**Nature-Based Solutions**

Editors

**Panayiotis Dimitrakopoulos Mario A. Pagnotta Miklas Scholz Arshiya Noorani**

Basel • Beijing • Wuhan • Barcelona • Belgrade • Novi Sad • Cluj • Manchester

*Editors*

Panayiotis Dimitrakopoulos University of the Aegean Mytilene Greece

Mario A. Pagnotta Tuscia University Viterbo Italy

Miklas Scholz atene KOM Berlin Germany

Arshiya Noorani FAO Rome Italy

*Editorial Office* MDPI St. Alban-Anlage 66 4052 Basel, Switzerland

This is a reprint of articles from the Topic published online in the open access journals *Sustainability* (ISSN 2071-1050), *Forests* (ISSN 1999-4907), *Land* (ISSN 2073-445X), and *Plants* (ISSN 2223-7747) (available at: https://www.mdpi.com/topics/Nat Sol).

For citation purposes, cite each article independently as indicated on the article page online and as indicated below:

Lastname, A.A.; Lastname, B.B. Article Title. *Journal Name* **Year**, *Volume Number*, Page Range.

**ISBN 978-3-0365-9206-0 (Hbk) ISBN 978-3-0365-9207-7 (PDF) doi.org/10.3390/books978-3-0365-9207-7**

Cover image courtesy of Panayiotis Dimitrakopoulos

© 2023 by the authors. Articles in this book are Open Access and distributed under the Creative Commons Attribution (CC BY) license. The book as a whole is distributed by MDPI under the terms and conditions of the Creative Commons Attribution-NonCommercial-NoDerivs (CC BY-NC-ND) license.

## **Contents**

Reprinted from: *Land* **2022**, *11*, 748, doi:10.3390/land11050748 .................... **149**

## **About the Editors**

#### **Panayiotis Dimitrakopoulos**

Panayiotis Dimitrakopoulos is Professor of Functional Ecology at the Department of Environment of the University of the Aegean, Greece. He obtained his Ph.D. degree from the University of the Aegean in 2001. His postdoctoral research was carried out at the University of Zurich, Switzerland, and was funded by the European Science Foundation (LINKECOL program). His research focuses on functional plant ecology, community ecology, biodiversity conservation, and conservation policy. He has served as President of the Hellenic Ecological Society (2012–2014), member of the "Natura 2000" National Committee (2010–2020), and Honorary Visiting Senior Fellow at Anglia Ruskin University, Cambridge (2019–2022). He serves as Section Editor-in-Chief of Ecology in Biology (Basel) and is a member of the editorial board of six journals and referee for more than 60 journals. He has published more than 90 papers in peer-reviewed journals.

#### **Mario A. Pagnotta**

Mario A. Pagnotta is Associate Professor of Agricultural genetics at the University of Tuscia. His activities have included project management, student supervising, lecturing, and participation in several national and international projects. The research activity focuses mainly on the assessment of genetic variability in natural populations, landraces, and the characterization of plant germplasm of several species, and the relationship between genetic variation and edaphic factors, as well as on topics related with the biodiversity conservation, adaptation and variety identification. The analyses are conducted using traditional and advanced methodologies, based on different kinds of molecular markers. Particular attention is paid to the resistance to abiotic stress, especially drought stress, looking also at the distribution and identification of SNP markers for genes related to drought and salt tolerance. He has reviewed several projects and edited scientific papers for several journals. He is on the Editorial Board of *Diversity* (MDPI), serving as Editor-in-Chief of the "Plant Diversity" section. He also acts as Associate Editor for *Frontiers in Plant Science*, in the "Plant Abiotic Stress" section.

#### **Miklas Scholz**

Miklas Scholz, cand ing, BEng (equiv), PgC, MSc, PhD, DSc, CWEM, CEnv, CSci, CEng, FHEA, FIEMA, FCIWEM, FICE, Fellow of IWA, Fellow of IETI is a Distinguished Professor at Johannesburg University, South Africa. Miklas holds the title of Chair in Civil Engineering as a Professor at The University of Salford, UK, and he is also a Senior Expert in Water Management for atene KOM, Germany, a Technical Specialist for Nexus by Sweden, Sweden, and a Hydraulic Engineer for Adams Kunststofftechnik, Germany. He has published 6 books and 311 journal articles. Prof. Scholz's total citations amount to approximately 13660 (above 8510 citations since 2018), resulting in an h-index of 57 and an i10-Index of 227. He belongs to the top 2% of academics regarding the i10-index in the past five years. Miklas also belongs to the World's Top 2% of scientists according to Stanford University. A bibliometric analysis of all constructed wetland-related publications and corresponding authors with a minimum number of 20 publications and 100 citations indicates that Miklas is 5th in the world out of approximately 70 authors (including those who have sadly passed away). In 2019, Prof. Scholz was awarded EURO 7M for the EU H2020 REA project Water Retention and Nutrient Recycling in Soils and Streams for Improved Agricultural Production (WATERAGRI). He received EURO 1.52M for the JPI Water 2018 project Research-based Assessment of Integrated approaches to Nature-based Solutions (RAINSOLUTIONS).

#### **Arshiya Noorani**

Arshiya Noorani is an Agricultural Officer based at at FAO headquarters in Rome, and is a member of the Seeds and Plant Genetic Resources Team, Plant Production and Protection Division (AGP). Arshiya has been with FAO since 2011 but has been working since 2000 in the conservation, assessment and management of biodiversity, including protected areas. She holds a PhD in Plant Conservation Genetics, an MSc in Environmental Protection and Management, and BSc (Hons) in Zoology. Prior to joining FAO, she worked on in situ conservation and on-farm management of plant genetic resources for food and agriculture at Bioversity International. She previously taught ecological surveying and protected area management planning in both terrestrial and freshwater habitats at the University of Edinburgh. At FAO, Arshiya works on developing and implementing projects, developing technical guidelines as well as assessing data submitted by Members when monitoring the conservation and use of plant genetic resources. She supports Members in the implementation of the rolling Global of Action for Plant Genetic Resources for Food and Agriculture and the associated reporting, which feed into the preparation of global periodic assessments. She is contributes to FAO's normative work, especially through the Commission on Genetic Resources for Food and Agriculture and the International Treaty on Plant Genetic Resources for Food and Agriculture.

### **Preface**

'Nature-based solutions' (NbS) is an umbrella term for ecosystem-based approaches. It includes several actions in harmony with natural principles to achieve development goals and addressing challenges while benefitting human livelihoods and the environment. The NbS approach encompasses actions that are carried out in a participatory manner, in collaboration with diverse stakeholders, such as local communities and policy makers, focusing on key elements such as protection, restoration or management of ecosystems and ecosystem services; sustainable management of water systems, coastal areas, arable, grassland, and forest areas; and the creation of green zones in and around urban and peri-urban areas. In this multidisciplinary topic, 18 review, research and data papers have been published covering a variety of topics including, inter alia, (a) natural and green infrastructures, (b) ecosystem-based management approaches, (c) ecosystem and biodiversity conservation, (d) ecosystem-based adaptation and climate change adaptation, and (e) nature-based recreational activities. As humanity faces two interdependent crises, i.e., the climate-biodiversity nexus, nature-based solutions are seen as the way forward in transformative change, implemented at the local, national and international level.

### **Panayiotis Dimitrakopoulos, Mario A. Pagnotta, Miklas Scholz, and Arshiya Noorani** *Editors*

### *Review* **Bibliometric Analysis and Comprehensive Review of Stormwater Treatment Wetlands: Global Research Trends and Existing Knowledge Gaps**

**Nash Jett D. G. Reyes, Franz Kevin F. Geronimo, Heidi B. Guerra and Lee-Hyung Kim \***

Civil and Environmental Engineering Department, Kongju National University, Cheonan City 31080, Republic of Korea

**\*** Correspondence<EMAIL_ADDRESS>
**Abstract:** Stormwater treatment wetlands are widely recognized as efficient and cost-effective solutions to growing stormwater problems. This study presented a new approach to evaluating the current status and trends in stormwater treatment wetlands research. The annual scientific productivity of different states was identified using a bibliometric analysis approach. The number of publications related to stormwater treatment wetlands has exhibited an increasing trend since the earliest record of publication. USA and China were among the states that had the most number of stormwater treatment wetlands-related publications and international collaborations. In terms of the population-to-publication ratio, Australia, Canada, and South Korea were found to have a higher level of scientific productivity. Analysis of frequently used keywords and terms in scientific publications revealed that the efficiency of stormwater treatment wetlands and the processes involved in the removal of nutrients and trace elements were adequately investigated; however, inquiries on the removal of organic micropollutants and emerging pollutants, such as pharmaceuticals and personal care products, microplastics, and industrial compounds, among others, are still lacking. Through the comprehensive review of related scientific works, the design, components, and primary factors affecting the performance of stormwater treatment wetlands were also identified. Future works that address the aforementioned knowledge gaps are recommended to optimize the benefits of stormwater treatment wetlands.

**Keywords:** bibliometrics; constructed wetland; nature-based solution; stormwater management

#### **1. Introduction**

Stormwater management is an essential component of land-use planning and development. Over the past decades, stormwater-related disasters have continued to aggravate due to the conversion of natural land cover into impermeable areas and other forms of land-use changes [1]. Flooding is a natural disaster that affects the largest number of people. In the year 2014, it was estimated that approximately 16 billion USD and 1500 casualties were recorded due to flooding incidents [2]. Despite being a natural phenomenon, flood risks may also be influenced by land use and land-use changes. Urban areas experience higher flood risks since urban areas are characterized by a high percentage of impervious land cover or built-up zones that facilitate increased rainfall-to-runoff conversion and greater overland flow. Moreover, deforestation and the loss of vegetative cover stimulate runoff formation in headwater locations [3].

Stormwater is also an imminent threat to the environment and human health. Stormwater runoff contains a complex mixture of pollutants from natural and anthropogenic sources. A number of studies have indicated that stormwater runoff serves as a major source of water pollution and toxicity. Heavy metals are among the most toxic compounds that can be found in stormwater. Ma et al. (2016) developed a hazard index to identify the heavy metal species present in stormwater that can pose the highest risk to human health. The

**Citation:** Reyes, N.J.D.G.; Geronimo, F.K.F.; Guerra, H.B.; Kim, L.-H. Bibliometric Analysis and Comprehensive Review of Stormwater Treatment Wetlands: Global Research Trends and Existing Knowledge Gaps. *Sustainability* **2023**, *15*, 2332. https://doi.org/10.3390/ su15032332

Academic Editors: Panayiotis Dimitrakopoulos, Mario A. Pagnotta, Miklas Scholz and Arshiya Noorani

Received: 6 December 2022 Revised: 20 January 2023 Accepted: 24 January 2023 Published: 27 January 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

1

results indicated that chromium (Cr), manganese (Mn), and lead (Pb) were among the most toxic heavy metals that pose adverse effects to human health despite their relatively low concentrations in stormwater [4]. Apart from heavy metals, xenobiotic organic carbons, including pesticides and polycyclic aromatic hydrocarbons (PAHs), may also have detrimental effects on the environment [5]. Pesticides are associated with aquatic toxicity and biodiversity loss, whereas PAHs are known to possess human health and environmental toxicity [6,7].

The characteristics and amounts of pollutants in stormwater greatly depend on the land use and potential sources of pollution within the catchment. In the study conducted by Yang and Toor (2018), non-point phosphorus pollution in urban catchments originated from stormwater runoff [8]. Lee et al. (2020) reported the presence of pathogenic bacteria, protists, and fungi in stormwater that can potentially trigger an increase in water-borne disease outbreaks [9]. In urban areas, high vehicular traffic and anthropogenic activities may increase the pollutant concentrations in stormwater. Variable concentrations of toxic compounds (i.e., heavy metals, PAHs, pesticides, etc.) were observed by Zgheib et al. (2012) in the stormwater samples collected from densely populated urban areas [10]. In a more recent study, Pramanik et al. (2020) identified different emerging pollutants, such as perand polyfluorinated substances and microplastics, in urban runoff [11]. The stormwater from agricultural areas also contains a considerable amount of pollutants that can potentially degrade the quality of receiving water bodies. Specifically, agrichemicals and organic materials that are incorporated in stormwater can be the primary drivers of water quality degradation. Generally, insufficient or inappropriate stormwater management schemes can lead to severe economic, environmental, and human health consequences.

