Long‐term experiment manipulating community assembly results in favorable restoration outcomes for invaded prairies

Invasive species are a common problem in restoration projects. Manipulating soil fertility and species arrival order has the potential to lower their abundance and achieve higher abundances of seeded native species. In a 7‐year experiment in Missouri, United States, we tested how nutrient addition and the timing of arrival of the invasive legume Lespedeza cuneata and seeded native prairie grass and forb species influenced overall community composition. Treatments that involved early arrival of seeded forb and grass species and late arrival of L. cuneata were most successful at creating community structure that fulfilled our restoration goals, displaying high abundance of seeded native forb species, low abundances of L. cuneata, and non‐native species. There were few treatment interactions, with the exception that timing seeded native forbs and timing of L. cuneata arrival interactively influenced the abundance of seeded native forbs. This suggests that the individual treatments are supporting the restoration goals, such as creating a community with low abundance of L. cuneate or high abundance of native seeded species, without restricting each other. This study demonstrates the importance of priority effects in disturbed habitats prone to invasion, the lasting effects of initial seeding on long‐term community composition, and the potential for fertilization to positively benefit restoration of degraded grasslands.     

Environmental variability counteracts priority effects to facilitate species coexistence: evidence from nectar microbes

The order of species arrival during community assembly can greatly affect species coexistence, but the strength of these effects, known as priority effects, appears highly variable across species and ecosystems. Furthermore, the causes of this variation remain unclear despite their fundamental importance in understanding species coexistence. Here, we show that one potential cause is environmental variability. In laboratory experiments using nectar-inhabiting microorganisms as a model system, we manipulated spatial and temporal variability of temperature, and examined consequences for priority effects. If species arrived sequentially, multiple species coexisted under variable temperature, but not under constant temperature. Temperature variability prevented extinction of late-arriving species that would have been excluded owing to priority effects if temperature had been constant. By contrast, if species arrived simultaneously, species coexisted under both variable and constant temperatures. We propose possible mechanisms underlying these results using a mathematical model that incorporates contrasting effects of microbial species on nectar pH and amino acids. Overall, our findings suggest that understanding consequences of priority effects for species coexistence requires explicit consideration of environmental variability.     

Exploring the potential of using priority effects during ecological restoration to resist biological invasions in the neotropics

Manipulating plant order of arrival, a process that creates priority effects, may be an unexplored powerful tool to hinder the establishment of invasive non‐native plants in sites under restoration. Knowledge and experimental studies on priority effects in the neotropics are scarce. Here, we propose a research agenda that investigates whether manipulating plant order of arrival can create priority effects in the neotropics, and if this strategy can be used to avoid the spread of undesired species in restoration projects. We also describe our view on expanding existing knowledge on priority effects to the neotropics and identifying key questions for future research.     

Priority effects vary with species identity and origin in an experiment varying the timing of seed arrival

Exotic species are sometimes phenologically distinct from native species in the invaded community, allowing them to be active when there may be reduced competition for resources. In southern California, annual species are particularly problematic invaders, and prior work has shown that these species germinate earlier in the growing season, giving them a competitive advantage over later‐germinating native species. This result begs the question, if being active earlier is advantageous, why have not native species adapted earlier cues for germination? We hypothesized native species would benefit less from earlier germination than exotic species (potentially due to slower growth following germination), thus negating potential selection for early germination. Here we manipulated planting time for common native and exotic species, growing them in all possible species pairs, to evaluate how competitive outcomes were altered by the time of arrival and the origin of competing species. In contrast to our hypotheses, the exotic species often had lower biomass when planted first, potentially due to disturbance when the second species was planted. In contrast, three out of our four native species benefited from earlier planting (a priority effect). Unlike the potential benefit of arriving early, we found no evidence that being planted one week later resulted in a competitive disadvantage, when compared to being planted simultaneously with a competitor. Further, we found that the magnitude and even direction of priority effects varied depending on the identity of the interacting species. Together these results suggest that a lack of directional selection may prevent adaptation towards earlier germination times of native species. Although this experiment was conducted with a limited suite of species, the results show that the role of seasonal priority effects varies among species, and that native species could benefit from seasonal priority effects in restoration efforts even when in competition with fast‐growing exotic annual species.     

