and describe a testable framework relying on root economics and seed dispersal traits to predict how plant species affect the soil metabolome and how they could respond to soil chemical legacies.

Among-population variation in drought responses is consistent across life stages but not between native and non-native ranges.

Understanding how widespread species adapt to variation in abiotic conditions across their ranges is fundamental to ecology. Insight may come from studying how among-population variation (APV) in the common garden corresponds with the environmental conditions of source populations. However, there are no such studies comparing native vs non-native populations across multiple life stages. We examined APV in the performance and functional traits of 59 Conyza canadensis populations, in response to drought, across large aridity gradients in the native (North America) and non-native (Eurasia) ranges in three experiments. Our treatment (dry vs wet) was applied at the recruitment, juvenile, and adult life stages. We found contrasting patterns of APV in drought responses between the two ranges. In the native range, plant performance was less reduced by drought in populations from xeric than mesic habitats, but such relationship was not apparent for non-native populations. These range-specific patterns were consistent across the life stages. The weak adaptive responses of non-native populations indicate that they can become highly abundant even without complete local adaptation to abiotic environments and suggest that long-established invaders may still be evolving to the abiotic environment. These findings may explain lag times in invasions and raise concern about future expansions.

Network motifs involving both competition and facilitation predict biodiversity in alpine plant communities.

Biological diversity depends on multiple, cooccurring ecological interactions. However, most studies focus on one interaction type at a time, leaving community ecologists unsure of how positive and negative associations among species combine to influence biodiversity patterns. Using surveys of plant populations in alpine communities worldwide, we explore patterns of positive and negative associations among triads of species (modules) and their relationship to local biodiversity. Three modules, each incorporating both positive and negative associations, were overrepresented, thus acting as "network motifs." Furthermore, the overrepresentation of these network motifs is positively linked to species diversity globally. A theoretical model illustrates that these network motifs, based on competition between facilitated species or facilitation between inferior competitors, increase local persistence. Our findings suggest that the interplay of competition and facilitation is crucial for maintaining biodiversity.

Rapid evolutionary trade-offs between resistance to herbivory and tolerance to abiotic stress in an invasive plant.

Release from enemies can lead to rapid evolution in invasive plants, including reduced metabolic investment in defence. Conversely, reassociation with enemies leads to renewed evolution of defence, but the potential costs of this evolution are poorly documented. We report increased resistance of the invader Ambrosia artemisiifolia after reassociation with a coevolved specialist herbivore, and that this increase corresponds with reduced abiotic stress tolerance. Herbivore resistance was higher, but drought tolerance was lower in plants from populations with a longer reassociation history, and this corresponded with changes in phenylpropanoids involved in insect resistance and abiotic stress tolerance. These changes were corroborated by shifts in the expression of underlying biosynthetic genes and plant anti-oxidants. Together, our findings suggest rapid evolution of plant traits after reassociation with coevolved enemies, resulting in genetically based shifts in investment between abiotic and biotic stress responses, providing insights into co-evolution, plant invasion and biological control.

Trade-offs in non-native plant herbivore defences enhance performance.

Non-native plants are typically released from specialist enemies but continue to be attacked by generalists, albeit at lower intensities. This reduced herbivory may lead to less investment in constitutive defences and greater investment in induced defences, potentially reducing defence costs. We compared herbivory on 27 non-native and 59 native species in the field and conducted bioassays and chemical analyses on 12 pairs of non-native and native congeners. Non-natives suffered less damage and had weaker constitutive defences, but stronger induced defences than natives. For non-natives, the strength of constitutive defences was correlated with the intensity of herbivory experienced, whereas induced defences showed the reverse. Investment in induced defences correlated positively with growth, suggesting a novel mechanism for the evolution of increased competitive ability. To our knowledge, these are the first linkages reported among trade-offs in plant defences related to the intensity of herbivory, allocation to constitutive versus induced defences, and growth.

Temporal stability of productivity is associated with complementarity and competitive intensities in intercropping.

