Towards a population approach for evaluating grassland restoration—a systematic review

Persistence of restored populations depends on growth, reproduction, dispersal, local adaptation, and a suitable landscape pattern to foster metapopulation dynamics. Although the negative effects of habitat fragmentation on plant population dynamics are well understood, particularly in grasslands, the population traits that control grassland restoration are less known. We reviewed the use of population traits for evaluating grassland restoration success based on 141 publications (1986–2015). The results demonstrated that population demography was relatively well‐assessed but detailed studies providing information on key stages of the life cycle were lacking despite their importance in determining population viability. Vegetative and generative performances have been thoroughly investigated, notably the components of plant fitness, such as reproductive output, while genetic and spatial population structures were largely ignored. More work on the population effects of ecological restoration would be welcomed, particularly with a focus on population genetics. Targeted species were principally common and dominant natives, or invasive plants while rare or threatened species were poorly considered. Evaluation of ecological restoration should be conducted at different scales of ecological complexity, but so far, communities and ecosystems are over represented, and more focus should be directed towards a population approach as population traits are essential indicators of restoration success.     

On the need of legal frameworks for assessing restoration projects success: new perspectives from São Paulo state (Brazil)

Despite growing worldwide commitment to large‐scale ecosystem restoration, national public policies on restoration are few, and those that exist tend to be vague. Brazil and especially São Paulo state stand out. In a pioneering attempt to improve restoration projects and their outcomes, the Secretariat for the Environment of the State of São Paulo has enacted a legal instrument to drive planning and to assess whether the goals and targets of mandatory ecological restoration are being achieved. Regardless of the restoration techniques applied, the effectiveness of mandatory or public‐funded projects will henceforth be assessed by using three ecological indicators: (1) ground coverage with native vegetation; (2) density of native plants spontaneously regenerating; and (3) number of spontaneously regenerating native plant species. We analyze how this science‐based legal framework is expected to promote greater restoration success, improve cost‐effectiveness, and help bridge the all‐too‐familiar knowledge‐action gap in environmental policies. Notably, scientists, professionals, public agents, and stakeholders from different institutions have collaborated to advance the refinement and rolling out of this legal instrument. By 2037, it is expected that more than 300,000 restoration projects will be carried out in São Paulo state and monitored using this set of indicators. We also suggest that this approach could be usefully applied to the growing number of ecological restoration programs being carried out worldwide, especially in the context of offset policies intended to achieve serious compensation for environmental degradation or loss of biodiversity.     

Management of invasive plants through ecological resistance

Despite debates on the real impact of plant invasion on native biodiversity, there remain many situations where exotic invasive plants must be managed and habitats restored. Restoration practices that build on plant community assembly principles could be useful to delay or prevent re-invasion after control, but there are still few syntheses of the biodiversity theory, ecological mechanisms and experimental evidence relevant to invasive plant management, possibly delaying applications. To provide such a synthesis, we review current knowledge on three key determinants of invasion success: biotic resistance, abiotic constraints, and propagule pressure. We elaborate on the ecological mechanisms at play for each determinant and emphasize, using case studies, their relevance for invasive plant management and ecological restoration. We find evidence that restoring a plant cover can enhance invasion resistance, but the challenge for both research and field applications is to understand how multiple determinants interact in relation to species traits in the fields. Failure to recognize these interactions and their effect on community assembly processes may explain some of the mixed species responses observed. While we need control and restoration case studies with local species at different sites, the development of a coherent, dynamic and adaptive framework around biotic/ecological resistance will have to go beyond the idiosyncrasy of the many species and systems being tested. Emphasizing the functional diversity of the restored community seems a promising approach when facing potentially multiple invaders and/or fluctuating abiotic conditions.     

Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type,restoration context and time

Mycorrhizal inoculation can enhance outcomes of ecological restoration, but the benefits may be context-dependent. Here, we performed a meta-analysis of field studies to elucidate conditions in which adding mycorrhizal fungi enhances restoration success. We found inoculation increased plant biomass by an average effect size of 1.7 in 70 independent comparisons from 26 field-based studies, with the largest increases to N-fixing woody plants, C4-grasses and plants growing in soils with low plant-available P. Growth responses to inoculation increased with time for the first 3 yr after inoculation, especially for N-fixing woody plants and plants growing in severely altered soils. We found that mycorrhizal inoculation increased species richness of restored plant communities by 30%, promoted establishment of target species, and enhanced similarity of restored to reference communities. We conclude that the addition of mycorrhizal fungi to restoration sites can facilitate rapid establishment of vegetation cover, and restoration of diverse plant communities more akin to reference sites.     

Deploying microbes as drivers and indicators in ecological restoration

Ecosystem degradation is a major environmental threat. Beyond conservation, restoration of degraded ecosystems is a prerequisite to reinstate their ability to provide essential services and benefits. Most of the restoration efforts focus on aboveground restoration, that is, plants, under the assumption that establishment of plant species will reestablish the faunal and microbial species. While this may be true for some cases, it is not a general rule. Reestablishment of microbial communities by dedicated efforts is also necessary for successful restoration, as cycling of essential nutrients for plant growth and decomposition of organic matter is dependent on them. The role of microbial fertilizers and efficient organisms used in agriculture needs to be explored in restoration. Testing of symbiotic interactions between potential plant growth-promoting Rhizobacteria and plants native to a degraded ecosystem can be conducted and utilized for successful establishment of plant species. However, utmost care must be taken while introducing new microbial species or non-native plant species to an area, as they can adversely affect the resident microbial community. Techniques like phospholipid fatty-acid analysis can be used for taxonomic identification of large microbial groups in non-degraded reference ecosystems before introducing microbial species into a degraded ecosystem. For use of microbes in restoration, more studies on microbe-plant interactions need to be conducted. For use of Soil Microbial Community (SMC) as indicators of restoration, their role and function in the ecology of the area need to be elucidated by employing all the available techniques.     

Monitoring ecological processes for restoration projects

Restoration of ecological processes is key to restoring the capacity of ecosystems to support social, economic, cultural and aesthetic values. The sustainability of the restored system also depends on processes associated with carbon, nutrient and hydrologic cycles, yet most restoration monitoring is limited to plant community composition. Our research has shown that short-term plant composition monitoring is a necessary but insufficient predictor of long-term restoration success. Long-term (up to 75 years) studies in the western United States show that short-term monitoring of plant community composition alone incorrectly predicted the failure of treatments that were ultimately successful, and the success of treatments that ultimately failed. We propose that vegetation composition monitoring be combined with one or more ecological process indicators reflecting changes in three fundamental ecosystem attributes on which restoration success depends: soil and site stability, hydrologic function and biotic integrity. These simple, rapid, plot-level indicators reflect changes in resource redistribution and vegetation structure. We include a case study involving restoration of mixed grass prairie on mineland in the west-central United States.     

Beyond the green: assessing quarry restoration success through plant and beetle communities

In assessing the effectiveness of ecological restoration actions, outcomes evaluation using a multi‐taxa approach can greatly contribute to a clearer understanding of their success/failure. Since comprehensive biodiversity assessments are rarely possible, choosing taxa groups that are indicative of the ecosystem's structural and functional recovery is of major importance. Our goal was to evaluate the success of revegetation actions performed in a Mediterranean limestone quarry, using plants and epigean beetles as indicators. We compared their abundance, diversity, and community composition between revegetated sites aged 5, 13, and 19 years and a natural reference. Total plant cover significantly increased with restoration age and quickly reached reference values. However, native woody species cover dropped in the oldest site, while non‐native species became dominant. The abundance of beetles was always lower in restoration sites when compared to the reference, increasing with age, although not significantly. The richness of both plant species and beetle families was lower in restoration sites and did not show any trend towards the reference values. Finally, using nonmetric multidimensional scaling, the composition of plant and beetle communities from restoration sites showed a clear separation from the reference. Restoration efforts have successfully modified post‐quarry sites, but considerable differences remain, probably largely related to the use of the non‐native species Pinus halepensis in restoration plans. P. halepensis high cover in restoration sites greatly affects the structure of the ecosystem, and most likely its functioning too, as well as related ecosystem services, causing divergence from the reference values and compromising restoration success.     