Dispersal enhances beta diversity in nectar microbes

Dispersal is considered a key driver of beta diversity, the variation in species composition among local communities, but empirical tests remain limited. We manipulated dispersal of nectar‐inhabiting bacteria and yeasts via flower‐visiting animals to examine how dispersal influenced microbial beta diversity among flowers. Contrary to the prevailing view that dispersal lowers beta diversity, we found beta diversity was highest when dispersal was least limited. Our analysis suggested that this unexpected pattern might have resulted from stronger priority effects under increased dispersal. Dispersal is highly stochastic, generating variability in species arrival history and consequently the potential for community divergence via priority effects, in these and likely many other microbial, plant, and animal communities. Yet most previous experiments eliminated this possibility. We suggest that the positive effects of dispersal on beta diversity, like the one we report here, may have been greatly underappreciated.     

Predation and priority effects in experimental zooplankton communities

During colonization of new habitats, the sequence of arrival among species is in many cases determined by chance. Priority effects imply that differences in arrival time may lead to long-lasting differences in species dominance. To evaluate the importance of priority effects, we performed a community assembly experiment, manipulating the inoculation order of three large cladoceran zooplankton species. The inoculation treatments were crossed with a predation treatment to test whether the presence of a predator (larvae of the phantom midge Chaoborus ) results in changes in the strength of species sorting and priority effects. Our results clearly demonstrate priority effects, but also that the presence of a predator impacts both community assembly and the strength of priority effects. In the predation-free treatments, communities were dominated by either Daphnia magna or Daphnia obtusa , depending on the species arrival sequence. Whenever D. obtusa was inoculated after D. magna , the species displayed negative growth. In the presence of Chaoborus predation, the communities were generally dominated by the third species, Simocephalus vetulus . Here, the growth of D. magna was negative when the species was inoculated as second or third. Overall, our results underscore the importance of both priority effects and species sorting during community assembly.     

Resource availability mediates the importance of priority effects in plant community assembly and ecosystem function

Assembly history, including the order in which species arrive into a community, can influence long‐term community structure; however we know less about how timing of species arrival may alter assembly especially under varying resource conditions. To explore how the timing of species arrival interacts with resource availability to alter community assembly, we constructed experimental plant communities and manipulated the interval between plantings of groups of seedlings (0, 5, 10, 15 or 20 days) at low and high levels of soil nutrient supply. To see if community changes influenced ecosystem‐scale processes, we measured parameters across the plant–soil continuum (e.g. plant biomass and net ecosystem carbon dioxide exchange). We found that the timing of species arrival had a large impact on community assembly, but the size of the effect depended on soil fertility. As planting interval increased, plant communities diverged further from the control, but the divergence was stronger at high than at low nutrient supply. Our data suggest that at high nutrient supply, early‐planted species preempted light resources more quickly, thus preventing the successful establishment of later arriving species even at short planting intervals. Finally, we found that assembly related divergence in plant communities scaled to impact ecosystem‐level characteristics such as green leaf chemistry, but had little effect on total community biomass and net ecosystem exchange of CO₂ and water vapor. Our data indicate that the effect of a stochastic factor, here the timing of species arrival on community composition, depends on the resource level under which the community assembles.     

Timing is everything: priority effects alter community invasibility after disturbance

Theory suggests that communities should be more open to the establishment of regional species following disturbance because disturbance may make more resources available to dispersers. However, after an initial period of high invasibility, growth of the resident community may lead to the monopolization of local resources and decreased probability of successful colonist establishment. During press disturbances (i.e., directional environmental change), it remains unclear what effect regional dispersal will have on local community structure if the establishment of later arriving species is affected by early arriving species (i.e., if priority effects are important). To determine the relationship between time‐since‐disturbance and invasibility, we conducted a fully factorial field mesocosm experiment that exposed tundra zooplankton communities to two emerging stressors – nutrient and salt addition, and manipulated the arrival timing of regional dispersers. Our results demonstrate that invasibility decreases with increasing time‐since‐disturbance as abundance (nutrient treatments) or species richness (salt treatments) increases in the resident community. Results suggest that the relative timing of dispersal and environmental change will modify the importance of priority effects in determining species composition after a press disturbance.     

Species divergence and trait convergence in experimental plant community assembly

Despite decades of research, it remains controversial whether ecological communities converge towards a common structure determined by environmental conditions irrespective of assembly history. Here, we show experimentally that the answer depends on the level of community organization considered. In a 9‐year grassland experiment, we manipulated initial plant composition on abandoned arable land and subsequently allowed natural colonization. Initial compositional variation caused plant communities to remain divergent in species identities, even though these same communities converged strongly in species traits. This contrast between species divergence and trait convergence could not be explained by dispersal limitation or community neutrality alone. Our results show that the simultaneous operation of trait‐based assembly rules and species‐level priority effects drives community assembly, making it both deterministic and historically contingent, but at different levels of community organization.     

