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Phylogenetic diversity meets conservation policy: small areas are key to preserving eucalypt lineages

Phylogenetic diversity meets conservation policy: small areas are key to preserving eucalypt... Phylogenetic diversity meets conservation policy: small areas are key to preserving rstb.royalsocietypublishing.org eucalypt lineages 1 2 3,4 1 Laura J. Pollock , Dan F. Rosauer , Andrew H. Thornhill , Heini Kujala , 2 4 1 Michael D. Crisp , Joseph T. Miller and Michael A. McCarthy Research School of Botany, The University of Melbourne, Parkville, Victoria, Australia Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia Cite this article: Pollock LJ, Rosauer DF, Australian Tropical Herbarium, James Cook University, Cairns, Queensland, Australia Thornhill AH, Kujala H, Crisp MD, Miller JT, Australian National Herbarium, CSIRO, Plant Industry, Canberra, Australian Capital Territory, Australia McCarthy MA. 2015 Phylogenetic diversity meets conservation policy: small areas are key Evolutionary and genetic knowledge is increasingly being valued in conserva- to preserving eucalypt lineages. Phil. tion theory, but is rarely considered in conservation planning and policy. Here, we integrate phylogenetic diversity (PD) with spatial reserve prioritization to Trans. R. Soc. B 370: 20140007. evaluate how well the existing reserve system in Victoria, Australia captures http://dx.doi.org/10.1098/rstb.2014.0007 the evolutionary lineages of eucalypts, which dominate forest canopies across the state. Forty-three per cent of remaining native woody vegetation One contribution of 17 to a discussion meeting in Victoria is located in protected areas (mostly national parks) representing issue ‘Phylogeny, extinction and conservation’. 48% of the extant PD found in the state. A modest expansion in protected areas of 5% (less than 1% of the state area) would increase protected PD by 33% over current levels. In a recent policy change, portions of the national Subject Areas: parks were opened for development. These tourism development zones environmental science, taxonomy and hold over half the PD found in national parks with some species and clades systematics falling entirely outside of protected zones within the national parks. This approach of using PD in spatial prioritization could be extended to any clade or area that has spatial and phylogenetic data. Our results demonstrate Keywords: the relevance of PD to regional conservation policy by highlighting that small Australia, Eucalyptus, phylogenetic diversity, but strategically located areas disproportionally impact the preservation of reserve selection, species distribution evolutionary lineages. modelling, spatial prioritization Author for correspondence: Laura J. Pollock 1. Introduction e-mail: laurajs@unimelb.edu.au The value of including evolutionary information in conservation has been well established, but evolutionary diversity is rarely considered in policy and manage- ment [1,2]. Using ancestral relationships when selecting species for conservation was suggested more than 20 years ago [3–5]. The essence of the argument is that species should be valued based on their contribution to the tree of life. The evol- utionary contribution of taxa is most commonly measured by phylogenetic diversity (PD) or the length of the shared pathway on a phylogeny represented by a set of taxa [5]. A large body of literature has since developed around several PD related subtopics, and the use of PD has reached fields as diverse as community ecology [6] and bioprospecting [7]. The uptake of PD into applied conservation has lagged behind the literature, but PD-type metrics are now being used to rank global species with the evolutionarily distinct globally endangered (EDGE) list [8] and assigning regional conservation priorities for species [9] and areas [10]. One of the arguments for why PD is not more fully integrated in conserva- tion is that PD is not always a surrogate for other conservation values [1], but conserving PD is a goal in itself if we value biodiversity in conservation [11]. There are many additional benefits of retaining the widest possible portion of the tree of life. Conservation scenarios with PD effectively select medically and economically important plants in the Cape of South Africa [12]. The bio- Electronic supplementary material is available active compounds in current use are so diverse that it would be difficult to at http://dx.doi.org/10.1098/rstb.2014.0007 or via http://rstb.royalsocietypublishing.org. & 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 pinpoint which types will be important in the future [13]. DIVERSITY-PD software [30], greedy algorithms [31] and integer Forexample, in eucalypts, a diversityof potentially useful chem- linear programming [32]. Many of these methods are limited to istry exists beyond the small subset of species and compounds few species or few planning units and do not consider effects currently used in products ranging from cough suppressants across the range of a species (but see Billionnet [33] for a sol- to insecticides [14]. Even in this relatively well-studied and ution that includes dependency in survival probabilities). commercially important plant group, new classes of chemicals More recent work has illustrated how phylogenies can be with potential for therapeutics, including cancer treatment, are used in a comprehensive planning framework. Strecker [10] actively being discovered [15]. Given less than 15% of plant used nodes on the phylogeny as conservation units in a spatial species have been screened for bioactivity [16], many useful prioritization for fishes in the Lower Colorado River Basin in but unknown compounds probably exist. Preserving PD the southwest United States using ZONATION software [34]. increases our ‘option values’ [17]—the likelihood that a species Here, we aim to enable wider use of PD in conservation by is potentially useful in the future does not go extinct [18]. providing a method that links phylogenies, species distribution Conservation funds are often disproportionately allocated models (SDMs) and spatial prioritization software. This to a few charismatic animal groups [19]. Using any diversity method could be used for any group of organisms with a phy- measure would distribute funds across more species, but con- logeny and distribution data and is especially suited to species servation of PD specifically aims to spread funds more evenly that have modelled distributions. Given the recent prolifera- across the tree of life [20]. For example, priorities based on PD tion of SDMs in the literature and their great potential for use differ from priorities based on the species conservation when in conservation and management more generally [35], we species richness and PD hotspots do not have spatial overlap hope this work will encourage uptake of SDMs for the specific [12,21,22]. This difference is more pronounced if phylogenies problem of conserving evolutionary diversity. We assign con- have deep radiation events [23]. servation priority with ZONATION software, which has the The use of well-resolved phylogenies in conservation helps advantage of being a widely used program that can accom- minimize taxonomic bias resulting from changing species con- modate the complexity of typical conservation problems by cepts or geographical differences in naming philosophy or including critical factors such as the cost of conservation, taxonomic effort [24,25]. For example, the same range of mor- species risk status and connectivity between populations phologic and genetic variation may be known from five species across multiple species and large landscapes [36]. in a well-studied region or a single species in less-studied We illustrate how this method can be used to quantify cur- region. Yet, the area with five species would be much more rent conservation status of evolutionary diversity and to favoured in a species-based prioritization than prioritization evaluate changes made to a regional conservation policy using with PD. a case study of 101 species of eucalypts (Corymbia Hill and The cost–benefit calculation of using PD for conservation is Johnson, Angophora Cav. and Eucalyptus L’He´rit, Myrtaceae) changing given the rapid expansion of spatial and phylogenetic in Victoria, Australia. Eucalypts dominate the canopy in nearly data such as Australia’s Virtual Herbarium, and the arrival of every woody vegetation type in Victoria—from shrubs less global databases such as Timetree (www.timetree.org), the than 2 m tall to wet forests of Eucalyptus regnans, the tallest flow- Open Tree of Life (opentreeoflife.org) and the Map of Life ering plant. Victoria has many diverse bioregions [37], but is (www.mappinglife.org). GIS tools and specialty programs also the most cleared state in Australia with rates of habitat such as BIODIVERSE [26] help to visualize patterns of diversity deterioration continuing to exceed protection and restoration. across the landscape. Also, the advent of high throughput Eucalypts in Victoria are an excellent case study not only for next generation sequencing techniques has reduced the cost their ecosystem dominance but also because suitable genetic and time in generating large species-level phylogenies [27]. data are available, and Victoria has exceptional state-level The tools necessary for using PD in conservation are available environmental and plant survey data [38]. or becoming available, but a simple framework for integrating We address three regional conservation questions: PD into a spatial prioritization and a demonstration of how PD (i) how much PD is represented in the current protected might be useful for policy is needed. areas? (ii) how much PD can we gain by expanding the protec- ted areas? and (iii) how might a new tourism development policy in national parks impact protection of eucalypt lineages? 