What is the effect of prescribed burning in temperate and boreal forest on biodiversity, beyond pyrophilous and saproxylic species? A systematic review

Background: While the effects of prescribed burning on tree regeneration and on pyrophilous and/or saproxylic species are relatively well known, effects on other organisms are less clear. The primary aim of this systematic review was to clarify how
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  Eales et al. Environ Evid (2018) 7:19 https://doi.org/10.1186/s13750-018-0131-5 SYSTEMATIC REVIEW What is the effect of prescribed burning in temperate and boreal forest on biodiversity, beyond pyrophilous and saproxylic species? A systematic review Jacqualyn Eales 1,2† , Neal R. Haddaway 1,3*†  , Claes Bernes 1 , Steven J. Cooke 4 , Bengt Gunnar Jonsson 5 , Jari Kouki 6 , Gillian Petrokofsky 7  and Jessica J. Taylor 4 Abstract   Background:  While the effects of prescribed burning on tree regeneration and on pyrophilous and/or saproxylic species are relatively well known, effects on other organisms are less clear. The primary aim of this systematic review was to clarify how biodiversity is affected by prescribed burning in temperate and boreal forests, and whether burn-ing may be useful as a means of conserving or restoring biodiversity, beyond that of pyrophilous and saproxylic species. Methods:  The review examined primary field studies of the effects of prescribed burning on biodiversity in boreal and temperate forests in protected areas or under commercial management. Non-intervention or alternate levels of intervention were comparators. Relevant outcomes were species richness and diversity, excluding that of pyrophilous and saproxylic species. Relevant studies were extracted from a recent systematic map of the evidence on biodiversity impacts of active management in forests set aside for conservation or restoration. Additional searches and a search update were undertaken using a strategy targeted to identify studies focused on prescribed burning interven-tions. Grey literature and bibliographies of relevant published reviews were also searched for evidence. Studies were assessed for internal and external validity and data were extracted, using validity assessment and data extraction tools specifically designed for this review. Studies were presented in a narrative synthesis and interactive map, and those which were suitable were quantitatively synthesised using meta-analyses, subgroup analysis and meta-regression. Results:  Searches generated a total of 12,971 unique records. After screening for relevance, 244 studies (from 235 articles) were included in this review. Most studied forests were located in the USA (172/244), with the rest located in Canada, Europe and Australia. Eighty-two studies reporting 219 comparisons were included in the quantitative synthesis. Within the meta-analyses for each group of taxa, we identified a small to moderate volume of evidence, and heterogeneity was ubiquitous. Prescribed burning had significant positive effects on vascular plant richness, non-native vascular plant richness, and in broadleaf forests, herbaceous plant richness. Time since the burn, forest type and climate zone were significant moderators predicting the effect of burning on herbaceous plant richness. No other significant relationships were identified. © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/ ), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the srcinal author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/  publi cdoma in/zero/1.0/ ) applies to the data made available in this article, unless otherwise stated. Open Access Environmental Evidence *Correspondence: neal_haddaway@hotmail.com; neal.haddaway@sei-international.org † Jacqualyn Eales and Neal R. Haddaway contributed equally to the manuscript 1  Mistra EviEM, Stockholm Environment Institute, Box 24218, 104 51 Stockholm, SwedenFull list of author information is available at the end of the article  Page 2 of 33Eales et al. Environ Evid (2018) 7:19 Background In boreal and temperate regions, the biodiversity of for-ests set aside from forestry practice is often considered best preserved by non-intervention [1]. However, in many protected forests, remaining biodiversity values are legacies of past disturbances, e.g. recurring fires, grazing, or small-scale felling [2]. ese forests may require active management to enhance or maintain the biodiversity characteristics that were the reason for protecting them [1, 3]. Such management can be particularly relevant where the aim is to restore lost ecological values, such as to restore particular seral stages or vegetation mosaics, upon which certain taxa