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PLoS One. 2007; 2(3): e296. Published online 2007 Mar 14. doi: 10.1371/journal.pone.0000296
PMCID: PMC1808424PMID: 17375184
Mammals on the EDGE: Conservation Priorities Based on Threat and Phylogeny
Nick J.B. Isaac, * Samuel T. Turvey, Ben Collen, Carly Waterman, and Jonathan E.M. Baillie
Walt Reid, Academic Editor
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Abstract
Conservation priority setting based on phylogenetic diversity has frequently been proposed but rarely implemented. Here, we define a simple index that measures the contribution made by different species to phylogenetic diversity and show how the index might contribute towards species-based conservation priorities. We describe procedures to control for missing species, incomplete phylogenetic resolution and uncertainty in node ages that make it possible to apply the method in poorly known clades. We also show that the index is independent of clade size in phylogenies of more than 100 species, indicating that scores from unrelated taxonomic groups are likely to be comparable. Similar scores are returned under two different species concepts, suggesting that the index is robust to taxonomic changes. The approach is applied to a near-complete species-level phylogeny of the Mammalia to generate a global priority list incorporating both phylogenetic diversity and extinction risk. The 100 highest-ranking species represent a high proportion of total mammalian diversity and include many species not usually recognised as conservation priorities. Many species that are both evolutionarily distinct and globally endangered (EDGE species) do not benefit from existing conservation projects or protected areas. The results suggest that global conservation priorities may have to be reassessed in order to prevent a disproportionately large amount of mammalian evolutionary history becoming extinct in the near future.

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Introduction
Our planet is currently experiencing a severe anthropogenically driven extinction event, comparable in magnitude to prehistoric mass extinctions. Global extinction rates are now elevated up to a thousand times higher than the background extinction rates shown by the fossil record, and may climb another order of magnitude in the near future [1]–[3]. The resources currently available for conservation are, unfortunately, insufficient to prevent the loss of much of the world's threatened biodiversity during this crisis, and conservation planners have been forced into the unenviable situation of having to prioritise which species should receive the most protection–this is ‘the agony of choice’ [4] or the ‘Noah’s Ark problem' [5].

A range of methods for setting species-based conservation priorities have been advocated by different researchers or organisations, focusing variously on threatened species, restricted-range endemics, ‘flagship’, ‘umbrella’, ‘keystone’, ‘landscape’ or ‘indicator’ species, or species with significant economic, ecological, scientific or cultural value [6]–[8]. To date, global priority-setting exercises have tended to focus on endemic (or restricted range) species [6], [9], [10], presumably because endemism is easier to measure than competing methods. However, recent data show that endemism is a poor predictor of total species richness or the number of threatened species [11].

It has also been argued that maximising Phylogenetic Diversity (PD) should be a key component of conservation priority setting [4], [12]–[14]. Species represent different amounts of evolutionary history, reflecting the tempo and mode of divergence across the Tree of Life. The extinction of a species in an old, monotypic or species-poor clade would therefore result in a greater loss of biodiversity than that of a young species with many close relatives [15], [16]. However, conserving such lineages may be difficult, since there is some evidence that they are more likely to be threatened with extinction than expected by chance [17]. This clumping of extinction risk in species-poor clades greatly increases the loss of PD compared with a null model of random extinction [18] and suggests that entire vertebrate orders may be lost within centuries [19]. Among mammals alone, at least 14 genera and three families have gone extinct since AD 1500 [20], and all members of a further 19 families and three orders are considered to be in imminent danger of extinction [2]. Many academic papers have suggested ways to maximise the conservation of PD [e.g. 12], [13], [21]–[23] and measure species' contributions to PD [e.g. 4], [23]–[25], but these have rarely been incorporated into conservation strategies. Therefore, it is possible that evolutionary history is being rapidly lost, yet the most distinct species are not being identified as high priorities in existing conservation frameworks.

There are several reasons why PD has not gained wider acceptance in the conservation community. First, although evolutionary history consists of two distinct components (the branching pattern of a phylogenetic tree and the length of its branches), complete dated species-level phylogenies for large taxonomic groups have only recently become available [26]. Early implementations of PD-based approaches were therefore unable to incorporate branch length data, and focused solely on measurements of branching pattern [4]. Second, PD removes the focus from species and so may lack wider tangible appeal to the public; conserving PD may be seen as less important than the protection of endemic or threatened species [16]. However, the current instability in species taxonomy [27] means that decisions based on PD might be more objective than those based on different species concepts [13], [16], [27]. Combining species' conservation status with a measure of their contribution to PD is therefore desirable, because species can be retained as units but weighted appropriately [5], [22]. This would generate a useful and transparent means for setting global priorities for species-based conservation [25].

This paper describes a new method for measuring species' relative contributions to phylogenetic diversity [the ‘originality’ of species: ref 24]. We explore the statistical properties of the resulting measure, which we call Evolutionary Distinctiveness (ED), and test its robustness to changing species concepts. ED scores are calculated for the Class Mammalia, and combined with values for species' extinction risk to generate a list of species that are both evolutionarily distinct and globally endangered (‘EDGE species’). The resultant list provides a set of priorities for mammalian conservation based not only on the likelihood that a species will be lost, but also on its irreplaceability.

Evolutionary Distinctiveness and its use in priority-setting
In order to calculate ED scores for each species, we divide the total phylogenetic diversity of a clade amongst its members. This is achieved by applying a value to each branch equal to its length divided by the number of species subtending the branch. The ED of a species is simply the sum of these values for all branches from which the species is descended, to the root of the phylogeny. For the examples in this paper, we have measured ED in units of time, such that each million years of evolution receives equal weighting and the branches terminate at the same point (i.e. the phylogeny is ultrametric). The method could be applied to non-ultrametric phylogenies if the conservation of other units [e.g. character diversity 28], [29] was prioritised [although see ref 30].

The basic procedure for calculating ED scores is illustrated in figure 1, which describes a clade of seven species (A–G). The ED score of species A is given by the sum of the ED scores for each of the four branches between A and the root. The terminal branch contains just one species (A) and is 1 million years (MY) long, so receives a score of 1 MY. The next two branches are both 1 MY long and contain two and three species, so each daughter species (A, B and C) receives 1/2 and 1/3 MY respectively. The deepest branch that is ancestral to species A is 2 MY long and is shared among five species (A to E), so the total ED score for species A is given by (1/1+1/2+1/3+2/5) = 2.23 MY. Species B is the sister taxon of A, so receives the same score. By the same arithmetic, C has a score of (2/1+1/3+2/5) = 2.73 MY, both D and E receive (1/1+2/2+2/5) = 2.4 MY, and both F and G receive (0.5/1+4.5/2) = 2.75 MY. The example illustrates that ED is not solely determined by a species' unique PD (i.e. the length of the terminal branch). Species F and G are the top-ranked species based on their ED scores, even though each represents just a small amount of unique evolutionary history (0.5 MY). This suggests that the conservation of both F and G should be prioritised, because the extinction of either would leave a single descendant of the oldest and most unusual lineage in the phylogeny [c.f. 15], [24]. The ED calculation is similar to the Equal Splits measure [25], which apportions branch length equally among daughter clades, rather than among descendent species

Extract only the main points for the information given above

Answer 1

- The National Library of Medicine (NLM) provides access to scientific literature but does not endorse or agree with the contents of the literature.
- Conservation priority setting based on phylogenetic diversity is proposed but rarely implemented.
- A new index called Evolutionary Distinctiveness (ED) measures the contribution of different species to phylogenetic diversity.
- The ED index is independent of clade size, making it comparable across different taxonomic groups.
- The approach is applied to a near-complete species-level phylogeny of mammals to generate a global priority list for conservation.
- The list includes many species not typically recognized as conservation priorities and highlights the need to reassess global conservation priorities.
- PD (Phylogenetic Diversity) has not gained wider acceptance in the conservation community due to a lack of complete phylogenetic data and a focus on endemic or threatened species.
- The new ED method incorporates both branch length data and conservation status to generate a prioritized list of species for conservation.
- The method is illustrated with an example of a clade of seven species, showing how ED scores are calculated based on the length of branches and the number of species subtending the branch.
- The example highlights that ED is not solely determined by a species' unique phylogenetic diversity but also considers the conservation of uncommon lineages.
- The ED calculation is similar to the Equal Splits measure, which apportions branch length equally among daughter clades.