Quantitatively Evaluating Restoration Experiments: Research Design, Statistical Analysis, and Data Management Considerations

Conceptual and logistical challenges associated with the design and analysis of ecological restoration experiments are often viewed as being insurmountable, thereby limiting the potential value of restoration experiments as tests of ecological theory. Such research constraints are, however, not unique within the environmental sciences. Numerous natural and anthropogenic disturbances represent unplanned, uncontrollable events that cannot be replicated or studied using traditional experimental approaches and statistical analyses. A broad mix of appropriate research approaches (e.g., long-term studies, large-scale comparative studies, space-for-time substitution, modeling, and focused experimentation) and analytical tools (e.g., observational, spatial, and temporal statistics) are available and required to advance restoration ecology as a scientific discipline. In this article, research design and analytical options are described and assessed in relation to their applicability to restoration ecology. Significant research benefits may be derived from explicitly defining conceptual models and presuppositions, developing multiple working hypotheses, and developing and archiving high-quality data and metadata. Flexibility in research approaches and statistical analyses, high-quality databases, and new sampling approaches that support research at broader spatial and temporal scales are critical for enhancing ecological understanding and supporting further development of restoration ecology as a scientific discipline.     

Echinacea angustifolia and its specialist ant‐tended aphid: a multi‐year study of manipulated and naturally‐occurring aphid infestation

1. The impact of herbivores on plant fitness depends on multiple ecological mechanisms, including interactions between herbivore guilds. 2. This study assessed the effects of a specialist aphid (Aphis echinaceae) on performance and foliar herbivore damage of a long‐lived perennial plant (Echinacea angustifolia) native to the North American tallgrass prairie. A 2‐year field experiment manipulating aphid infestation on 100 plants was compared with concurrent and past observations of unmanipulated plants in the same outdoor experimental plot. Because ants co‐occur with aphids, the experiment tested the combined effects of aphids and ants. 3. Neither manipulated nor naturally‐occurring aphid infestations led to measurable declines in plant performance. Results for foliar herbivore damage differed between experimental and observational studies: the occurrence of foliar herbivore damage decreased with aphid infestation in the first year of the experiment and increased with aphid infestation over 5 years in unmanipulated plants. 4. While the experimental results concur with other experiments of ant–hemipteran–herbivore relationships, the observational results suggest that ant–aphid interactions do not naturally play a major role in determining patterns of foliar herbivory in this system. This result demonstrates the value of using field observations to interpret the relevance of experimental results.     

Science, Art, or Application—the "Karma" of Restoration Ecology

The present state of restoration ecology is far away from Bradshaw’s “acid test for ecology.” The conclusions drawn from the series of papers in this issue and from the Jena workshop suggest some directions in which the field may progress. More attention must be paid to the degraded state, which should be evaluated by its specific features and carefully analyzed before any restoration plan is laid down. Restoration goals have to be realistic, which includes the appreciation of globally changing conditions, resulting in a paradigm‐shift toward “forward‐restoration.” Basically, the transition from the degraded state conditions to the target state is a kind of succession that is manipulated by the application of goal‐orientated and system‐specific disturbances. Whenever possible, restorationists should step back and make use of naturally occurring succession, which requires a sophisticated restoration strategy, involving flexible management responses, multiple alternative target states, robust measurements for the restoration progress, and careful long‐term monitoring. The unique feature of restoration ecology is the involvement of socioeconomic decisions, and conceptual frameworks for ecological restoration have to implement the specific links to natural succession. To bridge the gap between ecological theory and on the ground restoration, it is essential that restoration practice is translated into the vocabulary and thinking of basic ecology. If all these aspects are integrated, ecological restoration as an application—and restoration ecology as an applied science—may develop into an acid test for our understanding of interactions between people and their environment, rather than for pure ecology.     