Can pollination syndromes indicate ecological restoration success in tropical forests?

We evaluated the pollination syndromes of plant species occurring in revegetated patches of riparian Atlantic Forest in order to evaluate the success of restoration process. Between March 2013 and January 2014, the floral traits of all of the flowering plants found in, among four restoration sites of different ages and one reference site, were recorded and used to characterize pollination syndromes. Richness, abundance, and composition of pollination syndromes were related to season, age and width of the forest fragment, species richness and abundance of sampled plants, and also to the quality of the surrounding matrix. There were differences in the composition of syndromes among sampling units and among seasons. Richness and abundance of pollination syndromes varied among climatic periods, the highest values occurred at the end of the dry season and the start of the rainy season. Older, wider, and areas with more plants had higher values of richness and abundance of syndromes. The quality of the surrounding matrix influences only the richness of syndromes. It was concluded that floral traits are good indicators of ecological restoration of riparian forests and that the surrounding matrix contributes to the greater richness of syndromes. However, when planning for active restoration, attention should be given to the proper choice of plant species on the basis of pollination syndromes that should attract pollinators.     

Biotic interactions limit species richness in an alpine plant community,especially under experimental warming

The determinants of local species richness in plant communities have been the subject of much debate. Is species richness the result of stochastic events such as dispersal processes, or do local environmental filters sort species into communities according to their ecological niches? Recent studies suggest that these two processes simultaneously limit species richness, although their relative importance may vary in space and time. Understanding the limiting factors for species richness is especially important in light of the ongoing global warming, as new species establish in resident plant communities as a result of climate‐driven migration. We examined the relative importance of dispersal and environmental filtering during seedling recruitment and plant establishment in an alpine plant community subjected to seed addition and long‐term experimental warming. Seed addition increased species richness during the seedling recruitment stage, but this initial increase was cancelled out by a corresponding decrease in species richness during plant establishment, suggesting that environmental filters limit local species richness in the long term. While initial recruitment success of the sown species was related to both abiotic and biotic factors, long‐term establishment was controlled mainly by biotic factors, indicating an increase in the relative importance of biotic interactions once plants have germinated in a microhabitat with favourable abiotic conditions. The relative importance of biotic interactions also seemed to increase with experimental warming, suggesting that increased competition within the resident vegetation may decrease community invasibility as the climate warms.     

Plant history and soil history jointly influence the selection environment for plant species in a long‐term grassland biodiversity experiment

Long‐term biodiversity experiments have shown increasing strengths of biodiversity effects on plant productivity over time. However, little is known about rapid evolutionary processes in response to plant community diversity, which could contribute to explaining the strengthening positive relationship. To address this issue, we performed a transplant experiment with offspring of seeds collected from four grass species in a 14‐year‐old biodiversity experiment (Jena Experiment). We used two‐ and six‐species communities and removed the vegetation of the study plots to exclude plant–plant interactions. In a reciprocal design, we transplanted five “home” phytometers (same origin and actual environment), five “away‐same” phytometers (same species richness of origin and actual environment, but different plant composition), and five “away‐different” phytometers (different species richness of origin and actual environment) of the same species in the study plots. In the establishment year, plants transplanted in home soil produced more shoots than plants in away soil indicating that plant populations at low and high diversity developed differently over time depending on their associated soil community and/or conditions. In the second year, offspring of individuals selected at high diversity generally had a higher performance (biomass production and fitness) than offspring of individuals selected at low diversity, regardless of the transplant environment. This suggests that plants at low and high diversity showed rapid evolutionary responses measurable in their phenotype. Our findings provide first empirical evidence that loss of productivity at low diversity is not only caused by changes in abiotic and biotic conditions but also that plants respond to this by a change in their micro‐evolution. Thus, we conclude that eco‐evolutionary feedbacks of plants at low and high diversity are critical to fully understand why the positive influence of diversity on plant productivity is strengthening through time.     