Constructed wetlands (CWs) are increasingly utilized as efficient and effective stormwater treatment technologies. These engineered systems were designed as nature-based facilities that utilize biological and physico-chemical mechanisms to improve water quality. Additionally, CWs also provide provisioning, cultural, supporting, and other ecosystem services that benefit humans and the environment [12]. The effectiveness of CWs in treating stormwater runoff was widely reported in different scientific publications. Stefanakis (2019) highlighted the importance of CWs in urban stormwater and wastewater management [13]. The performance of CWs as stormwater runoff intervention facilities in the upstream regions of a watershed was investigated by Kabenge et al. (2018). It was found that vegetated microcosm wetlands effectively reduced pollutant concentrations in the stormwater by up to 76% [14]. Alihan et al. (2017) recommended the use of CWs for treating urban stormwater runoff. The CWs, which treat runoff from impervious roads and parking lots, effectively reduced the total runoff volume and pollutant concentrations by up to 37% and 81%, respectively [15]. Studies regarding the applicability of CWs in agricultural runoff treatment were also conducted by several authors. The horizontal subsurface flow CW evaluated by Grinberga and Lagzdins (2017) exhibited a considerably reduced concentration of nutrients in the stormwater runoff from an agricultural farmyard [16]. Apart from nutrients, McMaine et al. (2019) reported that constructed wetlands were capable of reducing the concentration of pesticides in plant nursery runoff by more than 79% [17]. The valuable contribution of constructed wetlands as sediment traps was highlighted in the study conducted by Ockenden et al. (2014). It was estimated that small CWs can intercept up to 70 tons of sediment from agricultural runoff over the period of three years, thus significantly reducing the sediment loads to waterways [18].

Review papers also provided considerable information regarding treatment efficiency, design, and other factors that affect the performance of constructed wetlands in managing stormwater. The removal pathways of heavy metals in constructed wetlands were reviewed by Headley and Tanner (2006), whereas Sharma et al. (2021) summarized the constructed wetland mechanisms involved in the effective removal of heavy metals and nutrients in stormwater [19,20]. Ingrao et al. (2020) compiled different studies related to the environmental and operational issues of constructed wetlands [21]. In the synthesis conducted by Li et al. (2018), several scientific publications regarding the performance of

constructed wetlands in treating non-point source (NPS) pollution were highlighted [22]. Despite a large number of studies and review papers, there are currently no bibliometric analyses conducted to determine the current status of publication about the application of constructed wetlands in stormwater management. Therefore, this study was conducted to establish the trends of scientific publications focused on constructed wetlands used for stormwater management through a bibliometric analysis approach. The data from the extensive collection of published research works were used to determine the scientific productivity of various authors, institutions, and states in terms of the number of publications and citations. A comprehensive review was also conducted to create a detailed summary of the facility and catchment area characteristics, pollutant concentrations, the effectiveness of stormwater treatment wetlands in improving water quality, and other pertinent information contained in relevant scientific publications. Ultimately, the major research hotspots, knowledge gaps, and future research directions were also identified in this review.

#### **2. Materials and Methods**

#### *2.1. Data Collection and Bibliometric Analysis*

The Web of Science (WoS) platform is one of the most reliable and comprehensive scientific databases that is commonly used for bibliometric analysis [23]. A standard document search was conducted in the Science Citation Index Expanded (SCI-Expanded) and Emerging Sources Citation Index (ESCI) collections of the WoS platform. The terms ("constructed wetland\*" OR "treatment wetland\*" OR "engineered wetland\*" OR "artificial wetland\*") AND ("stormwater\*" or "storm water\*") were used to retrieve all documents related to the search term. In the analysis field, all documents containing the search terms in the title, abstract, keywords, keywords plus, and publications from the earliest records available in WoS (1 January 1990) up to 31 December 2021 were considered. The bibliographic information exported from the database includes authors, titles, sources, abstracts, author keywords, affiliations, and cited references. Initial query results returned a total of 452 documents. Among the list, 414 documents were classified as articles, 34 were review papers, seven were proceedings papers, and seven documents were classified as editorial materials, corrections, and news items. The list was further downsized to articles written in English, thus resulting in a total of 413 documents used in the analysis. The detailed process of data collection and the processes associated with the bibliometric analysis were illustrated in Figure 1.

**Figure 1.** Data collection and analysis flowchart.

#### *2.2. Data Visualization and Science Mapping*

Aside from determining the trends and status of research, the bibliometric analysis approach also provides an overview of the interrelationships among the terms, authors, and other pertinent information that can be obtained from large volumes of bibliographic information [24]. Science mapping tools were utilized to generate accurate visualizations of bibliographic information. Co-authorship networks and keyword co-occurrence maps were created using the VOSviewer software, whereas contingency matrices were generated in the Cortext platform (www.cortext.net). VOSviewer is commonly used as a tool for generating maps or networks from an extensive collection of bibliographic information from different scientific databases. This software can be used to create visualizations of co-authorships, keyword co-occurrences, and co-citations, among others, in order to analyze the relationships or interrelationships among different variables. Cortext is an online platform that provides tools for textual analysis, text mining, and science mapping. It can also be used to generate diagrams that effectively show the frequency, correlation, and evolution of terms used in different scientific publications.

Prior to mapping, bibliographic entries were inspected to remove duplicates and erroneous items. Manual inspection and correction were also conducted to standardize the terms used in the analysis. The network map generated through VOSviewer provides information regarding the frequency, relatedness, and co-occurrence of keywords. Larger circles and labels indicate that the terms were used more frequently in different publications. The distance between the terms and the curved lines that connect the keywords indicate their relatedness based on co-occurrences. Terms are also grouped into clusters, as represented by the color groups, to signify a relatively higher degree of relations. The Cortext platform enables users to generate contingency matrices that show interrelationships among the different variables contained in a bibliographic dataset. A contingency matrix expresses the degree of correlations and anti-correlations between two selected parameters. Cells that are highlighted in red describe a positive relationship or a high degree of co-occurrence between the two parameters. On the other hand, blue-colored cells indicate anti-correlations or lower co-occurrences as compared to the expected number of co-occurrences. The white cells represent items that do not show any correlation. The Chi<sup>2</sup> score expresses the ratio between the square of the difference between the number of co-occurrences between A(i) and B(j) and its expected number of observations and the expected number of observations [25,26]. The data inputs and methods of analysis employed in the science mapping software were summarized in Table 1.

**Table 1.** Data inputs and methods of analyses used in VOSviewer and Cortext.

#### *2.3. Comprehensive Review*

A comprehensive review was performed to summarize important information provided in relevant scientific publications. From the downsized list of 413 research articles, only 282 documents were accessible or contained pertinent data. In order to limit the review to real-world application scenarios, studies that utilize computer models or simulate runoff events were excluded from the review. Inquiries that investigated combined sewer inflows or utilized mesocosms, lab-scale facilities, or synthetic stormwater runoff were also excluded to reflect the actual performance of stormwater treatment wetlands in reducing runoff pollutant concentrations. A total of 108 scientific publications were considered for the comprehensive review. Essential information, such as the size and characteristics of study areas, the types and components (i.e., filter media and plants) of stormwater treatment wetlands, and the investigated water quality parameters, were compiled from each of the valid documents.

#### **3. Results and Discussion**

#### *3.1. Bibliometric Analysis and Science Mapping*

#### 3.1.1. Trend of Scientific Productivity and Characteristics of Published Literature

The annual scientific productivity or number of published documents related to stormwater treatment wetlands was exhibited in Figure 2. Based on the records of the WoS database, papers that focused on constructed wetlands used for stormwater management were first published in the year 2012. The annual scientific productivity exhibited an increasing trend until the year 2017, when the maximum number of articles was reached (57 articles). Despite the relatively lower number of publications from the year 2018 to 2021, the number of documents published within this period was 10% to 55% higher than the number of publications in the year 2012. In terms of the number of citations, a continuously increasing trend was observed from 2012 to 2021. The initial number of citations in the year 2012 only amounted to 11, whereas the maximum number of citations, amounting to 1268, was observed in 2021. The number of citations proportionally increased alongside the surge in the number of publications since the network of researchers specializing in constructed wetlands and stormwater management also expanded over the years. Generally, the observed growth in the number of scientific publications and citations indicated that constructed wetlands have become an important component of stormwater management strategies.

**Figure 2.** Annual number of published documents and cumulative number of citations.

The contribution of various states to the total number of publications was illustrated in Figure 3. Researchers from 51 different states contributed to the total number of indexed publications. Authors from the USA had the largest contribution to scientific publication with a total of 165 articles and an average annual scientific productivity of 17 articles. The second-most productive state in terms of the number of publications was Australia, with a total of 71 documents. China (62 articles) and South Korea (31 articles) were the leading Asian states in stormwater treatment wetlands research, whereas France was found to be the most active European state in terms of the number of published papers in this particular field of research (31 articles) in this area of study. The scientific productivity of different states was also evaluated in terms of the population-to-publication ratio. This ratio is indicative of the state's contribution to a specific research field in relation to its total population. Australia, Canada, and South Korea were found to have the highest level of scientific productivity, with corresponding population-to-publication ratios of 36,000:1, 1,530,000:1, and 1,669,000:1. Despite having the largest number of scientific publications in the Asian Region, China had the lowest population-to-publication ratio, with approximately 23,000,000 people per article in the WoS database.

," " "

**Figure 3.** Annual scientific productivity of different states.

3.1.2. Journal Publications and Related Subject Areas

The research on constructed wetlands used for stormwater management covers a wide range of subject areas and specializations. The major subject areas related to stormwater treatment wetlands research was listed in Table 2. A total of 32 subject areas were identified among the list of publications. This indicated that studies on constructed wetlands and stormwater management are multi-faceted and established through complex collaborations among professionals and researchers from various fields of expertise. Among the 32 subject areas identified, approximately 81% of the published literature was directly relevant to "Environmental Sciences Ecology." Constructed wetlands are widely-used technologies for environmental preservation and restoration, and thus, most of the analyzed published literature is related to "Environmental Sciences Ecology." Publications that fall under "Engineering" (49%) and "Water Resources" (35%) were also found to be abundant. Despite being considered nature-based facilities, constructed wetlands are built systems that integrate advanced engineering techniques and natural processes to achieve water quality goals, mitigate flooding conditions, and support water resource conservation efforts. Generally, it was observed that individual documents can be classified into multiple subject areas, implying that most scientific publications are multi-disciplinary in nature.

**Table 2.** Major subject areas relevant to constructed wetlands and stormwater management research.

<sup>a</sup> Subject areas with less than 10 documents.

The journals having the most publications related to stormwater treatment wetlands were summarized in Table 3. The 413 articles retrieved in the query were published in 116 journals. The Ecological Engineering journal contains the largest number of publications, amounting to 83, followed by Science of the Total Environment with 26 and Water with 22 articles. Journal impact factors are commonly used to evaluate the quality of journals or the research articles published in a specific journal. Despite the opposition from several researchers and institutions, this metric is still widely used for journal rankings due to the lack of alternatives and ease of use [27,28]. Four of the most productive journals in stormwater treatment wetlands research have impact factors greater than three. Moreover, three of the journals on the list belong to Q1 (top 25%) in the ranking of Environmental Engineering journals.

**Table 3.** List of most productive journals in terms of the number of publications.

<sup>a</sup> Q1 journals in the field of Environmental Engineering. <sup>b</sup> Journals with less than 10 publications.

#### 3.1.3. Frequently Cited Research Works on Constructed Wetlands

Four out of the five most-cited articles presented results on the effectiveness of constructed wetlands in treating nutrients and heavy metals in stormwater. As listed in Table 4, the study conducted by Xu et al. (2017) received the highest number of citations. This study explored the mechanisms involved in the removal of nitrogen and phosphorus in stormwater. Specifically, the nutrient uptake capabilities of two wetland macrophytes (i.e., *Iris pseudacorus* and *Thalia dealbata*) were evaluated to determine their contribution to the nutrient removal process. A systematic plant harvesting strategy was also recommended to optimize the performance of the constructed wetland [29]. The second-highest number of citations was noted in the paper by Winston et al. (2013) about the conversion of stormwater ponds into floating treatment wetlands. While there were no significant statistical differences in pollutant removal observed after retrofitting the ponds, results suggested that the addition of plants to the system contributed to beneficial treatment mechanisms [30]. The article published by White and Cousins (2013) received a total of 80 citations within a period of eight years. This inquiry focused on the evaluation of the season-long nutrient

removal efficiency of a floating treatment wetland. The nutrient assimilation rates of two macrophytes (i.e., *Canna flaccida* and *Juncus effuses*) and the changes in physico-chemical characteristics of the wetland effluent were also documented in this study [31]. The papers published by Borne et al. (2013) and Payne et al. (2014) were also among the most cited literature related to constructed wetlands and stormwater. Borne et al. (2013) explored the heavy metal treatment performance of floating treatment wetlands, whereas Payne (2014) highlighted the fate and dominant processes involved in the removal of nitrogen from stormwater [32,33].