Year-to-year stability in crop production is a crucial aspect of feeding a growing global population. Evidence from natural ecosystems shows that increasing plant diversity generally increases the temporal stability of productivity; however, we have little knowledge of the mechanisms by which diversity affects stability. In fact, understanding the drivers of stability is a major knowledge gap in our understanding of biodiversity and ecosystem function in general. We varied resource inputs into crop monocultures and intercropping of maize/pea and maize/rapeseed for 3 years in field experiments to create a wide range of values for temporal stability, complementarity effects, selection effects, competition, and facilitation. We correlated whole-system temporal stability in productivity with these values and the stability of competitively subordinate species and competitively dominant species in the intercrops. We then used structural equation modeling (SEM), which combines complex path models with latent variables, to estimate how interspecific interactions for water, nitrogen, and phosphorus affected the relationships between stability and these values. Intercropping treatments did not increase stability, but the wide range of stability created by our experiments allowed us to explore the relationship of many factors with stability. Complementarity correlated positively with the temporal stability of grain yield and aboveground biomass, suggesting that either facilitative interactions or niche partitioning shifted over time in ways that promoted stability. Furthermore, the temporal stability of total productivity of intercropping relied most on the stability of more productive species. However, facilitation tested by relative interaction index independently did not correlate with stability, but the temporal stability of the whole system increased as the competitive effects of competitively dominant species (pea and rapeseed) on competitively subordinate species (maize) decreased and was highest when these competitive effects were virtually zero. SEM indicated that as competition for soil nitrogen from competitively dominant species on competitively subordinate species decreased, the overall temporal stability of whole-system aboveground biomass increased. This stability then led to greater stability in grain production. Our findings indicate that complex shifts in complementarity and competitive intensities are likely to be key mechanisms that maintain temporal stability in species-diverse agriculture and, potentially, in natural systems.

Competition for water and rapid exclusion of an island endemic by a pantropical species in a tropical climate.

Water availability has major effects on community structure and dynamics globally, yet our understanding of competition for water in the tropics is limited. On the tropical Trindade Island, we explored competition for water in the context of the rapid exclusion of an endemic sedge, Cyperus atlanticus (Cyperaceae), by a pantropical, N-fixing shrub, Guilandina bonduc (Fabaceae). Guilandina patches were generally surrounded by rings of bare soil, and dead Cyperus halos commonly surrounded these bare zones. With geo-referenced measurements, we showed that Guilandina patches and bare soil zones rapidly expanded and replaced adjacent Cyperus populations. We found that soil water potentials were much lower in bare soils than soils under Guilandina or Cyperus, and that leaf water potentials of Cyperus plants were lower when co-occurring with Guilandina than when alone. When Guilandina was removed experimentally, Cyperus populations expanded and largely covered the bare soil zones. Our results indicate that when Guilandina establishes, its root systems expand beyond its canopies and these roots pull water from soils beneath Cyperus and kill it, creating bare zone halos, and then Guilandina expands and repeats the process. This scenario indicates rapid competitive exclusion and displacement of an endemic by a common pantropical species, at least in part through competition for water.

The EICA is dead? Long live the EICA!

An important hypothesis for how plants respond to introduction to new ranges is the evolution of increased competitive ability (EICA). EICA predicts that biogeographical release from natural enemies initiates a trade-off in which exotic species in non-native ranges become larger and more competitive, but invest less in consumer defences, relative to populations in native ranges. This trade-off is exceptionally complex because detecting concomitant biogeographical shifts in competitive ability and consumer defence depends upon which traits are targeted, how competition is measured, the defence chemicals quantified, whether defence chemicals do more than defend, whether 'herbivory' is artificial or natural, and where consumers fall on the generalist-specialist spectrum. Previous meta-analyses have successfully identified patterns but have yet to fully disentangle this complexity. We used meta-analysis to reevaluate traditional metrics used to test EICA theory and then expanded on these metrics by partitioning competitive effect and competitive tolerance measures and testing Leaf-Specific Mass in detail as a response trait. Unlike previous syntheses, our meta-analyses detected evidence consistent with the classic trade-off inherent to EICA. Plants from non-native ranges imposed greater competitive effects than plants from native ranges and were less quantitatively defended than plants from native ranges. Our results for defence were not based on complex leaf chemistry, but instead were estimated from tannins, toughness traits and primarily Leaf-Specific Mass. Species specificity occurred but did not influence the general patterns. As for all evidence for EICA-like trade-offs, we do not know if the biogeographical differences we found were caused by trade-offs per se, but they are consistent with predictions derived from the overarching hypothesis. Underestimating physical leaf structure may have contributed to two decades of tepid perspectives on the trade-offs fundamental to EICA.

Interactions between nurse plants and parasitic beneficiaries: A theoretical approach to indirect facilitation.