Policy Language in Restoration Ecology

Relating restoration ecology to policy is one of the aims of the Society for Ecological Restoration and its journal Restoration Ecology. As an interdisciplinary team of researchers in both ecological science and political science, we have struggled with how policy‐relevant language is and could be deployed in restoration ecology. Using language in scientific publications that resonates with overarching policy questions may facilitate linkages between researcher investigations and decision‐makers' concerns on all levels. Climate change is the most important environmental problem of our time and to provide policymakers with new relevant knowledge on this problem is of outmost importance. To determine whether or not policy‐specific language was being included in restoration ecology science, we surveyed the field of restoration ecology from 2008 to 2010, identifying 1,029 articles, which we further examined for the inclusion of climate change as a key element of the research. We found that of the 58 articles with “climate change” or “global warming” in the abstract, only 3 identified specific policies relevant to the research results. We believe that restoration ecologists are failing to include themselves in policy formation and implementation of issues such as climate change within journals focused on restoration ecology. We suggest that more explicit reference to policies and terminology recognizable to policymakers might enhance the impact of restoration ecology on decision‐making processes.     

Insights from a Cross‐Disciplinary Seminar: 10 Pivotal Papers for Ecological Restoration

Restoration ecology is a deepening and diversifying field with current research incorporating multiple disciplines and infusing long‐standing ideas with fresh perspectives. We present a list of 10 recent pivotal papers exemplifying new directions in ecological restoration that were selected by students in a cross‐disciplinary graduate seminar at the University of California, Berkeley. We highlight research that applies ecological theory to improve restoration practice in the context of global change (e.g. climate modeling, evaluation of novel ecosystems) and discuss remaining knowledge gaps. We also discuss papers that recognize the social context of restoration and the coupled nature of social and ecological systems, ranging from the incorporation of cultural values and Traditional Ecological Knowledge into restoration, to the consideration of the broader impacts of markets on restoration practices. In addition, we include perspectives that focus on improving communication between social and natural scientists as well as between scientists and practitioners, developing effective ecological monitoring, and applying more integrated, whole‐landscape approaches to restoration. We conclude with insights on recurrent themes in the papers regarding planning restoration in human‐modified landscapes, application of ecological theory, improvements to restoration practice, and the social contexts of restoration. We share lessons from our cross‐disciplinary endeavor, and invite further discussion on the future directions of restoration ecology through contributions to our seminar blog site http://restecology.blogspot.com .     

Integrating trait‐based empirical and modeling research to improve ecological restoration

A global ecological restoration agenda has led to ambitious programs in environmental policy to mitigate declines in biodiversity and ecosystem services. Current restoration programs can incompletely return desired ecosystem service levels, while resilience of restored ecosystems to future threats is unknown. It is therefore essential to advance understanding and better utilize knowledge from ecological literature in restoration approaches. We identified an incomplete linkage between global change ecology, ecosystem function research, and restoration ecology. This gap impedes a full understanding of the interactive effects of changing environmental factors on the long‐term provision of ecosystem functions and a quantification of trade‐offs and synergies among multiple services. Approaches that account for the effects of multiple changing factors on the composition of plant traits and their direct and indirect impact on the provision of ecosystem functions and services can close this gap. However, studies on this multilayered relationship are currently missing. We therefore propose an integrated restoration agenda complementing trait‐based empirical studies with simulation modeling. We introduce an ongoing case study to demonstrate how this framework could allow systematic assessment of the impacts of interacting environmental factors on long‐term service provisioning. Our proposed agenda will benefit restoration programs by suggesting plant species compositions with specific traits that maximize the supply of multiple ecosystem services in the long term. Once the suggested compositions have been implemented in actual restoration projects, these assemblages should be monitored to assess whether they are resilient as well as to improve model parameterization. Additionally, the integration of empirical and simulation modeling research can improve global outcomes by raising the awareness of which restoration goals can be achieved, due to the quantification of trade‐offs and synergies among ecosystem services under a wide range of environmental conditions.     