**Table 4.** List of highly cited publications.

3.1.4. Co-Occurrence of Keywords and International Research Collaborations

Keywords are one of the most essential pieces of bibliographic information since they represent the important contents of a scientific publication [34]. Overall, 1120 unique keywords were identified from the 413 articles considered in this study. Keywords that were used at least two times in different documents only amounted to 268. Increasing the minimum number of keyword occurrences to three further limited the list to 127 unique terms. The considerable decrease in the number of unique keywords as the minimum number of occurrences increased implied that most studies were focused on a specific topic. In order to extract the terms most relevant to stormwater treatment wetlands, the minimum number of occurrences of a unique keyword should be increased. The network map shown in Figure 4a represents the most frequently used terms in publications related to stormwater treatment wetlands. The keywords exhibited in the figure were derived by setting the minimum number of occurrences to five. Among the initial 1120 unique keywords, only 67 terms met the threshold.

**Figure 4.** (**a**) Network map of keyword co-occurrence; (**b**) collaboration network among different states.

Excluding the terms used in the query, the most frequently used keywords in related documents were phosphorus (n = 37), water quality (n = 26), best management practice (n = 24), nutrient (n = 23), and nitrogen (n = 22). The frequently used keywords reflected the primary role of constructed wetlands in water quality improvement. Specifically, the ability of constructed wetlands to treat nutrients (i.e., nitrogen and phosphorus) incorporated in stormwater runoff was extensively studied. The application of constructed wetlands as a valuable stormwater best management practice can also be deduced from the map. In terms of co-occurrence, constructed wetlands had high relations with best management practices and stormwater management, whereas water quality exhibited considerable relations with stormwater control measures and nutrients. Phosphorus and nitrogen also had strong links, indicating that the two nutrient compounds are commonly studied jointly in scientific publications. There were seven clusters identified based on the relatedness of terms. The clusters represent the main topics associated with the research on stormwater treatment wetlands. Moreover, these groups also suggest topics that have been extensively investigated by past inquiries or publications.

Aside from the co-occurrence of keywords, the status of international collaboration can also be visualized through a network map. As illustrated in Figure 4b, the USA had the highest number of networks or co-authorships with other states. Aside from being the top publishing state, the USA established international collaboration networks that resulted in high scientific productivity. The highest link strength was observed between the USA and China, indicating that the two states had the most co-authored publications. The number of co-authored papers among European states, including France and Germany, was also relatively high; however, the collaboration among European and Asian states was found to be limited.

#### 3.1.5. Shifts in Research Interest and State-Specific Research Trends

Research trends change over time due to the changes in the policy of a specific state, the degree of saturation or number of current studies for a certain topic, and the advancements in analysis procedures that can significantly affect data acquisition, among others. It is also important to note the shifts in research interests to determine the existing knowledge gaps or potential research directions. The contingency matrix exhibited in Figure 5a shows the annual trend of keyword use. In the early year of research on stormwater treatment wetlands (2012), "stormwater runoff" and "phosphorus" were the most dominant keywords used in scientific publications. The terms "stormwater" and "floating treatment wetlands" emerged as the most commonly used keywords in the succeeding years, alongside the growth in the number of publications from different states. "Constructed wetland" and "water quality" became the most relevant terms in the years 2018 and 2019. Except for the year 2016, it was observed that there was a shift from using the term "floating treatment wetland" to a more general term, "constructed wetland." This also highlighted the developments in the design of engineered systems used for stormwater management. Aside from free-water surface wetlands, other variants of engineered wetlands (i.e., subsurface flow constructed wetlands and hybrid constructed wetlands) became available, thereby resulting in changes in the frequency of keywords used in publications. More recent studies published in the years 2020 and 2021 utilized the terms "nitrogen" and "stormwater management" more frequently. Generally, shifts or changes in the pattern of keyword use created a general idea of the current status of research in a particular subject area.

State-specific use of terms also provides significant information that can be useful for the development of policies and environmental management strategies. The contingency matrix of the most relevant keywords used by the researchers from the top publishing states is shown in Figure 5b. The term "phosphorus" had the highest correlation with the USA, implying that stormwater treatment wetlands in the USA were primarily used for treating phosphorus in stormwater. "Stormwater" and "stormwater runoff" were the dominant terms used in the publications from South Korea, China, Spain, and Australia. This suggested that constructed wetlands were extensively used as a tool for stormwater management in the aforementioned states. Publications from Canada and France have increased usage of the term "sediment", whereas Germany and India frequently used the keyword "constructed wetland." The term "nutrient" was highly associated with publications from the United Kingdom (UK), indicating that the function of stormwater treatment wetlands as nutrient sinks was of particular interest in the state.

**Figure 5.** Contingency matrix of (**a**) keywords and year of publication and (**b**) keywords and state.

#### *3.2. Data Synthesis and Comprehensive Review*

3.2.1. Land Use Types and Catchment Area Characteristics

Land use and catchment area characteristics are among the primary factors that affect the quality of stormwater runoff. The extent of anthropogenic activities and the intensity of development may also exhibit direct and indirect relationships with the distribution of pollutants within the catchment area. The list of typical land use types frequently investigated in different studies is summarized in Table 5. Most scientific inquiries focused on

the application of stormwater wetlands to treating runoff from urban catchments. Constructed wetlands emerged as cost-effective and socially acceptable stormwater treatment technologies due to their multiple benefits fit for an urban setting [35]. Wetlands designed for agricultural pollution mitigation were also extensively investigated. Treatment wetlands are commonly used as low-energy and low-cost alternatives for abating polluted agricultural runoff. Specific wetland components, such as plants and microorganisms, also contribute to efficient nutrient cycling to prevent the excessive deposition of pollutants in natural waterways [36]. The review of published literature also suggested that wetlands are extensively utilized to treat stormwater runoff from residential areas, parking lots, highways, and mixed land use catchments.

**Table 5.** Drainage areas (in ha) of dominant land use types in reviewed scientific publications.

<sup>a</sup> Land use types with a frequency of less than five (i.e., suburban, grassland, municipal, etc.).

The size of catchment areas investigated in previous studies varied greatly. As exhibited in Table 5, treatment wetlands were applied to site-specific or catchment-scale treatment of stormwater runoff. Parking lots, highways, and residential areas constituted relatively small catchment areas, with mean values ranging from 3.01 ha, 2.35 ha, and 76.61 ha, respectively. One major factor limiting the application of CWs is spatial constraints; however, recent developments have allowed the installation of CWs despite the limited space availability. The concept of "pocket wetlands" can be applied to small drainage basins to provide additional stormwater treatment or achieve water quality goals. The size of pocket wetlands is more restricted as compared to their catchment-scale counterparts, and thus, these systems are often used for stormwater runoff polishing [37,38]. Among the identified land uses where stormwater treatment wetlands were applied, the highest drainage area was recorded in an agricultural catchment (86,000 ha) located in a section of the Everglades agricultural area, South Florida, United States. With an approximate treatment area exceeding 27,000 ha, the Everglades Stormwater Treatment Areas (STAs) are considered the world's largest and most complex constructed wetlands. The construction of STAs was implemented through the Everglades Forever Act, which aims to reduce the TP loads discharged from predominantly agricultural areas upstream of the Everglades Protection Area [39–41].

#### 3.2.2. Types and Sizes of Stormwater Treatment Wetlands

The choice of design and components of stormwater treatment wetlands can be influenced by the climate, availability of materials, influent pollutant concentrations and water quality targets, public perception, and existing environmental regulations, among others [42–45]. Based on the reviewed literature, free water surfaces (FWS) (n = 40) and floating treatment wetlands (FTW) (n = 26) were commonly employed for stormwater treatment. FWS wetlands are commonly used as stormwater management facilities due to their high volume capacities. Apart from the intrinsic capability of FWS wetlands to attenuate flooding, these systems can also provide efficient treatment of stormwater due to the prolonged retention time in the system [46,47]. FTW systems were also extensively studied due to their potential for increasing the ecosystem benefits of existing stormwater infrastructure. Unlike other types of treatment wetlands with considerable space requirements for field-scale applications, FTW systems can be incorporated into existing stormwater ponds to improve their general function. In the study conducted by

Borne et al. (2013), retrofitted stormwater ponds with FTWs showed higher treatment efficiencies as compared to conventional detention ponds [32]. Winston et al. (2013) and Tirpak et al. (2022) also reported improvements in the pollutant removal performance of stormwater ponds retrofitted with FTWs; however, the treatment contributions provided by FTWs were found to be limited or highly influenced by the pond design [30,48]. Studies regarding other wetland designs, including hybrid, horizontal subsurface flow (HSSF), and vertical subsurface flow (VSSF) stormwater treatment wetlands, were relatively scarce, with reporting frequencies of five, four, and seven times, respectively.

The size of stormwater treatment wetlands from the compiled data ranged from 7 m2 to more than 270 km2. Small facilities were specifically designed to treat runoff from site-specific sources, whereas treatment wetlands with relatively large surface areas were designated for catchment-scale runoff management. The surface area-to-catchment area (SA/CA) ratios of stormwater treatment wetlands applied in various land use types were illustrated in Figure 6. The typical SA/CA ratios of FWS and hybrid treatment wetlands were approximately 0.5% to 3%, whereas HSSF treatment wetlands exhibited higher SA/CA ratios ranging from 1.65% to 12.78%. It can be noted that FTWs had low SA/CA ratios (0.07% to 0.38%), since these are compact and modular facilities that are used as additional features to a stormwater detention pond. Nature-based facilities, including stormwater treatment wetlands, usually have small surface areas relative to the drainage area. In the study conducted by Hong et al. (2016), low-impact development facilities with SA/CA ratios of 1% to 5% were capable of reducing runoff volume by more than 40% [49]. Choi et al. (2018) also indicated green stormwater infrastructures with SA/CA ratios of 1% to 2% can provide adequate pollutant removal from stormwater [50].

**Figure 6.** SA/CA ratio of stormwater treatment wetlands in different land uses.

#### 3.2.3. Choice of Filter Media and Substrates

Treatment wetlands that contain subsurface structures are equipped with filter media that help enhance the facilities' filtration and pollutant retention functions. In the case of FTWs, the platforms or modules where the treatment units are mounted also contain substrates that support the growth of plants. The summary of the usage rates of various filter media and substrates reported in relevant scientific publications is shown in Figure 7. Sand and gravel were the most common filter media used for HSSF, hybrid, and VSSF stormwater treatment wetlands. The high usage rate of sand (18% to 36%) and gravel (27% to 50%) can be attributed to their relative abundance as construction materials and effective pollutant removal performance [51,52]. Marine-grade foam (48%) and recycled plastic fibers (31%) were the most common compositions of FTWs. These materials provide buoyancy and bond the platform carrying the substrates and plants [19,53]. Other types of filter media, such as laterite, rubber mulch, pebbles, woodchips, volcanic rock, and bioceramic, were also utilized as filter media for stormwater treatment wetlands. The

treatment wetland presented in the study conducted by Adyel et al. (2016) utilized laterite aggregates to enhance phosphorus removal in stormwater. It was found that laterite acted as an important phosphorus sink due to the ligand exchange reaction that prompted effective phosphorus adsorption [54]. Packed rubber mulch and pebbles were primarily used to enhance the physico-chemical and biological processes in the filter bed. Han and Tao (2014) attributed the enhanced industrial runoff treatment to the effective biosorption and adsorption of pollutants in the packed rubber mulch and pebbles [55]. The tradeoff of using woodchip filter materials for treating stormwater was reported by Niu et al. (2018) [56]. Zhang et al. (2020) cited high adsorption capacity, porous properties, and resistance to degradation as the major advantages of using volcanic rock and bioceramics as filter media [57]. Woodchips serve as additional carbon sources for enhancing the denitrification process in a filtration system but may also lead to elevated chemical oxygen demand (COD) concentrations in the effluent. Based on the information presented in the reviewed articles, the choice of filter media or substrates was found to be influenced by the availability and properties of the materials.

