Animal Conservation.

Print ISSN 1367-9430

Prioritizing the worlds islands for vertebrate-eradication programmes

M. de L. Brooke1, G. M. Hilton2 & T. L. F. Martins3
1 Department of Zoology, University of Cambridge, Cambridge, UK 2 Royal Society for the Protection of Birds, Sandy, Bedfordshire, UK 3 Centre for Ecology and Conservation, University of Exeter in Cornwall, Tremough, Penryn, UK

Keywords rats; cats; goats; restoration; Red List birds. Correspondence M. de L. Brooke, Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK. Tel: 01223 336610; Fax: 01223 336676 Email: m.brooke@zoo.cam.ac.uk Received 4 May 2007; accepted 17 May 2007 doi:10.1111/j.1469-1795.2007.00123.x

Abstract
In the last 400 years, more species have become extinct on small islands than on continents. Yet, scant attention has hitherto been paid to prioritizing island restorations. Nevertheless, considerable conservation effort is now devoted to removing a major cause of these extinctions invasive alien vertebrates. Because modern techniques allow the clearance of invasive vertebrates from quite large islands (up to 1000 km2), many islands are candidates for restoration. A robust strategy for allocating available funds is urgently needed. It requires, for each candidate island, an objective estimation of conservation gain and a method for predicting its nancial cost. Our earlier work showed that a good rst-pass estimate of vertebrate eradication costs can be made using just island area and target species. Costs increase with island area, while rodents are more expensive per unit area than ungulates. Here, we develop a method for assessing the conservation benet of a proposed eradication and apply the method to threatened birds, but not other taxa. The method, combining information on how threatened a species is, on the impact of alien vertebrates on that species and on the islands on which the species occurs, allows us to present a means of determining which islands yield the greatest conservation benet per unit of expenditure on vertebrate eradication. In general, although greater overall benet would accrue to birds from eradication of invasive vertebrates on larger islands, benet per unit of expenditure is the highest on relatively small islands, and we identify those that should be priority targets for future eradications. Crucially, this quantitative assessment provides considerable efciency gains over more opportunistic targeting of islands. The method could be adapted to prioritize islands on a regional or national basis, or with different conservation gains in mind.

Introduction
From the dodo (see Supplementary Material Appendix S1 for species scientic names) of Mauritius to the moas Dinornithidae of New Zealand, there are countless examples of island bird species that have suffered grievous population reductions after the rst arrival of people at the islands where they evolved. It is no surprise then that the majority (111/127) of bird species known to have become extinct since 1500 are island endemics (Brooks, 2000). Similar, if less extreme, extinction bias towards island species is evident among other life forms (Baillie, HiltonTaylor & Stuart, 2004). For example, 219 of 599 plant taxa that have become extinct since 1600 are island taxa (Smith et al., 1993). In large measure, this devastation of island biotas has been caused by overkill, habitat damage and invasive alien species, coupled with synergistic interactions between the
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former three (Diamond, 1989). Habitat restoration is a major challenge for the future. Overkill can, in theory, be stopped by the development of effective management regimes, but both may fail to achieve population recovery if a species survival and/or fecundity are depressed by alien species. When alien species are removed from islands, threatened species often benet (Clout, 2001). Such removal is often a practical option because islands are, by denition, of generally modest area and because their isolation reduces, even if it does not eliminate, the chance that the removed alien species will re-establish themselves. Thus, the one-off expenditure of a successful alien-eradication programme can lead to lasting conservation benets for native island species (Towns & Ballantine, 1993; Simberloff, 2003). Provided the costs of maintaining any effective quarantine measures are slight, this may often be a more cost-effective procedure than the alternative, namely controlling the populations of

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alien species in perpetuity. The latter entails incurring substantial recurrent costs (Simberloff, 2002). It may have the further humanitarian drawback of eventually causing the death of more individuals of both the alien and native species (Clout & Veitch, 2002). It is heartening that the ability to remove alien vertebrates from islands is improving apace and the maximum size of island where eradication is practical is growing ever larger (Nogales et al., 2004; Campbell & Donlan, 2005). These trends have been assisted by the development of anti-coagulant toxins and effective bait-delivery systems that now allow islands of up to ca. 100 and 300 km2 to be cleared of rats Rattus spp. and cats Felis catus, respectively (Cooper et al., 1995; New Zealand Department of Conservation, 2003). The upshot is that the number of islands where alien vertebrate eradication is a useful and realistic possibility is growing fast. It is therefore timely to start to develop an internally consistent scheme for prioritizing sets of islands for eradication programmes. The aim of such a list would be to indicate where scarce funds to save species could be spent with the greatest cost-effectiveness. Our paper makes an attempt to develop a method for producing such a list. We would not wish to assert that the lists that emerge from this exercise are denitive; rather, they create an opportunity to discuss the merits and shortfalls of our approach. Furthermore, the lists are deliberately global. If our methodology has any value, then it can equally be applied to other subsets of islands, based on political or biogeographical groupings. As a prioritization exercise, the paper follows the spirit of much academic conservation effort in asking where scarce funds might be spent, on Protected Area networks for example, to protect the most threatened species (Lombard, 1995; Ando et al., 1998). Our approach is conceptually simple. We calculate the cost of a projected eradication programme on a certain island, relying on data collected by Martins et al. (2006), and we calculate the conservation benet accruing from the successful execution of that programme (benet method described below). We then identify the islands where the conservation benet of successful alien vertebrate eradication is the greatest and, crucially, where the benet/cost ratio is the highest.