Predicting individual plant performance in grasslands

Plant functional traits are widely used to predict community productivity. However, they are rarely used to predict individual plant performance in grasslands. To assess the relative importance of traits compared to environment, we planted seedlings of 20 common grassland species as phytometers into existing grassland communities varying in land‐use intensity. After 1 year, we dug out the plants and assessed root, leaf, and aboveground biomass, to measure plant performance. Furthermore, we determined the functional traits of the phytometers and of all plants growing in their local neighborhood. Neighborhood impacts were analyzed by calculating community‐weighted means (CWM) and functional diversity (FD) of every measured trait. We used model selection to identify the most important predictors of individual plant performance, which included phytometer traits, environmental conditions (climate, soil conditions, and land‐use intensity), as well as CWM and FD of the local neighborhood. Using variance partitioning, we found that most variation in individual plant performance was explained by the traits of the individual phytometer plant, ranging between 19.30% and 44.73% for leaf and aboveground dry mass, respectively. Similarly, in a linear mixed effects model across all species, performance was best predicted by phytometer traits. Among all environmental variables, only including land‐use intensity improved model quality. The models were also improved by functional characteristics of the local neighborhood, such as CWM of leaf dry matter content, root calcium concentration, and root mass per volume as well as FD of leaf potassium and root magnesium concentration and shoot dry matter content. However, their relative effect sizes were much lower than those of the phytometer traits. Our study clearly showed that under realistic field conditions, the performance of an individual plant can be predicted satisfyingly by its functional traits, presumably because traits also capture most of environmental and neighborhood conditions.     

A functional trait perspective on plant invasion

Background and Aims

Global environmental change will affect non-native plant invasions, with profound potential impacts on native plant populations, communities and ecosystems. In this context, we review plant functional traits, particularly those that drive invader abundance (invasiveness) and impacts, as well as the integration of these traits across multiple ecological scales, and as a basis for restoration and management.

Scope

We review the concepts and terminology surrounding functional traits and how functional traits influence processes at the individual level. We explore how phenotypic plasticity may lead to rapid evolution of novel traits facilitating invasiveness in changing environments and then ‘scale up’ to evaluate the relative importance of demographic traits and their links to invasion rates. We then suggest a functional trait framework for assessing per capita effects and, ultimately, impacts of invasive plants on plant communities and ecosystems. Lastly, we focus on the role of functional trait-based approaches in invasive species management and restoration in the context of rapid, global environmental change.

Conclusions

To understand how the abundance and impacts of invasive plants will respond to rapid environmental changes it is essential to link trait-based responses of invaders to changes in community and ecosystem properties. To do so requires a comprehensive effort that considers dynamic environmental controls and a targeted approach to understand key functional traits driving both invader abundance and impacts. If we are to predict future invasions, manage those at hand and use restoration technology to mitigate invasive species impacts, future research must focus on functional traits that promote invasiveness and invader impacts under changing conditions, and integrate major factors driving invasions from individual to ecosystem levels.     

Short-term effects of fire and competition on growth and plasticity of the yellow pitcher plant,Sarracenia alata (Sarraceniaceae)

Although recurrent fires are widely assumed to reduce competitive interference of plants of pine savannas, rarely has this assumption been tested explicitly. This 2-yr study reports on the interactive effects of fire and neighbors on short-term growth responses and plasticity in allocation patterns of a carnivorous plant, the yellow pitcher plant, Sarracenia alata. This species relies upon pitfall traps (pitchers) to attract and capture insects to obtain nutrients. Neighbors reduced the growth rate of individual ramet transplants (phytometers) in one but not both years of the study. The effect of neighbors on total (i.e., both above- and belowground) productivity of phytometers was not reduced by a winter fire. Neighbors had a greater effect on large plants than on small plants. Although fire did not affect the growth rate of phytometers in the short term, allocation patterns were greatly altered by both neighbors and fire. Allocation to pitchers increased at the expense of belowground organs following fire and in the absence of neighbors at the unburned site. Results of the current study suggest that adult pitcher plants may tolerate competition from neighboring vegetation by reducing allocation to costly pitchers during years without fire.     

