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Bibliometric Review of Biodiversity Offsetting During 1992−2019

Shuling YU Baoshan CUI Chengjie XIE Ying MAN Jing FU

YU Shuling, CUI Baoshan, XIE Chengjie, MAN Ying, FU Jing, 2022. Bibliometric Review of Biodiversity Offsetting During 1992−2019. Chinese Geographical Science, 32(2): 189−203 doi:  10.1007/s11769-022-1265-5
Citation: YU Shuling, CUI Baoshan, XIE Chengjie, MAN Ying, FU Jing, 2022. Bibliometric Review of Biodiversity Offsetting During 1992−2019. Chinese Geographical Science, 32(2): 189−203 doi:  10.1007/s11769-022-1265-5

doi: 10.1007/s11769-022-1265-5

Bibliometric Review of Biodiversity Offsetting During 1992−2019

Funds: Under the auspices of National Natural Science Foundation of China (No. U1901212, 51639001), Fund for Innovative Research Group of the National Natural Science Foundation of China (No. 51721093), National Key R & D Program of China (No. 2017YFC0404505)
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  • Figure  1.  Annual publication number and cumulative publication number in the 1992–2019 corpus of Biodiversity Offsetting publications

    Figure  2.  Three sections of the publication sources in the field of biodiversity offsetting. The core publication source is shown with bold dotted line. 1, Biological Conservation; 2, Plos One; 3, Journal of Applied Ecology; 4, Conservation Biology;5, Conservation Letters; 6, Ecological Applications; 7, Forest Ecology and Management; 8, Land Use Policy; 9, Nature; 10, Proceedings of the National Academy of Sciences of the United States of America; 11, Oryx; 12, Restoration Ecology; 13, Agriculture Ecosystems & Environment; 14, Biodiversity and Conservation; 15, Ecological Economics; 16, Ecosystem Services; 17, Environmental and Planning Law Journal; 18, Environmental Management; 19, Environmental Science & Policy; 20, Journal of Environmental Management; 21, Ecological Engineering; 22, Environmental Conservation; 23, Global Change Biology

    Figure  3.  Historical direct citation network of publications in the field of biodiversity offsetting. Point size indicates the citation frequency of this field, namely the local citation score value; lines indicate that the first publication is cited by the later publication. [1] Maron et al., 2015a; [2] Spash et al., 2015; [3] Ives and Bekessy, 2015; [4] Bull et al., 2014; [5] Maron et al., 2016; [6] Moreno-Mateos et al., 2015; [7] Gordon et al., 2015; [8] Maron et al., 2015b; [9] Rainey et al., 2015; [10] Goncalves et al., 2015; [11] Pickett et al., 2013; [12] Curran et al., 2014; [13] Bull et al., 2013a; [14] Overton et al., 2013; [15] Quétier et al., 2014; [16] Gardner et al., 2013; [17] Maron et al., 2013; [18] Pilgrim et al., 2013; [19] Virah-sawmy et al., 2014; [20] Maron et al., 2012; [21] Gordon et al., 2011; [22] Quétier and Lavorel, 2011; [23] Bekessy et al., 2010; [24] Moilanen et al., 2009; [25] Walker et al., 2009; [26] Mckenney and Kiesecker, 2010; [27] Norton , 2009; [28] Kiesecker et al., 2010; [29] Maron et al., 2010; [30] Kiesecker et al., 2009; [31] Burgin, 2008

    Figure  4.  Frequency of keywords (a), and research topics (b) in the field of biodiversity offsetting. The letter size of keywords represented their frequency in the studies, the larger the font, the more frequently it appeared in the studies

    Figure  5.  Publications number of different countries in the field of biodiversity offsetting

    Figure  6.  Academic collaborative relationships among the top 30 most productive countries in the field of biodiversity offsetting. The size of a circle represents the total number of publications in a country through international cooperation. The width of the line between the two countries represents the frequency of cooperation, and colors represent the cluster of countries, the countries with the same color (cluster) are more inclined to collaborate on writing papers than countries outside of their cluster

    Figure  7.  Local citation score (LCS) of the top 30 most productive authors (a), and the performances of the top 20 most productive authors in the field of biodiversity offsetting (b). Vaissiere A and Brownlie S, Vaissiere A and Brownlie S have the same article numbers and H-index, respectively

    Figure  8.  Publication volume per year of the top 10 most productive institutions in the field of biodiversity offsetting. Univ. Queensland, University of Queensland, Australia; Australian Univ., Australian National University, Australia; Univ. Copenhagen, University of Copenhagen, Denmark; Univ. Melbourne, University of Melbourne, Australia; Univ. Western, University of Western Australia, Australia; Univ. Helsinki, Australia University of Helsinki, Finland; Australia Rmit Univ., Royal Melbourne Institute of Technology; Univ. Cambridge, University of Cambridge; Ft. Collins., Fort Collins, USA; James Cook Univ., James Cook University, Australia