The effects of management on vegetation trajectories during the early‐stage restoration of previously arable land after hay transfer

The restoration of floodplain grasslands has benefited from many studies of the underlying mechanisms. Among the operational tools that resulted, hay transfer is now used increasingly to alleviate the effects of limited seed dispersal and recruitment. To improve this method, we still need to understand how it can affect restoration trajectories, and particularly their direction and magnitude during the early stages of restoration. Based on concepts from the field of community ecology theory, we investigated the effects of early‐stage management through grazing or mowing on restoration trajectories after soil harrowing and hay transfer. We established a randomized block design experiment and quantified several community‐related metrics to formalize restoration trajectories for 3 years after hay transfer on a previously arable alluvial island in southwestern France. Whatever the management treatment, the species richness and evenness were significantly higher in hay‐inoculated than in control plots. This effect was linked to the recruitment of species originating not only from the reference grassland through hay transfer, but also from the seed bank, a well‐known effect of soil harrowing. Although generally oriented toward the reference grassland, the origin, direction, and magnitude of the trajectory of hay‐inoculated plots all depended on the management applied. Sheep grazing applied at the same time as hay transfer enhanced the recruitment of reference species as from the first experimental year, because it controlled aboveground competition and maintained the window of opportunity open for a sufficiently longer period of time. Our findings show that the type of management applied simultaneously to hay transfer influences the origin of a grassland trajectory, while its direction and magnitude are dependent on the management applied in subsequent years. Grazing immediately after hay transfer may be appropriate to accelerate the recruitment of species from the reference grassland.     

The ecology of restoration: historical links, emerging issues and unexplored realms

Restoration ecology is a young academic field, but one with enough history to judge it against past and current expectations of the science's potential. The practice of ecological restoration has been identified as providing ideal experimental settings for tests of ecological theory; restoration was to be the 'acid test' of our ecological understanding. Over the past decade, restoration science has gained a strong academic foothold, addressing problems faced by restoration practitioners, bringing new focus to existing ecological theory and fostering a handful of novel ecological ideas. In particular, recent advances in plant community ecology have been strongly linked with issues in ecological restoration. Evolving models of succession, assembly and state-transition are at the heart of both community ecology and ecological restoration. Recent research on seed and recruitment limitation, soil processes, and diversity–function relationships also share strong links to restoration. Further opportunities may lie ahead in the ecology of plant ontogeny, and on the effects of contingency, such as year effects and priority effects. Ecology may inform current restoration practice, but there is considerable room for greater integration between academic scientists and restoration practitioners.     

On the Status of Restoration Science: Obstacles and Opportunities

Terrestrial restoration ecology is not as well developed as aquatic and wetland restoration. There are several key obstacles to progress in restoration ecology, but these obstacles may also be viewed as opportunities to exploit. One obstacle is demonstration science, or an overreliance on simplistic experiments with few treatment factors and few levels of those factors. Complex, multivariate experiments yield greater insights, especially when teamed with sophisticated methods of data analysis. A second key obstacle is myopic scholarship that has led to little synthesis and weak conceptual theory. A greater awareness of and explicit references to ecological principles will help develop the conceptual basis of restoration science. Where should restoration ecology be headed? We should consider forming partnerships with developers, landscape artists, and industry to do complex, large‐scale experiments and make restoration a more common part of everyday life.     

The restoration of tropical seed dispersal networks

Human activities have led to the loss of habitats and biodiversity in the Atlantic Rain Forest in Brazil. Ecological restoration aims to rebuild this biome and should include not only the reinstatement of species but also the reestablishment of complex ecological interactions and the ecological functions that they provide. One such function is seed dispersal, which is provided by the interactions between animal frugivores and plants. We studied seed dispersal networks in 3 different tropical forest sites restored 15, 25, and 57 years ago; temporal scales rarely observed in restoration studies. We investigated changes in network structure (nestedness, modularity, and network specialization) in these communities over restoration time. Although network size and the number of interactions increased with time since restoration, the networks were composed of generalist birds, and the large frugivores remained absent. Contrary to our expectations though, species richness was highest in the 25‐year‐old site, maybe due to the higher number of species used in the planting. Nestedness values were low in all 3 networks, but the highest nestedness was observed in the intermediate‐aged site. However, the oldest network was significantly modular and showed higher complementary specialization. These results suggest that 57 years after restoration, the complexity of mutualistic interactions in seed dispersal networks has increased, this enhancing ecosystem function in the Atlantic forest.     