depend [4].Naturally occurring fires (wildfires) are considered to be an essential part of boreo-temperate forest distur-bance dynamics [5]. It is well documented that in some regions wildfires have always occurred and have long-term patterns (fire regimes), probably related to large-scale and long-term climate and vegetation changes [6–8]. It is also recognised that humans have, for thou -sands of years, managed or altered ecosystems with fire, for example, the Maori colonization of the southern island of New Zealand around 700–800 years ago was characterized by widespread destruction of tropical for-ests by burning [9]. In general, fires modify the structure of a forest in a way that many forest-dwelling species find beneficial and are specifically adapted to [10]. Historical fire regimes are challenging to characterise but are clearly  variable in their frequency, extent, and intensity [11]. is inherent variability is likely to have important conse-quences for forest biodiversity, but it also makes it highly challenging to explore the ecological consequences in a systematic and detailed way.Fire suppression is a management practice to mini-mise the negative impacts of wildfires, particularly on commercially managed forests, and on human lives and livelihoods. Such practices, which began at least 100 years ago in the United States [12], have been increas-ingly common due to the desire to minimise catastrophic fire events [13]. Fire suppression can halt fires alto-gether, leading to a lack of specific habitats or resources for those species that are associated with fires and other natural disturbances [14]. is anthropogenic fire sup-pression has been shown to affect native forest biodiver-sity negatively [15], notably for pyrophilous (fire-loving) species and several saproxylic species (those dependent on dead wood) [16]. Furthermore, fire suppression has the potential to change many aspects of forest structure, disturbance dynamics, and succession, with equally clear consequences for forest-dwelling biota. In particular, northern Europe has seen drastic reductions in the extent and severity of forest fires [17, 18]. ere has been debate in the literature regarding whether fire suppression has contributed to the accumulation of dense woody vegeta-tion which could have implications for biodiversity and lead to increased fire risk, areas burned and fire inten-sity (debate summarised in [19]). is debate extends to peatlands [20]. Active, policy-driven fire suppression since the late nineteenth century, particularly in managed areas, and changed landscape structure are likely key fac-tors behind changes in fire regimes [21].Prescribed burning, also known as controlled burning or planned burning is currently used in some protected areas as an active management tool to enhance and main-tain habitats for biodiversity outcomes in boreo-temper-ate forests [22, 23]. Prescribed burning is also commonly used for the purpose of mitigating wildfire risk by man-aging the accumulation of fuel in forests when and where necessary. Historically, this has been the primary purpose in Australia, where the practice is widely applied [24, 25]. In this region, there is also recognition by management authorities that planned burns can have positive effects Conclusions:  Knowledge gaps exist for studies outside North America, in mixed forests and for non-plant organism outcomes. We identify a need to apply study designs consistently and appropriately, minimising the impact of con-founding factors wherever possible, and to provide extensive detail in study reports. We recommend that researchers build long-term datasets charting the impacts of prescribed burning on succession. The lack of consistent findings was likely due to high inter-study heterogeneity, and low numbers of comparable studies in each quantitative synthe-sis. We found no consistent effects of moderators, and were unable to test the effect of many potential moderators, due to a lack of reporting. Rather than making any general recommendations on the use of prescribed burning for biodiversity restoration, we provide an evidence atlas of previous studies for researchers and practitioners to use. We observe that outcomes are still difficult to predict, and any restoration project should include a component of moni-toring to build a stronger evidence base for recommendations and guidelines on how to best achieve conservation targets. Prescribed burning may have harmful effects on taxa that are conservation-dependent and careful planning is needed. Keywords:  Fire regime, Disturbance, Forest conservation, Controlled burn, Forest set-aside, Forest reserve, Habitat management, Prescribed burn  