2. Conservation applications with phylogenies Perhaps the largest example to date of integrating phylogenies (a) Delineating and modelling species distributions in species conservation is the EDGE list, which prioritizes Any type of distribution data associated with the tips of a species for conservation by combining evolutionary distinctive- phylogeny can be used in this method. In our example, each ness (ED) with global endangerment (GE) [8]. ED measures the tip of the phylogeny represents one species, and each species contribution of each species to the tree of life [8], so is useful for contains distribution information from SDMs or outlined ranking species for conservation such as in setting priorities for distributions. If SDMs are used, then predicted probabilities of which species should be collected and stored in seed banks [28]. occurrence (from data with known presences and absences) However, the actual geographical distributions of species and can be used directly in the analyses rather than using a threshold their co-occurrence are crucial to conservation decisions. Fur- to transform probabilities to binary presence/absence. If predic- thermore, priorities change as species or areas become tions are from presence-only data (e.g. herbarium records), then protected or threatened, so complementary-PD measures are the output should be scaled based on prevalence if suitable a more efficient way of summarizing marginal gains and prevalence data exist [39]. Many eucalypts have narrow losses in conservation than scoring approaches [29]. ranges that are overestimated with standard SDMs. Our goal There have been many approaches to combining PD and was to develop conservative estimates of species distribu- complementarity to select areas for conservation such as tions (i.e. underestimating unknown populations in favour of rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 more accurately identifying populations that are known to were sourced from the alignment prepared for a larger euca- be present). lypt phylogeny [44]. A Bayesian analysis was performed We used a range of modelling methods depending on the using MRBAYES v. 3.2 compiled on the CSIRO Burnett super- extent and prevalence of each species (see the electronic computer cluster. The Monte Carlo Markov chain was run for supplementary material, appendix S1 for a species list, distri- 40  10 generations and convergence was achieved with a bution type and cross-validated area under the receiver final split frequency value of 0.041825. The final tree was operating characteristic curve (AUC) values). Our decision on exported as a nexus file. Five species with missing molecular the type of model was based on a trade-off between having data were inserted into the nexus phylogeny file at the stem more reliable probabilities of occurrence (which are important node shared with assumed most closely related species as in this case because they are propagated through the phylogeny) in Rosauer et al. [45] with a branch length of zero (see the elec- and missing known populations (by using the smaller, presence– tronic supplementary material, appendix S1). The Victorian absence dataset that allows probabilities to be determined). eucalypt phylogeny is shown in electronic supplementary Common species were modelled using boosted regression trees material, appendix S3. Relationships between major groups (BRTs) [40] with a quadrats dataset from Victoria’s Biodiversity (genera and subgenera) are in agreement with existing Atlas (VBA) accessed October 2013. For range-restricted eucalypt phylogenies [46,47]. species, we added the additional records from VBA and the Australia’s Virtual Herbarium (AVH) and used MAXENT [41] (c) Linking species distribution models to the for modelling. For the AVH dataset, we removed any records outside of the species natural populations and retained only phylogeny post-1950 records, because the older records had high spatial Each cell in a grid has a modelled probability of occurrence uncertainty. However, we may have missed some locations (from SDMs) for each species (figure 1a). Each species is a where the species no longer occurs by eliminating these records. terminal branch of the phylogeny. We calculated the prob- Both datasets were clipped to the state of Victoria with a 100 km ability of occurrence for each internal branch in each cell. buffer to limit edge-effects. The final number of unique An internal branch occurs if any of the descendent species species  site combinations was 9137 AVH records and 89 454 occur in that cell. Thus, VBA records. Numbers of records per species ranged from Y B ¼ 1  (1  P ), (2:1) i,j n,j five to over 7000 in the case of wide-ranging Eucalyptus obliqua. n1 For MAXENT models, we masked out areas beyond the where B is the probability of an internal branch (i) occurring i,j known extent of each species, set a background of the loca- in cell j, m is the number of descendent species downstream tions of all records of all species and filtered records to of this internal branch and P is the probability of descen- n,j exclude duplicate species  locations within 100 m for species dent species n occurring in cell j. with fewer than 200 records and 5 km for species with more Probabilities of occurrences for branch lengths were calcu- than 200 records. We used only hinge features, because they lated in R [48]. Owing to the large size of the raster files provide smoother response curves, and scaled the output to (millions of pixels), calculation of probability layers for match prevalence calculated from the VBA quadrats dataset internal branches was performed directly in raster format [42]. Ten per cent of data was withheld for model testing and using a combination of customized functions and functions the final models were run on the full datasets. The average available within the ‘raster’ package [43]. Attributes of the 10-fold cross-validated AUC value for withheld data across phylogeny were extracted using functions from the ‘ape’ species was 0.96 (ranging from 0.85 to 0.99) for BRTs and package [49]. 0.98 (from 0.97 to 1.0) for MAXENT models. All modelling was done in the R package ‘dismo’ v. 0.8-17 [43] using a set of climatic and edaphic variables described in the electronic (d) Spatial prioritization supplementary material, appendix S2. Distributions were pre- We used ZONATION v. 4.0 for the spatial prioritization. dicted to 225 m grid cells across the state plus buffer zone ZONATION produces a conservation priority of sites (or grid including areas that are not currently native woody vegetation. cells) in a given landscape based on representation of biodi- This provided an estimate of how much of the distribution of versity features (e.g. species or, as in this case, branches), each species may have been lost owing to past clearing. Mod- feature weights and the cost of protecting a site. It starts by elled distributions are based on relatively recent point data, assuming that everything in the landscape is protected and so the amount of distributions lost is probably underestimated, then iteratively removes grid cells with the least conservation but nonetheless provides important information about species benefit (i.e. the least marginal loss) [36]. threat. For additional details on distribution modelling, see the At each step, the remaining proportion of the distribution electronic supplementary material, appendix S2. of each feature is calculated to determine which cell is the Distributions of three species that were isolated to a few least valuable based on principles of complementarity and populations (under 70 records) were delineated in ARCMAP irreplaceability, and hence will be removed next (figure 1b). v. 10.2 based on species descriptions and expert knowledge. Each time ZONATION recalculates the proportion of the distri- Polygons were assigned probabilities based on expert opinion bution of each branch remaining, it uses the probabilities in and/or species descriptions. each cell that were previously calculated according to equation (2.1). This means that even though branches are independent units, the branches remain mathematically (b) Phylogeny linked in the phylogenetic hierarchy at each step. We used We assembled a sequence matrix of 96 species plus outgroup both the basic Core Area Zonation (CAZ), which removes taxa based on four markers, two nuclear ITS, ETS, and two cells based on the maximum value in a cell for any given fea- nuclear matK and the psbA-trnH intergenic spacer. Sequences ture, and the Additive Benefit Function (ABF), which sums rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 (a)(b) 4 1.0 0.8 0.30 h 0.40 c 0.6 0.10 0.61 0.40 0.4 0.77 0.80 f 0.2 0.20 0.84 0 0.2 0.4 0.6 0.8 1.0 proportion of landscape removed Figure 1. Each branch on the phylogeny is considered a conservation ‘unit’ in the spatial prioritization and has an associated raster grid with a probability of occurrence in each cell (illustrated in lower right cell in a). Rasters for tip branches (i.e. species) are estimated with SDMs and rasters for internal branches (dotted lines) are calculated according to equation (2.1). (b) During the prioritization process, as cells are removed from the landscape, the proportion of the original distribution of each branch that is still remaining is recorded (grey solid lines, black dashed line shows the average across all branches). See text for further details on the prioritization process. values in cells [34]. The ABF approach represents total PD 4 481 600 cells) across the state of Victoria with the warp factor slightly better, but, as in other cases, the distribution of indi- (number of cells removed at a time) set at 100 and without vidual biodiversity features (phylogenetic branches in this considering connectivity. Portions of the ranges of species case) were preserved better with CAZ than with ABF [36], and clades that have already been lost to clearing was con- so we present the results of CAZ here. sidered by first ranking the cleared areas (some of which The performance of a ZONATION solution is typically have modelled species ranges), then ranking all areas that are measured by how original distributions