How mutualisms arise in phytoplankton communities: building eco‐evolutionary principles for aquatic microbes

Extensive sampling and metagenomics analyses of plankton communities across all aquatic environments are beginning to provide insights into the ecology of microbial communities. In particular, the importance of metabolic exchanges that provide a foundation for ecological interactions between microorganisms has emerged as a key factor in forging such communities. Here we show how both studies of environmental samples and physiological experimentation in the laboratory with defined microbial co‐cultures are being used to decipher the metabolic and molecular underpinnings of such exchanges. In addition, we explain how metabolic modelling may be used to conduct investigations in reverse, deducing novel molecular exchanges from analysis of large‐scale data sets, which can identify persistently co‐occurring species. Finally, we consider how knowledge of microbial community ecology can be built into evolutionary theories tailored to these species’ unique lifestyles. We propose a novel model for the evolution of metabolic auxotrophy in microorganisms that arises as a result of symbiosis, termed the Foraging‐to‐Farming hypothesis. The model has testable predictions, fits several known examples of mutualism in the aquatic world, and sheds light on how interactions, which cement dependencies within communities of microorganisms, might be initiated.     

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.     

Impacts of management and antecedent site condition on restoration outcomes in a sand prairie

Landscape context and site history, including antecedent site conditions, may constrain restoration potential despite the efforts of restoration practitioners. However, few experimental studies have investigated the relative importance of antecedent site conditions and the intensity of on‐site management in driving restoration outcomes. We established small‐scale prairie restoration experiments within the Lost Mound Unit of the Upper Mississippi River National Wildlife and Fish Refuge in Illinois, U.S.A. We investigated the effectiveness of two restoration treatments, herbicide application and seeding of native plants, on removal of invasive crown‐vetch (Securigera varia) and recovery of sand prairie plant communities. We replicated treatment plots across 15 locations with three levels of antecedent condition and fire treatment (burned, undegraded; burned, degraded; and unburned, degraded) to determine whether antecedent condition constrained the effectiveness of on‐site restoration. Two years after initial herbicide application crown‐vetch cover was significantly reduced relative to untreated controls. This effect was more pronounced in plots treated twice with herbicide. However, removal of crown‐vetch facilitated invasion by Kentucky bluegrass (Poa pratensis). Addition of native prairie seed had little effect on restoration outcomes, regardless of herbicide application. Native community recovery was greater in plots restored in less degraded locations. Herbicide application tended to increase native species cover, but importantly, this effect was significant only in the least degraded locations. Intensive restoration management conducted in degraded landscapes can result in undesirable outcomes such as secondary species invasion. Reestablishment of native species following restoration is more likely where the surrounding remnant communities are intact.     

An Assessment of Introductory Restoration Courses in the United States and Canada

A considerable number of institutions offer courses in restoration ecology and its application, ecological restoration. We quantified the scope and structure of introductory restoration courses at 67 post‐secondary institutions by reviewing institutional course catalogs and course syllabi. Most courses were available at Research‐level institutions. More than half of the courses were offered within departments that focused on natural resource management, and were required or optional in a degree program. Most courses were taught in classroom settings during the academic year and were geared toward advanced students. Course titles suggested an emphasis on the science of restoration ecology over the practice of ecological restoration, and learning objectives focused primarily on concepts and less on skills and attitudes. Assessment was largely via conventional methods, notably exams. Many courses assigned readings from the primary literature; there was little consensus in terms of text selection. We conclude that restoration is being presented to students as an advanced undertaking and in largely theoretical terms. Although we were unable to consider other important elements such as thematic content, class size, or pedagogical method, our study provides a baseline assessment of introductory restoration courses that can be used to evaluate changes in restoration education or opportunities for restoration education in other countries. These results can inform the development of new introductory restoration courses, and raise important considerations in light of the development of a Practitioners' Certification Program by the Society for Ecological Restoration.     