When a nurse species facilitates the density of more than one species, strong indirect interactions can occur between the facilitated, or beneficiary, species, and these could lead to cascading interactive effects on community dynamics. In this context, negative effects of beneficiaries on the growth or reproduction of nurses are much more common than positive effects. This suggests beneficiaries frequently act as parasites of their nurses, and the consequences of this are largely unexplored. Our general aim is to analyze whether competition between parasitic beneficiaries can lead to indirect facilitation to nurse species and how this influences nurse-beneficiary systems. We explored potential outcomes of such reciprocal interactions in the general case of one facilitator and two facultative parasitic beneficiary species with different strategies for competing for space, one having a high carrying capacity but low maximum intrinsic growth rate (K-species), and the other having low carrying capacity but a higher intrinsic growth rate (r-species). These are defined in terms of the logistic equation, and reflect the abundances they can reach when growing alone. By considering a set of ordinary differential equations for the abundances of the nurse and the two parasitic beneficiaries in the mean-field approximation (where spatial correlations do not play a role), we first show analytically that coexistence of the three species is only possible when the r-species beneficiary is, at the same time, more harmful than the K-species and receives more benefit from the nurse. We then show that only the K-species can indirectly facilitate the nurse in such system. These are general, analytic results, independent of particular values of the parameters. We then explore these results using a 2-D lattice model informed by cushion plants in alpine ecosystems, and their interactions with beneficiaries with r and K strategies. Interesting spatial effects emerge in this case, such as a seeding effect: facilitation by the nurse increases beneficiary abundances also outside nurse patches. These in turn generate a negative feedback to the nurse, due to local competition for space near its edge. Spatial distribution effects are also crucial for relaxing the conditions for the survival of the r-species, allowing an r-strategist with weaker parasitic effects to indirectly facilitate the nurse through suppression of a more harmful K-species. Unexpectedly, this also has an indirect positive effect on the K species because of increased abundance of nurses. In the case of the r-species representing a ruderal invader, our lattice results would suggest that invaders have the potential to benefit both nurse and native beneficiary species via indirect facilitation. More generally, our results indicate that facilitation of more than one other species varying in competitive ability and which act as parasites on a nurse, can in turn promote indirect facilitation effects. This form of indirect facilitation has not been explicitly studied before, although it may create substantial conditionality in the outcomes of interactions among multiple species and the dynamics of nurse-beneficiary systems.

Early Sibling Conflict May Ultimately Benefit the Family.

Relatives often interact differently with each other than with nonrelatives, and whether kin cooperate or compete has important consequences for the evolution of mating systems, seed size, dispersal, and competition. Previous research found that the larger of the size dimorphic seeds produced by the annual plant Aegilops triuncialis suppressed germination of their smaller sibs by 25%-60%. Here, we found evidence for kin recognition and sibling rivalry later in life among Aegilops seedlings that places seed-seed interactions in a broader context. In experiments with size dimorphic seeds, seedlings reduced the growth of sibling seedlings by ∼40% but that of nonsibling seedlings by ∼25%. These sequential antagonistic interactions between seeds and then seedlings provide insight into conflict and cooperation among kin. Kin-based conflict among seeds may maintain dormancy for some seeds until the coast is clear of more competitive siblings. If so, biotically induced seed dormancy may be a unique form of cooperation, which increases the inclusive fitness of maternal plants and offspring by minimizing competition among kin.

Relative importance of competition and plant-soil feedback, their synergy, context dependency and implications for coexistence.

Plants interact simultaneously with each other and with soil biota, yet the relative importance of competition vs. plant-soil feedback (PSF) on plant performance is poorly understood. Using a meta-analysis of 38 published studies and 150 plant species, we show that effects of interspecific competition (either growing plants with a competitor or singly, or comparing inter- vs. intraspecific competition) and PSF (comparing home vs. away soil, live vs. sterile soil, or control vs. fungicide-treated soil) depended on treatments but were predominantly negative, broadly comparable in magnitude, and additive or synergistic. Stronger competitors experienced more negative PSF than weaker competitors when controlling for density (inter- to intraspecific competition), suggesting that PSF could prevent competitive dominance and promote coexistence. When competition was measured against plants growing singly, the strength of competition overwhelmed PSF, indicating that the relative importance of PSF may depend not only on neighbour identity but also density. We evaluate how competition and PSFs might interact across resource gradients; PSF will likely strengthen competitive interactions in high resource environments and enhance facilitative interactions in low-resource environments. Finally, we provide a framework for filling key knowledge gaps and advancing our understanding of how these biotic interactions influence community structure.

Granivory from native rodents and competition from an exotic invader strongly and equally limit the establishment of native grasses.