of features are currently native woody vegetation (table 1). Including cleared retained by sites that correspond to a specific fraction of the land in the prioritization integrates the proportion of the spatial entire landscape, e.g. the best 10% of total area [36]. Here, distribution of species that have already been cleared. instead of individual branches, we are evaluating spatial prioritizations based on how well they represent total PD. Therefore, we calculated the proportion of PD remaining in 3. Ranking the landscape for phylogenetic the landscape at each step in the cell removal according to diversity "# ! X B 1 i:j j¼1 The most valuable areas for conservation of PD are distributed proportion PD remaining ¼  L  , P P k Q L B throughout the state. Notable regions include the mallee euca- i:j i i¼1 i¼1 j¼1 lypts in Murray-Sunset National Park in the northwest, the (2:2) Grampians National Park in the west, the heavily degraded box-ironbark forests in central Victoria and the East Gippsland where k is branches on the phylogeny, q is the remaining cells of region in the eastern part of the state (figure 2). This map shows native woody vegetation on the landscape, Q is the initial the relative conservation importance of areas across Victoria for number of cells (all cells present), B is the probability of occur- i,j PD, ignoring any existing land tenure. In order to identify next rence of branch i in cell j and L is the length of branch i. With all conservation priorities in a cost-effective manner, one needs to currently existing native woody vegetation represented as cells take into account that some species are already protected by on the landscape, the entirety of each branch is represented and existing reserve network. For example, the northwest part PD is the sum of all branch lengths as in Faith [5]. As grid cells of the state is an important resource for PD, but nearly all of are removed, loss of branches is represented by the proportion the remaining native vegetation is already protected within of the spatial distribution of each branch remaining weighted Murray-Sunset National Park. by branch length. We ran ZONATION for various scenarios (table 1) using mask files which alter the cell removal order to either force in or force out areas from the top priorities, such as existing protected 4. How well is phylogenetic diversity areas or proposed development areas. The impact of existing represented in national parks? and proposed land use types can then be quantified by com- paring the results of an altered solution to an unconstrained Widespread clearing has left less than 40% of Victoria with optimal solution [50]. We use the proportion of PD remaining native woody vegetation. Of that remaining vegetation, 43% (equation (2.2)) to evaluate scenarios of reserve expansion and is protected in nature reserves, most of which are national contraction. We ran the different prioritization scenarios at parks. The current configuration of conservation reserves is the resolution of the modelled distributions (225 m resolution, not optimal—only 48% of the total PD is currently located prop. distribution branches remaining rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 Table 1. List and description of ZONATION runs. (The optimal prioritization can be altered using mask files, which tell the program that some areas have predefined hierarchy, and removes categories of grid cells in specified order.) run mask files description optimal solution none prioritize all of Victoria optimal solution for 0—not native woody vegetation prioritize remaining native woody vegetation in Victoria remaining native woody 1—native woody vegetation vegetation evaluate conservation reserves 0—not native woody vegetation prioritize areas inside and outside conservation reserves to determine 1—native woody vegetation outside how much PD is already protected and how much remains outside current conservation areas the current extent of the reserve systems 2—native woody vegetation inside current conservation areas scenario 1: expand 0—not native woody vegetation compare amount of PD protected in reserves with that protected if conservation reserves 1—native woody vegetation outside the area of conservation reserves was increased by 5 or 20% current conservation areas 2—native woody vegetation inside current conservation areas scenario 2: tourism 0—outside native woody vegetation document the distribution of PD within national parks available for development in 1—native woody vegetation outside tourism and map vulnerable areas national parks national parks 2—native woody vegetation in national parks and open for development 3—native woody vegetation in national parks and protected from development in protected areas compared with 74% protected if reserves and must be a net public benefit, which includes increasing were located optimally following the prioritization in figure 2 public access to park resources [51]. (dashed and solid lines in figure 3a). We refer to areas within national parks as ‘protected zones’ If the protected areas were to be expanded in a cost-effi- and ‘development zones’ depending on whether they are open cient manner by 5% (less than 1% of the area of the state), for tourism development or not. National parks contain 42% of an additional 33% of PD could be protected (totalling 64% the PD of native woody vegetation, over half of which is found of the PD remaining today as native woody vegetation; red in development zones (figure 4). If the development zones in figure 3a). The hypothetical protected area expansion is were re-distributed to avoid as much eucalypt PD as possible, concentrated in central Victoria (figure 3b) and the South nearly twice as much PD could be represented in the protected East Corner Bioregion (electronic supplementary material, zones (33% of the PD rather than the current 18%; figure 4a). figure S4), but there are many smaller locations throughout Transferring even 10% of the area of development zones the state. Various other sizes and configurations of reserve to protected zones would increase the amount of PD that is expansions could be considered. In a less realistic scenario, fully protected to 31% (figure 4a). Many of these valuable we could increase the protected PD of eucalypts by 50% PD resources within development zones (red in figure 4b) with a 21% expansion of protected areas (figure 3b). are located in parks that are easily accessible from the metro- politan city of Melbourne and are, therefore, potentially at high risk of being developed for tourism. Extending the protection zone to the areas in red would help ensure that 5. Evaluating a policy change to the protected important evolutionary diversity is fully protected. area system We can also visualize which branches on the phylogeny National parks are an important repository of eucalypt PD but may be vulnerable to tourism development (figure 5). many areas within national parks are not fully protected For this we consider the entire spatial distribution of each because they are now available for tourism development. In branch, including the portions of the distribution that have 2013, portions of the national park system in Victoria were already been cleared. We calculate the proportion of the dis- made available for tourism development under the ‘Tourism tribution of each branch that is located outside national parks Investment Opportunities of Significance’. Development must and on protected and development zones in national parks. be sensitive to the park values, environmentally sustainable Potentially affected species are clustered on the phylogeny rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 priorities for native woody veg. not native woody veg. bottom 50% 50–75% 75–90% 90–95% top 5% 02550 100 150 200 km Figure 2. Priority ranking for all native woody vegetation in Victoria (inset), Australia. Ranks are the conservation benefit based on the PD of eucalypts not con- sidering land tenure. (a)(b) 1.0 expand protected areas not native woody veg. box-ironbark forests unprotected woody veg. 0.8 expand protected areas 20% expand protected areas 5% protected areas 0.6 0.4 0.2 unprotected protected 0 0.2 0.4 0.6 0.8 1.0 Melbourne proportion of native woody veg. removed 0 10 20 40 60 80 km Figure 3. Hypothetical protected area expansion for Victoria as PD-loss curves (a) and a map showing these priority areas for a subset of the state (b). Loss of PD is represented as the proportion of PD lost as cells of native woody vegetation are removed. Colours represent the protection status of native woody vegetation ( pink, unprotected; green, protected; red, expand protected areas by 5%; and blue, expand by 20%). (a) The dashed black line is the amount of PD that could be retained if all areas of native woody vegetation were available for protection. The solid black line is the amount of PD captured by the actual layout of protected areas (and also shows how much PD could be added with protected area expansion). The y-axis difference between the dashed and solid lines is the difference between the actual amount of PD that is protected and the amount that could be protected by a given proportion of land if protected areas were expanded efficiently. Red blocks are the amount of PD (horizontal block) and land area (vertical block) that could be included in protected areas if they were expanded by 5% of their existing land area. See the electronic supplementary material, appendix S4 for a statewide map. with subgenera Symphyomyrtus being particularly vulnerable portion of their distribution is in the tourism development (figure 5). The distributions of 20 species fall below 1% of zone. The last remaining 1% of the entire red gum clade their original distribution meaning that the last protected (including river red gum, Eucalyptus camaldulensis) is located proportion PD remaining expand PAs rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 subgenus Eucalyptus genera Corymbia/Angophora (a) (b) 7 1.0 national parks scenario outside