islands or continental areas, provided that, on the latter, the species was also threatened by alien vertebrates. The assessment of whether or not a species was threatened by alien vertebrates followed the BirdLife International World Bird Database (www.birdlife.org/datazone/index.html). The 1000 km2 cut-off was used because this is roughly the largest size of island from which eradication of vertebrates (i.e. goats) has been demonstrated to be practical with current techniques (Campbell, 2002). The cut-off is, however, substantially larger than islands that have hitherto been cleared of smaller problem vertebrates, such as rodents, rabbits and cats. The reason for the second criterion was as follows: if the key threat on the mainland is, say, habitat destruction, this can potentially be ameleriorated. If the key mainland threat is alien vertebrates, then these certainly cannot be removed, which means that the relative value of an island eradication increases. These restrictions deliberately exclude bird species not currently sharing any islands with threatening alien vertebrates. If aliens are not a threat, either because they are not found on the island(s) where the birds dwell or because they are believed to be harmless at present, then there is no case for eradicating them as a means of minimizing extinction risk. At this stage, we consider 130 qualifying bird species.

The islands
For each of the 130 bird species, we created a list of the island(s) on which they currently occur, again relying principally on information in the BirdLife International World Bird Database. There are 367 such islands (see justication in Supplementary Material Appendix S2). Twenty-six are larger than 1000 km2. Of the remainder, 270 have (and 71 lack) alien vertebrates. The former 270 (see Supplementary Material Appendix S3) form the island-set from which we select priorities for alien eradication. The latter 71 are islands on which globally threatened bird species are found that are not single-island endemics and that, on at least one of their other occupied islands, co-occur with alien vertebrates. For each of the 367 islands, we assembled information on the factors known to affect signicantly the cost of a proposed eradication (Martins et al., 2006). These are the islands area and the alien vertebrate species occurring and hence to be eradicated. Subsequent analysis has shown latitude also to be important.

Methods
The species
The method we shall describe uses only avian data to assess the conservation benet of a projected programme because our method requires precise information on which species are to be found on which island. Information at this level of detail across an entire taxonomic group for the whole world is readily available only for birds. Our rst step was to take the 2004 list of globally threatened birds (BirdLife International, 2004). From this list, we then selected (1) species occurring exclusively on islands o1000 km2 and threatened by alien vertebrates, (2) species occurring both on islands o1000 km2, and on larger

Estimating the costs

The 296 islands with aliens (including those larger than 1000 km2) harbour different combinations of alien species. On the basis that different eradication techniques are typically used for different types of alien species (Courchamp, Chapuis & Pascal, 2003), we divide the aliens into four categories as follows: (1) ungulates, most commonly goats; (2) carnivores, most commonly cats, dogs and mongooses (also includes possums, monkeys and hedgehogs);
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Vertebrate eradication programmes

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(3) rodents, namely rats, mice and rabbits; and (4) birds. Further analysis of the data collected by Martins et al. (2006) revealed a latitudinal effect on the cost of eradications. With latitude treated as a categorical variable, and all other variables from the Martins et al. (2006) GLM (table 2 in Martins et al. 2006) retained, islands located below 301 of latitude were signicantly (P= 0.028) more costly than islands situated above 301, while all other variables from the original GLM remained signicant and only marginally altered. Using this information, we were able to calculate, for an island of given area, the cost of eradicating aliens in a particular category. Because Martins et al. (2006) provided no estimate of the cost of eliminating birds, the bird cost was, in the absence of better information, calculated using the mean of the intercepts calculated for rodents, cats and ungulates. Specically, where costs are measured in year 2003 US dollars and island area in square kilometres:

species is (T ); and on the number of other islands, and their relative areas, occupied by the species (I ) and whether they too have alien vertebrates: (i) Impact severity (S ). This score is based on the assessment by BirdLife International (www.birdlife.net/datazone) of the severity of impact that alien vertebrates are having on a threatened bird species in those parts of the range where the threatened species co-occurs with the invasive(s). The categories are no decline, negligible decline, slow decline, rapid decline and very rapid decline. We scored these as 15, respectively. Hence, even if the threat does not cause a decline ( = no decline), there is some value to removing the threat, because it may still limit the population, or inhibit recovery. Two further categories of severity score are unknown and uctuations both of which were ranked as 1. Where the species was threatened by more than one type of threat from invasive vertebrates, we used the highest severity score.