Present State and Future Perspectives of Restoration Ecology—Introduction

Although the aim of and the need for ecological restoration, and restoration ecology as its scientific base, are obvious, the field is still struggling with defining its basics. This situation, reflected by the debate about alternative terms to replace “restoration,” the ambiguous self‐image as a movement, art, application, or science, and the lack of a unifying conceptual framework, results in an uncertainty about the future development of the field. In a 10‐year project, an interdisciplinary Research Training Group in Jena followed the regeneration of one degraded terrestrial and aquatic ecosystem, respectively, and suggested a conceptual model for regeneration and restoration that was derived from the shared features of the two systems. As part of the scientific discussion of this new approach, an international workshop “Present State and Future Perspectives of Restoration Ecology” was organized in Jena in November 2004. The following collection of 12 opinion papers and 1 concluding chapter reflect the discussions at the workshop and contributes to the “self‐finding” process of restoration ecology.     

Formalizing the definition of meta‐analysis in Molecular Ecology

Meta‐analysis, the statistical synthesis of pertinent literature to develop evidence‐based conclusions, is relatively new to the field of molecular ecology, with the first meta‐analysis published in the journal Molecular Ecology in 2003 (Slate & Phua 2003). The goal of this article is to formalize the definition of meta‐analysis for the authors, editors, reviewers and readers of Molecular Ecology by completing a review of the meta‐analyses previously published in this journal. We also provide a brief overview of the many components required for meta‐analysis with a more specific discussion of the issues related to the field of molecular ecology, including the use and statistical considerations of Wright's F_ST and its related analogues as effect sizes in meta‐analysis. We performed a literature review to identify articles published as ‘meta‐analyses’ in Molecular Ecology, which were then evaluated by at least two reviewers. We specifically targeted Molecular Ecology publications because as a flagship journal in this field, meta‐analyses published in Molecular Ecology have the potential to set the standard for meta‐analyses in other journals. We found that while many of these reviewed articles were strong meta‐analyses, others failed to follow standard meta‐analytical techniques. One of these unsatisfactory meta‐analyses was in fact a secondary analysis. Other studies attempted meta‐analyses but lacked the fundamental statistics that are considered necessary for an effective and powerful meta‐analysis. By drawing attention to the inconsistency of studies labelled as meta‐analyses, we emphasize the importance of understanding the components of traditional meta‐analyses to fully embrace the strengths of quantitative data synthesis in the field of molecular ecology.     

Heterogeneity of ecological patterns,processes, and funding of marine manipulative field experiments conducted in Southeastern Pacific coastal ecosystems

Ecological manipulative experiments conducted in marine coastal ecosystems have substantially improved ecological theory during the last decades and have provided useful knowledge for the management and conservation of coastal ecosystems. Although different studies report global trends in ecological patterns worldwide, Southeastern Pacific coastal ecosystems have been poorly considered. Given that the SE Pacific coast encompasses diverse coastal ecosystems, consideration of studies conducted along this range can shed light on the heterogeneity of processes regulating coastal communities. We reviewed the biotic interactions and habitat type considered, as well as the complexity in terms of spatial and temporal extent of manipulative field experimental studies conducted along the SE Pacific coast from 0°S to 56°S (Ecuador to Chile). We test the effect of funding reported by different studies as a main factor limiting experimental complexity. From field ecological studies published from 1970 to 2016, we found that 81 studies were truly manipulative, in which one or multiple factors were “manipulated.” Around 77% of these studies were located between 21°S and 40°S, and conducted in intertidal rocky habitats. An increase in experimental studies was observed between 2010 and 2015, especially focused on herbivore–alga interactions, although we found that both the temporal extent and spatial extent of these studies have shown a decrease in recent decades. Funding grant amount reported had a positive effect on elapsed time of field experiments, but no effect was observed on spatial extent or in the biotic interactions considered. Elapsed time of experiments was different among the main biotic interactions considered, that is, herbivory, predation, and competition. We suggest that to further progress in applied ecological knowledge, it will be necessary to consider pollution and urbanization processes explicitly using a field experimental framework. This information could improve our understanding of how ecosystems present along the SE Pacific coast respond to climate change and increased levels of human interventions.     

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.