national park 0.8 national park — tourism development Kamaroka state park national park — top 10% tourism development Greater Bendigo national park national park — protected 0.6 0.4 0.2 Grampians national park outside national park national park Melbourne 0 0.2 0.4 0.6 0.8 1.0 02 12.5 5 50 75 100 proportion of native woody km veg. removed Figure 4. Tourism development in national parks as PD-loss curves (a) and map (b). (a) The dashed line is the optimal solution for all woody native vegetation (as in figure 3a). The thin black line represents PD retained in the optimal configuration of protected zones within national parks. The thick black line is the PD retained when national park tourism development zones ( pink/red blocks) are prioritized first, followed by protected zones in national parks (green block). The top 10% of tourism development zones ranked by PD contribution are shown as red on the graph (a) and the map (b). These development zones could be transferred to protected zones to capture 72% more PD than currently is found in protected zones. The map shows one region north and west of the major metropolitan area, Melbourne, which contains many valuable national park lands open for tourism development (see the electronic supplementary material figure S5 for the statewide map). notable that the entire clade is under-represented with all tourism development scenario branches having less than 1% of their distributions found in Bisectae >5% distribution in protected zone protected zones within national parks (figure 5). Some other Dumaria last 1–5% in development zone Bisectae species are located almost exclusively in tourism development Adnataria last <1% in development zone zones. For example, nearly the entire range of Serra Range gum (Eucalyptus verrucata) is located in a tourism development outside national parks zone. Many more species and the entire Adnataria clade fall below 5% remaining in protected zones (figure 5) Exsertaria red gums It is important to note that the tourism development zones will not be fully developed, and therefore, not all of the PD Maidenaria located in these zones will be threatened or lost. However, one of the requirementsofany developmentis thatithas to be a net public benefit, and increasing visitor access is considered a E. splendens benefit [51], so impact could potentially extend beyond the actual development. This analysis has shown that some areas E. cinerea E. cadens within development zones are particularly important pools of E. yarraensis PD. Development zones contain a number of species and one E. ovata entire clade that are unrepresented in national parks or under- E. diversifolia represented in the protected zones within them. Less than 20% E. verrucata of the PD remaining as native vegetation is located on protected zones within national parks. Small but strategically located expansion of protected zones within national parks could increase protection of species and lineages. C. maculata 6. Other considerations when using phylogenetic Figure 5. Parts of the phylogeny vulnerable from tourism development in diversity in spatial prioritization national parks. Four species are found entirely outside of national parks Phylogenies are hypotheses with uncertaintyarising from many (black branches). Grey bars indicate when greater than 5% of the original sources including the underlying model of evolution, which spatial distribution of a branch is found on protected zones within national may affect conservation predictions based on them [25]. Euca- parks. Branches that are pink and red have 1 – 5% or less than 1% of their lypts are a particularly challenging taxonomic group, which respective distributions in protected zones within national parks. sometimes do not fully confirm to a bifurcating tree in cases of hybridization and introgression [52,53] and parallel evolution in tourism development areas. Many red gums, such as [54]. Fine-scale phylogenetic relationships will be increasingly E. camaldulensis are widespread and, therefore, might not be understood as new molecular technologies emerge [46,55]. impacted by any actions in national parks. However, it is In spatial prioritization with ZONATION, spatial uncertainty can subgenus Symphyomyrtus proportion PD remaining development zone top 10% dev. zone protected zone rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 be directly incorporated into the prioritization [56]. However, evolutionary diversity and areas important for other concerns much of the phylogenetic uncertainly involves the tree topology, may increase the likelihood of PD being considered. The box- and changing the topology changes the conservation features. ironbark forests in central Victoria (Victorian Midlands IBRA One way to account for phylogenetic uncertainty is to run the Bioregion and Goldfields Sub-bioregion) are one good example prioritization multiple times with different estimates of the of a region designated high priority in our analyses and other phylogeny to obtain a distribution around estimates. A similar conservation rankings, such as Trust for Nature spatial priori- type of uncertainty analysis could be done in ZONATION,but is tization [58]. In our analysis, parts of the box-ironbark region beyond the scope of this paper. were ranked highly across all native vegetation, were included Another consideration for any spatial prioritization is the in reserve expansion scenarios, and were in the highest 10% of effect of bounding the study area, because priorities tend to be the national parks areas open for tourism development. Edge- inflated near boundaries that bisect species distributions [57]. effects would have a minimal influence as the box-ironbark Further research is needed to understand boundary effects for region is centrally located. The box-ironbark region is heavily PD specifically. Boundaries might be an issue for PD even if degraded from the 1850s gold rush, logging, agriculture, devel- all species are found entirely within the study area, because opment and aridification from climate change [59]. Eucalypts the range of internal branches might be underestimated if related provide critical habitat for numerous organisms, especially species occur elsewhere. In this case, we suspect inflated priori- nectar-eating birds which depend on year-round flowering ties in the east and northwest, where some branches extend into by different eucalypts [60]. The box-ironbarks should be New South Wales or South Australia. Bounding the study area reinforced as a high priority because, in addition to having at Victoria is justified if the aim of the study is to manage Victor- many threatened species, they also are an important resource ia’s resources, reflecting its separate laws and regulations from for preserving eucalypt evolutionary history. surrounding states, and making use of the state’s independent datasets. Other options would be to weight endemic branches higher than branches that extend beyond the study area. For example, the Corymbia clade, which is rare in Victoria but wide- 8. Conclusion spread elsewhere, could be given a lower priority. One of the Real-world conservation efforts that consider PD are lagging benefits of using ZONATION or a similar software is that any behind interest from the scientific community. Here, we species (or branch) could be weighted for any desirable attribute attempted to facilitate the use of PD in conservation by provid- such as threat categories or functional attributes. However, if ing user-friendly methods and demonstrating how PD can be threat is included, such as International Union of Conservation relevant for conservation decisions. This method links two of Nature threat status, it is important to keep in mind that rapidly expanding data sources—phylogenies and SDMs— ZONATION considers rarity by the proportion of the distribu- with widely used spatial prioritization software. PD can be tion of a species remaining, so weighting by threat status may used in hypothetical or actual protected area scenarios for any over-emphasize listed species in the prioritization. study group that has a phylogeny and distribution data. For eucalypt trees in Victoria, a small 5% expansion to protected areas (less than 1% of the state), could capture 33% more PD. 7. Policy recommendations and conservation Following a recent policy change opening national parks to development, only 11% of PD is fully protected in Victoria, applications with some clades particularly vulnerable. However, small Our analysis suggests that the protected zones within national changes to development zones could greatly improve the out- parks could be modestly extended to include the most valuable look for species and lineages. This framework enables PD to 10% of the tourism development zones for eucalypt diversity in be included with other economic, ecological or sociological Victoria. The expansion of the protected zones would reduce factors that are needed in complex real-world planning. chances that species or even clades are negatively impacted. Given that eucalypts provide the forest habitat for many Acknowledgements. Thanks to Matt White and David Cantrill for provid- species, areas important for eucalypt diversity may also con- ing spatial data, Jane Elith for advice on species distribution models tain high diversity for other organisms, but similar analyses and Michael Bayly for advice on the phylogeny. Thanks to Simon could be done for other groups to determine additional diverse Linke and David Nipperess for discussions about methods. and threatened locations. Funding statement. This research was supported by the Environmental Given the multitude of concerns facing policy-makers and Decisions Hub of the National Environmental Research Program managers, finding overlap between areas that contain valuable and a grant from the Bjarne K. Dahl Trust. 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Phylogenetic diversity meets conservation policy: small areas are key to preserving eucalypt lineages