Interannual variation in precipitation and other planting conditions impacts seedling establishment in sown plant communities

Ecological restoration can reverse biodiversity loss worldwide, yet restoration goals and outcomes vary widely, which limits this potential. Divergent restoration outcomes may stem from variation in conditions at the outset of restoration, but empirical evidence is lacking and typically confounded with site differences. Additionally, precipitation is usually cited as the source of this variation, although a wide range of conditions can vary annually. We tested for effects of planting year on seedling establishment by installing identical restorations in three different years. Within those years, we manipulated rainfall with rain‐out shelters to disentangle the effects of precipitation from other annually variable conditions. Additionally, we tested whether increasing seed mix richness buffers against adverse planting conditions. For the first growing season after planting, we followed emergence and survival of sown prairie species and nonsown weed species to determine how planting year conditions influence an establishing plant community, if at all. We found that seedling establishment differed across planting years and precipitation treatments, and that varying emergence patterns by species led to differences in the composition of the first‐year community. We also found significant variation in sown species establishment across years when precipitation was held constant, illustrating the previously overlooked role of nonprecipitation drivers on planting year effects. Higher seed mix richness did not consistently improve establishment of sown species under different planting conditions. This research provides important experimental evidence for effects of interannual variation in planting conditions on first‐year establishment. Future work will examine how these initial changes affect longer‐term assembly dynamics.     

Sowing different mixtures in dry acidic grassland produced priority effects of varying strength

Several longer-term assembly studies on ex-arable land have found that species that arrive first at a disturbed site can play a key role in the further development of the community and that this priority effect influences aboveground productivity, species diversity and stability of the grassland communities that develop. Restoration of nutrient poor, species rich grasslands is often limited by seed dispersal as well as the accessibility of suitable microsites for establishment. Sowing species (i.e. creating priority effects for further assembly) may help overcome such dispersal barriers, but the potential of using priority effects for restoration has not been tested in this type of dry grassland. We tested the hypothesis that sowing two different seed mixtures used for dry acidic grassland restoration onto a sandy substrate (which formed an equivalent to a primary succession) would create priority effects, and that these priority effects would be sustained over a number of years. We followed community assembly and measured aboveground productivity for four years after sowing. We found that priority effects caused by sowing of differently diverse mixtures did also occur in dry acidic grassland habitat, but that how persistent they were over time depended on the response variable considered. Priority effects on species number were not as strong as found in previous ex-arable land studies, whereas priority effects for aboveground productivity were still visible after 4 years. In addition, functional composition of the community still reflected the composition of the seed mixtures 4 years later. Our results suggest that priority effects can occur in nutrient-poor dry acidic grassland but in contrast to more nutrient-rich sites the breadth of responses affected may not be as wide.     

Long‐term effects of prairie restoration on plant community structure and native population dynamics

The key to restoring degraded grassland habitats is identifying feasible and effective techniques to reduce the negative impacts of exotic species and promote self‐sustaining native populations. It is often difficult to extend monitoring of restoration efforts to evaluate long‐term success, but doing so is essential to understanding how initial outcomes change over time. To assess how initial treatment effects persist, we revisited degraded patches of Pacific Northwest prairie habitat 6 years after experimental restoration efforts ceased. We evaluated plant community composition to determine the lasting effects of supplemental native seeding and disturbance treatments (burning, mowing, and herbicide to reduce exotic species). We tracked the persistence of seeded species and measured spread of their populations to evaluate suitability of species for restoration and the ability of the habitat to support native plant populations. We found that plots that received supplemental seeding continued to exhibit higher richness of native species than those left unseeded, and that both seeding and disturbance treatments could positively influence native species abundance over the long term. The initially observed effects of disturbance treatments on reducing exotic grass abundance had diminished, highlighting the importance of long‐term monitoring and ongoing control of exotic species. Nevertheless, these treatments significantly influenced the population trajectories of 4 out of 8 seeded native species. There was evidence of spatial advance of most seeded species. Results from extended monitoring confirm that dispersal limitation of native species and difficulties maintaining the reduction of exotic grasses continue to be major barriers to success in restoration of invaded grasslands.     