Seed predation and resource competition are fundamental biotic filters that affect the assembly of plant communities, yet empirical studies rarely assess their importance relative to one another. Here, we used rodent exclosures and experimental seed additions to compare how rodent granivory and resource competition affected the net establishment of an exotic invader (Bromus tectorum) and two native bunchgrasses (Pseudoroegneria spicata and Elymus elymoides) in the Great Basin Desert, USA. Rodent granivory limited the establishment of both native grasses, but had no significant effect on B. tectorum. Competition from B. tectorum limited the establishment of both native grasses, but neither native grass imposed a significant competitive effect on B. tectorum. Interestingly, we found that rodent granivory and B. tectorum competition limited the establishment of native grasses to the same extent, suggesting that these biotic interactions may impose equally important barriers to the local establishment of P. spicata and E. elymoides. By evaluating the strength of multiple biotic interactions in simultaneous, coordinated experiments, we can understand their relative contributions to community-level patterns.

Competition does not come at the expense of colonization in seed morphs with increased size and dispersal.

PREMISE OF THE STUDY: Seed-level trade-offs of heterocarpic species remain poorly understood. We propose that seedlings emerging from seeds with a permanent pappus (dispersing seeds) are stronger competitors than those emerging from seeds without a pappus (nondispersing seeds) because dispersing seeds are larger and germinate faster than nondispersing seeds in Centaurea solstitialis. METHODS: We conducted a competition experiment with both seed morphs, in which we recorded emergence rate and proportion, estimated seed dispersal by wind (anemochory) and by mammals (exozoochory), and measured size and abundance of seed morphs. KEY RESULTS: We found that seedlings from pappus seeds had greater competitive abilities than those from non-pappus seeds. Similarly, pappus seedlings emerged at much faster rates and larger proportions than non-pappus seedlings. Pappus seeds were larger, were more numerous, and displayed improved exozoochory compared to non-pappus seeds. Anemochory was poor for both seed morphs. CONCLUSIONS: We found support for our hypothesis, raising in turn the possibility that competition and colonization are positively associated in seed morphs of heterocarpic species with enhanced exozoochory of larger seeds. These findings are not consistent with those from heterocarpic species with enhanced anemochory of smaller seeds or slower-germinating seeds. Our results additionally suggest that pappus and non-pappus seeds of C. solstitialis display a task-division strategy in which pappus morphs colonize and preempt unoccupied sites through improved dispersal and fast and large emergence of seedlings with increased competitive abilities, whereas non-pappus morphs promote site persistence through delayed germination and dormancy. This strategy may contribute to the success of C. solstitialis in highly variable environments.

Phylogenetic structure of arbuscular mycorrhizal fungal communities along an elevation gradient.

Despite the importance of arbuscular mycorrhizal (AM) fungi within terrestrial ecosystems, we know little about how natural AM fungal communities are structured. To date, the majority of studies examining AM fungal community diversity have focused on single habitats with similar environmental conditions, with relatively few studies having assessed the diversity of AM fungi over large-scale environmental gradients. In this study, we characterized AM fungal communities in the soil along a high-elevation gradient in the North American Rocky Mountains. We focused on phylogenetic patterns of AM fungal communities to gain insight into how AM fungal communities are naturally assembled. We found that alpine AM fungal communities had lower phylogenetic diversity relative to lower elevation communities, as well as being more heterogeneous in composition than either treeline or subalpine communities. AM fungal communities were phylogenetically clustered at all elevations sampled, suggesting that environmental filtering, either selection by host plants or fungal niches, is the primary ecological process structuring communities along the gradient.

Metabolic Profiling and Identification of Shikonins in Root Periderm of Two Invasive Echium spp. Weeds in Australia.

Metabolic profiling can be successfully implemented to analyse a living system's response to environmental conditions by providing critical information on an organism's physiological state at a particular point in time and allowing for both quantitative and qualitative assessment of a specific subset(s) of key metabolites. Shikonins are highly reactive chemicals that affect various cell signalling pathways and possess antifungal, antibacterial and allelopathic activity. Based on previous bioassay results, bioactive shikonins, are likely to play important roles in the regulation of rhizosphere interactions with neighbouring plants, microbes and herbivores. An effective platform allowing for rapid identification and accurate profiling of numerous structurally similar, difficult-to-separate bioactive isohexenylnaphthazarins (shikonins) was developed using UHPLC Q-TOF MS. Root periderm tissues of the invasive Australian weeds Echium plantagineum and its congener E. vulgare were extracted overnight in ethanol for shikonin profiling. Shikonin production was evaluated at seedling, rosette and flowering stages. Five populations of each species were compared for qualitative and quantitative differences in shikonin formation. Each species showed little populational variation in qualitative shikonin production; however, shikonin was considerably low in one population of E. plantagineum from Western New South Wales. Seedlings of all populations produced the bioactive metabolite acetylshikonin and production was upregulated over time. Mature plants of both species produced significantly higher total levels of shikonins and isovalerylshikonin > dimethylacrylshikonin > shikonin > acetylshikonin in mature E. plantagineum. Although qualitative metabolic profiles in both Echium spp. were nearly identical, shikonin abundance in mature plant periderm was approximately 2.5 times higher in perennial E. vulgare extracts in comparison to those of the annual E. plantagineum. These findings contribute to our understanding of the biosynthesis of shikonins in roots of two related invasive plants and their expression in relation to plant phenological stage.