Log ungulate cost 4:1728 0:14623 island latitude 0:80856 Log10 island area Log carnivore cost 4:4344 0:14623 island latitude 0:80856 Log10 island area Log rodent cost 4:3498 0:14623 island latitude 0:80856 Log10 island area Log bird cost 4:3190 0:14623 island latitude 0:80856 Log10 island area where island latitude is scored as 0 when within 301 of the equator, and 1 when beyond 301. We made the important assumption that the cost of ridding a given island of more than one species within one category, say rats and rabbits, would be the same as eliminating just one such species. This also entails the assumption that the costs of mouse and rat eradications are similar. While mouse eradications could be more costly because of the need for higher bait-application rates, this has not been tested critically. Then, to work out the total cost of eradicating all the alien vertebrates from an island, we assumed that the costs of removing aliens from different categories were additive. This is probably not strictly accurate, because there are generally likely to be logistic economies that arise when species from more than one category are targeted together, but we know of no basis for assessing the extent of those economies. We could now calculate a predicted total cost of eradicating all the alien species on the island, and used this as the denominator when, later in the paper, we calculate benet: cost ratios.

Estimating the benets

The global conservation gain deriving from the eradication of alien vertebrates was separately estimated for each qualifying threatened bird species, on each of the islands on which it lives. Conservation gain of eradicating invasive alien vertebrates from an island on which a given species occurs depends on the severity of the impact of the alien vertebrate(s) on that species (S ); on how highly threatened the
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Because this classication is a single number for each bird species, it fails to reect differences in impact severity between the several islands on which a threatened bird lives, and the different sets of alien vertebrates that it encounters. (ii) Threat score (T ). Although many analyses of factors that inuence species extinction risk (e.g. Purvis et al., 2000; Keane, Brooke & Mcgowan, 2005) use a simple linear approach (Vulnerable species scoring 1, Endangered 2 and Critically Endangered 3), the approach perhaps does not accurately reect the relative quantitative extinction risk of species in the three categories. This relative risk has been assessed, for Vulnerable:Endangered:Critically Endangered species, as 0.005:0.05:0.5, respectively (Butchart et al., 2004), and these are the values we use. They are not signicantly correlated with the species S scores (Pearsons correlation r = 0.032, n =130, NS). (iii) Island score (I ). Our starting point is that removing alien vertebrates from the sole island occupied by a single island endemic confers greater conservation benet than does removing vertebrates from one island among many that are occupied by another species. Thus, the marginal benet of eradication on a particular island decreases the more islands a species occupies, but never declines to zero, because the overall extinction risk for the species is still reduced, to a small degree, by ensuring that at least one (more) island among the few or many a species may occupy is free of aliens. These considerations are reected in two possible scores. The rst, I1, estimates the proportional increase in the number of predator-free islands occupied by the species

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M. de L. Brooke, G. M. Hilton and T. L. F. Martins

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following a given eradication: % of species islands free of aliens after % of species islands free of aliens before successful eradication on island X successful eradication on island X I1 % of species islands free of aliens before 1 successful eradication on island X While I1 captures the fact that it becomes progressively less worthwhile to clear further islands, once a threatened species is provided with several alien-free islands, it takes no account of the relative areas of the islands cleared. All else being equal, it may benet a threatened species more if aliens are cleared from one of the larger islands it occupies than one of the smaller islands. (Arguably, this is more relevant for landbirds than for colonial seabirds, which can cluster in large numbers in small areas.) This consideration is reected in our second island score, which estimates the proportional increase in predator-free space occupied by the species, following a given island eradication:

Determining the priority lists

It was then possible to produce ranked lists of candidate islands based on conservation benet (overall reduction in extinction risk among the species-set), or on benet:cost ratio (reduction in extinction risk per dollar spent). The initial lists of islands based on benet:cost ratios take no account of the fact that, once one island where a particular threatened bird species occurs is cleared of alien vertebrates, the conservation benet of removing alien vertebrates from further islands on which the species dwells might be considered to be lower. Recognizing this consid-

% of species range free of aliens after % of species range free of aliens before successful eradication on island X successful eradication on island X I2 % of species range free of aliens before 1 successful eradication on island X The values for I1 and I2 span some three and six orders of magnitude, respectively, large in comparison with the values for S and T, which span one and two orders, respectively. Therefore we also apply square roots to I1 and I2 to reduce the variation to one and three orders of magnitude, respectively. The impact of increasing the variation among S scores is considered in Results. For each species on each island on which it occurs, we then combined these three factors (Severity, Threat and Island score) multiplicatively. This means that the benet of an eradication programme is the greatest for species facing the severest alien impact; that are most highly threatened with extinction; that occur on one or few islands; and that have alien vertebrates on most or all the islands that they inhabit. Because island scores are scored in two ways and with/without square rooting, we were now able to generate, for each species on each island, one of four possible species scores. The overall benet (B) of eradicating aliens from any of the 270 candidate islands is thus:
in X i1

Species score

eration, we also re-calculated the top 20 lists, taking account of any island clearances higher in the list that affected the conservation benet of a proposed eradication on an island lower in the list. This approach is conceptually identical to a complementarity approach for reserve selection, whereby the value of providing a new reserve for a species diminishes once that species is already protected in one (or more) reserve(s) (Lombard, 1995; Howard et al., 1998). The complementarity lists were calculated by extracting the top-ranking island from the list, and assuming that, by virtue of an eradication project, it was now free of alien vertebrates. This automatically changed the benet scores for all other islands that share species with the extracted island. A new ranked list was then generated using these altered benet scores, and this procedure was iterated. To assess the degree to which our approach delivered improvements in efciency, 20 islands were drawn at random from the total list of 270 islands 500 times. The averaged benet:cost ratios of these random islands results could then be compared with the benet:cost ratios of those islands where the benet was the highest and those where the benet:cost ratio was the highest.