Priority effects: How the order of arrival of an invasive grass,Bromus tectorum,alters productivity and plant community structure when grown with native grass species

Theories and models attempt to explain how and why particular plant species grow together at particular sites or why invasive exotic species dominate plant communities. As local climates change and human‐use degrades and disturbs ecosystems, a better understanding of how plant communities assemble is pertinent, particularly when restoring grassland ecosystems that are frequently disturbed. One such community assembly theory is priority effects, which suggests that arrival order of species into a community alters plant–plant interactions and community assembly. Theoretically, priority effects can have lasting effects on ecosystems and will likely be altered as the risk of invasion by exotic species increases. It is difficult to predict how and when priority effects occur, as experimental reconstruction of arrival order is often difficult in adequate detail. As a result, limited experimental studies have explored priority effects on plant community assembly and plant invasions. To determine if and how priority effects affect the success of invasive species, we conducted a greenhouse study exploring how the arrival order of an invasive grass, Bromus tectorum, affects productivity and community composition when grown with native grasses. We found evidence for priority effects, as productivity was positively related to dominance of B. tectorum and was greater the earlier B. tectorum arrived. This suggests that priority effects could be important for plant communities as the early arrival of an invasive species drastically impacted the productivity and biodiversity of our system at the early establishment stages of plant community development.     

Priority Effects of Time of Arrival of Plant Functional Groups Override Sowing Interval or Density Effects: A Grassland Experiment

Priority effects occur when species that arrive first in a habitat significantly affect the establishment, growth, or reproduction of species arriving later and thus affect functioning of communities. However, we know little about how the timing of arrival of functionally different species may alter structure and function during assembly. Even less is known about how plant density might interact with initial assembly. In a greenhouse experiment legumes, grasses or forbs were sown a number of weeks before the other two plant functional types were sown (PFT) in combination with a sowing density treatment. Legumes, grasses or non-legume forbs were sown first at three different density levels followed by sowing of the remaining PFTs after three or six-weeks. We found that the order of arrival of different plant functional types had a much stronger influence on aboveground productivity than sowing density or interval between the sowing events. The sowing of legumes before the other PFTs produced the highest aboveground biomass. The larger sowing interval led to higher asymmetric competition, with highest dominance of the PFT sown first. It seems that legumes were better able to get a head-start and be productive before the later groups arrived, but that their traits allowed for better subsequent establishment of non-legume PFTs. Our study indicates that the manipulation of the order of arrival can create priority effects which favour functional groups of plants differently and thus induce different assembly routes and affect community composition and functioning.     

Priority effects can persist across floral generations in nectar microbial metacommunities

The order of species arrival can influence how species interact with one another and, consequently, which species may coexist in local communities. This phenomenon, called priority effects, has been observed in various types of communities, but it remains unclear whether priority effects persist over the long term spanning multiple generations of local communities in metacommunities. Focusing on bacteria and yeasts that colonize floral nectar of the sticky monkey flower, Mimulus aurantiacus, via hummingbirds and other flower‐visiting animals, we experimentally manipulated initial microbial dominance on plants (regarded as metacommunities) to examine whether its effects persisted across multiple generations of flowers (regarded as local microbial habitats). The experimental introduction of Neokomagataea (= Gluconobacter) bacteria and Metschnikowia yeasts into wild flowers showed that the effects of initial dominance were observable across multiple floral generations. Three weeks after introduction, corresponding approximately to three floral generations, Neokomagataea introduction led to exclusion of yeasts, whereas Metschnikowia introduction did not result in the exclusion of Neokomagataea. Our results suggest that, even when local habitats are ephemeral, priority effects may influence multiple generations of local communities within metacommunities.     

Species diversity, invasion, and alternative community states in sequentially assembled communities

The relationship between resident species diversity and invasion is generally negative in experimental studies but takes various forms in observational studies of natural communities. We hypothesized that stochastic species colonization, which applies to natural communities but not to experimental communities generally assembled through simultaneous species introduction, may lead to nonnegative diversity-invasion relationships via incurring priority effects. To test this hypothesis, we manipulated both resident species diversity and colonization history in sequentially assembled communities of bacterivorous protist species. We found that, despite a significant effect of assembly history on invader abundance, invader abundance decreased with diversity. This result was largely driven by positive selection effects associated with the dominant influence of an invasion-resistant species, which shared the most similar resource use pattern with the invader, and by the overall weak priority effects observed for the resident communities. Increasing species diversity, however, significantly strengthened priority effects, providing the first experimental support for the idea that larger species pools promote alternative community states. We suggest that elucidating mechanisms regulating the strength of priority effects may help in understanding variation in diversity-invasion relationships among natural communities.     