The need for broader ecological and socioeconomic tools to evaluate the effectiveness of coral restoration programs

Coral reef restoration initiatives are burgeoning in response to the need for novel management strategies to address dramatic global declines in coral cover. However, coral restoration programs typically lack rigor and critical evaluation of their effectiveness. A review of 83 peer‐reviewed papers that used coral transplantation for reef restoration reveals that growth and survival of coral fragments were the most widely used indicators of restoration success, with 88% of studies using these two indicators either solely (55%) or in combination with a limited number of other ecological factors (33%). In 53% of studies, reef condition was monitored for 1 year or less, while only 5% of reefs were monitored for more than 5 years post‐transplantation. These results highlight that coral reef restoration science has focused primarily on short‐term experiments to evaluate the feasibility of techniques for ecological restoration and the initial establishment phase post‐transplantation, rather than on longer‐term outcomes for coral reef communities. Here, we outline 10 socioecological indicators that comprehensively evaluate the effectiveness of coral reef restoration across the four pillars of sustainability (i.e. environmental, sociocultural, governance, and economic contributions to sustainable communities). We recommend that evaluations of the effectiveness of coral restoration programs integrate ecological indicators with sociocultural, economic, and governance considerations. Assessing the efficacy of coral restoration as a tool to support reef resilience will help to guide future efforts and ensure the sustainable maintenance of reef ecosystem goods and services.     

Genetically based differentiation in growth of multiple non-native plant species along a steep environmental gradient

A non-native plant species spreading along an environmental gradient may need to adjust its growth to the prevailing conditions that it encounters by a combination of phenotypic plasticity and genetic adaptation. There have been several studies of how non-native species respond to changing environmental conditions along latitudinal gradients, but much less is known about elevational gradients. We conducted a climate chamber experiment to investigate plastic and genetically based growth responses of 13 herbaceous non-native plants along an elevational gradient from 100 to 2,000?m a.s.l. in Tenerife. Conditions in the field ranged from high anthropogenic disturbance but generally favourable temperatures for plant growth in the lower half of the gradient, to low disturbance but much cooler conditions in the upper half. We collected seed from low, mid and high elevations and grew them in climate chambers under the characteristic temperatures at these three elevations. Growth of all species was reduced under lower temperatures along both halves of the gradient. We found consistent genetically based differences in growth over the upper elevational gradient, with plants from high-elevation sites growing more slowly than those from mid-elevation ones, while the pattern in the lower part of the gradient was more mixed. Our data suggest that many non-native plants might respond to climate along elevational gradients by genetically based changes in key traits, especially at higher elevations where low temperatures probably impose a stronger selection pressure. At lower elevations, where anthropogenic influences are greater, higher gene flow and frequent disturbance might favour genotypes with broad ecological amplitudes. Thus the importance of evolutionary processes for invasion success is likely to be context-dependent.     

Salicylic acid and photosynthesis: signalling and effects

Salicylic acid (SA) is a well-known signalling molecule playing a role in local and systemic acquired resistance against pathogens as well as in acclimation to certain abiotic stressors. As a stress-related signalling compound, it may directly or indirectly affect various physiological processes, including photosynthesis. The effects of exogenously applied SA on plant physiological processes under optimal environmental conditions are controversial. Several studies suggest that SA may have a positive effect on germination or plant growth in various plant species. However, SA may also act as a stress factor, having a negative influence on various physiological processes. Its mode of action depends greatly on several factors, such as the plant species, the environmental conditions (light, temperature, etc.) and the concentration. Exogenous SA may also alleviate the damaging effects of various stress factors, and this protection may also be manifested as higher photosynthetic capacity. Unfavourable environmental conditions have also been shown to increase the endogenous SA level in plants. Recent results strongly suggest that controlled SA levels are important in plants for optimal photosynthetic performance and for acclimation to changing environmental stimuli. The present review discusses the effects of exogenous and endogenous SA on the photosynthetic processes under optimal and stress conditions.     

Restoration Success: How Is It Being Measured?