Philosophical Transactions of the Royal Society B: Biological Sciences , Volume 370 (1662) – Feb 19, 2015

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Abstract

Phylogenetic diversity meets conservation policy: small areas are key to preserving rstb.royalsocietypublishing.org eucalypt lineages 1 2 3,4 1 Laura J. Pollock , Dan F. Rosauer , Andrew H. Thornhill , Heini Kujala , 2 4 1 Michael D. Crisp , Joseph T. Miller and Michael A. McCarthy Research School of Botany, The University of Melbourne, Parkville, Victoria, Australia Research School of Biology, Australian National University, Canberra, Australian Capital Territory, Australia Cite this article: Pollock LJ, Rosauer DF, Australian Tropical Herbarium, James Cook University, Cairns, Queensland, Australia Thornhill AH, Kujala H, Crisp MD, Miller JT, Australian National Herbarium, CSIRO, Plant Industry, Canberra, Australian Capital Territory, Australia McCarthy MA. 2015 Phylogenetic diversity meets conservation policy: small areas are key Evolutionary and genetic knowledge is increasingly being valued in conserva- to preserving eucalypt lineages. Phil. tion theory, but is rarely considered in conservation planning and policy. Here, we integrate phylogenetic diversity (PD) with spatial reserve prioritization to Trans. R. Soc. B 370: 20140007. evaluate how well the existing reserve system in Victoria, Australia captures http://dx.doi.org/10.1098/rstb.2014.0007 the evolutionary lineages of eucalypts, which dominate forest canopies across the state. Forty-three per cent of remaining native woody vegetation One contribution of 17 to a discussion meeting in Victoria is located in protected areas (mostly national parks) representing issue ‘Phylogeny, extinction and conservation’. 48% of the extant PD found in the state. A modest expansion in protected areas of 5% (less than 1% of the state area) would increase protected PD by 33% over current levels. In a recent policy change, portions of the national Subject Areas: parks were opened for development. These tourism development zones environmental science, taxonomy and hold over half the PD found in national parks with some species and clades systematics falling entirely outside of protected zones within the national parks. This approach of using PD in spatial prioritization could be extended to any clade or area that has spatial and phylogenetic data. Our results demonstrate Keywords: the relevance of PD to regional conservation policy by highlighting that small Australia, Eucalyptus, phylogenetic diversity, but strategically located areas disproportionally impact the preservation of reserve selection, species distribution evolutionary lineages. modelling, spatial prioritization Author for correspondence: Laura J. Pollock 1. Introduction e-mail: laurajs@unimelb.edu.au The value of including evolutionary information in conservation has been well established, but evolutionary diversity is rarely considered in policy and manage- ment [1,2]. Using ancestral relationships when selecting species for conservation was suggested more than 20 years ago [3–5]. The essence of the argument is that species should be valued based on their contribution to the tree of life. The evol- utionary contribution of taxa is most commonly measured by phylogenetic diversity (PD) or the length of the shared pathway on a phylogeny represented by a set of taxa [5]. A large body of literature has since developed around several PD related subtopics, and the use of PD has reached fields as diverse as community ecology [6] and bioprospecting [7]. The uptake of PD into applied conservation has lagged behind the literature, but PD-type metrics are now being used to rank global species with the evolutionarily distinct globally endangered (EDGE) list [8] and assigning regional conservation priorities for species [9] and areas [10]. One of the arguments for why PD is not more fully integrated in conserva- tion is that PD is not always a surrogate for other conservation values [1], but conserving PD is a goal in itself if we value biodiversity in conservation [11]. There are many additional benefits of retaining the widest possible portion of the tree of life. Conservation scenarios with PD effectively select medically and economically important plants in the Cape of South Africa [12]. The bio- Electronic supplementary material is available active compounds in current use are so diverse that it would be difficult to at http://dx.doi.org/10.1098/rstb.2014.0007 or via http://rstb.royalsocietypublishing.org. & 2015 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 pinpoint which types will be important in the future [13]. DIVERSITY-PD software [30], greedy algorithms [31] and integer Forexample, in eucalypts, a diversityof potentially useful chem- linear programming [32]. Many of these methods are limited to istry exists beyond the small subset of species and compounds few species or few planning units and do not consider effects currently used in products ranging from cough suppressants across the range of a species (but see Billionnet [33] for a sol- to insecticides [14]. Even in this relatively well-studied and ution that includes dependency in survival probabilities). commercially important plant group, new classes of chemicals More recent work has illustrated how phylogenies can be with potential for therapeutics, including cancer treatment, are used in a comprehensive planning framework. Strecker [10] actively being discovered [15]. Given less than 15% of plant used nodes on the phylogeny as conservation units in a spatial species have been screened for bioactivity [16], many useful prioritization for fishes in the Lower Colorado River Basin in but unknown compounds probably exist. Preserving PD the southwest United States using ZONATION software [34]. increases our ‘option values’ [17]—the likelihood that a species Here, we aim to enable wider use of PD in conservation by is potentially useful in the future does not go extinct [18]. providing a method that links phylogenies, species distribution Conservation funds are often disproportionately allocated models (SDMs) and spatial prioritization software. This to a few charismatic animal groups [19]. Using any diversity method could be used for any group of organisms with a phy- measure would distribute funds across more species, but con- logeny and distribution data and is especially suited to species servation of PD specifically aims to spread funds more evenly that have modelled distributions. Given the recent prolifera- across the tree of life [20]. For example, priorities based on PD tion of SDMs in the literature and their great potential for use differ from priorities based on the species conservation when in conservation and management more generally [35], we species richness and PD hotspots do not have spatial overlap hope this work will encourage uptake of SDMs for the specific [12,21,22]. This difference is more pronounced if phylogenies problem of conserving evolutionary diversity. We assign con- have deep radiation events [23]. servation priority with ZONATION software, which has the The use of well-resolved phylogenies in conservation helps advantage of being a widely used program that can accom- minimize taxonomic bias resulting from changing species con- modate the complexity of typical conservation problems by cepts or geographical differences in naming philosophy or including critical factors such as the cost of conservation, taxonomic effort [24,25]. For example, the same range of mor- species risk status and connectivity between populations phologic and genetic variation may be known from five species across multiple species and large landscapes [36]. in a well-studied region or a single species in less-studied We illustrate how this method can be used to quantify cur- region. Yet, the area with five species would be much more rent conservation status of evolutionary diversity and to favoured in a species-based prioritization than prioritization evaluate changes made to a regional conservation policy using with PD. a case study of 101 species of eucalypts (Corymbia Hill and The cost–benefit calculation of using PD for conservation is Johnson, Angophora Cav. and Eucalyptus L’He´rit, Myrtaceae) changing given the rapid expansion of spatial and phylogenetic in Victoria, Australia. Eucalypts dominate the canopy in nearly data such as Australia’s Virtual Herbarium, and the arrival of every woody vegetation type in Victoria—from shrubs less global databases such as Timetree (www.timetree.org), the than 2 m tall to wet forests of Eucalyptus regnans, the tallest flow- Open Tree of Life (opentreeoflife.org) and the Map of Life ering plant. Victoria has many diverse bioregions [37], but is (www.mappinglife.org). GIS tools and specialty programs also the most cleared state in Australia with rates of habitat such as BIODIVERSE [26] help to visualize patterns of diversity deterioration continuing to exceed protection and restoration. across the landscape. Also, the advent of high throughput Eucalypts in Victoria are an excellent case study not only for next generation sequencing techniques has reduced the cost their ecosystem dominance but also because suitable genetic and time in generating large species-level phylogenies [27]. data are available, and Victoria has exceptional state-level The tools necessary for using PD in conservation are available environmental and plant survey data [38]. or becoming available, but a simple framework for integrating We address three regional conservation questions: PD into a spatial prioritization and a demonstration of how PD (i) how much PD is represented in the current protected might be useful for policy is needed. areas? (ii) how much PD can we gain by expanding the protec- ted areas? and (iii) how might a new tourism development policy in national parks impact protection of eucalypt lineages? 