Within‐Year Soil Legacies Contribute to Strong Priority Effects of Exotics on Native California Grassland Communities

Understanding priority effects, in which one species in a habitat decreases the success of later species, may be essential for restoring native communities. Priority effects can operate in two ways: size‐asymmetric competition and creation of “soil legacies,” effects on soil that may last long after the competitive effect. We examined how these two types of priority effects, competition and soil legacies, drive interactions between seedlings of native and exotic California grassland plants. We established native and exotic communities in a mesocosm experiment. After 5 weeks, we removed the plants from half the treatments (soil legacy treatment) and retained the plants in the other half (priority effect treatment, which we interpret to include both competition and soil legacies). We then added native or exotic seed as the colonizing community. After 2 months, we measured the biomass of the colonizing community. When germinating first, both natives and exotics established priority effects, reducing colonist biomass by 86 and 92%, respectively. These priority effects were predominantly due to size‐asymmetric competition. Only exotics created soil legacies, and these legacies only affected native colonizers, reducing biomass by 74%. These results imply that exotic species priority effects can affect native grassland restorations. Although most restorations focus on removing exotic seedlings, amending soil to address soil legacies may also be critical. Additionally, because native species can exclude exotics if given a head start, ensuring that natives germinate first may be a cost‐effective restoration technique.     

Looking to the future: key points for sustainable management of northern Great Plains grasslands

The grasslands of the northern Great Plains (NGP) region of North America are considered endangered ecosystems and priority conservation areas yet have great ecological and economic importance. Grasslands in the NGP are no longer self‐regulating adaptive systems. The challenges to these grasslands are widespread and serious (e.g. climate change, invasive species, fragmentation, altered disturbance regimes, and anthropogenic chemical loads). Because the challenges facing the region are dynamic, complex, and persistent, a paradigm shift in how we approach restoration and management of the grasslands in the NGP is imperative. The goal of this article is to highlight four key points for land managers and restoration practitioners to consider when planning management or restoration actions. First, we discuss the appropriateness of using historical fidelity as a restoration or management target because of changing climate, widespread pervasiveness of invasive species, the high level of fragmentation, and altered disturbance regimes. Second, we highlight ecosystem resilience and long‐term population persistence as alternative targets. Third, because the NGP is so heavily impacted with anthropogenic chemical loading, we discuss the risks of ecological traps and extinction debt. Finally, we highlight the importance of using adaptive management and having patience during restoration and management. Consideration of these four points will help management and restoration of grasslands move toward a more successful and sustainable future. Although we specifically focus on the NGP of North America, these same issues and considerations apply to grasslands and many other ecosystems globally.     

Common and Uncommon Understory Species Differentially Respond to Restoration Treatments in Ponderosa Pine/Douglas-Fir Forests, Montana

Restoration treatments have been widely advocated to address declining conditions in Pinus ponderosa forests throughout the western United States. However, few studies have examined treatment effects on individual plant species or whether responses differ for common species and uncommon species (those with low abundance in the community)—information that may be critical in managing for long‐term biodiversity. We investigated understory species responses to restoration treatments in ponderosa pine/Douglas‐fir forests using a randomized block experimental design with three blocks and four treatments (control, burn‐only, thin‐only, and thin‐burn). Understory vegetation was sampled before treatment and for three consecutive years after treatment. We used richness and an index of uniqueness to compare responses of common and uncommon native understory species among treatments, and indicator species analysis to identify individual species that responded to each treatment. Treatments that included thinning had significantly more unique species assemblages than the control. The thin‐only treatment increased common native species richness, whereas all active treatments significantly increased uncommon native species richness over the control, especially the thin‐burn. Generally, life‐forms did not explain the responses of individual species, though in the final sampling year several graminoids were exclusively indicative of treatments that included thinning. Very few species had reduced abundance in the thinning and burning treatments by the final sample year, whereas many uncommon and short‐lived species benefited from active treatments, especially the combined thin‐burn treatment. Active restoration treatments in these forests may foster plant diversity by minimally impacting common species while significantly benefiting disturbance‐dependent native species.     

A framework for priority effects

History of species arrival can influence plant community assembly. In this issue of the Journal of Vegetation Science, Sarneel et al. show that the strength of such historical contingency, or priority effects, varies with soil moisture in riparian plants. We discuss this study within a theoretical framework describing how and when priority effects occur via destabilizing and equalizing mechanisms.