Intraspecific diversity buffers the inhibitory effects of soil biota.

Plant community productivity can increase with increasing intraspecific genotypic diversity. Previous studies have attributed the genetic diversity-productivity pattern to differential resource use among genotypes, as many studies have found for species. But here we ask whether suppression of productivity at low intraspecific diversity by soil biota might also drive a positive diversity-productivity relationship. In a previous study, we manipulated genetic diversity by varying the number of Pseudoroegneria accessions growing together in common garden plots, and used soil from that experiment to evaluate soil feedbacks. The total biomass of P. spicata plants grown in unsterilized soil increased with accession richness, specifically when comparing soil that had contained plants from 3 accessions to soil that had contained plants from either 8 or 12 population accessions. Furthermore, soil from high-richness (8 or 12-accession) plots drove neutral feedbacks, whereas soil in the 3-accession plots (3) drove negative feedbacks. However, within each level of richness, there was no relationship between relative yield and feedback. Our results suggest that soil biota might play an integral role in the emerging understanding of the relationship between intraspecific diversity and ecosystem productivity.

Solidago gigantea plants from nonnative ranges compensate more in response to damage than plants from the native range.

Resistance and tolerance are two ways that plants cope with herbivory. Tolerance, the ability of a plant to regrow or reproduce after being consumed, has been studied less than resistance, but this trait varies widely among species and has considerable potential to affect the ecology of plant species. One particular aspect of tolerance, compensatory responses, can evolve rapidly in plant species; providing insight into interactions between consumers and plants. However, compensation by invasive species has rarely been explored. We compared compensatory responses to the effects of simulated herbivory expressed by plants from seven Solidago gigantea populations from the native North American range to that expressed by plants from nine populations from the nonnative European range. Populations were also collected along elevational gradients to compare ecotypic variation within and between ranges. Solidago plants from the nonnative range of Europe were more tolerant to herbivory than plants from the native range of North America. Furthermore, plants from European populations increased in total biomass and growth rate with elevation, but decreased in compensatory response. There were no relationships between elevation and growth or compensation for North American populations. Our results suggest that Solidago gigantea may have evolved to better compensate for herbivory damage in Europe, perhaps in response to a shift to greater proportion of attack from generalists. Our results also suggest a possible trade-off between rapid growth and compensation to damage in European populations but not in North American populations.

Negative plant-soil feedbacks increase with plant abundance, and are unchanged by competition.

Plant-soil feedbacks and interspecific competition are ubiquitous interactions that strongly influence the performance of plants. Yet few studies have examined whether the strength of these interactions corresponds with the abundance of plant species in the field, or whether feedbacks and competition interact in ways that either ameliorate or exacerbate their effects in isolation. We sampled soil from two intermountain grassland communities where we also measured the relative abundance of plant species. In greenhouse experiments, we quantified the direction and magnitude of plant-soil feedbacks for 10 target species that spanned a range of abundances in the field. In soil from both sites, plant-soil feedbacks were mostly negative, with more abundant species suffering greater negative feedbacks than rare species. In contrast, the average response to competition for each species was unrelated with its abundance in the field. We also determined how competitive response varied among our target species when plants competed in live vs. sterile soil. Interspecific competition reduced plant size, but the strength of this negative effect was unchanged by plant-soil feedbacks. Finally, when plants competed interspecifically, we asked how conspecific-trained, heterospecific-trained, and sterile soil influenced the competitive responses of our target species and how this varied depending on whether target species were abundant or rare in the field. Here, we found that both abundant and rare species were not as harmed by competition when they grew in heterospecific-trained soil compared to when they grew in conspecific-cultured soil. Abundant species were also not as harmed by competition when growing in sterile vs. conspecific-trained soil, but this was not the case for rare species. Our results suggest that abundant plants accrue species-specific soil pathogens to a greater extent than rare species. Thus, negative feedbacks may be critical for preventing abundant species from becoming even more abundant than rare species.