2. Conservation applications with phylogenies Perhaps the largest example to date of integrating phylogenies (a) Delineating and modelling species distributions in species conservation is the EDGE list, which prioritizes Any type of distribution data associated with the tips of a species for conservation by combining evolutionary distinctive- phylogeny can be used in this method. In our example, each ness (ED) with global endangerment (GE) [8]. ED measures the tip of the phylogeny represents one species, and each species contribution of each species to the tree of life [8], so is useful for contains distribution information from SDMs or outlined ranking species for conservation such as in setting priorities for distributions. If SDMs are used, then predicted probabilities of which species should be collected and stored in seed banks [28]. occurrence (from data with known presences and absences) However, the actual geographical distributions of species and can be used directly in the analyses rather than using a threshold their co-occurrence are crucial to conservation decisions. Fur- to transform probabilities to binary presence/absence. If predic- thermore, priorities change as species or areas become tions are from presence-only data (e.g. herbarium records), then protected or threatened, so complementary-PD measures are the output should be scaled based on prevalence if suitable a more efficient way of summarizing marginal gains and prevalence data exist [39]. Many eucalypts have narrow losses in conservation than scoring approaches [29]. ranges that are overestimated with standard SDMs. Our goal There have been many approaches to combining PD and was to develop conservative estimates of species distribu- complementarity to select areas for conservation such as tions (i.e. underestimating unknown populations in favour of rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 more accurately identifying populations that are known to were sourced from the alignment prepared for a larger euca- be present). lypt phylogeny [44]. A Bayesian analysis was performed We used a range of modelling methods depending on the using MRBAYES v. 3.2 compiled on the CSIRO Burnett super- extent and prevalence of each species (see the electronic computer cluster. The Monte Carlo Markov chain was run for supplementary material, appendix S1 for a species list, distri- 40  10 generations and convergence was achieved with a bution type and cross-validated area under the receiver final split frequency value of 0.041825. The final tree was operating characteristic curve (AUC) values). Our decision on exported as a nexus file. Five species with missing molecular the type of model was based on a trade-off between having data were inserted into the nexus phylogeny file at the stem more reliable probabilities of occurrence (which are important node shared with assumed most closely related species as in this case because they are propagated through the phylogeny) in Rosauer et al. [45] with a branch length of zero (see the elec- and missing known populations (by using the smaller, presence– tronic supplementary material, appendix S1). The Victorian absence dataset that allows probabilities to be determined). eucalypt phylogeny is shown in electronic supplementary Common species were modelled using boosted regression trees material, appendix S3. Relationships between major groups (BRTs) [40] with a quadrats dataset from Victoria’s Biodiversity (genera and subgenera) are in agreement with existing Atlas (VBA) accessed October 2013. For range-restricted eucalypt phylogenies [46,47]. species, we added the additional records from VBA and the Australia’s Virtual Herbarium (AVH) and used MAXENT [41] (c) Linking species distribution models to the for modelling. For the AVH dataset, we removed any records outside of the species natural populations and retained only phylogeny post-1950 records, because the older records had high spatial Each cell in a grid has a modelled probability of occurrence uncertainty. However, we may have missed some locations (from SDMs) for each species (figure 1a). Each species is a where the species no longer occurs by eliminating these records. terminal branch of the phylogeny. We calculated the prob- Both datasets were clipped to the state of Victoria with a 100 km ability of occurrence for each internal branch in each cell. buffer to limit edge-effects. The final number of unique An internal branch occurs if any of the descendent species species  site combinations was 9137 AVH records and 89 454 occur in that cell. Thus, VBA records. Numbers of records per species ranged from Y B ¼ 1  (1  P ), (2:1) i,j n,j five to over 7000 in the case of wide-ranging Eucalyptus obliqua. n1 For MAXENT models, we masked out areas beyond the where B is the probability of an internal branch (i) occurring i,j known extent of each species, set a background of the loca- in cell j, m is the number of descendent species downstream tions of all records of all species and filtered records to of this internal branch and P is the probability of descen- n,j exclude duplicate species  locations within 100 m for species dent species n occurring in cell j. with fewer than 200 records and 5 km for species with more Probabilities of occurrences for branch lengths were calcu- than 200 records. We used only hinge features, because they lated in R [48]. Owing to the large size of the raster files provide smoother response curves, and scaled the output to (millions of pixels), calculation of probability layers for match prevalence calculated from the VBA quadrats dataset internal branches was performed directly in raster format [42]. Ten per cent of data was withheld for model testing and using a combination of customized functions and functions the final models were run on the full datasets. The average available within the ‘raster’ package [43]. Attributes of the 10-fold cross-validated AUC value for withheld data across phylogeny were extracted using functions from the ‘ape’ species was 0.96 (ranging from 0.85 to 0.99) for BRTs and package [49]. 0.98 (from 0.97 to 1.0) for MAXENT models. All modelling was done in the R package ‘dismo’ v. 0.8-17 [43] using a set of climatic and edaphic variables described in the electronic (d) Spatial prioritization supplementary material, appendix S2. Distributions were pre- We used ZONATION v. 4.0 for the spatial prioritization. dicted to 225 m grid cells across the state plus buffer zone ZONATION produces a conservation priority of sites (or grid including areas that are not currently native woody vegetation. cells) in a given landscape based on representation of biodi- This provided an estimate of how much of the distribution of versity features (e.g. species or, as in this case, branches), each species may have been lost owing to past clearing. Mod- feature weights and the cost of protecting a site. It starts by elled distributions are based on relatively recent point data, assuming that everything in the landscape is protected and so the amount of distributions lost is probably underestimated, then iteratively removes grid cells with the least conservation but nonetheless provides important information about species benefit (i.e. the least marginal loss) [36]. threat. For additional details on distribution modelling, see the At each step, the remaining proportion of the distribution electronic supplementary material, appendix S2. of each feature is calculated to determine which cell is the Distributions of three species that were isolated to a few least valuable based on principles of complementarity and populations (under 70 records) were delineated in ARCMAP irreplaceability, and hence will be removed next (figure 1b). v. 10.2 based on species descriptions and expert knowledge. Each time ZONATION recalculates the proportion of the distri- Polygons were assigned probabilities based on expert opinion bution of each branch remaining, it uses the probabilities in and/or species descriptions. each cell that were previously calculated according to equation (2.1). This means that even though branches are independent units, the branches remain mathematically (b) Phylogeny linked in the phylogenetic hierarchy at each step. We used We assembled a sequence matrix of 96 species plus outgroup both the basic Core Area Zonation (CAZ), which removes taxa based on four markers, two nuclear ITS, ETS, and two cells based on the maximum value in a cell for any given fea- nuclear matK and the psbA-trnH intergenic spacer. Sequences ture, and the Additive Benefit Function (ABF), which sums rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 (a)(b) 4 1.0 0.8 0.30 h 0.40 c 0.6 0.10 0.61 0.40 0.4 0.77 0.80 f 0.2 0.20 0.84 0 0.2 0.4 0.6 0.8 1.0 proportion of landscape removed Figure 1. Each branch on the phylogeny is considered a conservation ‘unit’ in the spatial prioritization and has an associated raster grid with a probability of occurrence in each cell (illustrated in lower right cell in a). Rasters for tip branches (i.e. species) are estimated with SDMs and rasters for internal branches (dotted lines) are calculated according to equation (2.1). (b) During the prioritization process, as cells are removed from the landscape, the proportion of the original distribution of each branch that is still remaining is recorded (grey solid lines, black dashed line shows the average across all branches). See text for further details on the prioritization process. values in cells [34]. The ABF approach represents total PD 4 481 600 cells) across the state of Victoria with the warp factor slightly better, but, as in other cases, the distribution of indi- (number of cells removed at a time) set at 100 and without vidual biodiversity features (phylogenetic branches in this considering connectivity. Portions of the ranges of species case) were preserved better with CAZ than with ABF [36], and clades that have already been lost to clearing was con- so we present the results of CAZ here. sidered by first ranking the cleared areas (some of which The performance of a ZONATION solution is typically have modelled species ranges), then ranking all areas that are measured by how original distributions of features are currently native woody vegetation (table 1). Including cleared retained by sites that correspond to a specific fraction of the land in the prioritization integrates the proportion of the spatial entire landscape, e.g. the best 10% of total area [36]. Here, distribution of species that have already been cleared. instead of individual branches, we are evaluating spatial prioritizations based on how well they represent total PD. Therefore, we calculated the proportion of PD remaining in 3. Ranking the landscape for phylogenetic the landscape at each step in the cell removal according to diversity "# ! X B 1 i:j j¼1 The most valuable areas for conservation of PD are distributed proportion PD remaining ¼  L  , P P k Q L B throughout the state. Notable regions include the mallee euca- i:j i i¼1 i¼1 j¼1 lypts in Murray-Sunset National Park in the northwest, the (2:2) Grampians National Park in the west, the heavily degraded box-ironbark forests in central Victoria and the East Gippsland where k is branches on the phylogeny, q is the remaining cells of region in the eastern part of the state (figure 2). This map shows native woody vegetation on the landscape, Q is the initial the relative conservation importance of areas across Victoria for number of cells (all cells present), B is the probability of occur- i,j PD, ignoring any existing land tenure. In order to identify next rence of branch i in cell j and L is the length of branch i. With all conservation priorities in a cost-effective manner, one needs to currently existing native woody vegetation represented as cells take into account that some species are already protected by on the landscape, the entirety of each branch is represented and existing reserve network. For example, the northwest part PD is the sum of all branch lengths as in Faith [5]. As grid cells of the state is an important resource for PD, but nearly all of are removed, loss of branches is represented by the proportion the remaining native vegetation is already protected within of the spatial distribution of each branch remaining weighted Murray-Sunset National Park. by branch length. We ran ZONATION for various scenarios (table 1) using mask files which alter the cell removal order to either force in or force out areas from the top priorities, such as existing protected 4. How well is phylogenetic diversity areas or proposed development areas. The impact of existing represented in national parks? and proposed land use types can then be quantified by com- paring the results of an altered solution to an unconstrained Widespread clearing has left less than 40% of Victoria with optimal solution [50]. We use the proportion of PD remaining native woody vegetation. Of that remaining vegetation, 43% (equation (2.2)) to evaluate scenarios of reserve expansion and is protected in nature reserves, most of which are national contraction. We ran the different prioritization scenarios at parks. The current configuration of conservation reserves is the resolution of the modelled distributions (225 m resolution, not optimal—only 48% of the total PD is currently located prop. distribution branches remaining rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 Table 1. List and description of ZONATION runs. (The optimal prioritization can be altered using mask files, which tell the program that some areas have predefined hierarchy, and removes categories of grid cells in specified order.) run mask files description optimal solution none prioritize all of Victoria optimal solution for 0—not native woody vegetation prioritize remaining native woody vegetation in Victoria remaining native woody 1—native woody vegetation vegetation evaluate conservation reserves 0—not native woody vegetation prioritize areas inside and outside conservation reserves to determine 1—native woody vegetation outside how much PD is already protected and how much remains outside current conservation areas the current extent of the reserve systems 2—native woody vegetation inside current conservation areas scenario 1: expand 0—not native woody vegetation compare amount of PD protected in reserves with that protected if conservation reserves 1—native woody vegetation outside the area of conservation reserves was increased by 5 or 20% current conservation areas 2—native woody vegetation inside current conservation areas scenario 2: tourism 0—outside native woody vegetation document the distribution of PD within national parks available for development in 1—native woody vegetation outside tourism and map vulnerable areas national parks national parks 2—native woody vegetation in national parks and open for development 3—native woody vegetation in national parks and protected from development in protected areas compared with 74% protected if reserves and must be a net public benefit, which includes increasing were located optimally following the prioritization in figure 2 public access to park resources [51]. (dashed and solid lines in figure 3a). We refer to areas within national parks as ‘protected zones’ If the protected areas were to be expanded in a cost-effi- and ‘development zones’ depending on whether they are open cient manner by 5% (less than 1% of the area of the state), for tourism development or not. National parks contain 42% of an additional 33% of PD could be protected (totalling 64% the PD of native woody vegetation, over half of which is found of the PD remaining today as native woody vegetation; red in development zones (figure 4). If the development zones in figure 3a). The hypothetical protected area expansion is were re-distributed to avoid as much eucalypt PD as possible, concentrated in central Victoria (figure 3b) and the South nearly twice as much PD could be represented in the protected East Corner Bioregion (electronic supplementary material, zones (33% of the PD rather than the current 18%; figure 4a). figure S4), but there are many smaller locations throughout Transferring even 10% of the area of development zones the state. Various other sizes and configurations of reserve to protected zones would increase the amount of PD that is expansions could be considered. In a less realistic scenario, fully protected to 31% (figure 4a). Many of these valuable we could increase the protected PD of eucalypts by 50% PD resources within development zones (red in figure 4b) with a 21% expansion of protected areas (figure 3b). are located in parks that are easily accessible from the metro- politan city of Melbourne and are, therefore, potentially at high risk of being developed for tourism. Extending the protection zone to the areas in red would help ensure that 5. Evaluating a policy change to the protected important evolutionary diversity is fully protected. area system We can also visualize which branches on the phylogeny National parks are an important repository of eucalypt PD but may be vulnerable to tourism development (figure 5). many areas within national parks are not fully protected For this we consider the entire spatial distribution of each because they are now available for tourism development. In branch, including the portions of the distribution that have 2013, portions of the national park system in Victoria were already been cleared. We calculate the proportion of the dis- made available for tourism development under the ‘Tourism tribution of each branch that is located outside national parks Investment Opportunities of Significance’. Development must and on protected and development zones in national parks. be sensitive to the park values, environmentally sustainable Potentially affected species are clustered on the phylogeny rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 priorities for native woody veg. not native woody veg. bottom 50% 50–75% 75–90% 90–95% top 5% 02550 100 150 200 km Figure 2. Priority ranking for all native woody vegetation in Victoria (inset), Australia. Ranks are the conservation benefit based on the PD of eucalypts not con- sidering land tenure. (a)(b) 1.0 expand protected areas not native woody veg. box-ironbark forests unprotected woody veg. 0.8 expand protected areas 20% expand protected areas 5% protected areas 0.6 0.4 0.2 unprotected protected 0 0.2 0.4 0.6 0.8 1.0 Melbourne proportion of native woody veg. removed 0 10 20 40 60 80 km Figure 3. Hypothetical protected area expansion for Victoria as PD-loss curves (a) and a map showing these priority areas for a subset of the state (b). Loss of PD is represented as the proportion of PD lost as cells of native woody vegetation are removed. Colours represent the protection status of native woody vegetation ( pink, unprotected; green, protected; red, expand protected areas by 5%; and blue, expand by 20%). (a) The dashed black line is the amount of PD that could be retained if all areas of native woody vegetation were available for protection. The solid black line is the amount of PD captured by the actual layout of protected areas (and also shows how much PD could be added with protected area expansion). The y-axis difference between the dashed and solid lines is the difference between the actual amount of PD that is protected and the amount that could be protected by a given proportion of land if protected areas were expanded efficiently. Red blocks are the amount of PD (horizontal block) and land area (vertical block) that could be included in protected areas if they were expanded by 5% of their existing land area. See the electronic supplementary material, appendix S4 for a statewide map. with subgenera Symphyomyrtus being particularly vulnerable portion of their distribution is in the tourism development (figure 5). The distributions of 20 species fall below 1% of zone. The last remaining 1% of the entire red gum clade their original distribution meaning that the last protected (including river red gum, Eucalyptus camaldulensis) is located proportion PD remaining expand PAs rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 subgenus Eucalyptus genera Corymbia/Angophora (a) (b) 7 1.0 national parks scenario outside national park 0.8 national park — tourism development