**Figure 7.** Usage rate of filter media and substrates used in stormwater treatment wetlands.

3.2.4. Plants in Stormwater Treatment Wetlands

Plants are considered essential components of stormwater treatment wetlands. The vegetative components of wetlands directly contribute to the efficient management of nutrients, the removal of toxic pollutants through plant uptake and assimilation, and the carbon storage functions of the system [58–60]. Plants can also enhance the treatment properties of wetlands by prompting efficient sedimentation of particulates in the wetland bed, providing favorable conditions for the growth of microorganisms, and preventing internal algal blooms through shading. A total of 94 genera and 160 species of wetland plants were identified from the reviewed articles (see Table S1). As exhibited in Figure 8, the five most common plant genera used in stormwater treatment wetlands include *Typha*, *Juncus*, *Carex*, *Phragmites*, and *Schoenoplectus*, with reporting frequencies of 45, 38, 29, 18, and 16 times, respectively.

**Figure 8.** Distribution of the most commonly used plants in stormwater treatment wetlands.

*Typha* is widely used in treatment wetlands due to its high pollutant uptake capabilities and extremely resilient properties. *Typha* is known to be an important nutrient sink, making it suitable for managing eutrophication [61]. Chandra and Yadav (2011) emphasized that *Typha* can be used for heavy metal phytoremediation since these plants can accumulate Cd, Cr, Cu, Fe, Ni, and Pb in their roots [62]. These plants also have a high phytotoxic tolerance, making them suitable components of wetlands receiving highly contaminated runoff [63]. *Juncus* is also a typical wetland plant known for its high ecosystem value. It was previously reported that different *Juncus* species have promising phytoremediation potential and high biomass yield [64–66]. Plants of the genus *Carex* are commonly applied on FTWs due to their adaptability, ability to uptake heavy metals, and ease of harvesting [20,67]. *Phragmites* are wetland plants known for being potent hyperaccumulators of trace elements [68–70]. *Phragmites* species are often planted in treatment wetlands to increase pollutant remediation; however, these plants are also considered ubiquitous, highly invasive, and phytotoxic due to the production of allelochemicals detrimental to the growth of other plant species [71]. Wetland plants belonging to the genus *Schoenoplectus* are leafless species with large underwater surface areas. These plants are commonly utilized in treatment wetlands due to their remarkable tolerance to physicochemical changes in water quality (i.e., pH, temperature, and salinity) and high nutrient-regulating properties [72,73].

#### 3.2.5. Runoff Water Quality and Treatment Performance of Stormwater Wetlands

A complex mixture of chemicals and compounds can be incorporated into stormwater as a factor of land use, geomorphological characteristics, and the patterns of pollutant deposition in the catchment area. Stormwater treatment wetlands are usually employed in different catchments due to their versatility in treating a wide range of pollutant compounds with substantially varying concentrations. A total of 91 unique water quality parameters and constituents were identified from the collection of reviewed articles concerning stormwater treatment wetlands. As shown in Figure 9, total phosphorus (TP) and total nitrogen (TN) were the most commonly investigated runoff constituents. Various nitrogen forms, including total Kjeldahl nitrogen (TKN) and nitrate-nitrogen (NO3-N), were also typically included in inquiries related to stormwater treatment wetlands. Nutrients are primary stormwater pollutants that can trigger eutrophication and algal blooms. Treatment wetlands are associated with the treatment of nutrients in stormwater runoff since these systems perform mechanisms that effectively remove different nitrogen and phosphorus forms in stormwater. Wetlands remove nitrogen from stormwater through the combination of physico-chemical and biological processes (i.e., adsorption, plant uptake, ammonification, etc.) involved in the transformation of nitrogen compounds. The removal of phosphorus in CWs can also be influenced by biological processes, such as biodegradation and plant uptake, but sedimentation and soil retention are considered the main pathways for long-term phosphorus removal in treatment wetlands [74]. Suspended solids (SS) concentration is also a well-represented water quality parameter in the reviewed articles since stormwater is a major transport route of sediments and particulates to waterways. The high reporting frequencies of SS in published literature can also be attributed to the relative simplicity of experimental methods for quantifying sediments or particulates in stormwater [75,76]. Heavy metals, such as calcium (Ca), copper (Cu), and zinc (Zn), and dissolved organic carbon (DOC) were also widely investigated, with reporting frequencies of more than 10. The presence of emerging stormwater pollutants, including pesticides, polycyclic aromatic hydrocarbons, and microplastics, was also documented in some studies, but the reporting frequencies of these compounds were relatively low [77–79].

**Figure 9.** Typical water quality parameters investigated in stormwater treatment wetlands research.

The concentrations of the three most frequently reported water quality parameters were summarized in Figure 10. The highest concentration of TP, amounting to 700 mg/L, was reported in the runoff from an agricultural catchment, whereas maximum TN (54 mg/L) and SS (1953 mg/L) concentrations were observed from a predominantly urban catchment. Phosphorus loads may originate from various natural or anthropogenicrelated processes; however, agricultural activities are known as the principal sources of excessive phosphorus loads in water bodies [80]. In urban areas, SS and TN concentrations are mostly influenced by the disturbance of natural features and the accumulation of pollutants on impermeable surfaces. Elevated SS concentrations in urban areas usually originate from construction activities, road and highway maintenance, traffic-related activities, and wet and dry atmospheric deposition [81,82]. High nitrogen concentrations in urban runoff were also reported, considering its diverse sources. The dominant sources of nitrogen in urban runoff include fertilizers applied to lawns, wastewater, atmospheric deposition, and combustion [83]. Among the different land use types identified in the review, parking lot and highway runoff had the lowest mean TP (0.17 mg/L), TN (1.64 mg/L), and SS (42 mg/L) concentrations. Highways and parking lots are usually maintained through sweeping or the removal of accumulated detritus. Since various pollutants are bound to particles, reducing the sediment build-up also resulted in a significant decrease in stormwater pollutant concentrations [84,85].

Stormwater treatment wetlands are capable of reducing pollutant concentrations to a certain extent. As seen in Figure 9, effluent pollutant concentrations were considerably lower than the observed concentrations in the inflow. The treatment wetland investigated by Byeon and Nam (2020) exhibited a pollutant removal performance of up to 99%, indicating that the facility is fit for mitigating the negative impacts of NPS pollution [86]. Li et al. (2020) also reported removal efficiencies exceeding 90%, citing the contribution of effective microorganisms in improving the overall performance of wetlands in treating nutrients in runoff [87]. The stormwater treatment wetlands monitored by Grinberga et al. (2021) showed relatively lower mean pollutant removal efficiencies, ranging from 17% to 80%. It was highlighted that the poor pollutant removal performance of the system can be attributed to the low influent pollutant concentrations caused by stormwater dilution [88]. Some studies also reported negative removal efficiencies or higher outflow concentrations after receiving treatment from stormwater treatment wetlands. Walaszek et al. (2018) recorded a negative removal of PAHs and heavy metals in a stormwater treatment wetland due to the resuspension of solids containing particulate heavy metal fractions in the system [78]. Howitt et al. (2014) emphasized the effect of external factors, including wind mixing, fine sediment resuspension, and external pollutant loading, on the performance of treatment wetlands [89]. The information compiled from the reviewed scientific literature clearly indicated that stormwater runoff management is essential in mitigating environmental degradation. Studies also suggested that treatment wetlands are effective green stormwater infrastructures, but the design of facilities should also be adapted to the stormwater characteristics and catchment area conditions.

**Figure 10.** Synopsis of pollutant concentrations in the runoff and stormwater treatment wetlands effluent.

#### *3.3. Knowledge Gaps and Future Research Directions*

Stormwater contains various types of pollutants derived from natural and anthropogenic sources. The typical pollutants in stormwater include sediments, nutrients (nitrogen and phosphorus), organics, and heavy metals; however, the occurrence of micropollutants and other emerging pollutants in stormwater was also identified in recent inquiries. Piñon-Colin et al. (2020) detected the presence of plastic particles smaller than 5 mm, known as microplastics, in stormwater. Furthermore, it was found that stormwater is the primary mode of microplastic deposition in water bodies [90]. In the year-long survey conducted by Wicke et al. (2021), different organic micropollutants, such as plasticizers, flame retardants, and PAHs, were identified in stormwater. It was estimated that the stormwater collected from the catchment composed of different land uses contained 24 μg/L of an organic micropollutant mixture [91]. Recent advancements in analysis and instrumentation methods have also enabled the detection of compounds present in minute concentrations. The stormwater samples analyzed by Tran et al. (2019) were contaminated by compounds used in the synthesis of pharmaceuticals and personal care products [92]. Similarly, Fairbairn et al. (2018) reported the presence of 123 different compounds, classified as emerging pollutants, in stormwater. The analysis also revealed that emerging pollutant loads from stormwater may exceed the treated wastewater effluent loads to receiving water bodies [93]. The detection of emerging pollutants and other organic micropollutants in stormwater raised major environmental concerns; however, studies that explore the feasibility of using constructed wetlands as potential treatment systems for the new suites of pollutants are still limited. Based on the analysis of terms, most studies related to stormwater treatment wetlands only focused on the treatment of trace elements (i.e., heavy metals) and nutrients in stormwater. It is, therefore, necessary to conduct inquiries on the applicability of stormwater treatment wetlands in the treatment of emerging pollutants to maximize their water quality treatment benefits.

International collaborations open the platform for scientific productivity. The bibliographic information extracted from published literature revealed that only selected states (i.e., the USA and China) have a well-established network of authors that collaborate on scientific publications. Furthermore, European states were found to be more active in terms of publication as compared to states from other regions. It is recommended to promote knowledge sharing through international collaboration in order to increase scientific productivity and improve the functions, design, and benefits of stormwater treatment wetlands.

#### **4. Conclusions**

The number of publications related to stormwater treatment wetlands has considerably increased over the years, indicating that green stormwater infrastructures and NBS have become relevant approaches in stormwater management. USA and China were found to be the most productive states in terms of the number of scientific publications and research collaborations; however, further analyses revealed that Australia, Canada, and South Korea had the highest level of scientific productivity in terms of population-topublication ratio. The typical design and components of stormwater treatment wetlands in different regions were identified through a comprehensive review of related scientific literature. FWS and FTW were the most common types of CWs used for stormwater treatment, and the size of facilities varied from 7 m2 to more than 270 km2. Sand and gravel were typically used as filter media for HSSF, VSSF, and hybrid treatment wetlands since these materials are abundant and have high pollutant removal performance. The most common plant genera used in CW systems include *Typha*, *Juncus*, *Carex*, *Phragmites*, and *Schoenoplectus*. These plants are considered hyperaccumulators of pollutants with high biomass yields and high resistance to toxic environments. Generally, studies on water quality parameters, including nutrients and heavy metals, were the most established field in stormwater treatment wetlands research; however, inquiries regarding the treatment of micropollutants and emerging pollutants by stormwater treatment wetlands are still lacking. This study identified the need for future works that focus on addressing the aforementioned research gaps that are necessary to optimize the benefits of stormwater treatment wetlands. Strengthening the collaboration among different states can also promote greater scientific productivity and new paradigms for the utilization of nature-based systems.

**Supplementary Materials:** The following supporting information can be downloaded at: https: //www.mdpi.com/article/10.3390/su15032332/s1, Table S1: List of plants used in stormwater treatment wetlands.

**Author Contributions:** Conceptualization, N.J.D.G.R., F.K.F.G., and H.B.G.; methodology, N.J.D.G.R.; software, N.J.D.G.R.; validation, N.J.D.G.R.; formal analysis, N.J.D.G.R.; investigation, N.J.D.G.R., F.K.F.G., and H.B.G.; resources, L.-H.K.; data curation, N.J.D.G.R.; writing—original draft preparation, N.J.D.G.R.; writing—review and editing, F.K.F.G., H.B.G., and L.-H.K.; visualization, N.J.D.G.R.; supervision, F.K.F.G., H.B.G., and L.-H.K.; project administration, L.-H.K.; funding acquisition, L.-H.K. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was supported by the National University Development Project by the Ministry of Education in 2022.

