Identifying global conservation priorities for terrestrial vertebrates based on multiple dimensions of biodiversity

The Kunming–Montreal Global Biodiversity Framework of the Convention on Biological Diversity calls for an expansion of the current protected areas (PAs) to cover at least 30% of global land and water areas by 2030 (i.e., the 30×30 target). Efficient spatial planning for PA expansion is an urgent need for global conservation practice. A spatial prioritization framework considering multiple dimensions of biodiversity is critical for improving the efficiency of the spatial planning of PAs, yet it remains a challenge. We developed an index for the identification of priority areas based on functionally rare, evolutionarily distinct, and globally endangered species (FREDGE) and applied it to 21,536 terrestrial vertebrates. We determined species distributions, conservation status (global endangerment), molecular phylogenies (evolutionary distinctiveness), and life‐history traits (functional rarity). Madagascar, Central America, and the Andes were of high priority for the conservation of multiple dimensions of terrestrial vertebrate biodiversity. However, 68.8% of grid cells in these priority areas had <17% of their area covered by PAs, and these priority areas were under intense anthropogenic and climate change threats. These results highlight the difficulties of conserving multiple dimensions of biodiversity. Our global analyses of the geographical patterns of multiple dimensions of terrestrial vertebrate biodiversity demonstrate the insufficiency of the conservation of different biodiversity dimensions, and our index, based on multiple dimensions of biodiversity, provides a useful tool for guiding future spatial prioritization of PA expansion to achieve the 30×30 target under serious pressures.


INTRODUCTION
Global biodiversity is being lost rapidly due to severe effects of climate change, habitat destruction, and overexploitation (Dirzo et al., 2014;Maxwell et al., 2016;Newbold et al., 2015;Scheffers et al., 2016).Some suggest Earth is undergoing its sixth mass extinction (Barnosky et al., 2011;Ceballos et al., 2015).Therefore, protection of global biodiversity is urgent.Protected areas (PAs), covering over 15.7% of global lands (UNEP-WCMC, 2021), are the most important means for global biodiversity conservation (Coetzee et al., 2014;Gray et al., 2016).Although the number and coverage of global PAs are increasing, biodiversity loss and ecosystem destruction have not been halted (Butchart et al., 2010;Cowie et al., 2022).In 2022, the COP15 conference announced the Kunming-Montreal Global Biodiversity Framework, which proposes that at least 30% of Earth's surface should be conserved in PAs by 2030 (i.e., 30×30 target) (CBD, 2022).Currently, identifying which areas should be prioritized for future expansion of PAs is one of the most important challenges for global biodiversity conservation.Previous studies on the spatial prioritization of biodiversity conservation have mostly been based on the taxonomic dimension of biodiversity (especially species richness [SR]) (Brooks et al., 2006;Eken et al., 2004;Myers et al., 2000).Although researchers have used strategies, such as quantitative methods and biodiversity monitoring, to better represent the taxonomic dimension of biodiversity in spatial prioritization (Moilanen et al., 2005;Pereira & Cooper, 2006), most of the existing PAs were established to preserve flagship species (Smith et al., 2012;Walpole & Leader-Williams, 2002) or areas with high SR (Rodrigues et al., 2004).However, phylogenetic and functional attributes of species play an important role in maintaining the function and stability of ecosystems (Cadotte et al., 2011;Gagic et al., 2015).Conservation strategies focused only on taxonomic diversity may overlook the degradation of ecosystem function induced by the loss of phylogenetic and functional dimensions of biodiversity (Flynn et al., 2011).
In recent years, an increasing number of studies have been published that explore the implications of taxonomic, phylogenetic, and functional diversity in conservation planning (Fritz & Rahbek, 2012;Huang et al., 2012;Mazel et al., 2014;Stuart-Smith et al., 2013) and show the great potential of increased PA coverage to enhance biodiversity conservation by combining these 3 dimensions of biodiversity (Pollock et al., 2017).However, taxonomic, phylogenetic, and functional diversity are spatially inconsistent (Brum et al., 2017;Pollock et al., 2017), which creates difficult trade-offs in the identification of priority conservation areas.For example, Brum et al. (2017) compared the priority areas identified by different biodiversity dimensions for terrestrial mammals (i.e., taxonomic, phylogenetic, and functional diversity) and found substantial mismatches between the priority areas of different biodiversity dimensions.Therefore, it is of great importance to consider different dimensions of biodiversity together rather than separately in the identification of priority conservation areas.
In an early study, Isaac et al. (2007) proposed an index to consider both taxonomic and phylogenetic dimensions of biodiversity in the spatial prioritization of conservation areas (i.e., evolutionarily distinct and globally endangered species [EDGE]).This index provides a tool for selecting priority areas (Tucker et al., 2017;Winter et al., 2013) and has been used in recent conservation planning studies (Daru et al., 2019;Gumbs et al., 2018).However, the EDGE index considers only taxonomic and phylogenetic dimensions of biodiversity, not the functional dimension of biodiversity that conservation professionals recently argued should be considered in conservation planning (Cernansky, 2017).Therefore, an index simultaneously reflecting the taxonomic, phylogenetic, and functional dimensions of biodiversity would greatly advance biodiversity and conservation planning.
Once one has identified priority areas for future expansion of PAs, whether and how protection is to be implemented in the priority areas are important questions.Addressing these questions requires investigating the PA coverage and the threat severity in the identified priority areas.Since the Aichi Targets were proposed in 2010 (CBD, 2012), the coverage of global PAs has continued to increase, providing irreplaceable protection for a large number of threatened species and ecosystems (Coetzee et al., 2014;Gray et al., 2016;Joppa et al., 2008).However, there is still a lack of knowledge about the differences in the PA coverage for different dimensions of global terrestrial vertebrate biodiversity (Rodrigues & Cazalis, 2020).Determining PA coverage in the priority areas identified by different dimensions of biodiversity provides a way to explore the gaps in terrestrial vertebrate biodiversity conservation and can help improve identification of PAs in the future (Llorente-Culebras et al., 2021).In addition, biodiversity tends to be positively correlated with the intensity of threats, such as human activities and climate change (Balmford et al., 2001;Ives et al., 2016;Schleicher et al., 2019).
This spatial consistency between biodiversity and threats brings challenges to conservation practice (Schleicher et al., 2019) and possibilities of synergy between local development and biodiversity conservation (Li, Jenkins et al., 2022).Incorporating conflicts between biodiversity conservation and threats into the identification of future priority areas for PA expansion would certainly improve the persistence (Gaston et al., 2008) of protected biodiversity and the conservation outcomes of protected sites (Butchart et al., 2015;Xu et al., 2017).Therefore, the PA coverage and the threat severity in identified priority areas must be considered in order to establish PAs in the most appropriate areas, which remains a current challenge (Smirennikova & Ukhanova, 2021;Vale et al., 2018).
We developed a new index for the identification of priority areas based on functionally rare, evolutionarily distinct, and globally endangered species (FREDGE as abbreviation) and applied it to terrestrial vertebrates.In the FREDGE index, information on the functional rarity (FR) of species (evaluated based on life-history traits), Evolutionarily distinc (ED), and threat level of globally endangered species in a region is combined.By integrating these 3 dimensions of biodiversity, FREDGE provides a new perspective on the selection of priority conservation areas.To analyze the PA coverage and threat severity in the priority areas identified by FREEDGE, we compiled the latest data on global PAs, human footprint, and future climate change.Specifically, we sought to identify the global priority areas based on FREDGE for different terrestrial vertebrate groups separately and tested whether the priority areas for biodiversity conservation based on FREDGE and previous indices were consistent.We also explored the PA coverage in the priority areas identified by different indices (i.e., FREDGE, FR, ED, and GE) and tested whether biodiversity of terrestrial vertebrates was equally covered in different priority areas.We evaluated the severity of human activities and future climate change in the priority areas identified based on FREDGE and tested whether the threat severity differed between priority and nonpriority areas.

METHODS
To facilitate the identification of priority conservation areas by considering multiple dimensions of biodiversity, we developed a new index of biodiversity, FREDGE, with data on the distributions, phylogenies, and life-history traits of 21,536 terrestrial vertebrate species.This index integrates 3 dimensions of biodiversity (i.e., functional, phylogenetic, and taxonomic diversity) and the global endangerment (GE) of species.We used Zonation to identify the priority areas for future PA expansion with FREDGE scores as the biodiversity feature.To evaluate the performance of FREDGE in the identification of conservation priorities, we compared the priority areas based on FREDGE with those based on previous indices (i.e., FR, ED, GE) in terms of the spatial mismatches in priority areas and the proportion of each biodiversity dimension covered under the different indices.We also evaluated the PA coverage and threat severity associated with human footprint and future climate change in the priority areas identified by FREDGE so as to inform future conservation planning.

Distributions and phylogenies of terrestrial vertebrates
Species distribution data for mammals and amphibians were obtained from the International Union for Conservation of Nature and Natural Resources (IUCN) (IUCN, 2020), and data for reptiles and birds were from Roll et al. (2017) and BirdLife International and Handbook of the Birds of the World (2020), respectively.We removed locally extinct and introduced mammal, amphibian, and bird species following the guidelines for the IUCN Red List spatial data (version 1.19) (IUCN, 2021).Specifically, we removed the presence code 4-6 and the origin code 3-5.According to Roll et al. (2017), introduced species are not included in the reptile distribution data.These species distribution data are in ESRI shapefile format, and we converted them into gridded maps with spatial resolution of 1 • × 1 • with the overlap function in R. The conservation status of each species was obtained from the IUCN Red List (IUCN, 2020).In identifying areas of conservation priority for terrestrial vertebrates, we focused on data deficit (DD), least concern (LC), near threatened (NT), vulnerable (VU), endangered (EN), and critically endangered (CR) species.
We obtained species-level phylogenies of the 4 terrestrial vertebrate groups from published and widely used data (Jetz & Pyron, 2018;Jetz et al., 2012;Tonini et al., 2016;Upham et al., 2019): mammals from Upham et al. (2019), amphibians from Jetz and Pyron (2018), reptiles from Tonini et al. (2016), and birds from Jetz et al. (2012).These phylogenies all contained polytomies for some species without DNA data (i.e., 30.67% for mammals, 43.89% for amphibians, 44.48% for reptiles, and 33.32% for birds).These were randomly resolved using tools for macroevolutionary analysis devised by the original authors.This method for resolving polytomies leads to a variety of relationships between the species without DNA data.To account for the potential influence of polytomy resolving in our analyses, we randomly selected 100 phylogenetic trees for each of the terrestrial vertebrate groups.Then, we repeated all phylogenetic analysis with these trees and used the average results across the 100 trees of each group as the final results (Gumbs et al., 2020;Pollock et al., 2017).

Life-history traits
To estimate the FR of species, major life-history traits of terrestrial vertebrate species were used following Carmona et al. (2021).Because different terrestrial vertebrate groups have different morphologies and life histories, we used different lifehistory traits for different groups.Traits for mammals were litter size (number of offspring), number of litters per year, adult body mass (g), longevity (years), gestation length (days), weaning length (days), time to female maturity (days), and snout-vent length (cm).Traits for birds were clutch size (number of eggs), number of clutches per year, adult body mass (g), incubation time (days), longevity (years), fledging age (days), egg mass (g), and snout-vent length (cm).Traits for reptiles were clutch size (number of eggs), number of clutches per year, adult body mass (g), incubation time (days), longevity (years), and snout-vent length (cm).Traits for amphibians were age at maturity (years), body size (measured as snout-vent length for Anura and as total length [mm] for Gymnophiona and Caudata), maximum litter size (number of individuals), and offspring size (mm).
We calculated the functional space of all species within each terrestrial vertebrate group with principal component analyses (PCAs) based on the log-transformed and scaled functional traits of each group.We extracted the first and second principal component (PC) axes of life-history trait variation for each group and the scores of each species on these first 2 PC axes.The functional space of life-history trait variation was constructed as the 2-dimensional space of the first 2 PC axes for each terrestrial vertebrate group separately.
After matching the species with these 3 data types simultaneously, 21,536 terrestrial vertebrate species (3256 terrestrial mammals, 5136 amphibians, 6061 reptiles, and 7083 birds) remained for analyses.

Environmental data
To evaluate the threats to biodiversity induced by future climate change, we obtained the present  and the future (2041-2070) climate data with spatial resolutions of 30 × 30 arc seconds (ca. 1 × 1 km 2 at the equatorial area) from CHELSA (https://chelsa-climate.org/).Specifically, we obtained the future climate data for the years 2041-2070 simulated by 4 global circulation models (GCMs): GFDL-ESM4, IPSL-CM6A-LR, MPI-ESM1-2-HR, and MRI-ESM2-0 under the lowest and highest emission scenarios (i.e., the SSP126 and SSP585) (Karger et al., 2017).These 4 GCMs were selected following the recommendation of model priorities in CHELSA.For each climate scenario, we calculated the average of each bioclimatic variable (i.e., bio1-bio19) across all the 4 GCMs for the following analyses.
To evaluate the threats to biodiversity induced by human activities, human footprint data with a spatial resolution of 1 × 1 km 2 were obtained from Venter et al. (2016).Human footprint was estimated using 8 variables representing the intensities of human activities, including built environments, population density, electric infrastructure, crop lands, pasture lands, roads, railways, and navigable waterways.Human footprint data have been widely used to measure the direct and indirect human pressures on the environment globally (Jones et al., 2018;Tucker et al., 2018).We used human footprint values from 2009.The maps of human footprint data were in the Mollowedie equal area projection (Venter et al., 2016) and were transformed into GCS_WGS_1984 before the analysis of threat severity in priority areas.
To evaluate the PA coverage in priority areas, the data for global PAs were obtained from the World Database on Protected Areas (WDPA) (UNEP-WCMC, 2021).Because the data for Chinese PAs in this database are not complete, we replaced the Chinese PAs in the WDPA data with the updated data on Chinese nature reserves (national-, provincial-, and county-level nature reserves) following (Shrestha et al., 2021).
The above data were all in raster format except the WDPA PA data, which were in ESRI shapefile format.We extracted them to a 1 • × 1 • raster layer in GCS_WGS_1984 projection based on the mean value of all 30 × 30 arc seconds grid cell with the zonal function in ArcGIS 10.4.

FREDGE index
The FREDGE index identifies species that are functionally and evolutionarily unique but severely threatened.In particular, the GE score of a species was assigned according to the conservation status of the species as indicated on the IUCN Red List (Isaac et al., 2007).In general, the higher the conservation status of a species, the higher its GE value.Following Shrestha et al. (2021), we assigned GE scores to all species: LC, 1; NT, 2; VU, 4; EN, 8; CR, 16.Some DD species may be highly threatened (Borgelt et al., 2022;Roberts et al., 2016).To better represent the potential threat to DD species, following Cox et al. (2022), we assigned the GE scores of DD species in each vertebrate group as the mean of the GE scores of other species in that group.
ED of species represents the branch length in the phylogeny unique to each species and is calculated as the sum of the branch lengths on a species' path to the phylogenetic root, where each branch is weighted inversely by the number of species it contains (Isaac et al., 2007).The unit of ED is millions of years before present, and a relatively large ED score of a species means the species is more evolutionarily distinct.FR measures the degree of species independence in the 2-dimensional functional space represented by the first 2 PC axes of life-history traits and was estimated as the average distance of a species in the functional space relative to all other species (Bagousse-Pinguet et al., 2021;Violle et al., 2017): where N is the number of species in a grid cell and d ij is the functional distance between species i and j calculated by the coordinates of species in the 2-dimensional functional space determined by the first 2 PC axes of life-history traits.For species i, a large FR i value means the species has a large average distance from all other species in the functional space and thus is functionally rare.After calculating the FR, ED, and GE values for each species separately, we rescaled each of them to be between 0 and 1 (metric rescal = [metric − metric min ]/[metric max − metric min ]) and summed the 3 to obtain the FREDGE index of the species: A high FREDGE value indicates the species is under serious threat or has important evolutionary and functional roles and hence is of high conservation priority.

Spatial prioritization
We conducted spatial prioritization analyses for different indices separately (i.e., FR, ED, GE, and FREDGE) with Zonation 5.0 (Moilanen et al., 2022).Zonation calculates the marginal loss of each grid cell in each iteration based on biodiversity features and feature weight and iteratively removes the grid cell with the lowest value until all the grid cells in the study area are removed.Thus, Zonation produces a priority ranking through all grid cells in the study area, and the priority ranking of a grid cell is the order in which the grid cell is removed.Zonation 5.0 provides 5 alternatives for the marginal loss rule, and we used the CAZMAX algorithm (same as CAZ [Core-Area Zonation] in earlier versions of Zonation).The CAZMAX aims to cover high-occurrence locations for all species and favors species with narrow distribution ranges; hence, it is suitable for analyzing maximization of global biodiversity (Moilanen et al., 2022).
For each index, we conducted Zonation analyses with the species distributions as input layers and the index score of each species as the weight.We identified the priority areas of each index as the areas with the highest priority ranking.The following thresholds of percentages of global terrestrial lands were used for the identification of priority areas: 2.5%, 5%, 10%, 17%, 30%, 50%, 75%, and 100% (e.g., 2.5% means the 2.5% of global terrestrial lands with the highest priority ranking).To compare the advantages of different indices for selecting priority areas, we calculated the total SR and the mean of other biodiversity indices (FR, ED, GE, summing and dividing by SR) for the 2.5% of areas of the highest priority identified based on FR, ED, GE, and FREDGE.For each of the vertebrate group, we ranked the priority areas identified with FR, ED, GE, and FREDGE based on the level of preservation of the 4 biodiversity dimensions (SR, FR, ED, and GE).A high rank indicated high performance of the index on which the rank was based.
To investigate the spatial differences in the priority areas determined by FR, ED, GE, and FREDGE, we overlaid identified areas for the different indices.We used 1 threshold of the percentage of global terrestrial lands for the identification of priority areas: 17%.To delineate the integrated priority areas (i.e., areas identified as the 17% of areas of the highest priority for any terrestrial vertebrate group), we overlaid the 17% of areas of the highest priority identified with FREDGE.Based on the number of terrestrial vertebrate groups that overlapped, the 1 • × 1 • grid cells in the priority areas were classified into 4 levels (e.g., level 4 means a grid cell was the priority area for 4 terrestrial vertebrate groups and thus had the highest priority for conservation).To reflect the potential responsibilities of different countries in biodiversity conservation, we calculated the proportion of each country's internal priority conservation area to its national territory.

PA coverage and threat severity in the priority areas
To estimate the PA coverage in the priority areas identified by FREDGE, we overlaid the integrated priority areas for the vertebrate groups with global PAs.To reduce the calculation load, we converted the data layers of the priority areas and global PAs into raster format at a resolution of 30 arc seconds.Then, we calculated the percentage of priority areas covered by PAs for the integrated priority areas.
To compare the climate change levels between priority and nonpriority areas, we conducted a PCA with the bioclimatic variables (i.e., bio1-bio19) at present  and future (2041-2070) values and extracted the first and second PC axes.The level of climate change in a grid cell was estimated as the distance between the 2 positions of this grid cell in the climatic space of the first 2 PC axes, which reflected current and future climates.To facilitate comparison between human footprint and climate changes, we normalized the values of human footprint and future climate change across all grid cells to be from 0 to 1. Finally, we summed the values of human footprint and future climate change in each grid cell to represent the severity of threats to biodiversity.To evaluate the overlap between the areas with severe threats and the priority areas for conservation, we extracted the 2.5%, 5%, 10%, 17%, and 30% of the terrestrial lands with highest severity of threats (e.g., 2.5% means the 2.5% of the world with the highest threat) and overlaid the threat maps and the priority area maps.

Global priority areas
The FREDGE scores varied among species and ranged from 0.0058 to 1.82 for mammal species, 0.023 to 2.18 for amphibian species, 0.0070 to 1.59 for reptile species, and 0.0046 to 2.28 for bird species (Appendix S1).The median of FREDGE score for amphibian species (0.38) was much higher than those of the other 3 vertebrate groups (0.18 for mammals, 0.16 for reptiles, and 0.19 for birds) (Appendix S2).The total FREDGE scores of the species in each 1 • × 1 • grid cell were highest in South America, central Africa, and Southeast Asia (Figure 1).The total FREDGE scores per grid cell in the 2.5% of land areas with the highest FREDGE values were 24.49-37.67for mammals, 19.95-55.96 for amphibians, 26.75-33.26 for reptiles, and 112.65-178.19 for birds (Figure 1).
The global priority areas identified based on FREDGE differed among taxa (Figure 2).For mammals, Southeast Asia, central Africa, Central America, and northwestern South America had high priority ranking (2.5% of the world with the highest priority ranking).For amphibians, Central America, the Andes, and southern China had high priority ranking.For reptiles, Central America, west Asia, and east Africa had high priority ranking.For birds, the Andes, the Himalayas, and central Indian had high priority ranking.Despite the differences in the priority areas of FREDGE scores among taxa, several regions had high priority ranking for all 4 terrestrial vertebrate groups, including Madagascar, Central America, and the Andes.
The 17% of the most important priority areas identified based on FR, ED, GE, and FREDGE differed from each other (Figure 3; Appendices S3-S7).The priority areas overlapping across all 4 indices (i.e., gray area in Figure 3) accounted for 52.1% (mean of the 4 terrestrial vertebrate groups, 43.7% for mammals, 65.2% for amphibians, 53.6% for reptiles, and 45.6% for birds, separately) of all priority areas selected by these indices.Notably, 47.9% of the priority areas (other colors in Figure 3) were identified by fewer than 4 indices.The FREDGE index was more comprehensive in that it identified priority areas that could only be identified by multiple other indices but not by any other single dimensional index (warm colors in Figure 3).This was true for central Africa and southeast Asia for mammals, southern China for amphibians, southeastern South America and west Asia for reptiles, and southwestern China and central India for birds.
The performance of priority areas in preserving biodiversity differed among indices (Appendix S8).The priority areas identified by FREDGE had the highest rankings in the conservation of multiple dimensions of biodiversity for mammals, reptiles, birds, and all terrestrial vertebrates (scores of 12, 11, 11, and 45, respectively), suggesting that the FREDGE index was the best at identifying the most effective conservation priorities in these groups.

Integrated priority areas
The overlap between priority areas identified based on FREDGE across the 4 terrestrial vertebrate groups indicated that the integrated priority areas of all groups were mainly distributed in tropical and subtropical regions and rarely occurred at high latitudes in the northern hemisphere (Figure 4a).When these priority areas were grouped into 4 levels according to the number of overlapping vertebrate groups, ranging from level 4 (areas identified as priority areas for 4 vertebrate groups) to level 1 (areas identified as priority areas for 1 vertebrate group).The level 4 priority areas were concentrated in Central America, the Andes, southwestern South America, central Africa, Madagascar, and southeast Asia, which are mainly tropical.
The distribution of the integrated priority areas was uneven among countries (Appendix S1).Sixty-eight countries were completely covered by the integrated priority areas, among which 4 countries, Dominica, Guadeloupe, Jamaica, and Singapore, were completely covered by the level 4 priority areas.Nineteen countries were not covered by any priority areas.These were located primarily in northern Europe and western Asia (e.g., Norway, Iceland, Qatar, and Kuwait).
By overlapping the integrated priority areas and the existing PAs (Figure 4b), we found that only 18.5% of the grid cells in the integrated priority areas had PA coverages over 30%, and these grid cells were located mainly in central and northern South America, eastern Africa, southern Europe, and southeast Asia.In contrast, 68.8% of the grid cells in the integrated priority areas had low levels of PA coverage (<17%), including those in southeastern North America, India, and southern China.

Threat severity in priority areas
South Asia, East Asia, Europe, and eastern North America had high human footprint values (Appendix S9).In contrast, South America and Southeast Asia had larger future climate change than the rest of the world under the SSP585 scenario, and South America, western India, and southern China had large future cli-mate change under the SSP126 scenario (Appendix S10).Over one half (54.4%) of the integrated priority areas were within the 30% of areas that were most threatened.Interestingly, 60.7% of the 2.5% most globally threatened areas were in the integrated priority areas under the SSP585 scenario (Appendix S11), and 57.9% of the 2.5% most globally threatened areas were in the integrated priority areas under the SSP585 scenario (Appendix

FIGURE 4
The integrated priority conservation areas (i.e., areas identified as the 17% of areas of the highest priority based on any terrestrial vertebrate group) for terrestrial mammals, amphibians, reptiles, and birds identified with the FREDGE (functionally rare, evolutionarily distinct, and globally endangered species) index and the protected area coverage in these priority areas: (a) overlap between the 17% of areas of the highest priority identified with FREDGE for all the 4 terrestrial vertebrate groups (levels 1-4, areas identified as priority areas for 1-4 terrestrial vertebrate groups, respectively) and (b) percentage of area protected in the integrated priority conservation areas.S12).These highly threatened areas were concentrated in India, East Asia, and southern Europe (Figure 5a; Appendix S13).
The mean threat values were higher in the integrated priority areas than in nonpriority areas (integrated priority areas: 0.32; nonpriority areas: 0.18) and increased from the level 1 integrated priority areas to level 4 (levels 1-4: 0.29, 0.33, 0.36, and 0.38, respectively) (Figure 5).

DISCUSSION
Priority areas identified by FREDGE better conserved the biodiversity of terrestrial vertebrates than those identified by FR, ED, and GE.These results suggest that FREDGE was better at selecting priority areas for conservation based on multiple dimensions of biodiversity and hence provides a useful tool for conservation.We also found that over one half of the integrated priority areas across the 4 terrestrial vertebrate groups are under intense threat induced by human footprint and future climate change, suggesting that future conservation planning is facing the challenge of conflict between biodiversity and threat pressure.

The FREDGE index
The FREDGE index integrates 3 dimensions of biodiversity and reflects GE, ED, and FR of species.Therefore, this index FIGURE 5 Threat severity in the integrated priority areas (i.e., areas identified as the 17% of areas of the highest priority based on any terrestrial vertebrate group) identified with the FREDGE (functionally rare, evolutionarily distinct, and globally endangered species) index for terrestrial mammals, amphibians, reptiles, and birds: (a) geographical variation in the threat severity (i.e., sum of the human footprint and future climate change) (SSP585 scenario; all grid cells in integrated priority areas divided into 8 classes according to their percentiles in the frequency distribution of threat severity) and differences in threat severity (b) for different levels of integrated priority areas and (c) between the integrated priority areas and nonpriority areas (levels 1-4, areas identified as priority areas for 1-4 terrestrial vertebrate groups, respectively).
addresses the need for the development of spatial prioritization based on multiple dimensions of biodiversity.Although there were differences among the priority areas of different terrestrial vertebrate groups, Madagascar, central Africa, central America, Southeast Asia, and the Andes were ranked at the top for the conservation of all 4 vertebrate groups (Figure 2), suggesting that these areas not only have high SR, but also have high diversity of evolutionarily and functionally unique species and severely threatened species that need to be focused on in future conservation planning.
Compared with previous assessments of priority areas for the conservation of terrestrial vertebrates (Gumbs et al., 2020;Jetz & Pyron, 2018;Pollock et al., 2017), our results showed that after combining multiple dimensions, the priority areas obtained differed significantly from those based on a single dimension.In contrast to our study, a previous study based on threatened SR of terrestrial vertebrates demonstrated the high priority of Southeast Asia for conservation (Howard et al., 2020).Daru et al. (2019) focused on ED and GE and identified some island regions as the priority areas for conservation of terrestrial vertebrate species.The discrepancy between these studies may be because they emphasized different dimensions of biodiversity and thus highlighted different priority areas (Brum et al., 2017;Pollock et al., 2017).These findings suggest that priority areas obtained from the analysis of a single biodiversity dimension may be biased and may not protect other dimensions of biodiversity well.Goal A of the Kunming-Montreal Global Biodiversity Framework, which reflects a consideration for the conservation of multiple dimensions of biodiversity, states that the risk of species extinctions across all taxonomic and functional groups needs to be halved and that genetic diversity of all species should be maintained (CBD, 2022).Therefore, spatial prioritization based on multiple dimensions of biodiversity needs to be strengthened in future conservation planning.
Our FREDGE index offered more comprehensiveness results than other indices used to identify priority conservation areas.It can be used to identify areas that cannot be identified by other indices alone.We also found that the priority areas identified based on FREDGE better conserved terrestrial vertebrates than areas identified based on other indices.Therefore, the FREDGE index is effective for use in the spatial conservation prioritization of multiple biodiversity dimensions.

PA coverage in priority areas
The effectiveness of existing PAs is of great concern (Rahman & Islam, 2021;Wolf et al., 2021).Although many PAs have been established to conserve individual target species (e.g., giant panda [Ailuropoda melanoleuca]), current PAs covered 16.2% of the integrated priority areas aiming to preserve multiple dimensions of biodiversity of terrestrial vertebrates.This result suggests that biodiversity dimensions other than individual species or SR can also be protected to some extent by the current PAs.This may be because areas with high SR tend to also have more species with unique evolutionary or life-history traits.Moreover, in conservation practices, people usually tend to conserve areas with unique species (e.g., flagship species and umbrella species) rather than the areas with the highest SR (Caro & O'Doherty, 1999), and these unique species may make large contributions to ED and FR.However, only 18.5% of the grid cells in the integrated priority areas had PA coverages over 30%, which suggests that more conservation actions are needed in the future for the conservation of multiple dimensions of biodiversity.

Threat severity in priority areas
Areas with high biodiversity are often accompanied by high anthropogenic threat pressure, which has attracted widespread attention from researchers and conservation practitioners (Allan et al., 2019;Balmford, 2001;Luck, 2007).Conservation practitioners recognize that high threats in areas with high biodiversity have become a major challenge in conservation planning (Nyhus, 2016;Redpath et al., 2013).To help address this challenge in future conservation planning for global terrestrial vertebrates, we evaluated the threat severity in the identified priority areas based on FREDGE.Our results are in line with the expectation that over one half of the integrated priority areas for terrestrial vertebrates are under intense pressure induced by anthropogenic threats and future climate change.Moreover, the integrated priority areas identified for all 4 groups of terrestrial vertebrates had the highest threat severity compared with the priority areas identified for 3 or fewer groups.In the priority areas with severe threats, vertebrate biodiversity and ecosystems are more vulnerable due to intense climate change and anthropogenic pressures (Chapin et al., 2000;Thomas et al., 2004).Therefore, these priority areas deserve more attention in future conservation planning and practice.It is worrying that the PA coverage in 68.8% of these integrated priority areas is still <17%.Moreover, the amount of human activities in these priority areas is great, which means that conservation planning in these areas is costly and difficult (Venter et al., 2014).Therefore, appropriate conservation plans and improved investment strategies are needed in the future expansion of PAs to achieve the synergy between human development and biodiversity conservation (Li, Zhao, et al., 2022).

FIGURE 1
FIGURE 1Global patterns in FREDGE (functionally rare, evolutionarily distinct, and globally endangered species) index scores for terrestrial (a) mammals, (b) amphibians, (c) reptiles, and (d) birds (the higher the value, the more unique and threatened the species in the area).

FIGURE 2
FIGURE 2 Priority conservation areas identified with the FREDGE (functionally rare, evolutionarily distinct, and globally endangered species) index for (a) mammals, (b) amphibians, (c) reptiles, and (d) birds.Percentages are of terrestrial land with the highest priority ranking evaluated with Zonation (Moilanen et al., 2022).

FIGURE 3
FIGURE 3 Spatial inconsistency in the priority conservation areas identified based on FREDGE (functionally rare, evolutionarily distinct, and globally endangered species) and other biodiversity indices for (a) mammals, (b) amphibians, (c) reptiles, and (d) birds (colors, overlap between the priority areas identified by different indices; index dimensions: FR, functional rarity; ED, evolutionary distinctiveness; GE, global endangerment and FREDGE; 1 dim, priority areas identified base on 1 dimension of the indices; 2 dim, priority areas identified based on 2 dimensions of the indices [i.e., FR and ED, FR and GE, ED and GE]; 3 dim, priority areas identified based on 3 dimensions of the indices [i.e., FR, ED, and GE]).