Kamaroka state park national park — top 10% tourism development Greater Bendigo national park national park — protected 0.6 0.4 0.2 Grampians national park outside national park national park Melbourne 0 0.2 0.4 0.6 0.8 1.0 02 12.5 5 50 75 100 proportion of native woody km veg. removed Figure 4. Tourism development in national parks as PD-loss curves (a) and map (b). (a) The dashed line is the optimal solution for all woody native vegetation (as in figure 3a). The thin black line represents PD retained in the optimal configuration of protected zones within national parks. The thick black line is the PD retained when national park tourism development zones ( pink/red blocks) are prioritized first, followed by protected zones in national parks (green block). The top 10% of tourism development zones ranked by PD contribution are shown as red on the graph (a) and the map (b). These development zones could be transferred to protected zones to capture 72% more PD than currently is found in protected zones. The map shows one region north and west of the major metropolitan area, Melbourne, which contains many valuable national park lands open for tourism development (see the electronic supplementary material figure S5 for the statewide map). notable that the entire clade is under-represented with all tourism development scenario branches having less than 1% of their distributions found in Bisectae >5% distribution in protected zone protected zones within national parks (figure 5). Some other Dumaria last 1–5% in development zone Bisectae species are located almost exclusively in tourism development Adnataria last <1% in development zone zones. For example, nearly the entire range of Serra Range gum (Eucalyptus verrucata) is located in a tourism development outside national parks zone. Many more species and the entire Adnataria clade fall below 5% remaining in protected zones (figure 5) Exsertaria red gums It is important to note that the tourism development zones will not be fully developed, and therefore, not all of the PD Maidenaria located in these zones will be threatened or lost. However, one of the requirementsofany developmentis thatithas to be a net public benefit, and increasing visitor access is considered a E. splendens benefit [51], so impact could potentially extend beyond the actual development. This analysis has shown that some areas E. cinerea E. cadens within development zones are particularly important pools of E. yarraensis PD. Development zones contain a number of species and one E. ovata entire clade that are unrepresented in national parks or under- E. diversifolia represented in the protected zones within them. Less than 20% E. verrucata of the PD remaining as native vegetation is located on protected zones within national parks. Small but strategically located expansion of protected zones within national parks could increase protection of species and lineages. C. maculata 6. Other considerations when using phylogenetic Figure 5. Parts of the phylogeny vulnerable from tourism development in diversity in spatial prioritization national parks. Four species are found entirely outside of national parks Phylogenies are hypotheses with uncertaintyarising from many (black branches). Grey bars indicate when greater than 5% of the original sources including the underlying model of evolution, which spatial distribution of a branch is found on protected zones within national may affect conservation predictions based on them [25]. Euca- parks. Branches that are pink and red have 1 – 5% or less than 1% of their lypts are a particularly challenging taxonomic group, which respective distributions in protected zones within national parks. sometimes do not fully confirm to a bifurcating tree in cases of hybridization and introgression [52,53] and parallel evolution in tourism development areas. Many red gums, such as [54]. Fine-scale phylogenetic relationships will be increasingly E. camaldulensis are widespread and, therefore, might not be understood as new molecular technologies emerge [46,55]. impacted by any actions in national parks. However, it is In spatial prioritization with ZONATION, spatial uncertainty can subgenus Symphyomyrtus proportion PD remaining development zone top 10% dev. zone protected zone rstb.royalsocietypublishing.org Phil. Trans. R. Soc. B 370: 20140007 be directly incorporated into the prioritization [56]. However, evolutionary diversity and areas important for other concerns much of the phylogenetic uncertainly involves the tree topology, may increase the likelihood of PD being considered. The box- and changing the topology changes the conservation features. ironbark forests in central Victoria (Victorian Midlands IBRA One way to account for phylogenetic uncertainty is to run the Bioregion and Goldfields Sub-bioregion) are one good example prioritization multiple times with different estimates of the of a region designated high priority in our analyses and other phylogeny to obtain a distribution around estimates. A similar conservation rankings, such as Trust for Nature spatial priori- type of uncertainty analysis could be done in ZONATION,but is tization [58]. In our analysis, parts of the box-ironbark region beyond the scope of this paper. were ranked highly across all native vegetation, were included Another consideration for any spatial prioritization is the in reserve expansion scenarios, and were in the highest 10% of effect of bounding the study area, because priorities tend to be the national parks areas open for tourism development. Edge- inflated near boundaries that bisect species distributions [57]. effects would have a minimal influence as the box-ironbark Further research is needed to understand boundary effects for region is centrally located. The box-ironbark region is heavily PD specifically. Boundaries might be an issue for PD even if degraded from the 1850s gold rush, logging, agriculture, devel- all species are found entirely within the study area, because opment and aridification from climate change [59]. Eucalypts the range of internal branches might be underestimated if related provide critical habitat for numerous organisms, especially species occur elsewhere. In this case, we suspect inflated priori- nectar-eating birds which depend on year-round flowering ties in the east and northwest, where some branches extend into by different eucalypts [60]. The box-ironbarks should be New South Wales or South Australia. Bounding the study area reinforced as a high priority because, in addition to having at Victoria is justified if the aim of the study is to manage Victor- many threatened species, they also are an important resource ia’s resources, reflecting its separate laws and regulations from for preserving eucalypt evolutionary history. surrounding states, and making use of the state’s independent datasets. Other options would be to weight endemic branches higher than branches that extend beyond the study area. For example, the Corymbia clade, which is rare in Victoria but wide- 8. Conclusion spread elsewhere, could be given a lower priority. One of the Real-world conservation efforts that consider PD are lagging benefits of using ZONATION or a similar software is that any behind interest from the scientific community. Here, we species (or branch) could be weighted for any desirable attribute attempted to facilitate the use of PD in conservation by provid- such as threat categories or functional attributes. However, if ing user-friendly methods and demonstrating how PD can be threat is included, such as International Union of Conservation relevant for conservation decisions. This method links two of Nature threat status, it is important to keep in mind that rapidly expanding data sources—phylogenies and SDMs— ZONATION considers rarity by the proportion of the distribu- with widely used spatial prioritization software. PD can be tion of a species remaining, so weighting by threat status may used in hypothetical or actual protected area scenarios for any over-emphasize listed species in the prioritization. study group that has a phylogeny and distribution data. For eucalypt trees in Victoria, a small 5% expansion to protected areas (less than 1% of the state), could capture 33% more PD. 7. Policy recommendations and conservation Following a recent policy change opening national parks to development, only 11% of PD is fully protected in Victoria, applications with some clades particularly vulnerable. However, small Our analysis suggests that the protected zones within national changes to development zones could greatly improve the out- parks could be modestly extended to include the most valuable look for species and lineages. This framework enables PD to 10% of the tourism development zones for eucalypt diversity in be included with other economic, ecological or sociological Victoria. The expansion of the protected zones would reduce factors that are needed in complex real-world planning. chances that species or even clades are negatively impacted. Given that eucalypts provide the forest habitat for many Acknowledgements. Thanks to Matt White and David Cantrill for provid- species, areas important for eucalypt diversity may also con- ing spatial data, Jane Elith for advice on species distribution models tain high diversity for other organisms, but similar analyses and Michael Bayly for advice on the phylogeny. Thanks to Simon could be done for other groups to determine additional diverse Linke and David Nipperess for discussions about methods. and threatened locations. Funding statement. This research was supported by the Environmental Given the multitude of concerns facing policy-makers and Decisions Hub of the National Environmental Research Program managers, finding overlap between areas that contain valuable and a grant from the Bjarne K. Dahl Trust. 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Philosophical Transactions of the Royal Society B: Biological SciencesPubmed Central

Published: Feb 19, 2015

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