**Institutional Review Board Statement:** Not applicable.

**Informed Consent Statement:** Not applicable.

**Data Availability Statement:** Not applicable.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**

**Disclaimer/Publisher's Note:** The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

## **A Review of Ecosystem Service Trade-Offs/Synergies: Enlightenment for the Optimization of Forest Ecosystem Functions in Karst Desertification Control**

**Xuehua Deng 1, Kangning Xiong 1,2,\*, Yanghua Yu 1,2, Shihao Zhang 1,2, Lingwei Kong 1,2 and Yu Zhang <sup>3</sup>**

**\*** Correspondence<EMAIL_ADDRESS>
**Abstract:** Ecosystem services provide regulation, provisioning, support, and cultural benefits for human survival, but it needs to be clarified how the trade-off/synergy relationships can be used to optimize function. Based on the Web of Science (WOS) and China National Knowledge Infrastructure (CNKI) databases, we collected 254 articles on the ecosystem trade-offs/synergies and functional optimization. Through a systematic review of the literature, this paper summarized the research progress and landmark achievements from three aspects: trade-offs/synergies, functional optimization, and evaluation methods. The results indicated the following: (1) In terms of the number of articles published, there were no reports before 2005; from 2006 to 2022, the annual number of published papers increased from 1 to 72, showing an overall growth trend year by year. This mainly includes three stages: initial (1970–2005), slow development (2005–2014), and rapid development (2014–2022). (2) In terms of research areas, focus was placed mainly on Asia, North America, and Europe, accounting for 40.47%, 25.55%, and 15.07% of all regions, respectively. (3) In the future, it is necessary to focus on scientific issues such as the improvement of forest ecosystem functions, the trade-off/synergy relationships between services, the scale of spatiotemporal research, and the driving factors and evaluation methods for the management of rocky karst desertification. The aim is to provide a theoretical basis to optimize the forest ecosystem service functions.

**Keywords:** desertification control; ecosystem services; forests; functions; trade-offs/synergies

#### **1. Introduction**

Ecosystem services, as the term of a scientific period, began in 1970 with the publication of the UN University's report on "Human Impact on the Global Environment" [1]. Since then, Costanza [2] has proposed that ecosystem services are benefits derived directly or indirectly by human beings from the ecosystem, which are used to maintain the natural environmental conditions and utilities on which human beings depend for survival and development. Since the concept was proposed, it has attracted extensive attention from the academic community, and ecosystem services have been classified. People have widely accepted the classification of ecosystem services established by the Millennium Ecosystem Assessment, which is divided into provision, regulation, support, and cultural services [3]. Various factors regulate the services, and there are differences and overlaps in handling different services. This leads to complex interrelationships between other ecosystem services [4], manifesting as synergies and trade-offs between mutual gains and losses.

Trade-offs, as a fundamental concept, first appeared in economics and were defined as opportunity costs. Where resources are scarce, an individual or group must give up a certain amount of additional scarce resources to obtain more of the scarce resources [5]. Begong believes that a "trade-off" is a relationship between two life history traits. Due to the imbalance in the distribution of resources, an increase in the payoff from one feature

**Citation:** Deng, X.; Xiong, K.; Yu, Y.; Zhang, S.; Kong, L.; Zhang, Y. A Review of Ecosystem Service Trade-Offs/Synergies: Enlightenment for the Optimization of Forest Ecosystem Functions in Karst Desertification Control. *Forests* **2023**, *14*, 88. https://doi.org/10.3390/ f14010088

Academic Editors: Panayiotis Dimitrakopoulos, Mario A. Pagnotta, Miklas Scholz and Arshiya Noorani

Received: 14 November 2022 Revised: 29 December 2022 Accepted: 30 December 2022 Published: 3 January 2023

**Copyright:** © 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

is associated with a decrease in the payoff from the other feature [6]. Synergy was first introduced by the German theoretical physicist Haken in 1971 [7]. He considered "synergy" as the joint action and collective behavior of the parts of a system that collaborate or cooperate, leading to a new structure and characteristics of the whole system. In 2005, the Millennium Ecosystem Assessment (MA) [3] defined ecosystem service trade-offs as follows: within a particular spatial and temporal scale, when the supply level of an ecosystem service is enhanced, it is at the cost of reducing the resilience of its ecosystem and the supply function of other ecosystem services. in contrast, a synergistic relationship is manifested as a joint increase or decrease in various service supply capabilities [8]. It is clear from this line of development that the study of ecosystem service trade-offs/synergies is still a hot topic for future research.

Karst desertification refers to the land degradation phenomenon caused by the disturbance and destruction of unreasonable human social and economic activities under the fragile karst environment in the subtropical zone, which is manifested by soil erosion, gradual rock exposure, land productivity degradation, and a desert-like landscape on the surface [9]. Karst landscapes are widely distributed around the world, covering 22 million km2, accounting for 12–15% of the land area [10,11]. They are mainly distributed in the Mediterranean region, the east and central of North America, and southern China. Due to the fragile ecological environment and unreasonable human activities in these areas, karst desertification is a major problem, which threatens the security of ecological environment and restricts the development of the economy and society [9]. In order to reduce land degradation and promote ecological and economic development, scholars regard forest as the preferred goal of ecological restoration in this area [11,12]. The results of management over the years show that forests, as the main provider of ecosystem services, have the functions of water conservation, soil and water conservation, carbon sequestration, and climate change mitigation [13]. In particular, they play an irreplaceable role in managing karst desertification. However, as time has passed, the problems of forest ecosystems in karst rocky desertification areas have become more and more prominent such as the competition between communities, leading to a reduction in biodiversity and the weakening of service functions. To promote the sustainable development of forest ecosystems in karst desertification areas, it is necessary to review studies related to the trade-offs and synergies of forest ecosystem services.

In recent years, studies on ecosystem service trade-offs/synergies have mainly focused on watershed [14], wetland [15], and vulnerable functional areas [16], and have achieved good results. The karst rocky desertification forest ecosystem is an important part of the terrestrial ecosystem, but its trade-offs/synergies are rarely reported, which hinders the research on functional optimization strategies. In order to solve this problem, based on a systematic review of the literature, this study summarizes the progress and landmark achievements of global ecosystem service trade-offs/synergies. It summarizes the key scientific questions about the function of forest ecosystems in managing karst rocky desertification, the trade-off/synergy relationships, the spatial research scale, driving factors, and evaluation methods. It aims to enlighten future research directions on optimizing forest ecosystem service functions in stone desertification management and provide theoretical references to enhance its service supply capacity.

#### **2. Materials and Methods**

This study was based on platforms such as the CNKI (China National Knowledge Infrastructure) and the Foreign Journal Resource Service System of Guizhou Normal University Library (Web of Science) (http://lib.gznu.edu.cn/data/weibu/waiwen/waiwen.htm, accessed on 22 October 2022). The search period was the maximum time range of both databases, and the search time was up to 22 October 2022 (Figure 1). First, we searched the WOS database by entering "ecosystem service" and "trade-offs/synergy", and again by entering "forest ecosystems" and "function optimization." A total of 234 documents were retrieved. Second, the CNKI database was searched by entering "ecosystem service", "trade-offs/synergy", "forest ecosystems", and "function optimization", and a total of 399 Chinese documents were retrieved. After the manual screening, a total of 564 documents were obtained. Finally, the articles' titles, abstracts, and keywords were screened based on the research themes related to trade-offs/synergies and functional optimization of ecosystem services. Following this, we further combined the literature for ecosystem services, trade-offs/synergies among services, functional optimization, and assessment methods. After, the full text of the alternative literature was browsed, and a total of 254 articles were screened. Among them, 93 papers were obtained from the WOS database (92 articles and one conference paper), and 161 papers were obtained from the CNKI database (109 journal papers, 42 master's theses, five doctoral dissertations, and three conference papers).

**Figure 1.** The process of the literature search.

#### **3. Results**

#### *3.1. Annual Distribution of the Literature*

From the annual distribution of the literature (Figure 2), the research related to ecosystem service trade-offs/synergies and functional optimization started in 2005 and reached its peak in 2022. This can be roughly divided into three stages. The first stage was from 2006 to 2014, when there were few studies on ecosystem service trade-offs/synergies and functional optimization, with only three literature articles in total; this was the starting stage. The second stage was from 2014 to 2018, and the literature showed a fluctuating growth trend, which was 16.3 times that of the first stage. In addition, there were already articles related to karst ecosystem research in this stage, but the number of types of literature was small; this is the development stage. The third phase was from 2017–2022, with a surge in the number of types of literature, 4.12 times more than in the second phase, but there were only 12 articles on the ecosystem service trade-offs/synergies and functional optimization of karst rocky desert ecosystem services. The overall trend shows that the number of articles on this topic will continue to grow.

**Figure 2.** Annual distribution of the literature. The dark green is the first half of the year (January– June); the light green is the second half of the year (July–December).

#### *3.2. Content Distribution of Documents*

This paper classified and summarize all of the reviewed literature according to the classification method. It was also divided into studies related to ecosystem service tradeoffs/synergies, the optimization of ecosystem service functions, and assessment methods according to the content of the studies. Ecosystem service trade-offs/synergies account for 61% of the literature, dominated by theoretical studies such as trade-offs/synergies, spatiotemporal characteristics, and relationship identification. In addition, in this literature, studies related to wetlands, oceans, watersheds, and fragile functional areas were dominant, and there were fewer studies on forest ecosystems in karst stone desert areas. The ecosystem service functional optimization literature accounts for 20%, which contains strategies for forest service functional optimization such as strategies for ecological corridor construction applied in northeast China, and ecological restoration and compensation strategies used in karst stone desertification areas in southern China. Assessment methods and other literature accounted for 11% and 8%, respectively, of which the assessment methods included both ecosystem services and trade-offs/synergies. The proportion of this literature indicates that the study of ecosystem service trade-offs/synergies is becoming more mature. However, the optimization of ecosystem service functions and assessment methods is still in the exploration and development stage.

#### *3.3. Distribution of Research Institutions Publishing Documents*

The regional distribution of the literature shows that China, the United States, and Germany dominate the research on ecosystem service trade-offs/synergies and functional optimization. The unique landscapes in China such as the northwest desert belt, fragile functional areas, and southern karst have attracted more Chinese scholars to study these areas and publish their research results. Thus, the overall number of publications was the highest. Next, developed countries such as Canada, France, Spain, Finland, Sweden, and Australia also had more relevant studies. In addition, Brazil, South Africa, Singapore, and other countries such as Iran had few studies. In terms of the overall publication volume, Asia had the highest number of publications, followed by North American states, Europe, Oceania, South American states, and Africa, accounting for 40.47%, 25.55%, 15.07%, 8.3%, 5.58%, and 5.03% of all regions, respectively. This correlated more significantly with each region's natural resources, social environment, policy support, and management experience.

The distribution of institutions publishing literature related to trade-offs/synergies and the functional optimization of ecosystem services was deciphered and analyzed. The acquired institutions were divided into four categories: higher education institutions, research institutions (centers), business units, and grassroots organizations, with percentages of 77.1%, 13.50%, 5.7%, and 3.5%, respectively. The rates showed that higher education institutions and research institutes (centers) have paid more attention to research related to trade-offs/synergies and the functional optimization of ecosystem services. However, due to the limited space of the figure, only institutions with a higher number of publications are marked in Figure 3.

**Figure 3.** Distribution of countries and institutions studied in the literature. The different color bands and numbers at the bottom indicate the number of publications; the darker green the color, the higher the number of publications.

#### *3.4. Research Stage Division*

Ecosystem services appeared as a technical term in the Human Impact on the Global Environment report published by the United Nations University in 1970. Ecosystem service trade-offs/synergies emerged from the 2005 Millennium Ecosystem Assessment [3]. Ecosystem services are the basis, and an essential part, of the ecosystem service tradeoff/synergy research. Thus, the first stage began in 1970 when ecosystem services were proposed. According to the research background of the changes in the theoretical studies, classification systems, and assessment methods, the development stages of ecosystem service trade-off/synergy and functional optimization were divided into the initial stage, the slow development stage, and the rapid development stage (Table 1).

**Table 1.** Division of the research stages.

**Table 1.** *Cont.*

*3.5. Research Progress and Landmark Results*

3.5.1. Ecosystem Service Trade-Off/Synergy

1. Spatial and temporal characteristics of ecosystem service trade-off/synergy

The trade-off/synergy among ecosystem services is spatial and temporal scale-dependent and nonlinear, and the trade-off and synergistic relationships of ecosystem services may change at different spatial and temporal scales [17]. Current studies on the time scale of the trade-offs and synergies of ecosystem services rarely use continuous time series and usually choose years with certain time intervals. For example, Niu et al. [18] analyzed the tradeoff/synergistic relationships of ecosystem services in the Songhua River basin in China during 2000–2018. They concluded that there was a synergistic relationship between water harvesting, soil conservation, biodiversity, and carbon sequestration, and a trade-off relationship between broadleaf forests, coniferous forests, and crops. Schroder et al. [19] found a short-term trade-off and long-term synergistic relationship between national forest fire risk management (logging) and owl habitat protection and water quality regulation in the United States. Chen et al. [20] found an increasing trend in net primary productivity, water production, and soil retention capacity from 2000 to 2018 during their study in a karst watershed. Still, the ecosystem synergy in the region was poor, and the trade-offs were particularly pronounced in karst stone desertification areas.