    Figure  9.  Academic cooperation among active authors (a) and institutions (b) in the field of biodiversity offsetting. In this network model, nodes in (a) are authors and edges indicate the number of coauthored publications, and colors represent authors’ clustering. Nodes in (b) are institutions and edges indicate the number of publications resulting from cooperation, and colors represent institutional clustering. Univ. Adelaide, University of Adelaide, Australia; Univ. Glasgow, University of Glasgow, UK; Univ. Montana, University of Montana, USA; Chengdu Inst. Biol., Chengdu Institute of Biology, China; Univ. Hawaii, University of Hawaii, USA; Univ. Stellenbosch, University of Stellenbosch, South Africa; Univ. Alberta, University of Alberta, Canada; Univ. Puerto Rico, University of Puerto Rico, USA; Univ. Michigan, University of Michigan, USA; Univ. Stirling, University of Stirling, UK; Arizona State Univ., Arizona State University, USA; Univ. New Hampshire, University of New Hampshire, USA; Bangor Univ., Bangor University, UK; Georgia So Univ., Georgia So University, USA; Univ. Calif Berkeley, University of California Berkeley, USA; Simon Fraser Univ., Simon Fraser University, Canada; Griffith Univ., Griffith University, Australia; Univ. Kent, University of Kent, UK; James Cook Univ., James Cook University, Australia; Univ. Hong Kong, University of Hong Kong, China; Univ. Oxford, University of Oxford, UK; Univ. London Imperial Coll, University of London Imperial Coll, UK; Univ. Maryland, University of Maryland, USA; Univ. Queensland, University of Queensland, Australia; Univ. Copenhagen, University of Copenhagen, Denmark; Australian Nati Univ., Australian National University, Australia

    Table  1.   Conceptual and practical issues on biodiversity offsetting

    ProblemDescription
    No net loss To achieve the amount of biodiversity attributes or value provided by compensation equals or exceeds the total impact
    Currency To achieve no net loss of biodiversity, metrics for measuring biodiversity value or attribute need to be chosen
    Equivalence Equally balanced biodiversity losses and gains
    Additionality The potential quantum of biodiversity gain associated with protecting or restoring a site, limitations on the availability of biodiversity target can lead to in-kind versus out-of-kind offset
    Ratios Offset ratios, which also be called multipliers, are used to determine how much biodiversity needs to be restored elsewhere to achieve no net loss relative to the quantity and quality of impact
    Location Where offsets should occur, spatial allocation of offsets in relation to impacts (on-site versus off-site)
    Time lags The temporal gap between losses of the impact and offset gains
    Duration To determine how long an offset scheme should continue
    Uncertainty Some uncertainties throughout the offset process, such as the risk of failure
    Thresholds Defining different threshold of biodiversity values to determine different offset types, and beyond which offsets are not acceptable
    Effectiveness To examine the feasibility and availability of restoration offsets or avoided loss offsets
    Notes: cited from Bull et al., 2013a; Mckennney and Kiesecker, 2010; Maron et al., 2013
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    Table  2.   The percentage of studies related to different ecosystem types in the field of biodiversity offsetting

    Ecosystem typesSub-ecosystem typesPercentage of studies related / %
    Terrestrial environmentsForest57
    Agriculture7
    Grass9
    Water environmentsWetland10
    Watershed1
    Marsh1
    River7
    Marine environmentsMarine8
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出版历程
  • 收稿日期:  2020-11-25
  • 网络出版日期:  2022-03-03
  • 刊出日期:  2022-04-01

Bibliometric Review of Biodiversity Offsetting During 1992−2019

doi: 10.1007/s11769-022-1265-5
    基金项目:  Under the auspices of National Natural Science Foundation of China (No. U1901212, 51639001), Fund for Innovative Research Group of the National Natural Science Foundation of China (No. 51721093), National Key R & D Program of China (No. 2017YFC0404505)
    通讯作者: CUI Baoshan. E-mail: cuibs@bnu.edu.cn

English Abstract

YU Shuling, CUI Baoshan, XIE Chengjie, MAN Ying, FU Jing, 2022. Bibliometric Review of Biodiversity Offsetting During 1992−2019. Chinese Geographical Science, 32(2): 189−203 doi:  10.1007/s11769-022-1265-5
Citation: YU Shuling, CUI Baoshan, XIE Chengjie, MAN Ying, FU Jing, 2022. Bibliometric Review of Biodiversity Offsetting During 1992−2019. Chinese Geographical Science, 32(2): 189−203 doi:  10.1007/s11769-022-1265-5
    • Human activities have resulted in about one-third to one-half of earth’s habitats being degraded, damaged, or destroyed (Vitousek et al., 1997), causing considerable impacts to biodiversity and ecosystem services (Benayas et al., 2009). With global economic output expected to double over the next two decades (World Bank, 2006), with accompanying increase in urbanization and resource extraction, such impacts could increase dramatically even though there is widespread recognition of the need to slow and ultimately prevent the loss of biodiversity (Díaz et al., 2020). In the face of development pressure, it may be difficult to stop all ecosystem transformations (Simmonds et al., 2020). Therefore, governments, developers and policy makers need coordinated development and conservation tools to reduce the rate of biodiversity loss.

      Biodiversity offsetting is becoming a key policy for managing the impact of development on natural habitats and has been adopted in many countries (Maron, 2015a; Gibbons et al., 2018). This mechanism aims to compensate the losses from a given development with equivalent gains elsewhere, typically with the aim to achieve no net loss (Moilanen et al., 2009; Griffiths et al., 2019). It is the last step of the mitigation hierarchy which also consists of avoidance, minimization of the duration, intensity, or extent of impacts that cannot be completely avoided, and restoration/rehabilitation of disturbed areas onsite (BBOP, 2012; IUCN, 2018). However, biodiversity offsetting is often misused and misunderstood (Maron, 2015a; Yu et al., 2018), such as there is often a confusion between Biodiversity Offsetting (BO) and Payments for Environmental Services (PES). BO is clearly related to biodiversity losses, while PES is usually not. If a PES project fails, payments can be stopped; if a BO fails, biodiversity losses still exist. The confusion can have negative implications for biodiversity conservation (Vaissière et al., 2020). It may be due to the absence of adequate frameworks (Gardner et al., 2013), and substantial problems existing with the perception and definitions of this concept (Bull et al., 2013a).

      Review is an important tool to advance a field (Noguchi, 2006; Sheble, 2017). Most previous reviews of biodiversity offsetting focused on the theoretical offset framework (McKenney and Kieseckerm, 2010; Gardner et al., 2013), loss and gain calculation methods (Moilanen et al., 2009; Maron et al., 2013), and ecological outcomes of biodiversity offsetting (zu Ermgassen et al., 2019). However, although many papers have been published in this important field, there are few papers summarizing recent research progress, social networks and comprehensive reviews. The difficulty in identifying key research topics, methods, authors, and institutions may hinder the development and application of biodiversity offsetting. It is also likely making it more difficult for new investigators to quickly learn and apply the theory of biodiversity offsetting.

      In this study, we used a bibliometric analysis method, which has been widely used in providing an innovative perspective for the evaluation of research trends (VanderWaal and Deen, 2018) through citation analysis and content analysis. We reviewed publications in the field between 1992 and 2019. First, we identified major journals, development trend of the publications, outstanding authors, key countries and institutions. Second, word cloud and key references were analyzed to identify the major theoretical and methodological topics. Third, we characterized collaboration networks to evaluate the contributions from different countries, institutions and scientists. We aimed to understand how the academic community contributes to addressing the issues and how future research can enhance the implementation of biodiversity offsetting.

    • To increase the possibility of detecting related publications and reduce known deviations and issues of individual database (Pautasso, 2014; Calver et al., 2017), we retrieved the Web of Science (WoS) (http://isiknowledge.com/) and Elsevier Scopus (Scopus) (http://www.scopus.com) databases for related English language publications between 1990 and 2019. Since the earliest study on biodiversity offsetting appeared in 1992, the data analysis in this study began in 1992. Our search focused on the term ‘biodiversity offset*’. Searches were executed manually, and publication information and abstracts were downloaded in ‘.txt’ and ‘.bib’ files, respectively. .txt and .bib files were read in R and all fields were extracted using the bibliometrix package to make sure a data frame with the same structure could be created, the fields included title, authors, abstract, keywords, publication year, source, and sources cited. This process resulted in 924 publications were found in WoS, including research articles (87.88%), review papers (6.17%), and other publications; 862 publications were found in Scopus, including research articles (77.61%), review papers (7.54%), and other publications (14.85%). The total dataset included in our analysis consisted of 1190 publications from Scopus and WoS, not excluding duplicate documents and publications accepted in 2019 but published in 2020.

    • Bibliometric analysis is a valid method for the quantitative analysis of academic papers using statistical techniques (Zhang et al., 2015). It mainly consists in investigation and analysis of different journals, countries, institutions, authors, and citations, and aims to assess the current research status and development trends in specific fields, to determine future research directions. To facilitate the bibliometric analysis, the bibliometrix package in R was utilized (Aria, 2017). It can extract the basic information of each searched publication, including authors, countries and institutions, publication year and journal, total number of citations and keywords, so as to analyze the key characteristics of related research results in detail.

    • We plotted the number of articles published annually and the accumulated number of articles, to infer the development status of biodiversity offsetting and predict its future development trend. The accumulated number of articles can represent the growth of literature. According to the exponential and logical curve model of literature growth, de Solla Price (1961) put forward four stages of literature growth, which have certain guiding significance to the actual scientific research. 1) At the early stage of the discipline’s birth, the literature growth was unstable and the theory was not perfect, so it was difficult to express by mathematical formula; 2) During the period of discipline development, professional theories developed rapidly, absolute number of papers increased rapidly, and the law of exponential growth was strictly followed; 3) As the discipline theory becomes more and more mature, the number of papers grows slowly and becomes a linear growth, and only a fixed literature growth is maintained; 4) The discipline theory is complete, the number of discipline papers is decreasing day by day, the curve is gradually parallel to the horizontal axis, or shows irregular fluctuations. Therefore, according to the fitting curve of literature growth, the discipline development stage can be judged, so as to guide the actual scientific research.

      We divided the publication sources into three sections with the same number of articles in each section, the publication sources of the first 1/3 articles were called the core publication sources, which was divided according to Law of Bradford (Chen and Leimkuhler, 1986).

      We analyzed the top 31 important publications of the research field and their citations per year, identified based on local citation score (LCS), and built their historical citation network (Chung, 2007). LCS refers to the number of citations of the collected literature by other references in the collected documents, also known as the number of citations in the field. The higher the number of local citations of a document, the greater its influence in this field. We used point size to illustrate the number of citations in the field (LCS), and lines to indicate that published documents were cited by the documents published later.

    • Tracking the research trends of outstanding scientists allows us to quickly grasp the research hotspots and research directions in the field. We identified the top 30 highly cited authors in this field based on LCS, defined as important authors. We used the H-index, which is based on a simple combination of the amount of publications and the number of citations to assess the academic impact of the top most productive authors: The H-index indicates that scientists have published at least H articles that have been cited at least H times (Hirsch, 2005; Hirsch and Buela-Casal, 2014). It is an objective indicator of both the quantity and quality of a scientist’s output and has been widely used to evaluate the academic level of journals or countries/regions (Bornmann et al., 2011).

    • Statistical analysis of the volume of publications of research institutions (or universities) can highlight the publication mode of research institutions in this field, and tracking the research results of important research institutions (universities) in a certain field can help us quickly grasp the research trends in this field. How do we know that a research institution (university) is an important research institution in this field? And how do we know which institutions are more active in the field? The amount of publications is the most obvious indicator. The higher the number of publications per year of an institution in a given field, the more active it is in this field. In this study, we obtained the publications from key research institutions and explored how active they are in the field. The relationship between the cumulative percentage of the number of research institutions and the cumulative percentage of the publication volume is also discussed.

    • An author cooperation network is a type of social network which plays a critical role in the creating and sharing of knowledge. Therefore, through the analysis and visualization of the social network structure between authors, the mode of author cooperation can be clearly demonstrated. In this study, to evaluate the contributions from different countries, institutions and scientists, we used social network analysis to analyze academic cooperation of different countries and authors. First, we analyzed the connections between authors in a network graph. Authors and relationships were represented by weighted nodes and links, respectively (Ye et al., 2012). Second, we analyzed a collaborative network with the co-authors’ countries represented by nodes, the connection between nodes representing the frequency index of the two countries’ cooperative publication of papers, and color representing connected component membership. This process was analyzed in R, and networks visualization was done via VOSviewer 1.6.15 (Waltman et al., 2010; Van Eck and Waltman, 2014).

      The phenomenon by which at least two or more research institutions participate in the same research is defined as cooperation between research institutions. We used the networkPlot function in the Bibliometrix package and the net2VOSviewer function (via VOSviewer software) to visualize a network of collaborations between research institutions and explore how collaboration between research institutions evolved through the study period.

    • Annual number of publications and cumulative number of publications are divided into two periods. Before 2001, the development of biodiversity offsetting was slow, and the number of papers published per year was less than 10, with an average annual publication of 3.2. In 2002, the number exceeded 10. Between 2002 and 2019, the average annual number of publications was 64.3, with a maximum of 141. From 2015 to 2019, more than 100 papers were published, with an average annual publication of 126.8 (Fig. 1). During this period, biodiversity offsetting achieved relatively rapid development.

      Figure 1.  Annual publication number and cumulative publication number in the 1992–2019 corpus of Biodiversity Offsetting publications

      The Cumulative Publication Number Curve shows that the growth rate was slow from 1992 to 2001, increased from 2002 to 2014, and increased significantly from 2015 to 2019, indicating that research on biodiversity offsetting was entering a rapid development stage (Fig. 1). Fig. 1 shows that the quadratic polynomial curve fitted the literature growth curve well. It indicates that the accumulation of literature in this field would continue to increase rapidly in the future. At present, the research on biodiversity offsetting is still at the beginning of the second stage. The absolute number of papers increases rapidly, but the total amount is still small, and the theory and research methods could still be improved.

      All 1190 publications were published in 471 sources, the core publication sources including 19 journals. The journal which most frequently published articles on biodiversity offsetting was Biological Conservation, followed by the broad scope journal PLOS One. Most of the core journals focused on biodiversity conservation, ecosystem restoration, and ecosystem management. It is worth noting that top journals Nature and Proceeding of The National Academy of Sciences of the United States of America (PNAS) are also among the core journals, indicating that high attention has been paid to biodiversity offsetting (Fig. 2).

      Figure 2.  Three sections of the publication sources in the field of biodiversity offsetting. The core publication source is shown with bold dotted line. 1, Biological Conservation; 2, Plos One; 3, Journal of Applied Ecology; 4, Conservation Biology;5, Conservation Letters; 6, Ecological Applications; 7, Forest Ecology and Management; 8, Land Use Policy; 9, Nature; 10, Proceedings of the National Academy of Sciences of the United States of America; 11, Oryx; 12, Restoration Ecology; 13, Agriculture Ecosystems & Environment; 14, Biodiversity and Conservation; 15, Ecological Economics; 16, Ecosystem Services; 17, Environmental and Planning Law Journal; 18, Environmental Management; 19, Environmental Science & Policy; 20, Journal of Environmental Management; 21, Ecological Engineering; 22, Environmental Conservation; 23, Global Change Biology

      Among the 31 important publications, the LCS values of Mckennney, 2010, Maron, 2013, and Bull, 2013a (Fig. 3) were significantly higher than that of other publications, and which are important nodes for literature growth. These three papers are reviews of important theoretical and practical issues, and future challenges in the area, concepts including: currency, no net loss, equivalence, additionality, ratios, location, time lags, duration, uncertainty, thresholds, and effectiveness (Table 1), which are the most recent relevant issues considered in subsequent studies, especially offset ratios calculation (Gibbons et al., 2016; Yu et al., 2017; 2018). These nodal literatures led to an increase in the rate of subsequent publications in the literature.

      Figure 3.  Historical direct citation network of publications in the field of biodiversity offsetting. Point size indicates the citation frequency of this field, namely the local citation score value; lines indicate that the first publication is cited by the later publication. [1] Maron et al., 2015a; [2] Spash et al., 2015; [3] Ives and Bekessy, 2015; [4] Bull et al., 2014; [5] Maron et al., 2016; [6] Moreno-Mateos et al., 2015; [7] Gordon et al., 2015; [8] Maron et al., 2015b; [9] Rainey et al., 2015; [10] Goncalves et al., 2015; [11] Pickett et al., 2013; [12] Curran et al., 2014; [13] Bull et al., 2013a; [14] Overton et al., 2013; [15] Quétier et al., 2014; [16] Gardner et al., 2013; [17] Maron et al., 2013; [18] Pilgrim et al., 2013; [19] Virah-sawmy et al., 2014; [20] Maron et al., 2012; [21] Gordon et al., 2011; [22] Quétier and Lavorel, 2011; [23] Bekessy et al., 2010; [24] Moilanen et al., 2009; [25] Walker et al., 2009; [26] Mckenney and Kiesecker, 2010; [27] Norton , 2009; [28] Kiesecker et al., 2010; [29] Maron et al., 2010; [30] Kiesecker et al., 2009; [31] Burgin, 2008

      Table 1.  Conceptual and practical issues on biodiversity offsetting

      ProblemDescription
      No net loss To achieve the amount of biodiversity attributes or value provided by compensation equals or exceeds the total impact
      Currency To achieve no net loss of biodiversity, metrics for measuring biodiversity value or attribute need to be chosen
      Equivalence Equally balanced biodiversity losses and gains
      Additionality The potential quantum of biodiversity gain associated with protecting or restoring a site, limitations on the availability of biodiversity target can lead to in-kind versus out-of-kind offset
      Ratios Offset ratios, which also be called multipliers, are used to determine how much biodiversity needs to be restored elsewhere to achieve no net loss relative to the quantity and quality of impact
      Location Where offsets should occur, spatial allocation of offsets in relation to impacts (on-site versus off-site)
      Time lags The temporal gap between losses of the impact and offset gains
      Duration To determine how long an offset scheme should continue
      Uncertainty Some uncertainties throughout the offset process, such as the risk of failure
      Thresholds Defining different threshold of biodiversity values to determine different offset types, and beyond which offsets are not acceptable
      Effectiveness To examine the feasibility and availability of restoration offsets or avoided loss offsets
      Notes: cited from Bull et al., 2013a; Mckennney and Kiesecker, 2010; Maron et al., 2013
    • We made a Word Cloud using Keywords-Plus and analyzed the current research topics, the hot issues and research trends of biodiversity offsetting. There were 5104 keywords, and 4949 left after the following keywords were deleted: ‘biodiversity offset’, ‘biodiversity offsets’ and ‘biodiversity offsetting’. A total of 56.8% of the total 4949 keywords appeared only once (Fig. 4a). The keywords indicate that the main studies in this field focused on ecosystem services, management, ecosystem restoration, no net loss, climate change, impacts and biodiversity conservation (Fig. 4b). The research topics shown in Fig. 4 indicate that keywords mainly focused on biodiversity conservation, no net loss of ecosystem services, and the implications for policymakers and management, while other keywords focused on research models, carbon offsets to deal with climate change, and some other fields (Fig. 4b). Our statistical analysis showed that out of a total of 678 publications studying biodiversity offsetting for different ecosystem types, the majority of studies related to terrestrial environments (72%), in particular forest ecosystems (57%), followed by water environments (19%), especially wetland ecosystems (10%), while some other studies explored the marine environment (8%) (Table 2).

      Figure 4.  Frequency of keywords (a), and research topics (b) in the field of biodiversity offsetting. The letter size of keywords represented their frequency in the studies, the larger the font, the more frequently it appeared in the studies

      Table 2.  The percentage of studies related to different ecosystem types in the field of biodiversity offsetting

      Ecosystem typesSub-ecosystem typesPercentage of studies related / %
      Terrestrial environmentsForest57
      Agriculture7
      Grass9
      Water environmentsWetland10
      Watershed1
      Marsh1
      River7
      Marine environmentsMarine8
    • As shown in Fig. 5, the top three most productive countries extracted by tracking authors’ addresses were the United States, Australia, and the United Kingdom with 240, 181 and 149 publications, respectively (Fig. 5). With the exception of Japan, Hungary, and Singapore, which mainly published articles with co-authors from a single country, other countries published a significant amount of publications involving multi-country cooperation. China, Brazil, Denmark, Italy, Portugal, Costa Rica and Antigua published more articles involving multiple countries than from a single country, while other countries published more articles from a single country than with multi-country collaborations (Fig. 5).

      Figure 5.  Publications number of different countries in the field of biodiversity offsetting

    • Fig. 6 shows five clusters in the academic collaborative relationships among the top 30 most productive countries. The circle size of the USA, the United Kingdom and Australia are bigger than the other countries, which indicates that the more international countries are the most active in this area. The line between USA, United Kingdom, Australia, China, Germany and France are thicker than others, which shows that the authors in these countries have a closer collaboration relationship. These countries are familiar with international cooperation and regard it as an important research strategy.

      Figure 6.  Academic collaborative relationships among the top 30 most productive countries in the field of biodiversity offsetting. The size of a circle represents the total number of publications in a country through international cooperation. The width of the line between the two countries represents the frequency of cooperation, and colors represent the cluster of countries, the countries with the same color (cluster) are more inclined to collaborate on writing papers than countries outside of their cluster

    • Maron M from the University of Queensland and Bull J from the University of Kent have published 23 and 22 articles respectively and are the top two productive authors in the field of biodiversity offsetting. At the same time, according to the analysis results of the importance of literatures on the historical direct citation Network, Maron M and Bull J were listed as 31 important literatures in the field of Biodiversity Offsetting (Fig. 3), and the citation frequency (LCS) of Maron M and Bull J in the current dataset was relatively high (Fig. 7a). H index is an index used to evaluate scientists. It can be seen that although the two authors have more publications and higher citation rates, their H-index is relatively low, indicating that their other publications did not receive enough citations. The authors of the top 31 most productive authors were mostly located among the top 10 most productive countries, with Australia having the most influential authors, followed by France (Fig. 7b).

      Figure 7.  Local citation score (LCS) of the top 30 most productive authors (a), and the performances of the top 20 most productive authors in the field of biodiversity offsetting (b). Vaissiere A and Brownlie S, Vaissiere A and Brownlie S have the same article numbers and H-index, respectively

    • Fig. 8 shows the publication volume per year of the top 10 most productive institutions. The volume of publications is the most direct manifestation of the high degree of activity of a scientific research institution. If the research institution produces output every year in this field, it means that the research institution is active in this field. The higher the number of publications per year, the more active it is in this field. In recent years, seven institutions, including University of Queensland, Australia (Univ. Queensland), Australian National University, Australia (Australian Univ.), University of Copenhagen, Denmark (Univ. Copenhagen), University of Melbourne, Australia (Univ. Melbourne), University of Western Australia, Australia (Univ. Western Australia), University of Helsinki, Finland (Univ. Helsinki), Royal Melbourne Institute of Technology, Australia (Rmit Univ.) and University of Cambridge (Univ. Cambridge) were active in the field of biodiversity offsetting. Among them, Univ. Queensland, Australian Univ. and Univ. Copenhagen were highly active. The research output of these institutions may thus be worthy of our attention. Institutions such as Colorado State University, USA (Colorado State) and James Cook University, Australia (James Cook Univ.) have not published in recent years, they may have shifted their research interest. Among the top 10 most productive institutions, nine are universities.

      Figure 8.  Publication volume per year of the top 10 most productive institutions in the field of biodiversity offsetting. Univ. Queensland, University of Queensland, Australia; Australian Univ., Australian National University, Australia; Univ. Copenhagen, University of Copenhagen, Denmark; Univ. Melbourne, University of Melbourne, Australia; Univ. Western, University of Western Australia, Australia; Univ. Helsinki, Australia University of Helsinki, Finland; Australia Rmit Univ., Royal Melbourne Institute of Technology; Univ. Cambridge, University of Cambridge; Ft. Collins., Fort Collins, USA; James Cook Univ., James Cook University, Australia

    • Fig. 9 presents the academic cooperation among the active authors and institutions in the research area of biodiversity offsetting. We identified 200 unique authors, mainly clustered in four cooperative clusters, contributing 84%, 11.5%, 4% and 0.5% of the output in the field, respectively. The largest component (n = 168) consisted in co-authors of one article published in the journal Science, about the impact of conservation on the status of the world’s vertebrates (Hoffmann et al. 2010). The next largest component (n = 23) included most of the top 30 most productive authors, such as Maron M, Bull J, Gordon A, Kiesecker J, Gardner T, Lindenmayer D, Von H, Pilgrim J, Possingham H, Gibbons P and Evans M. They are the main researchers on biodiversity offsetting.

      Figure 9.  Academic cooperation among active authors (a) and institutions (b) in the field of biodiversity offsetting. In this network model, nodes in (a) are authors and edges indicate the number of coauthored publications, and colors represent authors’ clustering. Nodes in (b) are institutions and edges indicate the number of publications resulting from cooperation, and colors represent institutional clustering. Univ. Adelaide, University of Adelaide, Australia; Univ. Glasgow, University of Glasgow, UK; Univ. Montana, University of Montana, USA; Chengdu Inst. Biol., Chengdu Institute of Biology, China; Univ. Hawaii, University of Hawaii, USA; Univ. Stellenbosch, University of Stellenbosch, South Africa; Univ. Alberta, University of Alberta, Canada; Univ. Puerto Rico, University of Puerto Rico, USA; Univ. Michigan, University of Michigan, USA; Univ. Stirling, University of Stirling, UK; Arizona State Univ., Arizona State University, USA; Univ. New Hampshire, University of New Hampshire, USA; Bangor Univ., Bangor University, UK; Georgia So Univ., Georgia So University, USA; Univ. Calif Berkeley, University of California Berkeley, USA; Simon Fraser Univ., Simon Fraser University, Canada; Griffith Univ., Griffith University, Australia; Univ. Kent, University of Kent, UK; James Cook Univ., James Cook University, Australia; Univ. Hong Kong, University of Hong Kong, China; Univ. Oxford, University of Oxford, UK; Univ. London Imperial Coll, University of London Imperial Coll, UK; Univ. Maryland, University of Maryland, USA; Univ. Queensland, University of Queensland, Australia; Univ. Copenhagen, University of Copenhagen, Denmark; Australian Nati Univ., Australian National University, Australia

      We identified 37 unique institutions in this research area, which mainly consisted of two cooperative clusters, the largest component (n = 24, 64.9%) were from the published article on the journal of Science, the second component (n = 13) included the institutions in the top 10 most productive institutions, such as Univ. Queensland, Australian Univ., Univ. Copenhagen, and James Cook Univ.. Otherwise, University of Kent (Univ. Kent) was also an important cooperative institution.

    • Although there is a long history of development and applications of biodiversity offsetting, the total amount of publications is still small, most of them focusing on conceptual framework and methodological studies. The topics mainly focused on biodiversity conservation and sustainability of socio-ecological systems, including studies of conservation planning, impacts on the biodiversity of different land uses changes, compensation of ecosystem services, and models on offset ratios and suitable habitat (Fig. 4).

      The evaluation of the equivalence has been the subject of numerous papers lately, which was often concentrated on the offset ratios (Moilanen et al., 2009; Gibbons et al., 2016). Offset ratio models are an important research area of biodiversity offsetting, related to whether the ecological function and ecosystem service can achieve no net loss. Different offset ratio calculation methods may be more common or appropriate for different applications, but the main principles of equivalence and additionality were all followed in these models (Bull et al., 2014). Some studies also took into consideration time lags, the risk of failure (Yu et al., 2017), and longevity (Laitila et al., 2014) (Table 1) to deal with the uncertainties in offset effectiveness. Offset ratio model construction usually needs to choose a metric for measuring biodiversity, commonly forest cover, biodiversity, fisheries, land productive capacity or carbon sequestration (Bull et al., 2014; Yu et al., 2017; Budiharta et al., 2018; Maron et al., 2018). However, biodiversity offsetting should include not only the assessment of species and habitats, but also the assessment of ecological processes (Gardner et al., 2013; Pilgrim et al., 2013; Bigard et al., 2017) and ecological functions to ensure that compensation fully takes into account all aspects of sustainable development (Bull et al., 2013a, Moreno-Mateos et al., 2015). Such as one ecological process that biodiversity offsetting should consider is ecological connectivity, because the lack of connectivity may increase the time required for compensation to achieve its goals, and/or may increase the costs associated with the maintenance and restoration of the offset area, or even lead to the possibility of compensation failure (Yu et al., 2018). Besides, there are still few quantitative approaches for offsetting that can consider multiple ecosystem services simultaneously, because of the trade-offs and synergy between different ecosystem services, the compensation scenarios for multiple ecosystem services are more complicated (Yu et al., 2021). We recommend that when making decisions to restore multiple ecosystem services, priority should be given to trade-offs and synergies.

      The 31 most important papers and their historical direct citation network (Fig. 3), can give a quick overview to researchers of the theory, development and direction of biodiversity offsetting. The other most discussed conceptual issues in the biodiversity offsetting literature recently were flexibility and effectiveness. Flexibility in biodiversity offsetting refers to existing options for offsetting impacts in space and time. Spatial flexibility is the number of options available in a given area, while temporal flexibility is the time lag between development and when gains are required (Wissel and Wätzold, 2010; Bull et al., 2015; Yu et al., 2018). Flexibility is often introduced to improve the offset trading market functionality and increase the feasibility of compensation, when area-based offsets are not sufficient to address biodiversity impacts (Bull et al., 2013b). However, increasing flexibility in space might reduce the compensated ecosystem services, undermining the effectiveness of offsetting, because the ecosystem services loss of local communities affected by development should benefit from the compensation location. The further away the offset site is, the less additional benefit for local communities (Yu et al., 2018, Maseyk et al., 2020). Existing policies overemphasize the flexibility of compensation, which leads to many compensation projects becoming tricky things (zu Ermgassen et al., 2020). We suggest that future researches could focus on the threshold of flexibility. There was also an increasing research focused on the effectiveness of offset projects and policies in different scale and ecosystem types, such as the study of zu Ermgassen indicated that there is a huge gap between the implementation of offsets globally and the evidence to prove their effectiveness (zu Ermgassen et al., 2019). Through meta-analysis, Curran (2014) showed that the probability of failure in restoration offsetting due to time lags was 82%. Jones and Schmitz (2009) analyzed 240 cases and found that the success rate of biodiversity restoration was only 23%. How to improve the effectiveness of biodiversity compensation has become a key problem to be solved urgently. In addition, our results showed that there were more biodiversity offsetting being applied in terrestrial ecosystem, rarely studied in aquatic ecosystem and marine ecosystem (Table 2 and Fig 4b), which was consistent with the previous studies (zu Ermgassen et al., 2019; Jacob et al., 2020). It may be due to the complexity of aquatic and Marine ecosystems and the difficulties in implementing biodiversity offsetting. Therefore, we suggest that to increase research on compensation based on ecological processes and on the tradeoff between the flexibility and feasibility of compensation policies to ensure the effectiveness of compensation policies, especially with regard to aquatic ecosystem and marine ecosystem.

    • We showed that the average annual number of publications increased since 2001 (Fig. 1), which may be the result of political changes related to biodiversity offsetting (Coralie et al., 2015). The number of publications on this topic increased since the USA wetland mitigation system was published by the National Research Council (NRC), a principal reference in the corpus of biodiversity offsetting (National Research Council, 2001). The concept of “ecosystem services” was also adopted by politicians in 2000s (Barnaud and Antona, 2014).

      Cultural and political systems play an important role in the adoption of mechanisms. A detailed comparison of the number of biodiversity offsetting publications in country-level showed that the USA had the largest number of publications (Fig. 5). The result is not surprising, since the United States set a precedent in the early 1970s for offsetting biodiversity through its wetlands mitigation program (Ambrose, 2000). In 1990, the target of no net loss of area or function was established under the Clean Water Act (USA) (Corps and EPA, 1990). With 30 years of experience in wetland and conservation banking (USA), the USA has perhaps the most comprehensive set of methods in the world to assess and offset the impact of projects on wetlands, streams, and listed endangered species, which influenced the different biodiversity offsetting schemes worldwide (Burgin, 2008; Boisvert et al., 2013).

      Australia has the second largest number of publications, and it has developed many methods of biodiversity offsetting. The habitat hectares method was first elaborated during the public consultation phase for the Victorian Native Vegetation Management Framework and was subsequently endorsed by the Australian Government (Parkes et al., 2003). In 2006, the Net Environmental Benefit approach was first broadly described by Western Australia’s Environmental Protection Authority (EPA) (Authority, 2006), and subsequently in 2008, specific Guidance on Biodiversity Offsetting was made available by the EPA (Authority, 2008). The first edition of the South Australian Strategic Plan, an overarching State policy document, included a target that all clearance of native vegetation would be offset by a significant biodiversity gain.

      There is also extensive research in European countries, especially the United Kingdom. Europe has launched the ‘No Net Loss’ initiative, which includes the development of a biodiversity offsetting scheme as one of the policy options, and the European Parliament urged the European Commission to develop an valid regulatory framework based on the 2012 initiative (Treweek and ten Kate, 2012). At present, it is a legal requirement in Europe to compensate for the inevitable negative impacts on biodiversity through the Birds and Habitat Directive (the Europe institutions) and the Environmental Responsibility Directive (the Europe Union) (McKenney and Kiesecker, 2010). These countries have taken the lead in institutionalizing the regulation of biodiversity offsetting procedures (McKenney and Kiesecker, 2010). In this study, we highlighted the major authors who have supported the development of biodiversity offsetting, in particular Australian researchers and European researchers (Fig. 7). The two most-frequently cited authors were Maron M and Bull J, who were also the top two most prolific authors. Most of the productive authors were co-authors in many articles.

      The USA, United Kingdom and Australia are currently highly collaborative and well-connected countries (Fig. 6). A few environmental Non-Governmental Organizations (NGOs) have played a critical role in this, such as the ‘Business and Biodiversity Offsets Programme’ (BBOP, 2009) with the purpose to diffuse biodiversity offsetting standards and processes (Hrabanski, 2015). Other environmental NGOs have also made significant contributions, such as The Nature Conservancy, Conservation International and the Union for Conservation of Nature. These NGOs have promoted the development and promotion of biodiversity offsetting worldwide, and boosted offsite compensation via the use of market-based approaches based on function transfer (Moilanen and Laitila, 2016).

      The results had also shown that although there was a better cooperation with other countries, the amount of publications of China was still small (Fig. 5), because China’s main approach is to restore degraded habitats, protect areas that are about to or expected to lose biodiversity, or provide economic compensation for restoring degraded ecosystems. However, economic compensation is usually not based on the principles associated with biodiversity offsetting (Ali et al., 2018). We suggest that it should not only strengthen the cooperation between China and other countries, but enhance the research and popularization of the theory of biodiversity offsetting. In order to enable new investigators to quickly learn and apply the theory of biodiversity offsetting, we suggest starting with core journals, important literature and works by important authors. And we also recommend the productive institutions that visiting students who are interested in this field can contact.

    • Biodiversity offsetting is critical to promote sustainable natural resources management. This paper has completed a comprehensive review, summarized the recent progress of biodiversity offsetting in the academic field, and clarified its driving forces and theoretical problems. We adopted a bibliometric analysis method to analyze the academic features of English language publications on biodiversity offsetting indexed by Web of Science and Scopus during 1992–2019. The publication trends results showed that the research on biodiversity offsetting is still in the initial stage of development, with the absolute number of papers increasing rapidly, but the total amount remaining small. The journal Biological Conservation is the most productive journal in this field. The United States, Australia, and the United Kingdom are the top three most productive countries, and are currently highly collaborative and well connected.

      We highlighted the major authors who have supported the development of biodiversity offsetting, and showed that the growth of biodiversity offsetting was main driven by the cultural and political systems of the countries. According to the keyword analysis, the majority of studies related to terrestrial environments, followed by aquatic environments, especially wetland ecosystems. The important theoretical and practical issues, and future challenges in the area focused on currency, no net loss, equivalence, additionality, ratios, location, time lags, duration, uncertainty, thresholds, and effectiveness. The evaluation of the equivalence was mainly concentrated on the offset ratios, but usually chose a metric for measuring biodiversity or ecosystem service, methods based on ecological processes or multiple ecosystem services were still lacking. Recently, the most discussed conceptual issues in the biodiversity offsetting literature were flexibility and effectiveness, emphasizing that flexibility in space may be a tricky thing in realizing offset effectiveness. These findings can provide valuable insights for researchers working in the field, which can lead to more research results to guide sustainable natural resource utilization and biodiversity conservation.

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