Biological Conservation 97 (2001) 99105

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A comparison of taxonomic distinctness versus richness as criteria for setting conservation priorities for North American birds
Stephen Polasky a,*, Blair Csuti b, Christian A. Vossler c, and S. Mark Meyers d
Department of Applied Economics, University of Minnesota, St. Paul, MN 55108, USA b Oregon Zoo, 4001 SW Canyon Road, Portland, OR 97221-2799, USA c Department of Agricultural, Resource and Managerial Economics, Cornell University, Ithaca, NY 14853-7801, USA d Department of Geosciences, Oregon State University, Corvallis, OR 97331, USA Received 4 November 1999; received in revised form 1 April 2000; accepted 5 June 2000
a

Abstract In choosing sites for a conservation reserve network, representation of the greatest number of species in the sites selected is a common objective. This approach implicitly assumes that all species have equal conservation value. An alternative objective is to represent the greatest genetic diversity in selected sites. This approach gives greater weight to species that are more genetically distinct. Such species tend to contain more unique genetic material, which would be lost if such species became extinct. In this paper, we calculate a diversity measure for a given set of species based on the branch length of the phylogenetic tree for the set. We use genetic distances between bird species in 147 genera based on the results of DNA hybridization research. Distribution information for bird species in the US comes from the Breeding Bird Survey. We compare resulting conservation reserve networks when the objective is the number of genera represented versus the diversity of genera represented. We nd that the dierent objectives produce notably similar results. # 2000 Elsevier Science Ltd. All rights reserved.

1. Introduction With certain caveats, the protection of natural areas in conservation reserves is a simple yet eective way to conserve global biological diversity. Because of competing demands for natural resources, few jurisdictions are able to dedicate more than a small fraction of their total area to conservation reserves. The ecient selection of these reserves, is, therefore, a matter of concern. As Margules (1989, p. 10) observed, ``Techniques for managing reserve systems to prevent extinctions will not maintain diversity if the reserve systems being managed do not contain the full range of species in the rst place.'' Pressey (1994) points out that most existing natural areas were not selected with the intention of maximizing the amount of biological diversity represented within them. In recent years, reserve selection algorithms have been used to choose reserve networks eciently (e.g. Margules
* Corresponding author. Tel.: +1-612-625-9213; fax: +1-612-6252729. E-mail address: spolasky@dept.agecon.umn.edu (S. Polasky).

et al., 1988; Nicholls and Margules 1993; Church et al. 1996; Csuti et al. 1997; Ando et al., 1998). These exercises typically use the objective of representing the greatest number of species, though some studies take as an objective conserving a given percentage of a land cover type. Several authors (e.g. May, 1990, VaneWright et al., 1991; Faith, 1992, 1994; Solow et al., 1993; Weitzman, 1992; Williams and Humphries, 1994) have suggested that the total amount of phylogenetic diversity represented in a set of species is an additional criterion that should be considered when selecting natural areas. Behind this suggestion is the notion that genetically distinct species should count more than species with close genetic neighbors. Losing a species without close relatives tends to lead to a greater loss of genetic information than losing species with close relatives. When the unit of account is genetic material, preventing extinction of genetically unique species has a higher priority than saving a species closely related to other surviving species. While this notion is appealing, the lack of phylogenetic distance data for large numbers of species has impeded the application of this concept. In this paper,