At the spatial scale, Zhang et al. analyzed the trade-off/synergistic effects of forest ecosystem services in the Fuyu Mountain region. They found that the synergistic relationship between services was better on the south slope than on the north slope, and that the best synergistic relationship between services was found in the middle mountain deciduous broadleaf forest belt on the south slope. The worst synergistic relationship was found in the low mountain deciduous broadleaf forest belt on the north slope [21]. Han et al. studied the trade-off and synergistic relationships between ecosystem services and land use change in the karst region response, finding synergistic relationships between soil water yield and soil retention, soil water yield and carbon storage, and soil retention and carbon storage. In contrast, most of the relationships between other crops were trade-offs [22]. In summary, the trade-off/synergistic relationships among services showed significant differences at different temporal and spatial scales due to the natural recovery status and the selectivity of human use of the services.

#### 2. Drivers of ecosystem service trade-off/synergy

The drivers of changes in the ecosystem service trade-offs and synergies are mainly divided into anthropogenic and natural factors [23]. As one of the typical fragile ecosystems in the world, the generation of trade-off/synergistic relationships between services in karst ecosystems mainly comes from the coupling effect of two significant factors: anthropogenic and natural. Scholars have studied the causes of the changes in the synergistic relationships of service trade-offs in karst ecosystems. For example, Han et al. suggested that climate is the leading natural factor for the transformation of service trade-off/synergistic relationships, which changes the temperature and precipitation intensity in karst regions through climate change, thus affecting the distribution pattern of plants, causing competition for species' ecological niches, and indirectly changing the relationship between services [24]. Chen et al. found that lithology is also one of the factors influencing the trade-off/synergistic relationships, and that karst areas dominated by dolomite and limestone, where limestone is more susceptible to dissolution by running water, have a poorer soil retention capacity. Therefore, the trade-off relationship between soil conservation and services such as water production is more significant in this region [25]. In addition, some scholars also believe that factors such as soil erosion [10], vegetation degradation [9], and reduced biodiversity [26] have a more significant impact on the trade-off/synergistic relationship between services. With the rapid development of society, the economy, and urbanization, many karst ecosystems such as agricultural land, forests, and wetlands have been occupied by human activities. This approach has not only changed the land use pattern and disrupted the material and energy balance of the karst soil–vegetation system [27], but also induced the reverse evolution of the soil–vegetation system. In addition, the supply capacity of karst ecosystem services will also be reduced, directly affecting the relationship between the benefits of the karst ecosystem [28]. In addition, to meet the needs of human survival and development, a large amount of scrub was reclaimed for cultivation, which contributed to the loss of organic carbon from the surface layer of karst limestone soils and the intensification of surface erosion, resulting in the weakening of soil carbon and nitrogen sequestration capacity, which affected the relationship between the services to some extent [29]. Thus, it is clear that human activities are a key factor in the structural and functional changes of karst ecosystems.

#### 3. Synergistic relationship of forest ecosystem service trade-offs

Forest ecosystems provide vital ecological services to the Earth's ecological environment, and the conservation of biodiversity and the development of forest industries are necessary ecological safeguards [12]. Karst forests are a special type of forest ecosystem developed on karst landscapes in the context of forest climate conditions [30]. However, long-term anthropogenic disturbances have exacerbated the problem of stone desertification in karst regions, reducing the stability of existing forest structures and leaving them in a state of fragmentation or secondary degradation succession. This significantly reduces the capacity of karst forest ecosystems in terms of water containment, soil conservation, biodiversity, and ecological product supply [31], creating trade-offs or synergistic relationships among services (Figure 4).

In recent years, some scholars have carried out studies related to the service relationships of karst forest ecosystems. For example, Wang et al. found that the relationship between the services in karst fallow forest areas (Grain for Green) was a trade-off between soil and water conservation and net primary productivity and water connotation, and a synergistic relationship between net primary productivity and water connotation [32]. Chen et al. found that the forest cover area in the karst area could enhance the forest's net primary productivity and soil erosion resistance. Still, expansion of the forest cover area will increase the uptake of water resources by vegetation, causing a decrease in surface water production service capacity so that the net primary productivity and water production form a trade-off relationship [33]. In turn, the trade-offs between services may impact the supply capacity of each service and hinder the ecological restoration process [9]. Therefore, based on the trade-offs between services, taking corresponding measures to optimize the service functions to maintain the structure and function of forest ecosystems is a critical way to achieve a "win–win" situation for economic development and ecological conservation [34].

**Figure 4.** Trade-offs/synergies between forest ecosystem services.

3.5.2. Optimization of Ecosystem Service Functions

4. Ecological compensation

Ecological compensation and payment are differentiated regulation strategies for the interaction between ecosystem services and human welfare, which should be adapted to the current ecological environment and social and economic system. As a mechanism to stimulate ecological construction and environmental protection, ecological compensation can realize the effect of internalizing the external ecological benefits [35]. Through the analysis of the spatial flow of supply, demand, and trade-offs, the key benefits and losses of ecosystem services are obtained, and the conditional payment transaction from service users to service providers is facilitated [36]. In general, a combination of remote sensing data and location-based observations is used to measure the profit and loss of supply, regulation, support, and cultural services. Complementary compensation strategies have been developed based on matching supply, demand, and trade-offs/synergies of ecosystem services. For example, Sun analyzed ecosystem service processes in crucial ecological function areas in Xinjiang. According to the total value of ecosystem services, all counties in the autonomous region can be divided into three compensation levels: priority compensation, secondary compensation, and potential compensation areas [37]. Thus, the efficiency of the ecological compensation mechanism can be improved. It was more difficult to compensate for the particular habitat of the karst desert region, and further funds were used. However, certain shortcomings in financial compensation can result in poor compensation outcomes. As a result, alternative ways to precisely refine and structure economic compensation methods exist such as improving the ecosystem structure stabilization and enhancing ecosystem service functions.

#### 5. Enhance forest ecosystem service functions based on site conditions

A fragile ecological environment, fragmented surface morphology, and severe soil erosion and desertification characterize karst regions. The essence is the destruction of the ecosystem structure, which leads to a decline in and loss of ecosystem functions [38]. Given the uneven spatial distribution of forest ecosystem services and the selectivity of human use, the ecosystem service cascade framework was developed to increase the stability of the forest ecosystem structure, improve the function of forest ecosystem services, and promote regional synergies (Figure 5). According to the trade-off/synergy differentiation of the services, some scholars have proposed that plant communities can be adjusted and configured through functional groups to enhance the overall ecosystem service capacity [39]. Chen [40] offered optimal control strategies for the forest, irrigation, and grass communities in different rock desertification classes, considering the growth traits, adaptation strategies, ecological niches, and functional group types of tree species. Zhang [12] constructed a model for the ecological restoration of forests of different stone desertification classes with species adaptation strategies and ecological service functions. Zhang [41] proposed plant community optimization techniques by studying the plant species diversity, leaf functional traits of established species in plant communities, spatial patterns of plant communities, and interspecific correlations in the rocky desertification succession of different grades. Yu [39] took the upper reaches of the Chishui River as the study area, divided 32 water resource conservation forest tree species into seven water resource conservation function groups, and proposed optimization and adjustment strategies for the different function groups on this basis. Therefore, the conservation strategies for forest ecosystems in karst areas should be more targeted and specific.

**Figure 5.** Forest ecosystem services.

#### 3.5.3. Assessment Methods

Ecosystem service assessment is a complex process that needs to be refined and quantified. Currently, the main ecosystem service assessment methods include economical methods, plant functional traits, biophysical models, energy value conversion techniques [42], quality methods [43], modeling methods, and value quantity methods [44].

Several scholars have explored the spatial and temporal characteristics and the relationship between trade-offs and synergies of the forest ecosystem services. From the research perspective, the content mainly involves the expression form, dynamic change, scale effect, and scenario simulation of ecosystem service trade-off/synergy relationships [45]. The research scale includes country, region, and river basin [46]. The main research methods are statistical analysis [47], spatial analysis [48], scenario analysis [49], and service mobility analysis [50,51] (Table 2).

**Table 2.** Research methods of ecosystem service trade-offs/synergies.

#### **4. Discussion**

#### *4.1. Trade-Offs/Synergies and Functional Optimization of Annual Posting Volume Differences*

The number of publications related to ecosystem service trade-offs/synergies and functional optimization is increasing rapidly with annual changes (Figure 2). For the forestry sector, this is both a challenge and an opportunity. Since the rise in ecosystem service trade-off/synergy research, the number of published articles has been increasing, accounting for 74.4% of the total articles published, which will continue to grow in the future. Studies on the trade-off/synergy relationships are mainly related to river basins, watersheds, and mountains. There needs to be more relevant studies on forests, as there is currently a lack of articles on karst stone desertification forests. It is speculated that the complex environment of karst desertification zones, with significant differences in different karst environments (canyons, depressions, rocky slopes, rocky forests, rocky troughs) [11], is more difficult for scholars to study, resulting in a low number of publications in these areas. Regarding functional optimization, there are relatively few studies on forest ecosystem service functions, accounting for only 25.6%. The current studies on functional optimization focus on the optimization of single services or the optimization of overall services, and there needs to be more studies on the optimization of services based on trade-off relationships. It is assumed that the concept and connotation of functional optimization need to be clearly defined [52], leading scholars to ignore the trade-offs between services in studying the functional optimization strategies in forest ecosystems. The characteristics of trade-off relationships and the driving mechanisms need to be better understood. The optimization methods for transforming trade-off relationships into synergistic relationships cannot be easily explored.

#### *4.2. Differences in the Distribution of Study Areas*

Regional differences in the natural conditions and social situations have led to the uneven development of research on ecosystem trade-offs/synergies and functional optimization (Figure 4). Regarding the number of publications, Asia has the highest number, with 40.47% of the total. Among the countries in Asia, China had the highest number of publications, with a total share of 86.97%, which may be related to the attention of national policies and research institutions [53], and possibly the use of the CNKI database. The emergence of a series of global problems such as resource and environmental degradation has made people deeply aware of the importance of the sustainable development of ecosystems [54,55]. As a result, there is a growing interest in the benefits provided by

ecosystems, and the number of publications is increasing. South America had the second highest number of publications, with a total share of 25.55%. The region is advanced in education, science, and technology, but may have focused its research horizon on ecosystem function, biodiversity, and other related aspects, with less research on trade-offs/synergies and functional optimization. The lowest number of publications was found in Africa, accounting for 5.03% of the total number of publications. Compared with the Asian region, this region is poor in resources and lagging in education, science, and technology. More attention should be paid to the research on ecosystem trade-offs/synergies and functional optimization, and there were fewer relevant studies.

#### *4.3. Key Scientific Questions to Be Addressed*

1. Severe soil erosion, weak stability of vegetation communities, and deteriorating ecosystems in karst stone desertification areas. Karst systems have a unique, binary, three-dimensional spatial structure. However, due to their structural peculiarities, this exacerbates the water and soil leakage condition, making the soil layer in the area thin, causing challenges in retaining nutrients, along with a poor soil quality. In addition, to meet people's survival and development needs, the original vegetation in karst rocky desertification areas has been destroyed, so the existing forests are mostly planted and secondary forests. However, most planted and secondary forests have simple structures, poor biodiversity, low primary productivity, and poor soil and water retention functions. The vegetation shows a tendency to retreat, reducing the stability of the forest ecosystems [56] (Figure 6).

(**a**) (**b**)

2. Karst stone desertification forest ecosystem services present trade-off/synergy relationships. This region has cultivated large areas of mature and overgrown forests using methods such as closed forestry and plantation, which have reached a certain high level of service capacity in terms of water content, net primary productivity, species diversity, and material production. However, the bias in human demand for forest ecosystem services and the tendency of forest communities to compete for ecological niche occupation [48] has led to trade-off/synergy relationships among services. Thus far, there are fewer studies on the trade-off/synergy of karst forest ecosystem services. During future research, understanding ecosystem services such as the water content and net primary productivity of karst forests should be enhanced to clarify the trade-off/synergistic relationships among services.