where n is the number of threatened bird species occurring on that island. B1 is calculated using species scores; S TI1 p B2 is calculated using species scores; S T I1 B3 is calculated using species scores; S T I2 p B4 is calculated using species scores; S T I2

Results
Ranking of islands by conservation benet
The 270 islands in our nal island-set vary in area between 979 km2 Santa Cruz (Galapagos), whose estimated restoration cost is 22 300 000 USD, and 1 ha Eboshi-Jima, ve orders of magnitude smaller and four to ve orders less
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Vertebrate eradication programmes

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Table 1 Lists of the worlds top 20 islands, with areas o1000 km2, ranked in terms of conservation benet to threatened birds arising from the eradication of alien vertebrates from those islands Benet score Rank 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 B1 Fatu Hiva Guadalupe Madeira Socorro Robinson Crusoe Sao Tome Chatham Grenada Nuku Hiva Amsterdam Norfolk Rota Pohnpei Floreana Santa Cruz (Galapagos) San Cristobal Santiago Moheli Anjouan (= Ndzuani) Sangihe (Siau) B2 Fatu Hiva Guadalupe Madeira Socorro Chatham Robinson Crusoe Sao Tome Grenada Floreana Santa Cruz (Galapagos) San Cristobal Santiago Nuku Hiva Amsterdam Norfolk Rota Fregate Pohnpei Moheli Anjouan ( =Ndzuani) B3 Fatu Hiva Guadalupe Madeira Chatham Socorro Robinson Crusoe Sao Tome Grenada Nuku Hiva Amsterdam Norfolk Rota Mahe Pohnpei Moheli Anjouan (= Ndzuani) Sangihe (Siau) Rangiroa Santa Cruz (Galapagos) Fregate B4 Fatu Hiva Guadalupe Madeira Socorro Chatham Robinson Crusoe Sao Tome Grenada Nuku Hiva Amsterdam Santa Cruz (Galapagos) Rangiroa Santiago San Cristobal Norfolk Rota Mahe Menorca Pohnpei Moheli Summed ranks Fatu Hiva Guadalupe Madeira Socorro Chatham Robinson Crusoe Sao Tome Grenada Nuku Hiva Amsterdam Norfolk Santa Cruz (Galapagos) Rota Pohnpei San Cristobal Santiago Anjouan ( =Ndzuani) Mahe Moheli Sangihe (Siau)

The benets are calculated in four ways as explained in the text. The nal column shows ranking when ranks across all four calculation methods are summed.

costly. Most of the islands support a single bird species from our species-set, while Auckland Island (sub-Antarctic, New Zealand) holds a maximum of ve species. Table 1 shows the islands where the greatest conservation benets will accrue from the eradication of alien vertebrates. The top-ranked island for conservation benet score is Fatu Hiva in the Marquesas, which supports two seabirds: Polynesian storm-petrel (Vulnerable) and Phoenix petrel (Endangered), plus Fatuhiva monarch (Critically Endangered) and ultramarine lorikeet (Endangered). It is followed by Guadalupe, off western Mexico, home to two Critically Endangered single-island endemics (Guadalupe junco, Guadalupe storm-petrel) and a further Vulnerable species: the black-vented shearwater. The lowest-ranking islands, not shown in Table 1, are those supporting a single Vulnerable species that inhabits a large number of other islands, for example islands in the Falklands supporting Cobbs wren, and in the central Pacic supporting Polynesian stormpetrel. Two other points stand out in Table 1. The rst is that, despite calculating the benets in various ways, the same islands repeatedly re-appear in the top 20 lists. Indeed, 15 islands appear in each of the four lists. In total, the lists contain just 24 islands (Table 2), out of a maximum possible of 80. The full ranked lists of all 270 islands are highly correlated with one another. Correlations of island rankings between the six possible pairs of lists are consistently high (Table 3a). The second point is that these 24 islands are mostly relatively large islands (median area = 329 km2)
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where several threatened bird species co-occur. While highly benecial, alien eradication would neither be easy nor cheap at such sites.

Ranking of islands by conservation benet per unit cost

Our next step was to rank islands according to conservation benet per unit of eradication expenditure. The full lists are shown in Supplementary Material Appendix S3. Correlations of island rankings between the six possible pairs of lists were again high (Table 3b). It is evident from the lists in the supplementary materials that some individual threatened species occur repeatedly on several of the top-ranked islands, whichever of the four ways they are calculated. This is most obvious for several Seychelles endemic species occurring, for example, on Aride, Cousin and Cousine, and for Balearic shearwater breeding on Bosc, Malgrats and other islands in the Balearic archipelago. To circumvent the issue of whether, once one (or more) of a species islands become alien-free, the value of eradication programmes on further islands inhabited by the species diminishes, a complementarity analysis was undertaken. This analysis (Tables 4 and 5) reduces but does not eliminate multiple occurrences of the same species in the top 20 list. In marked contrast to the islands that are ranked the highest for overall conservation gain, those that are highly ranked for conservation benet:cost ratio are mostly small (median area of the 38 islands in Table 5 = 2.2 km2). Seabird

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Table 2 Some features of the 24 islands appearing in Table 1 Islands Amsterdam Anjouan (= Ndzuani) Chatham Fatu Hiva Floreana Fregate Grenada Guadalupe Madeira Mahe Menorca Moheli Norfolk Nuku Hiva Pohnpei Rangiroa Robinson Crusoe Rota San Cristobal Santa Cruz (Galapagos) Sangihe Santiago Sao Tome Socorro Location Southern Ocean Comoros No. of threatened bird Area species (km2) 1 1 881 433 745 78 173 2 323 264 750 154 693 205 37 345 334 44 93

Table 3 Pearsons correlation coefcients across 270 candidate islands for the various measures of benets used (see text for further details) B1 (a) For the benet scores B1 B2 0.872 B3 0.718 B4 0.751 (b) For the benet:cost scores B1 B2 0.913 B3 0.589 B4 0.788 All signicant Po0.001. B2 B3 B4

Off New Zealand 4 Marquesas, S. 4 Pacic Galapagos 3 Seychelles 3 West Indies 1 Off W. Mexico 3 Sub-tropical Atlantic 1 Seychelles 4 W. Mediterranean 1 Comoros 1 W. Pacic 3 Marquesas, S. 4 Pacic Micronesia (Faichuck 2 group) Tuamotus, French 3 Polynesia 3 Juan Fernandez group, off central Chile Marianas, W. Pacic 3 Galapagos 3 Galapagos 4 Indonesia Galapagos Gulf of Guinea Off W. Mexico 1 3 4 3

0.663 0.830

0.932

0.461 0.834

0.821

96 547 979 552 585 855 190

The islands are listed alphabetically. The number of threatened bird species is the number on the island facing adverse impacts from introduced vertebrates and therefore may, in some cases, be lower than the number of threatened bird species on the island.

colonies are frequently located on such small, often remote islands and, although seabirds comprise about three percent of the worlds bird species, 12 of 41 species in Table 5 are seabirds. Only three islands (Cousin, Cousine and Fatu Hiva) appear in all four complementary lists in Table 4, which, in total, contain 38 islands out of a maximum 80. The top 20 lists generated using B2 and B4 are quite similar. The lists generated by applying B1 and B3 are more divergent from each other and also from the B2 and B4 lists, mainly because the B1 and B3 top-ranked islands tend to be larger, and indeed include several islands larger than 100 km2. Not only are such islands at the limit of what is practical for rodent eradication using present-day technology, they are also inhabited, a feature that militates against embarking on eradication projects. The Table 5 islands are very often sites where only one or two threatened species occur, and the overall benet of

eradication is not especially large. Benet:cost ratios seem to be the highest on islands with relatively low benet scores, but that are small and therefore cheap. Consequently, there is only limited overlap between the islands appearing in Tables 1 and 2 on the one hand and Tables 4 and 5 on the other. In fact, only 13 islands appear in both top 20 benet and complementarity-based benet:cost sets. The greater emphasis on small islands, which may be one of the several on which a species occurs, delivered by the application of B2 and B4 is a consequence of square-rooting the island scores. The effect of doing this is to reduce the relative benet of restoring islands that comprise a large part of the species range, thereby emphasizing small, cheap islands with highly threatened species. We also explored the impact of increasing the range of variation in the (essentially arbitrary) S score (varies from 1 to 5 in results hitherto presented), but found that multiplying T and I scores by S2 instead of S had a negligible effect. For example if adjusted B4/total cost rankings are generated using S2 and then compared, for all 270 islands, with those obtained using S (as was done in Supplementary Material Appendix S3), the correlation between island ranks is 0.97 (Pearsons correlation on ranked benet:cost scores, n =270, Po0.001). To assess whether our prioritization approach delivers signicant cost efciency gains, we calculated the aggregate cost of eradicating vertebrates from the top 20 islands ranked in various ways. The benet scores used were B3 and B4 (see Discussion for particular merits of these scores). The results are presented in Table 6, which shows that targeting islands on the basis of their benet:cost ratios delivers an efciency gain (in terms of conservation benets per unit of expenditure) of two to seven times compared with targeting the islands where the benets are the greatest, and of six to 18 times compared with picking islands at random from the listed islands, which, it must be noted, are themselves a highly selected group. Comparable efciency gains are evident with B1 and B2 instead of B3 and B4 (results not shown). Because the complementarity approach entails adjusting benet scores downwards to account for islands already cleared, it is accompanied in Table 6 by a slight reduction in apparent efciency.
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Table 4 Complementarity lists of the worlds top 20 islands, with areas o1000 km2, ranked in terms of conservation benet per unit of expenditure on eradicating all alien vertebrate species present on the island Benet:cost index Rank 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 Island area (km2) Median Range B1/total cost Cousin Conception Teraina (= Washington) Open Bay Malgrats Fatu Hiva Robinson Crusoe Bosc Cousine Vedranell Isla Pan de Azucar Espartar Norfolk Eboshi-jima Henderson Socorro Guadalupe Aguijan Moheli Illa de lAire 0.30 0.01264 B2/total cost Cousin Malgrats Bosc Vedranell Espartar Illa de lAire Conception Cousine Teraina (= Washington) Eboshi-jima Open Bay Conillera (Eivissa) ` Vedra Conillera (Cabrera) Birnie Aride Tagomago Isla Pan de Azucar Fatu Hiva Dragonera 0.26 0.0178 B3/total cost Aride Fatu Hiva Robinson Crusoe Norfolk Rangiroa Henderson Socorro Guadalupe Moheli Grenada Madeira Cousine La Vieja Anjouan (=Ndzuani) Rota Mohotani Niuafoou Nuku Hiva Cousin Sangihe (Siau) 78 0.2749 B4/total cost Cousin Cousine Aride Malgrats Bosc Vedranell Espartar Illa de lAire Fatu Hiva Conillera (Eivissa) Matureivavao Conillera (Cabrera) Conception Dragonera Robinson Crusoe Fregate ` Vedra Isla Pan de Azucar Norfolk Tagomago 0.80 0.178

The benets are calculated in four ways (B1B4), with each islands benet recalculated on the basis of a successful eradication on any island(s) placed higher in the list. Islands 4100 km2 are shown in bold.

Discussion
Our aim has been to outline how a worldwide prioritization scheme for island restoration might be developed. This should facilitate raising funds for eradication projects across the world because islands that consistently appear towards the top of such quantitatively calculated lists are clearly high global priorities. It falls to the conservation community to impress upon donors the merits of a strategic approach that delivers striking efciency gains (Table 6), and for the two groups to work in partnership to secure the well-being of the key islands for posterity. Furthermore, the approach is malleable and provides a conceptual framework that can be re-worked to deliver national or regional priorities, or assess different taxa. In general, the islands where the conservation benet of eradication would be the greatest are relatively large (Tables 1 and 2). This is as anticipated because some such islands hold several threatened species, whereas smaller islands generally hold only one or two. Because these islands are large and typically inhabited, then some sort of conservation activity, but not necessarily vertebrate eradication, is already underway on most of them. However, a consistent output of the ranking process described is that large islands tend to score less highly when benet, howsoever calculated, is divided by cost (Tables 4 and
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5 and Supplementary Material Appendix S3). This pattern does not arise because we fail to account for the fact that eradication on larger islands would be helping a larger proportion of the species population (and thereby reducing extinction risk by a greater margin); the B3 and B4 scores do precisely this. Moreover, this selection of smaller islands arises despite the fact that costs per unit area decrease with area (Martins et al., 2006). Rather, the result arises because total costs tend to increase with area more rapidly than the benets. It was striking that the list of islands selected as leading candidates for eradication projects was not greatly inuenced by the different Island (I) scores we used (see Methods). Both I1 and I2 explicitly take into account islands that a species occupies that are already free of alien vertebrates, the former by taking account of the percentage increase in the number of predator-free islands that a proposed eradication would achieve, and the latter by taking account of the percentage increase in the predator-free area a proposed eradication would achieve. It may be that I1 is the more appropriate metric for seabirds where population size is often not closely correlated with island area and large, viable populations can persist on small islands, while I2 is the better metric for landbirds whose population size is more likely to be limited by island area. Re-introduction of alien species to cleared islands, either naturally (especially relevant for birds) or via anthropogenic

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Table 5 An alphabetically arranged list of the islands of Table 4, showing their location, the threatened bird species facing adverse impacts from the alien vertebrates that occur on them, whether they are (y) or are not (n) inhabited, and their areas Island Aguijan Anjouan (= Ndzuani) Aride Birnie Bosc Conception Conillera (Cabrera) Conillera (Eivissa) Cousin Cousine Dragonera Eboshi-jima Espartar Fatu Hiva Location Marianas, W. Pacic Comoros, Indian Ocean Seychelles Kiribati Balearics, W. Mediterranean Seychelles Balearics, W. Mediterranean Balearics, W. Mediterranean Seychelles Seychelles Balearics, W. Mediterranean Off Kyushu, Japan Balearics, W. Mediterranean Marquesas Threatened bird species Nightingale Reed-warbler, Guam Swiftlet, Micronesian Megapode Anjouan Scops Owl Seychelles Magpie-robin, Seychelles Fody Polynesian Storm-petrel, Phoenix Petrel Balearic Shearwater Seychelles Kestrel, Seychelles White-eye Balearic Shearwater Balearic Shearwater Seychelles Magpie-robin, Seychelles Fody Seychelles Magpie-robin, Seychelles Fody Balearic Shearwater Japanese Murrelet Balearic Shearwater Polynesian Storm-petrel, Phoenix Petrel, Ultramarine Lorikeet, Fatuhiva Monarch Seychelles Fody, Seychelles Magpie-robin Grenada Dove Guadalupe Junco, Guadalupe Stormpetrel, Black-vented Shearwater Henderson Petrel, Henderson Rail, Henderson Reed-warbler Balearic Shearwater Peruvian Diving-petrel Peruvian Diving-petrel Zinos Petrel Balearic Shearwater Tuamotu Sandpiper, Polynesian Ground-dove Moheli Scops Owl Polynesian Storm-petrel, Phoenix Petrel, Marquesan Monarch Polynesian Megapode Norfolk Island Green Parrot, Whitechested White-eye, Slender-billed White-eye Polynesian Storm-petrel, Phoenix Petrel, Ultramarine Lorikeet, Marquesan Imperial Pigeon Fiordland Crested Penguin Tuamotu Sandpiper, Blue Lorikeet, Polynesian Ground-dove Dellipis Petrel, Pink-footed Shearwater, Juan Fernandez Firecrown Micronesian Megapode, Mariana Crow, Rota Bridled White-eye Sangihe White-eye Balearic Shearwater Alien vertebrates R, C, U R B R R R, B R R B B R R R R, C Inhabited? n y y n n n n n y y n n n y Area (km2) 7 433 1 0.20 0.17 0.60 1.56 1.05 0.20 0.26 2.88 0.01 0.20 78

Fregate Grenada Guadalupe Henderson Illa de lAire Isla Pan de Azucar La Vieja Madeira Malgrats Matureivavao Moheli Mohotani Niuafoou Norfolk

Seychelles Caribbean Off W. Mexico Central S. Pacic Balearics, W. Mediterranean Off N. Chile Off Peru N. Atlantic Balearics, W. Mediterranean Tuamotus, French Polynesia Comoros Marquesas Tonga group, W. Pacic W. Pacic

R, C, B R, C C, U R R R, C R, C R, C, U R R, C R R, C, U, B C, U R, C, U, B

y y y n n n y y n n y y y y

2.2 323 264 37.3 0.31 1.1 12 749 0.09 15 205 12.2 52.3 36.8

Nuku Hiva

Marquesas

R, C, U

345

Open Bay Rangiroa Robinson Crusoe

Westland, New Zealand Tuamotus, French Polynesia Juan Fernandez group, off Chile

R, C, B R, C R, C, U

n y y

0.15 44 93

Rota Sangihe (Siau) Tagomago

Maraianas, W. Pacic Indonesia Balearics, W. Mediterranean

R, C, U, B R R, C

y y y

95.7 552 0.63

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Table 5. Continued. Island Teraina (Washington) ` Vedra Vedranell Location Kiribati, central Pacic Balearics, W. Mediterranean Balearics, W. Mediterranean Threatened bird species Polynesian Storm-petrel, Phoenix Petrel, Kuhls Lorikeet Balearic Shearwater Balearic Shearwater Alien vertebrates R, C, U R, U R Inhabited? y n n Area (km2) 0.15 0.63 0.17

R, rodents, C, carnivores; B, birds; U, ungulates (see Methods).

Table 6 Benet:cost (B:C) ratios of eradicating vertebrates from various lists of islands Cost C (USD) Islands assessed using B3 metric Random 20 islands Top 20 islands ranked by B3 (see Table 1) Top 20 islands ranked by B3/cost (see Supplementary Material Appendix S3) Top 20 islands ranked by B3/cost with complementarity applied (see Table 3) Islands assessed using B4metric Random 20 islands Top 20 islands ranked by B4 (see Table 1) Top 20 islands ranked by B4/cost (see Supplementary Material Appendix S3) Top 20 islands ranked by B4/cost with complementarity applied (see Table 3) 31 200 000 118 000 000 41 800 000 52 000 000 Benet B (arbitrary units) 1526 2082 1440 1550 B:C 106 4.89 17.6 34.4 29.3 Relative improvement compared with random N/A 3.6 7.0 6.0

31 200 000 141 000 000 5 400 000 5 900 000

222 230.2 61.4 53.6

0.624 1.64 11.4 9.08

N/A 2.6 18.3 14.6

activity, is a risk we could not quantify, and therefore was not considered. However, in our view, the probability of recolonization should not be part of the benet:cost prioritization procedure. Rather, a truly denitive island-set should exclude a priori any islands for which re-colonization is considered to be an unavoidable and signicant likelihood. Many of the islands in the tables are both uninhabited and isolated and, provided due caution is maintained by any human visitors, unlikely to be re-colonized. However, the likelihood of re-colonization should be very carefully considered when project decisions are made. For this reason, we doubt whether ridding the highly ranked Seychelles islands of Aride, Cousin and Cousin (Table 4) of alien birds such as Indian mynahs and barn owls should be given the high priority the lists suggest. The prioritization exercise described here gives an objective means of developing a list of candidate islands that is ranked according to conservation benet:cost considerations. Clearly, secondary lters need to be applied subsequently to this list. Other issues, social, political and biological, must also be considered when decisions are made with regard to a proposed eradication (Myers et al., 2000; Courchamp et al., 2003). It is vital that sufcient resources are available to complete the programme, which must be undertaken with clear lines of authority and strong public support. Without these ingredients, the programme is likely to fail and the money to be wasted. Biologically, it is important that the natural history of the target species is adequately known and that the species can be detected at a very low density, so that the last, crucial animals can be
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eliminated. These requirements are met in the case of cats, rats and ungulates, the aliens that occur most often on the islands in our spreadsheets, and where eradication procedures are reasonably well established. However, they are less satisfactorily met in the case of alien birds and mice. It is also vital that managers be alert to the possibility of unwanted side effects when species are eliminated (Courchamp, Langlais & Sugihara, 2000; Krajick, 2005). The likelihood of such side effects, for example an explosion of rat numbers when cats are eradicated (Courchamp, Langlais & Sugihara, 1999), can be reduced by eradicating all aliens in one combined project, and it was partly for this reason that our calculations assume that all alien vertebrates on an island are eliminated at once. It emerged from the results (Tables 4 and 5) that, even with the application of a complementarity approach, several islands holding the same small group of threatened bird species were highly ranked. In part, this is because the approach we adopted achieves only partial complementarity. The current methodology reduces an islands benet score resulting from the increase in predator-free islands or area from which the species has beneted via the prior clearance of higher-ranking islands. However, it did not take account of a second factor. The species concerned would also have become less at risk of extinction, potentially downlisted in Red List terminology and merit a lower T score (see Methods), which would further reduce the benet of removing alien vertebrates from other islands on which the species occurs. That said, the repeated selection of islands within a region where the same species occurs

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M. de L. Brooke, G. M. Hilton and T. L. F. Martins

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does have the practical merit that a single eradication programme, perhaps funded from a single source, could be organized to target several high-priority islands at once, for example in the Balearic Islands. This would be likely to bring nancial economies of scale. Another drawback of the complementarity approach is that it is based on the assumption that eradication projects will systematically work down the priority lists we have generated. This assumption is very unlikely to be realized in practice. Consequently, the raw lists presented in the Supplementary Material Appendix S3 may often be more useful as a guide to priorities than the lists based on complementarity in Table 4. Future work should aim to include other taxa when assessing the benets of eradication on particular islands. As explained in the Introduction, we were unable to do this for lack of adequate global databases for groups other than birds. However, there is no doubt that some current national or regional databases would allow the integration of information from other plant or animal groups into the protocol, and hence national or regional prioritization exercises might be based on a more rounded assessment of biodiversity benet. Not captured by our approach are other potential benets of island vertebrate eradication. For example, alien-free islands could serve as localities for potential re-establishment (with or without assistance) of extirpated populations. As mentioned in Supplementary Material Appendix S2, we deliberately included only speciesisland combinations which are still extant. Further, the removal of aliens may encourage recovery of non-threatened species and overall ecosystem recovery, with potential concomitant economic benets. These benets, not reected in our rankings, are likely, in general, to favour the restoration of larger islands that tend to support more viable and varied ecosystems, and that deliver greater ecosystem services. This is an important counterpoint to the conclusion reached from our benet:cost analyses that small islands deliver the greatest reduction in net extinction risk among the threatened species set. These other types of conservation benets could and should be quantied and built into the prioritization scheme described here, although it is less straightforward to do so than to use the overall reduction in extinction risk that can be derived from Red List classications. In conclusion, our preliminary study suggests that the reduction of extinction risk to threatened birds can be improved substantially by strategic targeting of whatever funds are available for vertebrate eradication, and that often the islands so targeted will be relatively small. This nding is remarkably robust in the face of several different measures of reduction of extinction risk. Because we acknowledge that the study, focused only on threatened birds, is taxonomically restricted, the challenge for the future is to integrate other conservation benets into the prioritization process so that theoreticians, managers and funders can all be condent that scarce eradication funds are directed towards those of the worlds islands where the conservation gains will be the greatest.

Acknowledgements
We thank Alastair Gammell for suggesting this project, and Debbie Pain and the RSPB for supporting part of TLFMs involvement, which was also partly funded by the European Social Fund. Jenny Gould and Sarah Farnsworth carried out early work on assembling data, helped by Stuart Butchart and Martin Sneary of BirdLife International. Many correspondents, often contacted via the newsletter Aliens sympathetically edited by Maj de Poorter, have patiently answered our queries. We would particularly like to highlight the input of Keith Broome and Ian McFadden (Department of Conservation, New Zealand), Derek Brown, Ian Bullock (RSPB), Falklands Conservation, Paige Martin and Josh Adams (Ashy Storm-petrel), Miguel McMinn Grive and Ana Rodr guez (Balearic Islands), John Ratcliffe (Countryside Council for Wales), James Russell (University of Auckland) and Bernie Tershy (Island Conservation). Tom Brooks, John Croxall and Debbie Pain commented on an earlier draft of the paper. Guy Cowlishaw has been a supportive and painstaking editor.

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Supplementary material
The following material is available for this article online: Appendix S1 Scientic names of species mentioned in the text and Table 5, arranged alphabetically by common name. Appendix S2 The assessment we describe addresses only those islands where threatened bird species, facing a known danger from alien vertebrates, are found today. Further justication in Appendix. Appendix S3 Lists of the worlds candidate islands. This material is available as part of the online article from http://www.blackwell-synergy.com/doi/abs/10.1111/ j.1469-1795.2007.00123.x Please note: Blackwell Publishing are not responsible for the content or functionality of any supplementary materials supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author for the article.

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