The criteria of restoration success should be clearly established to evaluate restoration projects. Recently, the Society of Ecological Restoration International (SER) has produced a Primer that includes ecosystem attributes that should be considered when evaluating restoration success. To determine how restoration success has been evaluated in restoration projects, we reviewed articles published in Restoration Ecology (Vols. 1[1]–11[4]). Specifically, we addressed the following questions: (1) what measures of ecosystem attributes are assessed and (2) how are these measures used to determine restoration success. No study has measured all the SER Primer attributes, but most studies did include at least one measure in each of three general categories of the ecosystem attributes: diversity, vegetation structure, and ecological processes. Most of the reviewed studies are using multiple measures to evaluate restoration success, but we would encourage future projects to include: (1) at least two variables within each of the three ecosystem attributes that clearly related to ecosystem functioning and (2) at least two reference sites to capture the variation that exist in ecosystems.     

Phylogenetic relatedness as a tool in restoration ecology: a meta-analysis

Biotic interactions assembling plant communities can be positive (facilitation) or negative (competition) and operate simultaneously. Facilitative interactions and posterior competition are among the mechanisms triggering succession, thus representing a good scenario for ecological restoration. As distantly related species tend to have different phenotypes, and therefore different ecological requirements, they can coexist, maximizing facilitation and minimizing competition. We suggest including phylogenetic relatedness together with phenotypic information as a predictor for the net effects of the balance between facilitation and competition in nurse-based restoration experiments. We quantify, by means of a Bayesian meta-analysis of nurse-based restoration experiments performed worldwide, the importance of phylogenetic relatedness and life-form disparity in the survival, growth and density of facilitated plants. We find that the more similar the life forms of neighbouring plants are the greater the positive effect of phylogenetic distance is on survival and density. This result suggests that other characteristics beyond life form are also contained in the phylogeny, and the larger the phylogenetic distance, the less is the niche overlap, and therefore the less is the competition. As a general rule, we can maximize the success of the nurse-based practices by increasing life-form disparity and phylogenetic distances between the neighbour and the facilitated plant.     

Ants as Indicators of Restoration Success: Relationship with Soil Microbial Biomass in the Australian Seasonal Tropics

Ants are widely used as bioindicators in Australian land assessment and monitoring programs, particularly in relation to ecosystem restoration following mining. Little is known, however, about the relationship between ant community development and key ecological processes such as nutrient cycling. We have examined the relationship between ant species richness and soil microbial biomass at 17 sites subject to disturbance by mining in the Kakadu region of Australia's Northern Territory. The number of ant species recorded ranged from 7 at an unvegetated site undergoing restoration to 43 at a site that was undisturbed except for edge effects. Soil microbial biomass ranged from 19.3 to 134.3 μgC/g. Ant species richness was positively correlated with soil microbial biomass (r= 0.638), more so than was plant species richness (r= 0.342 for total plant species, r= 0.499 for woody species only). Our findings demonstrate a correlation between aboveground ant activity and belowground decomposition processes at disturbed sites, thereby providing support for the use of ants as indicators of restoration success following disturbance. Interestingly, when a range of undisturbed sites in the region was considered, a negative rather than positive relationship between ant richness and soil microbial biomass was found. This illustrates the importance of distinguishing between variation within a habitat due to disturbance and variation across different habitats when searching for indicators of ecological change.     

Conservation efforts based on local ecological knowledge: The role of social variables in identifying environmental indicators

The incorporation of local ecological knowledge in monitoring processes has been one of the great challenges of conservation initiatives worldwide. Therefore, it is essential to use indicators as local evaluation tools of the conditions of a species in order to support conservation actions. Local populations observe the environment, climate change and the influence of these factors on the species they use. However, their observations and perceptions may vary depending on different social factors. We used as model two species of economic importance involved in sociobiodiversity product chains to evaluate the role of social variables in the identification of conservation indicators for this plants. The species studied were: Caryocar coriaceum Wittm. (locally known as pequi), and Himatanthus drasticus (Mart.) Plumel (locally known as janaguba). We also registered which indicators are perceived as the most important and what they are measuring. Our results show that the knowledge among collectors is homogeneous and that, generally, the social factors do not affect the knowledge on local indicators. Age and extraction time were factors that influenced the knowledge on climate indicators and population structure only for C. coriaceum. In the communities studied, collectors not only monitor the biological characteristics of the species, but also the environmental and climatic phenomena that are threatening the sustainability of the species. These results can help to improve our ability to manage information about natural resources, incorporating local ecological knowledge in the scientific process of evaluation and monitoring of biodiversity.