3. The spatial scale of forest ecosystem service trade-off/synergy studies is limited to large scales or single factors. Due to the successful development of 3S (remote sensing, geographic information systems, and global positioning systems) technologies, based on their ability to access spatial data quickly, the existing results of ecosystem service tradeoffs/synergies are large-scale studies such as watersheds [57] and functional areas [58]. However, these studies typically use a single research scale, and the results cannot be verified. Especially in karst areas, the topographic conditions are complex, with numerous plateau mountains, peaks, and valleys, and the information identified by remote sensing needs to reflect the actual conditions. Therefore, in the future, we should strengthen the research on a small scale and obtain experimental data through the combination of field monitoring and 3S technology to clarify the process and mechanism of each ecosystem service.

4. The unclear trade-off/synergistic driving mechanisms of karst forest ecosystem services. The influences on ecosystem services arise from natural and socioeconomic systems, covering topography, soil, biology, climate, land use, socioeconomics, and human activities [59]. Due to regional differences in development, the uneven regional distribution, and diversification of socioeconomic factors such as population, education, social class, policies and regulations, religion and culture, urbanization, and economic level, local people develop preferences for ecosystem services. Additionally, in the selection process, they indirectly or directly influence ecosystem services, creating trade-off/synergistic relationships. Therefore, in the future, it is essential to explore what factors play a dominant role at the spatial and temporal scales, the relevance of driving mechanisms at the spatial and temporal scales, and to clarify the coupling of various factors at different spatial and temporal scales [60].

5. Given the multitude of ecosystem service assessment methods, there needs to be more certainty in the results of trade-off/synergy studies among karst forest ecosystem services. Ecosystem service assessment involves many aspects including forestry, econometrics, management, and ecology. There are more indicators of each service function and complex mechanisms of the action process. Additionally, there are significant differences among regions, research scales, and assessment methods. Especially in karst stone desertification areas, the ecological environment is special, and multiple processes can be selected for comparative studies to enhance the scientific nature of the research methods.

#### *4.4. Enlightenment on the Optimization of Forest Ecosystem Service Functions for Karst Desertification Control*

Good social, economic, and ecological benefits have been achieved in participating forest ecosystems in managing karst rock desertification [61]. However, the fragility of the karst rock desertification ecological environment [62] makes the forest ecosystem in this area less able to resist external disturbances and less stable [63]. Once unreasonable human activities occur and exacerbate the fragility of stone desertification habitats, they will change the forest ecosystem's structural configuration and species composition [64] and affect the service provisioning capacity and trade-off/synergistic relationships. Therefore, the work summarized and reviewed in this paper on the above ecosystem trade-off/synergy and functional optimization was synthesized. Insights into the optimization of forest ecosystem service functions in karst rock desertification management were provided regarding the forest ecosystem structure–function and trade-off relationships among services.

For the ecological structure–function, the karst stone desertification area has a shallow soil layer, discontinuous soil, high rock exposure rate, and rich soil calcium and magnesium content [56]. The suitability for small habitats should be considered when selecting restoration species, and drought-tolerant, calcium-loving, rocky, fast-growing, widely applicable, ecologically and economically valuable trees, bushes, vines, and grasses should be selected for ecological restoration such as species of any bean, cedar, and lady's mantle [65]. Second, we should adjust the cultivation methods of natural forests and plantations, which are sound ecological construction systems and natural gene pools with strong regulation and restoration abilities. The conservation of natural forests is mainly based on "no access to protected forest areas" measures to preserve their species and genetic diversity and maintain the community structure and function [66]. For natural secondary forests in poor health, we adopted the measure of "managing the forest closed and adjusting the structure of the trees", and promoted better plant growth through artificial support measures such as replanting, nurturing, and inter-logging. For the planted plantations in natural forest areas, measures that support a "change of management approaches while protecting the forest in culturing" were adopted. Through the nurturing of mixed conifer and broadleaf forests, and the regular replanting of native species, we can induce succession in native forests and optimize the community structure and function [31]. Regarding the trade-offs between services, the trade-offs between forest ecosystem services in karst stone desertification areas resulted from a combination of natural and human factors.

Due to the poor soil in this area, plants compete with other species spatially to occupy more ecological niches during growth, leading to trade-off relationships between some services such as water connotation and soil conservation, nutrient netting, etc. [67]. Natural restoration or scientific fertilization can enhance soil quality in the stone desertification area and promote the balance of nutrient supply and demand. In addition, the appropriate stand density and planting depth need to be determined during planting to provide a wider space for plants to grow. The competition between plants for ecological niches should be reduced and the service capacity of water connotation and carbon sequestration and oxygen release should be improved while optimizing their trade-off relationship. The most important point is to reduce human interference in the forest ecosystem in stone desertification areas. The impact on the service function can be minimized by prohibiting deforestation, stepping on the protected forest area, reclaiming scrubland for cultivation, and planning the land for urban construction and highway construction in a reasonable way, in order to maintain the original state of the service function and reduce the formation of trade-off relationships.

#### **5. Conclusions**

This paper conducted a literature search for the trade-offs/synergies and functional optimization of forest ecosystem services through two databases, the Web of Science and CNKI. This study analyzed and reviewed 254 selected papers. The following conclusions were drawn. (1) The number of publications has shown a rapid growth trend since 2014, and the research process has gone through three stages: start (1970–2005), slow development (2005–2014), and rapid development (2014–2022). (2) Research regions are mainly concentrated in Asia, North America, and Europe, accounting for 40.47%, 25.55%, and 15.07% of all regions, respectively. (3) In the research, the content trade-off/synergy relationships were the most abundant, accounting for 61% of the total, followed by functional optimization and assessment methods, accounting for 20% and 11% of the total, respectively. (4) The following are future scientific questions to focus on and ideas for solutions: -<sup>1</sup> Given the severe soil erosion, weak stability of vegetation communities, and deteriorating ecosystems in karst stone desertification areas, a combination of forest sealing and artificial planting could enhance the vegetation cover, strengthen the ability to fix soil and retain water, and improve the system's stability. -<sup>2</sup> Given that karst stone desertification forest ecosystem services present trade-off/synergistic relationships, the reasons for the formation of inter-service trade-offs can be explored, and the trade-offs can be mitigated by enhancing the capacity of individual and multiple services. -3 Given that the spatial scale of forest ecosystem service trade-off/synergy studies is limited to large scales or single factors, the diversity of research dimensions should be increased, and a combination of remote sensing images and field monitoring should be used for research and validation. -<sup>4</sup> Given the unclear trade-off/synergistic driving mechanisms of karst forest ecosystem services, the human-made and natural factors that cause trade-offs between services should be fully explored, and their specific drivers should be identified. -5 Given the multitude of ecosystem service assessment methods, there is a problem of uncertainty in the results of trade-off/synergy studies among karst forest ecosystem services. The research should be conducted using methods applicable to small watersheds such as habitat monitoring and analysis to enhance the scientific validity of the research results.

**Author Contributions:** Conceptualization, methodology, data curation, writing—original draft preparation, X.D.; Formal analysis, K.X.; Writing—review and editing, X.D., Y.Y. and S.Z.; Supervision, Y.Z.; Funding acquisition, K.X.; Software L.K. All authors have read and agreed to the published version of the manuscript.

**Funding:** This research was supported by the Key Science and Technology Program of Guizhou Provence: Poverty alleviation model and technology demonstration for eco-industries derivated from the karst desertification control (No. 5411 2017 Qiankehe Pingtai Rencai); the Science and Technology Research Project of Higher Education Institutions in Hebei Province: Comparative study of model and technology for characteristic high efficiency forestry from the karst desertification control in North and South China Karst (No. QN2021412); the Scientific Foundation of Tangshan Normal University: Comparative analysis on vegetation restoration and characteristic high-efficiency forestry in the desertification of South and North China Karst (No. 2021A07) and the project of Guizhou Geographical Society: Research on characteristic high efficiency forestry from vegetation restoration of the karst desertification control (No. 2020HX05).

**Data Availability Statement:** The data presented in this study are available in the article.

**Acknowledgments:** The authors would like to thank Liyang Fu, Mingjun Feng, and Dong Chen for their help with the grammar, translation, and revision of the drawings.

**Conflicts of Interest:** The authors declare no conflict of interest.

#### **References**

**Disclaimer/Publisher's Note:** The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

### *Article* **Momoge Internationally Important Wetland: Ecosystem Integrity Remote Assessment and Spatial Pattern Optimization Study**

**Jiaqi Han 1,2, Dongyan Wang 1,\* and Shuwen Zhang <sup>2</sup>**

	- **\*** Correspondence<EMAIL_ADDRESS>
**Abstract:** Along the migration route between East Asia and Australia, numerous migratory birds use the Momoge Internationally Important Wetland as a habitat. Human activities and climate variability cause salinization and meadowization. We developed the "Quality-Pressure-Pattern-Service" remote assessment framework for ecosystem integrity, using a three level approach (TLA). The model was used to assess ecosystem integrity, identify improper wetland development, and provide spatial optimization strategies. The research region was dominated by wetlands, followed by dry fields. Wetlands continued to decrease between 1965 and 2019, as arable land and construction land continued to increase. Over the course of 54 years, ecosystem integrity declined. In 2019, around half of the areas had poor or extremely poor ecosystem integrity. Because the eastern study area contained many pristine inland beaches, the eastern study area displayed greater ecosystem integrity than the central and western areas. Priority should therefore be given to wetland restoration in the HJ core area (one of the three core areas of the reserve), where most of the herb marsh has been converted to arable land. This study revealed the integrity and authenticity of wetland ecosystems. Our results can aid in the protection of wetland habitats, encourage sustainable development, and help in the building of a national park in northeastern China.

**Keywords:** CORONA; environmental indicators; land use; national nature reserve; remote sensing

#### **1. Introduction**

The historical legacy of nature reserves is one of China's most significant environmental issues. In China's 474 national nature reserves, there are currently 29 urban built-up areas, 531 built-up areas consisting of formed townships, and 779 administrative villages [1]. Over the past three decades, scholars have created a variety of frameworks for assessing ecosystem integrity to characterize the natural and wilderness states of unaltered nature reserves. Initially, ecosystem integrity was recommended as a scientific evaluation criterion for ecosystem management in national parks in Canada [2]. Traditional frameworks for assessing ecosystem integrity and authenticity include the Index of Biotic Integrity (IBI) [3–5], the Ecosystem Integrity Assessment Framework (EIAF) [6], and the Ecosystem Integrity Assessment System Based on Essential Ecosystem Characteristics (EECs) [7]. In general, local and international scholars have centered their evaluations of ecosystem integrity on environmental stress, ecological processes, and biodiversity [8].

Wetlands exhibit some combined functions with those of terrestrial and aquatic ecosystems and they are among the most critical ecosystems [9–13]. However, the global wetland area has decreased by 35% during the past 50 years (https://www.global-wetland-outlook. ramsar.org/ (accessed on 17 December 2021)). Land use and development contribute significantly to the loss of wetland habitats. Various reports have discussed the loss of wetlands as a result of land use change, such as the extensive and rapid transformation of natural wetlands in Asia [14], the loss of 33% of the total domestic wetland in China between 1978

**Citation:** Han, J.; Wang, D.; Zhang, S. Momoge Internationally Important Wetland: Ecosystem Integrity Remote Assessment and Spatial Pattern Optimization Study. *Land* **2022**, *11*, 1344. https://doi.org/10.3390/ land11081344

Academic Editors: Panayiotis Dimitrakopoulos, Mario A. Pagnotta, Miklas Scholz and Arshiya Noorani

Received: 7 July 2022 Accepted: 12 August 2022 Published: 18 August 2022

**Publisher's Note:** MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

**Copyright:** © 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

and 2008 [15], and the extensive conversion of marshland to construction and arable land in China [16]. The conventional methodology used for assessing ecosystem integrity requires very high-altitude survey data and is challenging to apply to complex wetland habitats. The remote evaluation framework of the Three Level Approach (TLA) has established a number of evaluation indicators that can be evaluated through remote sensing [17,18]. On this basis, numerous evaluations of ecosystem integrity have been performed through the adoption of a Geographic Information System (GIS) analysis [19,20].