Page 3 of 33Eales et al. Environ Evid (2018) 7:19 on native biota [22]. In North America, recognition of the ecological and hazard reduction benefits has been slow, particularly when fire has been publicly viewed as incom-patible with timber production [16]. us, the extent and purpose of prescribed burning varies in this region. As acceptance of prescribed burning grows, there is inter-est in investigating how the amount and distribution of fuel will impact forest structural complexity and the biota associated with this complexity, following fires [22]. Pre- scribed burning for wildlife in southern Europe is far less developed than in other areas of the world, and the envi-ronmental implications remain poorly understood [26]. Across all boreo-temperate regions, it is clear that where prescribed burning is undertaken, it requires engagement with local and regional communities, since the practice typically involves potentially contentious trade-offs [21].Forest burning can impact organisms and habitats directly and/or indirectly via beneficial effects on pyroph-ilous or saproxylic species. In general, the direct effects appear to be clear and quick, with overall positive effects on forest biodiversity [27–29]. e immediate effects of fire on pyrophilous and saproxylic species, and also tree regeneration, are well documented [22]. However, the impact of prescribed burning on other components of biodiversity are less clear and/or consistent. e rela-tive importance of the frequency, extent, and intensity of burns on restoration success also remains undetermined. Identification of review topic A systematic map published in 2015 identified studies on a variety of active management interventions that could be useful for conserving or restoring forest biodiversity in boreal and temperate regions [30]. A total of 812 stud- ies describing a variety of interventions were identified as relevant to the map. Since the map was based on evidence relevant to the Swedish environment, it focused on forest types that are represented in Sweden (i.e. boreal and tem-perate), but such forests exist in many parts of the world (e.g., Russia, northern North America, southern parts of Australia). In accordance with accepted systematic map-ping guidance [31], the map gives an overview of the evidence base by providing a database with descriptions of relevant studies, but it does not synthesise reported results.e map identified four potential subtopic areas that were sufficiently covered by existing studies to be included in a full systematic review. e selection of top-ics was also based on their significance for managers of forest reserves and other stakeholders, and on their rel-evance to Swedish forests. Two of the suggested system-atic reviews are currently in progress (the impact of dead wood on biodiversity [32]; the impacts of grazing on bio-diversity [33]).A third suggested review topic was the effects of pre-scribed burning on the diversity of species other than those directly dependent on fire and dead wood. e direct impacts of fire on tree regeneration, pyrophilous and saproxylic species have been well studied, and one of the systematic reviews in progress is investigating the effect of dead-wood manipulation (e.g. through burning) on biodiversity in forests [32]. Furthermore, one recent systematic review investigated the impact of restora-tion burning on tree regeneration in boreal forests [34]. However, the systematic review described herein focuses on the effects of prescribed burning on other aspects of biodiversity.It would be valuable to broaden knowledge of how pre-scribed burning affects forest biodiversity, particularly because such effects could be viewed as either negative or positive. Additionally, the practice of prescribed burn-ing is now fairly common in temperate and boreal for-ests worldwide, further indicating the need for thorough investigation of its impacts on species other than those that can be considered as pyrophilous or saproxylic. For example, the Life +  Taiga project is a 5-year European Union funded programme (2015–2019) ongoing in Swe-den [35]. e project involves 14 regional County Admin-istrative Boards and aims to perform 120 controlled fires in boreal forests, with the aim of conserving and restor-ing biodiversity.A total of 227 studies in the systematic map of manage-ment interventions in temperate or boreal forests [30] described effects of prescribed burning. Additional stud-ies in the topic area have become available more recently, since the last search for evidence was undertaken by the map authors in 2015. e current literature lacks an up-to-date systematic review assessing the full evidence base on the impact of prescribed burning on biodiversity of temperate and boreal forests worldwide. is review addresses this need by exploring the often-ignored wider impacts of prescribed burning. Stakeholder engagement We established the scope and focus of the review in close cooperation with stakeholders, following the outputs provided by the systematic map [30]. e stakeholders were based primarily in Sweden and included research-ers (e.g. academic researchers from the University of Umeå), practitioners and managers, forestry companies (e.g. Bergvik Skog), local and governmental administra-tion boards (e.g. the Swedish Environmental Protection Agency), and global conservation charities (e.g. World Wildlife Fund). Before submission, peer review, and final publication of the protocol, a draft version was open for public review at the website of the Mistra Council for Evidence-Based Environmental Management (Mistra  Page 4 of 33Eales et al. Environ Evid (2018) 7:19 EviEM) in July 2016. e draft was also sent directly to stakeholders. e draft protocol was revised in response to appropriate comments. Objective of the systematic review e primary aim of this systematic review was to clarify if, and how, the diversity and richness of non-pyrophilous and non-saproxylic species in boreal and temperate for-ests is affected by prescribed burning. We searched not only for studies of interventions in actual forest reserves and other kinds of set-asides, but also for appropriate evi-dence from non-protected and commercially managed forests, since some of the practices applied in commercial forestry may be relevant to conservation or restoration. Quantitative synthesis of selected studies and a narrative synthesis were used to fulfil this aim.e secondary aim of this systematic review was to provide an overview of available evidence on how biodi- versity of boreal and temperate forests (apart from that of pyrophilous and saproxylic species) is affected by pre-scribed burning. A systematic map of the evidence base was used to provide this overview.e ultimate purpose of the review was to investigate whether prescribed burning may be used as a means of conserving or restoring biodiversity in forest set-asides, and if so, what conditions increase its effectiveness. Primary question What is the effect of prescribed burning in temperate and boreal forest on biodiversity, not including pyrophilous and saproxylic species? Components of the question Population: boreal and temperate forests.Intervention: prescribed burning.Comparator: no burning or alternative levels of burn-ing, before burning.Outcomes: diversity and richness of species (excluding pyrophilous and saproxylic species) as one of a number of measures of biodiversity reported in the literature. Methods is review follows the methods outlined in an a priori protocol [36]. It has been conducted according to CEE’s Guidelines for Systematic Reviews [37]. Due to the large  volume of evidence identified that was not suitable for quantitative synthesis we deviate from the protocol in that we added an extra first step before full synthesis: we initially produced a detailed systematic map data-base describing all studies, followed by a quantitative synthesis of all studies that provided sufficient data for meta-analysis. Searches for literature A subset of the evidence base examined in this system-atic review was identified by a systematic map of man-agement interventions in temperate or boreal forests [30]. Searches for the map were performed in May–August 2014, with an update in March 2015. Of the 812 studies included in the map, 227 reported on impacts of prescribed burning and were therefore potentially relevant to this review. However, we also conducted additional searches for evidence, both to find recently published literature and because the searches for the systematic map were focused on forest types occurring in Sweden, whilst we aimed to be more inclusive in this review. Search string e search string for the additional literature searches was based on a subset of the search terms used for the systematic map [30], focusing on terms related to pre-scribed burning. We conducted a scoping exercise in May 2016 to assess alternative search terms, testing them against a set of articles suggested by review team members and known to be relevant. Searches were undertaken in July 2016. Details of the scoping exercise and search string development are provided in the pro-tocol for this review [36].During article screening a small number of additional synonyms were added to the search string and used in a set of supplementary searches in December 2016. e additional population terms were “stand*”, “plantation*”, “wood*”, “tree*”, “clone*”, “tract*” and “savanna*”. e additional intervention terms were “prescri*”, “intro-duce*” and “broadcast”. e additional outcome term was “richness”. e search string was adapted to spe-cific databases using appropriate syntax. Details of the July 2016 and December 2016 strings are given in Addi-tional file 1 together with search dates and the number of articles found. e search string is summarised in Table 1. is string differs from that presented in the protocol due to the supplementary searches conducted in December 2016. Bibliographic databases Searches were conducted in the following online biblio-graphic databases: 1. Web of Science Core Collections (Stockholm Univer-sity Library subscription).2. Scopus (Stockholm University Library subscription).3. CAB abstracts (Oxford University library subscrip-tion).  Page 5 of 33Eales et al. Environ Evid (2018) 7:19 Searches were made using topic words or title, abstract and keywords. No subject category limitations were used. No language or document type restrictions were applied, but searches were performed using Eng-lish search terms only. Search engines An internet search was performed using Google Scholar (schol ar.googl e.com) and a subset of the search terms described above (see Additional file 1 for details). Search results were extracted using the software Publish or Per-ish [38] (up to 1000 results viewable and extractable). Duplicates within sets of search results were removed within EndNote. Citations were then uploaded to the review management software EPPI Reviewer (eppi.ioe.ac.uk/eppireviewer4) and screened together with biblio-graphic database search results. Specialist websites e websites of 28 specialist organisations (listed below) were searched for relevant evidence. ese websites were searched using both the built-in search facilities where available and by hand searching for research studies. e search terms used were based on the search string described in Table 1, adjusted for the searching capa-bilities of each website. e search terms used across all websites are listed in Additional file 1. All potentially rel-evant evidence was recorded. Searches were performed in Danish, English, Finnish, French, Norwegian, and Swedish according to the language of the website (see Additional file 1).  1. Ancient Tree Forum (www.ancie nt-tree-forum .org. uk). 2. Australian Department of Environment and Energy (www.austr alia.gov.au/direc torie s/Austr alia/envir onmen t). 3. Bureau of Land Management, US Dept. of the Inte-rior (www.blm.gov ). 4. Environment Canada (www.ec.gc.ca). 5. European Commission Joint Research Centre (ec.europa.eu/dgs/jrc). 6. European Environment Agency (www.eea.europ a.eu). 7. Food and Agriculture Organization of the United Nations (www.fao.org). 8. Finland’s environmental administration (www. ympar isto.fi). 9. International Union for Conservation of Nature (www.iucn.org). 10. Metsähallitus (www.metsa .fi).  11. Natural Resources Canada (www.nrcan .gc.ca).  12. e Nebraska Prescribed Fire conference (out-doornebraska.gov/prescribedfire). 13. New Zealand Ministry for the Environment (www.mfe.govt.nz). 14. Nordic Council of Ministers (www.norde n.org).  15. Norwegian Environment Agency (www.miljødirek-toratet.no). 16. Norwegian Forest and Landscape Institute (www.skogo gland skap.no).  17. Norwegian Institute for Nature Research (www.nina.no). 18. Parks Canada (www.pc.gc.ca).  19. Society for Ecological Restoration (www.ser.org).  20. Swedish County Administrative Boards (www.lanss  tyrel sen.se). 21. Swedish Environmental Protection Agency (www.natur  vards  verke t.se).  22. Swedish Forest Agency (www.skogs styre lsen.se).  23. Swedish University of Agricultural Sciences (www.slu.se). 24. UK Environment Agency (www.envir onmen t-agenc  y.gov.uk). 25. United Nations Environment Programme (www.unep.org). 26. United States Environmental Protection Agency (www.epa.gov ). 27. United States National Parks Service (www.nps.gov ). 28. US Forest Service (www.fs.fed.us). Table 1 The search string to which the combined database searches are equivalent Search string Population terms(forest* OR woodland* OR “wood* pasture*” OR “wood* meadow*” OR stand* OR plantation* OR wood* OR tree* OR clone* OR tract* OR savanna*)ANDIntervention terms((prescribed OR control* OR experiment* OR prescri* OR introduce* OR broadcast) AND (burn* OR fire))ANDOutcome terms(*diversity OR (species AND (richness OR focal OR target OR keystone OR umbrella OR red-list* OR threatened OR endangered OR rare)) OR “species density” OR “number of species” OR indicator* OR abundance OR “forest structure” OR habitat* OR richness)
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