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we take advantage of a large existing phylogenetic data set compiled by Sibley and Ahlquist (1990) for bird species. We combine this data with distributional data on bird species in the US, from the US Fish and Wildlife Service's Breeding Bird Survey, to compare the results of richness-driven versus phylogenetic diversitydriven conservation reserve site selection. 2. Data and methods 2.1. Distribution of North American birds In response to widespread concern over the decline of songbirds in North America (Price et al., 1995), the US Fish and Wildlife Service, with the cooperation of the Canadian Wildlife Service, pioneered a yearly, systematic series of bird survey routes, which we will refer to hereafter as sites, in the United States and Canada known as the Breeding Bird Survey (BBS) (Robbins et al., 1986). The rst survey, in 1966, included only 60 sites. At present, however, there are around 3000 sites surveyed annually. Dr. Raymond J. O'Connor and his colleagues at the University of Maine, Orono compiled BBS data for the years 19811990 for use in biogeographic analysis (O'Connor et al., 1996). The US (excluding Alaska and Hawaii) was overlain with a grid of hexagonal cells, each measuring 635 km2 (White et al., 1992). To reduce over-sampling of certain geographic areas, particularly in the eastern US, only one site per hexagon was chosen. Sites with fewer than 7 years of data were also eliminated from the analysis (O'Connor et al., 1996), reducing the total number of sites to 1223. These data provide distributional information for 531 North American bird species in 241 genera. 2.2. Phylogenetic distance The monumental work of Sibley and Ahlquist (1990) provides phylogenetic distances between birds of the world based on a measure of DNADNA hybridization (T50 H values). Sibley and Ahlquist were most concerned with higher order phylogeny and taxonomy. They did not report many of the interspecic distances within a genus. In order to secure a larger sample, we elected to use intergeneric data available for 167 genera of North American birds. The data for intergeneric distances were taken from branch lengths of UPGMA phylogenetic trees of birds reported in Sibley and Ahlquist (1990, pp. 838870). Of these 167 genera, 147 are represented in the distributional data set described earlier. Of the 531 species included in the distributional data, 70% (n=373) are included in these 147 genera. Note that by the nature of phylogenetic data, the phylogenetic distance between any species in one genus to any species in another genus is the same.

For a set of genera, phylogenetic diversity is dened as the branch length of the phylogenetic tree that includes only those genera. In a phylogenetic tree, assuming a constant rate of DNA changes for all taxa, the branch length is proportional to the time of the split from a common ancestor. Longer branch lengths correspond to greater evolutionary time and, presumably, genetically more unique taxonomic groups. Including more genera adds additional branches to the tree. Adding relatively diverse genera adds relatively long branches to the tree. For a simple example of calculating phylogenetic diversity, consider the group of ve genera represented in Fig. 1. Phylogenetic diversity for a group of genera is calculated by adding all the relevant branch lengths between all genera, without double counting. The diversity measure for the set including genera 1 and 2, D(1, 2), is equal to 2A. The diversity measure for the set including genera 1 and 3, D(1, 3), is equal to 2A+2B. For genera 1, 2 and 3, the diversity measure, D(1, 2, 3), is 3A+2B. Adding genera to a set with closely related genera does not add much to the diversity measure. Adding genus 2 to the set with genera 1 and 3 adds only A. However, adding genus 2 to a set that includes genera 4 and 5 adds A+B+C+D: D(4, 5)=2E; D(2, 4, 5)=A+B+C+D+2E. While it is easy to understand the phylogenetic diversity given a phylogenetic tree, it proved easier to have an alternative method in writing a computer program to calculate diversity. An equivalent, though less obvious, way to calculate the diversity measure of a set is as follows.

Fig. 1. Phylogenetic tree for set of ve genera.

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The phylogenetic diversity of a set is equal to the maximum distance between any two members of the set, plus half the sum over all other members of the set (excluding the two with the maximum distance) of the distance between it and its nearest neighbor in the set. Calculation via this method requires only a matrix of pairwise distances between members of the set rather than the phylogenetic tree itself. In Table 1, we represent the information contained in a phylogenetic tree in Fig. 1 as a 55 matrix. To calculate D(1, 2, 3) via this method, note that the maximum distance is between 3 and 1 (or 2), which is 2A+2B. Adding in the nearest neighbor distance between 2 (or 1) and the set consisting of 3 and 1 (or 2) is 2A, half of which is A. Therefore, D(1, 2, 3)=2A+2B+A=3A+2B, as stated above. We recorded the branch lengths from the phylogenetic tree of Sibley and Ahlquist in a 147147 matrix of the pairwise distances (taxonomic distinctness) between genera in our sample (available on request from the authors). Because of the nature of the data, there was considerable redundancy in this matrix. For example, all genera in the largest family, Fringillidae, are equidistant from all genera in all other families of the Passeroidea. 2.3. Prioritization algorithm In previous work, we compared the eciency and spatial solutions of several dierent reserve selection algorithms (Csuti et al., 1997). Optimization algorithms from operations research, usually based on branch-andbound integer programming techniques, can often nd slightly better solutions than iterative heuristic algorithms, also known as ``greedy'' algorithms (e.g. Church et al., 1996; Pressey et al., 1996, 1997). However, optimization algorithms can present computational diculties (Pressey et al., 1996). In particular, it is dicult to solve optimization algorithms when the objective is to maximize a diversity measure based on the branch lengths of the phylogenetic tree for species represented in the set of chosen sites. For this reason, we have used a greedy heuristic algorithm to choose reserve sites. The greedy algorithm we use begins by picking the site with the greatest diversity value, or greatest number of genera, depending upon the objective. Next, it picks a second site that adds the greatest additional diversity (number of genera) to that already contained in the rst site. At
Table 1 55 distance matrix 1 1 2 3 4 5 0 2A 2(A+B) 2(A+B+C) 2(A+B+C) 2 2A 0 2(A+B) 2(A+B+C) 2(A+B+C)

each subsequent step, the algorithm picks the site that contributes the greatest increase in the diversity measure (number of genera) of any remaining sites, until the maximum diversity measure (number of genera) is achieved. The general pattern of site selection using a greedy algorithm or an optimization algorithm tends to be similar (Csuti et al., 1997). 3. Results In this section, we compare the results using the greedy algorithm applied to the reserve site selection problem, using the BBS distribution data and the Sibley and Ahlquist (1990) phylogenetic distance data, for the case when the objective is to maximize the number of represented genera versus the genetic diversity measure. Table 2 shows the results when the objective is to maximize the genetic diversity measure. It takes 15 sites to represent all 147 genera using the greedy algorithm to maximize the increase in the genetic diversity measure at each step. Much of the diversity is represented after the rst few sites are included. The rst site represents 58% of the diversity present in the 147 genera. Over 90% of the total diversity is represented with six sites. The percentage of genera represented is slightly lower: 50% in one site and 87% in six sites. The diversity accumulation curve, which illustrates the rapid initial accumulation and the slower approach to complete representation, is shown in Fig. 2. Table 3 shows the results when the objective is to maximize the number of genera represented. Not surprisingly, selecting sites to maximize the increase in the number of genera represented at each step as compared to selecting sites to maximize the increase in diversity at each step results in initially faster accumulation of genera represented but less diversity. It is surprising, however, that it takes more sites, 16 versus 15, to represent all genera. This result is an artifact of using the greedy algorithm on this particular data set. Using an algorithm that could nd the minimum number of sites to represent all genera would result in a solution with 15, or possibly fewer, sites in total. The accumulation curve when maximizing the increase in the number of genera represented at each step is shown in Fig. 3. The general pattern is similar to that shown in Fig. 2.

3 2(A+B) 2(A+B) 0 2(A+B+C) 2(A+B+C)

4 2(A+B+C) 2(A+B+C) 2(A+B+C) 0 2E

5 2(A+B+C) 2(A+B+C) 2(A+B+C) 2E 0

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Table 2 Accumulation of diversity and genera when prioritizing for phylogenetic distance Site number 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Diversity measure 352.4 433.7 471.8 503.8 527.3 548.2 562.3 572.3 579.4 584.8 589.7 594.3 597.3 600.2 602.2 Number of genera 74 93 102 113 118 128 133 137 139 141 143 144 145 146 147

While the sites highlighted in Figs. 4 and 5 are indicative of high priority sites for US breeding birds, it is important to be cautious about using these results in deriving actual conservation strategies. A system of reserves to conserve avifauna would also need to consider migratory stopovers and wintering areas (some of which lie outside the US). The results are based on the current presence of species at sites but do not take into account the quality of habitat at various sites and whether viable populations can be maintained at a given site. These results also do not say anything about priority sites for other taxonomic groups. 4. Discussion The results of choosing reserves on the basis of a diversity measure based on phylogenetic diversity versus simple richness are remarkably similar. The set of sites chosen under the two objectives largely overlaps. The pattern of accumulation under the two objectives is also quite similar. These results suggest that the more complicated objective of maximizing phylogenetic diversity represented in a reserve network is reasonably well accomplished simply by representing the maximum richness in the network. Although these results arise from a data set using a specic taxonomic group (birds) in a specic geographic area (the US, excluding Alaska and Hawaii), there is reason to believe that the similarity of results under the two dierent objectives is more general. Following from the denitions of the two measures, richness and phylogenetic diversity at a site (or collection of sites) should

The spatial pattern of the sites selected by the two algorithms is shown in Figs. 4 and 5. It is striking how similar the geographic pattern of the selections is using the two objectives. The same site was selected rst under both objectives. Overall, 12 sites were chosen under both objectives, though not always in the same order. For example, the second site selected for maximizing richness was selected sixth when maximizing phylogenetic diversity. Both solutions display the inuence of the principle of complementarity (Pressey et al., 1993). Sites chosen tend to sample distant and ecologically divergent regions, presumably with considerably dierent avifaunas. In both solutions, sites in close proximity to earlier selections were chosen late in the selection process.

Fig. 2. Accumulation curve when prioritizing for phylogenetic distance.

S. Polasky et al. / Biological Conservation 97 (2001) 99105 Table 3 Accumulation of diversity and genera when prioritizing for the number of genera Site number 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 Diversity measure 352.4 420.8 462.7 494.8 511.9 535.4 545.4 554.3 561.6 568.7 587.0 589.0 592.0 594.7 599.3 602.2 Number of genera 74 96 106 116 124 129 133 136 138 140 142 143 144 145 146 147

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be positively correlated. As more taxa are progressively added both richness and phylogenetic diversity will increase. Measures that do not use branch length but are based on the number of branching nodes, such as used by Vane-Wright et al. (1991), also increase as taxa are added and should be positively correlated to richness as well. The results of Nee and May (1997) show that increasing the number of species conserved increases phylogenetic diversity conserved (see especially Fig. 2, Nee and May 1997, p. 693). Because sites that have more genera tend to have greater phylogenetic diversity, the same set of sites would tend to be selected regardless of which objective is used. For this not to be the case,

those sites with relatively many genera must also have relatively closely related genera so that the greater number of branches represented by the greater number of genera still translates into small total branch length. For example, Hacker et al. (1998) report that Madagascar scores well relative to continental sites on taxon richness for African primates but scores poorly on character diversity, which is based on the number of branching nodes in an evolutionary tree, because only lemurs are present. In general, however, both Williams and Humphries (1996) and Hacker et al. (1998) found that taxon richness and character diversity showed a similar pattern across sites. Looking at the geographic distribution of the sites selected by either solution shows that a majority of the selected sites were on the coast or near the borders of the US with Mexico or Canada. Few sites were selected from the interior. The selection of sites at the periphery of the study area most likely reects the presence of peripheral species at the edge of their range. Two sites in Florida, two in Texas, and two in Arizona all are likely to contribute regular records of tropical species (trogons, parrots, anhingas) at the northern edge of their range. For this reason, it is important to consider the results of a study of one geographic area, particularly when based on political rather than biogeographic boundaries, in the context of studies of other areas. Consideration of conservation eorts in other places (e.g. Canada, Mexico, or the Caribbean) may well change conservation priorities in the US We agree with May (1990), Vane-Wright et al. (1991), and others that phylogenetic dierence between taxa merits recognition when selecting biological reserves. However, as a practical matter, taxonomic richness may

Fig. 3. Accumulation curve when prioritizing for number of genera.

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Fig. 4. Sites selected when prioritizing for phytogenetic diversity.

Fig. 5. Sites selected when prioritizing for genus richness.

serve as a good proxy for phylogenetic diversity for the purpose of choosing reserve sites. Given that data on richness is both more available and easier to work with than data on phylogenetic diversity, those that work on setting conservation priorities need not be defensive about maximizing richness as their objective.

Acknowledgements This research was made possible by a grant for the study of Decision Making and Valuation for Environmental Policy from the US Environmental Protection Agency/National Science Foundation to Woods Hole

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Oceanographic Institution's Center for Marine Policy. Additional funding was provided by the Strategic Environmental Research and Development Program to support activities of the Biodiversity Research Consortium. We thank Dr. Raymond J. O'Connor, Department of Wildlife Ecology, University of Maine, Orono, for providing compiled Breeding Bird Survey data. References
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