There is an urgent need to develop ecosystem integrity assessment frameworks that can be applied more frequently and repeatedly to nature wetlands to evaluate, monitor, and report on the condition of the region's ecosystems. Natural wetland parcels are generally fragmented, and delineating multiple natural land use types at fine scales is a limited process. Wetland data from the Third National Land Survey of China (2019) and the Second National Wetland Survey (2013) provide more fine-scale wetland vector data. However, it is difficult to obtain sufficient vector data for most wetland studies. Therefore, few previous studies have studied wetland changes over periods longer than 50 years and studies have failed to explore the more primitive wetland landscapes in history.

Several research findings have emphasized the viability of employing CORONA images to gain information on fine wetland types [21,22]. However, it has been noted that CORONA images have certain deficiencies in terms of both feature identification and band calculation [23]. In this study, we gathered historical information on the research area, such as county records, almanacs, and reports outlining the distribution of wetlands and hydrothermal conditions, to address this issue. In addition, we employed a human visual interpretation technique to adjust the land use change data piece by piece, which dramatically enhanced our ability to identify natural wetland types with precision.

Managing wetland areas with historical legacies is essential in order to safeguard core wetland areas and repair degraded wetlands. In response to numerous unknown factors concerning the degradation and development of wetland areas in the study area [24,25], an area of inappropriate development was identified, and the spatial pattern of the wetland areas was modified to meet ecological requirements to the greatest extent possible. In addition to the basic functions of natural wetland systems, wetlands with historical legacies are typically tightly linked to the production activities and living situations of humans [26–28]. Consequently, resolving historical legacy issues in wetland nature reserves plays a crucial role in fostering high-quality economic development and high-level ecological environmental protection through synergistic means.

On the basis of RS and GIS technologies, we developed a framework for assessing the integrity of ecosystems that is less expensive and requires less time. Such a framework will not replace assessment methods based on rigorous field surveys, but it will aid in the constant monitoring of changes in ecosystem integrity and provide essential data for addressing legacy concerns in nature reserves. In this study, we investigated the spatial and temporal aspects of a wetland from 1965 to 2019, utilizing the Momoge National Nature Reserve as a case study. On the basis of the "Quality-Pressure-Pattern-Service" ecosystem integrity remote assessment methodology, wetland ecosystem integrity was assessed. The optimization of the spatial pattern in the reserve was also performed to assist in providing fine control over the wetland's ecology.

#### **2. Materials and Methods**

#### *2.1. Study Area*

The Momoge Internationally Important Wetland is situated in Baicheng City, in the western portion of Jilin Province (Figure 1). The research area encompasses 144,000 ha and has a semi-humid, temperate continental monsoon climate. It sits at the western boundary of the Sonnen Plain, which was produced by the second northern subsidence zone of the Neocathasia tectonic structure. This structure is the Yingtai structure, which faces north-northeast. In the reserve, swamps have evolved in lakefront depressions, river floodplains, and low-lying places. The primary soil types of the reserve include

meadow soil, chernozem soil, and alluvial soil. There are as many as 55 different varieties of vegetation in the Momoge wetland, which belongs to the Eurasian steppe region. The major plant communities consist of a *Phragmities australis* community, a *Deyeuxia angusrifolia* community, a *Carex spp* community, etc. It is one of the three greatest soda saline land distribution zones in the world and is a crucial stopover for 90 percent of the world's large waterfowls and wading birds, such as *Grus leucogeranus*, migrating between Siberia and Oceania. The area was Established as a natural reserve in 1981 and designated as a globally significant wetland in 2013.

**Figure 1.** Location of Momoge Internationally Important Wetland.

#### *2.2. Data Sources and Data Processing*

#### 2.2.1. Ecological Assessment Unit

To balance the time- consumption of land use modeling and the richness of picture information, a 1 km × 1 km grid was used as the assessment cell size. First, all variable data were transformed to single-precision TIF images with the same raster size, and then 1 km grid cells were counted.

#### 2.2.2. Basic Geographic Data

In this study, we utilized meteorological data, DEM data, and land use data as the basic forms of geographic data. Meteorological data and some data on vegetation cover were collected from the National Earth System Science Data Center, National Science and Technology Infrastructure of China (http://www.geodata.cn/ (accessed on 9 December 2021)). For the years 1965, 2015, and 2019, the monthly precipitation and annual mean temperature of China were computed with a 1 km resolution. Since it was difficult to collect data on the vegetation cover in 1965, we used Landsat 3 images of the Momoge Nature Reserve from 1981 for our calculations. The geospatial data cloud (http://www.gscloud.cn/ (accessed on 10 May 2020)) provided the ASTERG DEMv2.0 data with a spatial resolution of 30 m. In this study, we made use of the 2013 wetland survey data from the forestry department, the 2013 land use change data from the Second National Land Survey, and the 2019 data from the Third National Land Survey.

#### 2.2.3. Remote Sensing Images

The Third National Land Survey utilized satellite remote sensing images with a resolution of over 1 m and classified wetlands in detail, whereas the Second National Land Survey utilized SPOT-5 satellite images with a resolution of 2.5 m and did not classify wetland types. To differentiate wetland types using the 2013 land use change data, this study should be complemented with by the use of additional remote sensing data with a m resolution. We chose the 1965 KH-4A satellite and the 2015 ZY-3 satellite as remote sensing information sources (Table 1).

**Table 1.** ZY-3 satellite and KH-4A satellite specification information.

Coronal images have panoramic aberrations. We used corrected ZY-3 satellite data as a reference for calibration. The root-mean-square error of the geometric correction results was less than 1.0. The 1965 and 2015 land cover vector data in the research region were finally generated by changing the 2013 land use change data patches. To maintain consistency in the classification accuracy of the data, we analyzed the 2019 land use vector data and combined road and ditch patches with widths of less than 2 m into adjacent land classes. In addition, industrial and mining land patches were eliminated from the land use map. We evaluated the accuracy of the 2015 and 2019 classification results using high-resolution Google Earth images. Due to the paucity of historical geographic data, we validated the correctness of the 1965 classification by creating a pseudo-color composite image of the Corona image using the density segmentation function. The results demonstrated that the overall accuracy of the secondary image classification reached 90%.

#### *2.3. Method*

The selection of 1965, 2015, and 2019 as the years for our analysis of land use type data was based on three main considerations:

This paper is structured as the follows (Figure 2). First, we merge several meterresolution remote sensing photographs to obtain land use type data for 1965, 2015, and 2019 in the research area. Then, we model land use dynamics and discuss land use changes. We present the final version of the " Quality-Pressure-Pattern-Service " ecosystem integrity remote assessment framework based on the TLA remote assessment framework. Finally, by evaluating the ecosystem integrity and authenticity of the study area, we identify the inappropriate development areas within the reserve and make recommendations for optimizing its spatial pattern.

**Figure 2.** Flowchart of the study.

2.3.1. Land Classification System

We determined the land classification system employed in this work by referring to prior wetland classification studies, such as the Ramsar Convention, the Third National Land Survey Classification, and the National Forestry Administration wetland survey classification (Table 2). Our analysis focused on wetlands and we divided them into narrow wetlands and water.

**Table 2.** The land classification system used in this study.

2.3.2. Land Use Dynamic Model

The single land use change rate is the rate of a specific land use or cover change in the research region, and it is computed as follows [29]:

$$\mathbf{V} = \frac{B\_1 - B\_0}{B\_0} \times \frac{1}{T} \times 100\% \tag{1}$$

In Equation (1), *B*<sup>0</sup> and *B*<sup>1</sup> are the area of a certain land use type at the beginning and conclusion of the study period, respectively, and *T* = 54 is the length of the study period.

#### 2.3.3. Ecosystem Integrity Evaluation Index System

Ecosystem integrity can be understood in terms of the quality of the ecosystem, the stability of the landscape, the ecological services supplied by the ecosystem, and its capacity to withstand less external pressure. Consequently, we developed a "Quality-Pressure-Pattern-Service" ecosystem integrity remote assessment framework (Figure 3) by referring to the three-level approach (TLA).

**Figure 3.** "Quality-Pressure-Pattern-Service" ecosystem integrity remote assessment framework.

The evaluation framework consists of four factors: ecosystem quality, ecological stressors, ecosystem patterns, and ecosystem services. The indicators were chosen based on the characteristics of wetland ecosystems and the concepts of comprehensiveness, representativeness, practicality, accessibility, and measurability. Table 3 displays the indicator system used to evaluate the ecosystem integrity of the Momoge Internationally Important Wetland. We selected 24 variables relevant to the integrity of wetland ecosystems, including 7 natural attribute variables, 5 spatial density variables, 3 landscape pattern variables, and

9 functional value variables, based on previous research. We did not select socio-economic characteristics in consideration of the reserve's real population and economic growth.

**Table 3.** "Quality-Pressure-Pattern-Service" ecosystem integrity evaluation factor table.

2.3.4. Ecosystem Service Indicators

Using the global ecosystem service function evaluation model [40], Gao et al. determined the ecosystem service values per unit area in China [41]. Their findings established one standard equivalence factor for the net profit of food production per unit area of a farmland ecosystem. For research and comparison purposes, the 2007 grain price (449.1 CNY/hm2) was used as 1 ecological service value equivalent factor.

To make the evaluation model more regionally applicable, we revised the ecological service value per unit area of Chinese ecosystems (2007) [41]. The biomass factor in Jilin Province was 0.96 [3], compared to a national average biomass factor of 1. First, we used this factor to adjust the value of ecological services per unit area of the ecosystem and obtained an initial value factor appropriate for the Momoge Nature Reserve. The ecological value coefficients of farmland were then adjusted using the equivalence factors of paddy fields and drylands (Table 4) [38]. Finally, the ecological service value per unit area suited to the actual conditions of the research region was determined (Table 5).

**Table 4.** Equivalent value per unit area of cropland ecosystem services in China (2011).

**Table 5.** Nature Reserve ecological service values per unit area (CNY/haa<sup>−</sup>1).

2.3.5. Weighting and Standardization of Evaluation Indicators

The Decision-making Trial and Evaluation Laboratory (Dematel) was used to calculate the degree of influence of each element on the other elements and the degree of influence to determine the causal relationship between the indicators and the weight of each indication in the system [42]. Table 6 displays the relative importance of the ecosystem integrity indicators used in this study. The min–max normalization approach was used to standardize the evaluation indexes to make them comparable [43].

#### 2.3.6. The Integrity Index and Grading Standards for Ecosystems

The ecosystem integrity index is a composite score that evaluates the significance and influence of each evaluation index on ecosystem integrity [20,44]. In this study, we used the comprehensive index method to calculate the Momoge Internationally Important Wetland's ecosystem integrity index. The ecosystem integrity index is determined by the following formula:

$$EI = \sum\_{i=1}^{n} \omega\_i A\_i \tag{2}$$

In Equation (2), *EI* is the ecosystem integrity index, *n* is the number of indicators, *ω<sup>i</sup>* is the weight value of the *i*th indicator, and *Ai* is the normalized value of the ith indicator. The higher the *EI*, the more intact the ecosystem is.

To examine the relative levels of ecosystem integrity in various regions, in this study, we constructed the Momoge Internationally Important Wetland Ecosystem Integrity Evaluation Scale based on the natural breakpoint method (Table 7).

**Table 6.** "Quality-Pressure-Pattern-Service" ecosystem integrity evaluation factor weighting table.

**Table 7.** Evaluation and grading of Ecosystem Integrity results.

#### 2.3.7. Spatial Pattern Optimization Method

Based on the above ecosystem integrity remote assessment framework and the measurement method presented by Wei et al. [45], the integrated ecological function assessment value was subdivided into four degrees to illustrate the strength of the ecological function in different regions.

For the classification of the levels, we took into account the probability distribution of the values under all grids and established a, b, and c as the cut-off values for the integrated ecological functioning of the district, ranging from the lowest to the highest. Then, with reference to the functional area border of the Nature Reserve designated by the State Environmental Protection Administration (SEPA) in 2007, the principle of establishing the important ecological protection area as the area with the highest expected value of ecosystem integrity was chosen. According to the system integrity index distribution of all units assessed, the expected value of the core area was designated a a, and the expected value of the pilot area was designated a d (the minimum value of ecosystem integrity for the pilot area). The expected value for the buffer zone decreased with increasing distance from the core zone (divided into 25 classes with a value range of d–a). Finally, the actual value of the comprehensive evaluation of wetland ecological functioning was subtracted from the expected value, and if the result was less than a predetermined threshold value (we set this threshold value to −0.04), this indicated that the proposed development of the wetland was disproportionate.

The ultimate purpose of assessing ecosystem integrity is to provide scientific evidence for the transformation of future land use in a sensible manner. We assumed the following conditions for the future restoration of wetland areas: