article: It is widely recognized that we are entering an extinction event on a scale approaching the mass extinctions seen in the fossil record. Present-day rates of extinction are estimated to be several orders of magnitude greater than background rates and are projected to increase further if current trends continue. In vertebrates, species traits, such as body size, fecundity, and geographic range, are important predictors of vulnerability. Although plants are the basis for life on Earth, our knowledge of plant extinctions and vulnerabilities is lagging. Here, we disentangle the underlying drivers of extinction risk in plants, focusing on the Cape of South Africa, a global biodiversity hotspot. By comparing Red List data for the British and South African floras, we demonstrate that the taxonomic distribution of extinction risk differs significantly between regions, inconsistent with a simple, trait-based model of extinction. Using a comprehensive phylogenetic tree for the Cape, we reveal a phylogenetic signal in the distribution of plant extinction risks but show that the most threatened species cluster within short branches at the tips of the phylogeny—opposite to trends in mammals. From analyzing the distribution of threatened species across 11 exemplar clades, we suggest that mode of speciation best explains the unusual phylogenetic structure of extinction risks in plants of the Cape. Our results demonstrate that explanations for elevated extinction risk in plants of the Cape flora differ dramatically from those recognized for vertebrates. In the Cape, extinction risk is higher for young and fast-evolving plant lineages and cannot be explained by correlations with simple biological traits. Critically, we find that the most vulnerable plant species are nonetheless marching towards extinction at a more rapid pace but, surprisingly, independently from anthropogenic effects. Our results have important implications for conservation priorities and cast doubts on the utility of current Red List criteria for plants in regions such as the Cape, where speciation has been rapid, if our aim is to maximize the preservation of the tree-of-life.
  The rapid and accelerating loss of biodiversity is the most significant ecological challenge we face today. Current rates of extinction are already estimated to be several orders of magnitude greater than background rates [1] and are projected to increase another order of magnitude within the next few hundred years [2]. The terrestrial environment is now dominated by people—approximately one-third of land area has been transformed for human use [3] and one-fourth of global productivity diverted to human consumption [4]. The main direct human-induced drivers that impact biodiversity now are habitat loss and fragmentation, whereas climate change is likely to become a dominant future driver [5]. With each extinction event, we lose an element of biodiversity along with the associated ecosystem services it provides and the unique evolutionary history it represents. For over four decades the Red List of Threatened Species from the International Union for Conservation of Nature (IUCN; http: //www. iucnredlist. org/) has provided a record of the incremental slide towards extinction of much of current biodiversity [6]–[8]. Based on detailed, peer-reviewed assessments [9], species are placed into one of the following seven categories, in order of increasing extinction risk: least concern (LC), near-threatened (NT), vulnerable (VU), endangered (EN), critically endangered (CR), extinct in the wild (EW), and finally, extinct (EX). There are currently 47,978 species on the IUCN Red List, of which 17,315 are classified as threatened with extinction; the vast majority (75%) of these records are from animals. In vertebrates, including mammals, birds, and amphibians, the proportion of species falling within the different threat categories differs significantly between higher taxa [10]–[13], indicating taxonomic selectivity in species vulnerabilities. Species traits linked with body size, generation times, and geographic range size are commonly associated with threat status [10], [13]–[16], with the most vulnerable species tending to be nested within species-poor clades [12], [13]. Identifying the key traits linked to high extinction risk is critical for predicting future declines and provides an opportunity for implementing preemptive conservation measures [17], although the particular attributes that influence vulnerability can differ among clades and geographic regions [18], [19]. Our knowledge of extinction in plants is much poorer than for vertebrates, with <5% of known plant species assessed (10,916 species) by the IUCN using current criteria. Nonetheless, current listings are still informative, especially if we focus on regions where taxonomic sampling has been more complete. Within flowering plants, over 70% of currently listed species are classified as at risk of extinction (category VU or higher; Figure 1), a much higher percentage than that reported for vertebrate groups (22% listed species). In large part, this likely reflects the relative incompleteness of the dataset for plants, and recent efforts suggest the proportion of threatened plants might be similar to that for mammals [20], although these estimates assume an even distribution of threatened species within higher taxa. Parallel to trends for vertebrates, plants also demonstrate an uneven distribution of threat across taxonomic ranks in both local floras [21]–[23] and globally, as shown here (p<0. 001 and p = 0. 002 from randomizations for families and orders, respectively; see Materials and Methods, Tables S1 and S2) and suggested elsewhere [24]. However, plant studies based on local floras show that life history traits (e. g. , pollination syndrome, sexual system, habit, height, and dispersal mode) seem to only correlate poorly with species rarity (relative frequency of occurrence) or threat (index of species' decline or vulnerability to future decline) [25]–[27], and putative key traits differ between studies [23], [26], [28], [29]. Significant taxonomic structure in the distribution of threat in the absence of any strong correlation with heritable biological traits requires an explanation—although it remains possible that important traits have yet to be identified. Further, in contrast to findings for vertebrates, threatened plant species, as indexed by rarity, tend to be over-represented within species-rich taxa [21], . This trend suggests a potential link between the processes of speciation and extinction [30]. We have not attempted to differentiate between rarity and threat status here, because rarity does not have a standard definition or geographical scale and might refer to both local and global scales [21], [30] or relate more directly to extinction risk [21], [22]. Whilst rarity may not always match to estimates of global threat status as defined by the IUCN, it is a central criterion in Red List (e. g. , Criteria A, C, and D), and regional rarity would be expected to provide a good indicator of regional Red List status in the absence of more comprehensive IUCN assessments. Further, a recent study [31] demonstrated that regional Red Lists typically correlate strongly with global listings, and for endemic species, regional status will translate directly to global status. In this study, we explore the distribution of extinction risks for two of the best-studied floras, the Cape of South Africa and the United Kingdom, for which practically complete regional Red List data have recently been published (Materials and Methods). These two regions represent very different floristic histories, the former assembled via post-glacial recolonization and range expansion, the latter a global biodiversity hotspot [32] with extraordinary high endemism [33] suggesting a rich history of in situ diversification. If the processes of speciation and extinction are coupled, the Cape flora likely provides the best opportunity for detecting the imprint of any such links. Moreover, if there are similarities in the distribution of extinction risks between the UK and Cape floras, it would be strong evidence for common trends across angiosperms. Here, we contrast the taxonomic distribution of extinction risks between the Cape and the UK floras. We then use detailed phylogenetic data for the Cape to identify the factors likely driving extinctions. Phylogenetic approaches not only allow us to correct for the non-independence of characters given the evolutionary relationships between species but also provide information on species' evolutionary histories. We reveal an unusual phylogenetic signal in extinction risks for plants and demonstrate how species' present-day vulnerabilities can be explained by their recent evolutionary past.
  As we move towards assembling the complete tree-of-life, there has been increasing emphasis on preserving phylogenetic diversity [50], [51]. Recently, Vamosi and Wilson [24] suggested that globally we risk losing a disproportionate amount of angiosperm evolutionary history as we lose the most vulnerable species to extinctions. Using more detailed phylogenetic information, we show that plant extinctions may result in little loss of evolutionary history, at least in biodiversity hotspots where much of present-day diversity is a product of recent speciation. It is possible that the processes driving extinction in relict lineages are different from those for young diversifying lineages and that there exist two classes of globally threatened plant species. Estimating the true impact of plant extinctions on the loss of evolutionary history across the angiosperm tree-of-life will therefore require detailed knowledge of the interspecific phylogenetic relationships within higher taxa. Our results linking speciation and extinction derive from an analysis of the unique flora found within the Cape region of South Africa and might not extrapolate across less diverse biomes with different evolutionary histories. However, we note that the trend for threatened species to fall within species-poor clades has been observed within the relatively depauperate floras of the UK [22] and North America [21]. We suggest that species turnover (speciation and extinction) might be rapid generally for plants, and high extinction rates may not be unusual over evolutionary timescales. Because even rapid speciation occurs over timescales too long for practical management [52], conservation efforts must focus urgently on reducing rates at which species are being lost [53]–[55]. However, if we wish to maximize the preservation of the tree-of-life [11], we must consider whether plants and animals may be best served by different assessment criteria when deciding upon conservation priorities. For example, for plants, investing in currently less threatened but still vulnerable species in more evolutionary distinct clades might be the most sensible conservation strategy, whereas for vertebrates the IUCN Red List may provide a more straightforward index for conservation decision making.
  Plant species Red List data were extracted from the following sources: (1) Global data: The IUCN Red List of Threatened Species (http: //www. iucnredlist. org, accessed August 2009); (2) UK flora: Joint Nature Conservation Committee' s Vascular Plant Red Data List for Great Britain 2006 (http: //www. jncc. gov. uk); and (3) South African flora: the Interim Global Status for plants published online by the South African National Biodiversity Institute (SANBI: http: //www. sanbi. org/; accessed June 2008), and the Beta version of South African Plant Red List including all assessed taxa and their status (SANBI: http: //www. sanbi. org/; accessed October 2010). An updated print version is now available from the Pretoria National Botanical Garden [35]. Plant names were synonymized to agree with the Angiosperm Phylogeny Group [56] taxonomy. We used IUCN Red List categories to classify each listed species as either threatened (vulnerable [VU], endangered [EN], critically endangered [CR], extinct in the wild [EW], and extinct [EX]) or non-threatened (least concern [LC] and near-threatened [NT]). Taxonomic structure was evaluated by recording the ratio of threatened to non-threatened species recorded within higher taxa (families, orders, and, for the local floras, APG [56] higher taxonomic class) and calculating the variance across taxa. Significance was assessed by randomizing species membership among taxa and recalculating the ratio of threatened species within each random assemblage, keeping number of species per taxon constant. Taxa with significantly more or less threatened species were identified by comparing the observed proportion of threatened species with expectations from the randomizations. The p values were determined from 1,000 random draws. Last, we synonymized 1996 [57] and 2007 Interim Global Status for the South African flora so that extinction risk categories were broadly equivalent, and we scored species included in both listing as +1 if threat increased or −1 if threat decreased. We then derived an index of change in threat status by summing species values within each genus. Because criteria used in the 1996 and 2007 listing were not directly comparable, we evaluated whether species identified as the most vulnerable to extinction in the 1996 listing were more or less threatened in the subsequent assessment by contrasting trends between the top third most threatened taxa with trends within the bottom third (least threatened taxa), ranked using the 1996 listing. We quantified phylogenetic signal in extinction risk for the Cape flora using Blomberg' s K-statistic [38] on the recent comprehensive phylogenetic tree of Cape genera [36]. We use the proportion of threatened species within genera, as described above, as our index of threat. Significance was calculated by randomizing the tips of the tree and recalculating K (1,000 replicates). The K statistic compares the distribution of phylogenetically independent contrasts across nodes within the clade [58], to expectations under a Brownian motion model of trait evolution. Because our metric of extinction risk is bounded between 1 and 0 and therefore violates assumptions of normality, we report only the p values from randomizations. Within the Cape flora, we characterized the phylogenetic distribution of extinction risk across 11 exemplar clades resolved at the species level (Table 2). For each clade we then described variance in extinction risk between and within clades using Harmon and colleagues' index of disparity through time (DTT) [40]. DTT is derived from the standardized mean pair-wise distance between species and therefore does not necessitate the reconstruction of ancestral states. Values of DTT near 0 indicate that most of the variation is partitioned between clades, whereas values near 1 indicate that most variation is among species within subclades. Because at the limits DTT must be 1 at the root and 0 at the tips, we compared observed values to two alternative null models. First, we derived expectations under a null model of Brownian motion. Second, we simulated a model of punctuated evolution in which daughter lineages are assigned trait values asymmetrically at speciation. Following divergence, one daughter lineage inherits a value that differed from the parental lineage by some constant factor, and the other daughter lineage assumes the parental value. Prior to subsequent diversification, both lineages evolve trait distances with a drift factor taken from a normal distribution with mean zero and a given standard deviation plus an evolutionary trend for the smaller lineage to expand in size. This latter simulation might be considered to approximate a model of range size evolution assuming speciation via peripheral isolates, in which one daughter lineage has restricted initial geographic distribution. To evaluate the link between speciation mode and extinction risk directly, we then repeated the analysis of DTT using range size as the trait of interest. Here we estimate range size as the number of quarter degree squares with presence data for each species [37]. If speciation via peripheral isolates is common, we would expect large disparity in range size between species within clades towards the tips of the phylogeny. We did not attempt to link speciation and extinction rates with trait values because to compare DTT plots phylogenetic topology must be identical. Simulations were implemented in the Geiger R-library [59]. R-code for the punctuated model is available from the authors. For all Cape genera we compiled data on species richness (n) [60], time to most recent common ancestor (millions of years; my), and net diversification rates (log[n]/my). We then constructed a series of regression models to describe the relationships between threat and taxon age, richness, and diversification rate. Statistical models were constructed in the R statistical package (http: //www. r-project. org/). First, we generated a series of single-predictor generalized linear models (GLMs) with the proportion of threatened species in each genus as the response and assuming binomial errors. Species richness and diversification rates were log transformed, and taxon ages square-root transformed prior to model fitting. Second, we constructed a two-predictor model including both species richness and age as explanatory variables. Model fits were assessed using Akaike' s information criterion. The marginal contributions of each variable in the two-predictor model were estimated as the additional percent deviance explained by inclusion of that variable to the reduced model. Because missing lineages might result in overestimation of taxon ages and hence underestimation of diversification rates, we focused our analyses on genera endemic to the Cape. Cape endemics are most likely to have their sister clades also included in the phylogenetic tree, and therefore subtending branches will not be broken by the addition of missing taxa; nonetheless, models including all Cape genera also supported the significant relationship between taxon age and threat (not shown). We evaluated model sensitivity in two ways. First, we repeated the set of regression models weighting the data by (1) the logarithm of the number of Red List records for each genus, thereby assuming our estimates of threat are more reliable for genera where multiple species have been assessed, although this will also down-weight the influence of species-poor taxa, and (2) the ratio of listed species to total clade species richness, providing an indication of the impact of missing (unlisted) species. Second, we generated a phylogenetic distance matrix (√my) and used partial Mantel tests to determine the relationship between threat and diversification whilst controlling for phylogenetic relatedness. We extracted the list of genera within each quarter degree square in the Cape from the PRECIS database [37]. We then calculated the mean proportion of threatened species and mean diversification rate for genera within cells, as well as a per-cell index of human impact on the environment [45]. Spatial correlation coefficients were calculated using Pearson' s correlation coefficient (r) for grid cells and controlling for spatial covariance when estimating the statistical significance by adjusting degrees of freedom [61]. First, we estimated the correlation strength between mean threat and human impact, because habitat transformation is thought to be a key driver of species extinctions. Second, we estimated the correlation strength between threat and diversification, because this was the best of our predictor variables from the regression models (above). Spatial analysis was performed in ArcMap (9. 2 Environmental Systems Research Institute Inc.) and SAM (Spatial Analysis in Marcoecology v3. 0) [62].
summary: The rapid loss of biodiversity is the most significant ecological challenge we face today. Over the past few years, the International Union for Conservation of Nature has published Red Lists documenting the inexorable slide towards extinction of species; recent losses include the Hawaiian crow, golden toad, Baiji dolphin, and the West African black rhino. In groups we know well, such as mammals, the risk of extinction has been related to biology, with the most vulnerable species tending to be large, slow breeding, and narrowly distributed. Although plants are the basis for life on Earth, our knowledge of the drivers of plant extinctions is poor. Here, we disentangle the causes of plant extinctions. We show that the processes linked with extinction risks in plants of the Cape, South Africa differ from those for vertebrates more generally. The most vulnerable species are found within young and fast-evolving plant lineages, opposite to patterns in vertebrates. Our results illustrate the intricate link between the processes of speciation and extinction. We also show that the most threatened species are marching towards extinction at faster rates, but surprisingly, the risk appears independent of human effects.
keywords: ecology/global change ecology
  ecology/evolutionary ecology
  evolutionary biology/evolutionary ecology
  ecology/conservation and restoration ecology
title: Extinction Risk and Diversification Are Linked in a Plant
                      Biodiversity Hotspot