Research Article

The Impact of Conservation on the Status of the World’s Vertebrates

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Science  10 Dec 2010:
Vol. 330, Issue 6010, pp. 1503-1509
DOI: 10.1126/science.1194442

Abstract

Using data for 25,780 species categorized on the International Union for Conservation of Nature Red List, we present an assessment of the status of the world’s vertebrates. One-fifth of species are classified as Threatened, and we show that this figure is increasing: On average, 52 species of mammals, birds, and amphibians move one category closer to extinction each year. However, this overall pattern conceals the impact of conservation successes, and we show that the rate of deterioration would have been at least one-fifth again as much in the absence of these. Nonetheless, current conservation efforts remain insufficient to offset the main drivers of biodiversity loss in these groups: agricultural expansion, logging, overexploitation, and invasive alien species.

In the past four decades, individual populations of many species have undergone declines and many habitats have suffered losses of original cover (1, 2) through anthropogenic activity. These losses are manifested in species extinction rates that exceed normal background rates by two to three orders of magnitude (3), with substantial detrimental societal and economic consequences (4). In response to this crisis, 193 parties to the Convention on Biological Diversity (CBD; adopted 1992) agreed “to achieve by 2010 a significant reduction of the current rate of biodiversity loss at the global, regional, and national level as a contribution to poverty alleviation and to the benefit of all life on Earth” (5). That the target has not been met was borne out by empirical testing against 31 cross-disciplinary indicators developed within the CBD framework itself (1). However, this does not mean that conservation efforts have been ineffective. Conservation actions have helped to prevent extinctions (6, 7) and improve population trajectories (8), but there has been limited assessment of the overall impact of ongoing efforts in reducing losses in biodiversity (9, 10). Here, we assess the overall status of the world’s vertebrates, determine temporal trajectories of extinction risk for three vertebrate classes, and estimate the degree to which conservation actions have reduced biodiversity loss.

Described vertebrates include 5498 mammals, 10,027 birds, 9084 reptiles, 6638 amphibians, and 31,327 fishes (table S1). Vertebrates are found at nearly all elevations and depths, occupy most major habitat types, and display remarkable variation in body size and life history. Although they constitute just 3% of known species, vertebrates play vital roles in ecosystems (11) and have great cultural importance (12). Under the auspices of the International Union for Conservation of Nature (IUCN) Species Survival Commission, we compiled data on the taxonomy, distribution, population trend, major threats, conservation measures, and threat status for 25,780 vertebrate species, including all mammals, birds, amphibians, cartilaginous fishes, and statistically representative samples of reptiles and bony fishes [~1500 species each (13)].

The IUCN Red List is the widely accepted standard for assessing species’ global risk of extinction according to established quantitative criteria (14). Species are categorized in one of eight categories of extinction risk, with those in the categories Critically Endangered, Endangered, or Vulnerable classified as Threatened. Assessments are designed to be transparent, objective, and consultative, increasingly facilitated through workshops and Web-based open-access systems. All data are made freely available for consultation (15) and can therefore be challenged and improved upon as part of an iterative process toward ensuring repeatable assessments over time.

Status, trends, and threats. Almost one-fifth of extant vertebrate species are classified as Threatened, ranging from 13% of birds to 41% of amphibians, which is broadly comparable with the range observed in the few invertebrate and plant taxa completely or representatively assessed to date (Fig. 1 and table S2). When we incorporate the uncertainty that Data Deficient species (those with insufficient information for determining risk of extinction) introduce, the proportion of all vertebrate species classified as Threatened is between 16% and 33% (midpoint = 19%; table S3). [Further details of the data and assumptions behind these values are provided in (16) and tables S2 and S3.] Threatened vertebrates occur mainly in tropical regions (Fig. 2), and these concentrations are generally disproportionately high even when accounting for their high overall species richness (fig. S4, A and B). These patterns highlight regions where large numbers of species with restricted distributions (17) coincide with intensive direct and indirect anthropogenic pressures, such as deforestation (18) and fisheries (19).

Fig. 1

The proportion of vertebrate species in different Red List categories compared with completely (or representatively) assessed invertebrate and plant taxa on the 2010 IUCN Red List (15). EW, Extinct in the Wild; CR, Critically Endangered; EN, Endangered; VU, Vulnerable; NT, Near Threatened; LC, Least Concern; DD, Data Deficient. Extinct species are excluded. Taxa are ordered according to the estimated percentage (shown by horizontal red lines and given in parentheses at tops of bars) of extant species considered Threatened if Data Deficient species are Threatened in the same proportion as data-sufficient species. Numbers above the bars represent numbers of extant species assessed in the group; asterisks indicate those groups in which estimates are derived from a randomized sampling approach.

Fig. 2

Global patterns of threat, for land (terrestrial and freshwater, in brown) and marine (in blue) vertebrates, based on the number of globally Threatened species in total.

To investigate temporal trends in extinction risk of vertebrates, we used the IUCN Red List Index (RLI) methodology (20) that has been adopted for reporting against global targets (1, 2). We calculated the change in RLI for birds (1988, 1994, 2000, 2004, and 2008), mammals (1996 and 2008), and amphibians (1980 and 2004); global trend data are not yet available for other vertebrate groups, although regional indices have been developed (21). The RLI methodology is explained in detail in (16), but in summary the index is an aggregated measure of extinction risk calculated from the Red List categories of all assessed species in a taxon, excluding Data Deficient species. Changes in the RLI over time result from species changing categories between assessments (Table 1). Only real improvements or deteriorations in status (termed “genuine” changes) are considered; recategorizations attributable to improved knowledge, taxonomy, or criteria change (“nongenuine” changes) are excluded (22). Accordingly, the RLI is calculated only after earlier Red List categorizations are retrospectively corrected using current information and taxonomy, to ensure that the same species are considered throughout and that only genuine changes are included. For example, the greater red musk shrew (Crocidura flavescens) was classified as Vulnerable in 1996 and as Least Concern in 2008; however, current evidence indicates that the species was also Least Concern in 1996, and the apparent improvement is therefore a nongenuine change. In contrast, Hose’s broadbill (Calyptomena hosii) was one of 72 bird species to deteriorate one Red List category between 1994 and 2000, from Least Concern to Near Threatened, mainly because of accelerating habitat loss in the Sundaic lowlands in the 1990s. Such a deterioration in a species’ conservation status leads to a decline in the RLI (corresponding to increased aggregated extinction risk); an improvement would lead to an increase in the RLI.

Table 1

Net number of species qualifying for revised IUCN Red List categories between assessments owing to genuine improvement or deterioration in status, for birds (1988 to 2008), mammals (1996 to 2008), and amphibians (1980 to 2004). Category abbreviations are as for Fig. 1; CR(PE/PEW) denotes Critically Endangered (Possibly Extinct or Possibly Extinct in the Wild). CR excludes PE/PEW. Species undergoing an improvement (i.e., moving from a higher to a lower category of threat) are indicated by “+”; species deteriorating in status (i.e., moving from a lower to a higher category of threat) are indicated by “–”. Species changing categories for nongenuine reasons, such as improved knowledge or revised taxonomy, are excluded. In the case of birds, for which multiple assessments have been undertaken, values in parentheses correspond to the sum of all changes between consecutive assessments; the same species may therefore contribute to the table more than once [see (16)].

View this table:

Temporal trajectories reveal declining RLIs for all three taxa. Among birds, the RLI (Fig. 3A) showed that their status deteriorated from 1988 to 2008, with index values declining by 0.49%, an average of 0.02% per year (table S4). For mammals, the RLI declined by 0.8% from 1996 to 2008, a faster rate (0.07% per year) than for birds. Proportionally, amphibians were more threatened than either birds or mammals; RLI values declined 3.4% from 1980 to 2004 (0.14% per year). Although the absolute and proportional declines in RLIs for each taxonomic group were small, these represent considerable biodiversity losses. For example, the deterioration for amphibians was equivalent to 662 amphibian species each moving one Red List category closer to extinction over the assessment period. The deteriorations for birds and mammals equate to 223 and 156 species, respectively, deteriorating at least one category. On average, 52 species per year moved one Red List category closer to extinction from 1980 to 2008. Note that the RLI does not reflect ongoing population changes that are occurring too slowly to trigger change to different categories of threat. Other indicators based on vertebrate population sizes showed declines of 30% between 1970 and 2007 (1, 2, 22).

Fig. 3

(A) Trends in the Red List Index (RLI) for the world’s birds, mammals, and amphibians. (B to D) Observed change in the RLI for each group (black) compared with RLI trends that would be expected if species that underwent an improvement in status due to conservation action had undergone no change (red). The difference is attributable to conservation. An RLI value of 1 equates to all species being Least Concern; an RLI value of 0 equates to all species being Extinct. Improvements in species conservation status lead to increases in the RLI; deteriorations lead to declines. A downward trend in the RLI value means that the net expected rate of species extinctions is increasing. Shading shows 95% confidence intervals. Note: RLI scales for (B), (C), and (D) vary.

Global patterns of increase in overall extinction risk are most marked in Southeast Asia (Fig. 4 and figs. S5A and S6). It is known that the planting of perennial export crops (such as oil palm), commercial hardwood timber operations, agricultural conversion to rice paddies, and unsustainable hunting have been detrimental to species in the region (23), but here we show the accelerating rate at which these forces are driving change. In California, Central America, the tropical Andean regions of South America, and Australia, patterns have been driven mainly by the “enigmatic” deteriorations among amphibians (24), which have increasingly been linked to the infectious disease chytridiomycosis, caused by the presumed invasive fungal pathogen Batrachochytrium dendrobatidis (25). Almost 40 amphibians have deteriorated in status by three or more IUCN Red List categories between 1980 and 2004 (Table 1).

Fig. 4

Global patterns of net change in overall extinction risk across birds, mammals, and amphibians (for the periods plotted in Fig. 3) mapped as average number of genuine Red List category changes per cell per year. Purple corresponds to net deterioration (i.e., net increase in extinction risk) in that cell; green, net improvement (i.e., decrease in extinction risk); white, no change. The uniform pattern of improvement at sea is driven by improvements of migratory marine mammals with cosmopolitan distributions (e.g., the humpback whale). Deteriorations on islands [e.g., the nightingale reed-warbler (Acrocephalus luscinius) in the Northern Mariana Islands] and improvements on islands [e.g., the Rarotonga monarch (Pomarea dimidiata) in the Cook Islands] are hard to discern; islands showing overall net improvements are shown in blue. Note that the intensity of improvements never matches the intensity of deteriorations.

Although chytridiomycosis has been perhaps the most virulent threat affecting vertebrates to emerge in recent years, it is not the only novel cause of rapid declines. The toxic effects of the veterinary drug diclofenac on Asian vultures have caused estimated population declines exceeding 99% over the past two decades in certain Gyps species, and have resulted in three species moving from Near Threatened to Critically Endangered between 1994 and 2000. Numbers of Tasmanian devils (Sarcophilus harrisii) have fallen by more than 60% in the past 10 years because of the emergence of devil facial tumor disease (resulting in three step changes from Least Concern to Endangered). Climate change is not yet adequately captured by the IUCN Red List (26, 27) but has been directly implicated in the deteriorating status of several vertebrates and may interact with other threats to hasten extinction (28). However, there is no evidence of a parallel to the systemwide deteriorations documented for reef-building corals affected by bleaching events related to El Niño–Southern Oscillation occurrences (29).

Most deteriorations in status are reversible, but in 13% of cases they have resulted in extinction. Two bird species—the kamao (Myadestes myadestinus) from Hawaii and the Alaotra grebe (Tachybaptus rufolavatus) from Madagascar—became extinct between 1988 and 2008, and a further six Critically Endangered species have been flagged as “possibly extinct” during this period (Table 1 and table S5). At least nine amphibian species vanished during the two decades after 1980, including the golden toad (Incilius periglenes) from Costa Rica and both of Australia’s unique gastric-brooding frog species (genus Rheobatrachus); a further 95 became possibly extinct, 18 of them harlequin toads in the Neotropical genus Atelopus (23% of species). No mammals are listed as Extinct for the period 1996 to 2008, although the possible extinction of the Yangtze River dolphin (Lipotes vexillifer) would be the first megafauna vertebrate species extinction since the Caribbean monk seal in the 1950s (30).

Estimates of conservation success. These results support previous findings that the state of biodiversity continues to decline, despite increasing trends in responses such as protected areas coverage and adoption of national legislation (1, 2). Next, we asked whether conservation efforts have made any measurable contribution to reducing declines or improving the status of biodiversity.

The RLI trends reported here are derived from 928 cases of recategorization on the IUCN Red List (Table 1 and table S6), but not all of these refer to deteriorations. In 7% of cases (68/928), species underwent an improvement in status, all but four due to conservation action. For example, the Asian crested ibis (Nipponia nippon) changed from Critically Endangered in 1994 to Endangered in 2000 owing to protection of nesting trees, control of agrochemicals in rice fields, and prohibition of firearms; the four exceptions were improvements resulting from natural processes, such as unassisted habitat regeneration (tables S7 and S8). Nearly all of these improvements involved mammals and birds, where the history of conservation extends farther back and where the bulk of species-focused conservation funding and attention is directed (31). Only four amphibian species underwent improvements, because the amphibian extinction crisis is such a new phenomenon and a plan for action has only recently been developed (32).

To estimate the impact of conservation successes, we compared the observed changes in the RLI with the RLI trends expected if all 64 species that underwent an improvement in status due to conservation action had not done so (16). Our explicit assumption is that in the absence of conservation, these species would have remained unchanged in their original category, although we note that this approach is conservative because it is likely that some would have deteriorated [in the sense of (6)]. The resulting difference between the two RLIs can be attributed to conservation. We show that the index would have declined by an additional 18% for both birds and mammals in the absence of conservation (Fig. 3, B and C, and table S4). There was little difference for amphibians (+1.4%; Fig. 3D) given the paucity of species improvements. For birds, conservation action reduced the decline in the RLI from 0.58% to 0.49%, equivalent to preventing 39 species each moving one Red List category closer to extinction between 1988 and 2008. For mammals, conservation action reduced the RLI decline from 0.94% to 0.8%, equivalent to preventing 29 species moving one category closer to extinction between 1996 and 2008.

These results grossly underestimate the impact of conservation, because they do not account for species that either (i) would have deteriorated further in the absence of conservation actions, or (ii) improved numerically, although not enough to change Red List status. As an example among the former, the black stilt (Himantopus novaezelandiae) would have gone extinct were it not for reintroduction and predator control efforts, and its Critically Endangered listing has thus remained unchanged (6). Among the latter, conservation efforts improved the total population numbers of 33 Critically Endangered birds during the period 1994 to 2004, but not sufficiently for any species to be moved to a lower category of threat (33). As many as 9% of mammals, birds, and amphibians classified as Threatened or Near Threatened have stable or increasing populations (15) largely due to conservation efforts, but it will take time for these successes to translate into improvements in status. Conservation efforts have also helped to avoid the deterioration in status of Least Concern species. Finally, conservation actions have benefited many other Threatened species besides birds, mammals, and amphibians, but this cannot yet be quantified through the RLI for groups that have been assessed only once [e.g., salmon shark (Lamna ditropis) numbers have improved as the result of a 1992 U.N. moratorium on large-scale pelagic driftnet fisheries].

Confronting threats. Species recovery is complex and case-specific, but threat mitigation is always required. We investigated the main drivers of increased extinction risk by identifying, for each species that deteriorated in status, the primary threat responsible for that change. To understand which drivers of increased extinction risk are being mitigated most successfully, we identified, for each species that improved in status, the primary threat offset by successful conservation (table S6).

We found that for any single threat, regardless of the taxa involved, deteriorations outnumber improvements; conservation actions have not yet succeeded in offsetting any major driver of increased extinction risk (fig. S7). On a per-species basis, amphibians are in an especially dire situation, suffering the double jeopardy of exceptionally high levels of threat coupled with low levels of conservation effort. Still, there are conservation successes among birds and mammals, and here we investigate the degree to which particular threats have been addressed.

Conservation actions have been relatively successful at offsetting the threat of invasive alien species for birds and mammals: For every five species that deteriorated in status because of this threat, two improved through its mitigation. These successes have resulted from the implementation of targeted control or eradication programs [e.g., introduced cats have been eradicated from 37 islands since the mid-1980s (34)] coupled with reintroduction initiatives [e.g., the Seychelles magpie-robin (Copsychus sechellarum) population was 12 to 15 birds in 1965 but had increased to 150 birds by 2005 (fig. S8)]. Many of these improvements have occurred on small islands but also in Australia, owing in part to control of the red fox (Vulpes vulpes) (Fig. 4 and fig. S5B). However, among amphibians, only a single species—the Mallorcan midwife toad (Alytes muletensis)—improved in status as a result of mitigation of the threat posed by invasive alien species, compared with 208 species that deteriorated. This is because there is still a lack of understanding of the pathways by which chytridiomycosis is spread and may be controlled, and in situ conservation management options are only just beginning to be identified [e.g., (35)]. Meanwhile, the establishment of select, targeted captive populations with the goal of reintroducing species in the wild may offer valuable opportunities once impacts in their native habitat are brought under control [e.g., the Kihansi spray toad (Nectophrynoides asperginis), categorized as Extinct in the Wild because of drastic alteration of its spray zone habitat].

For mammals and birds, the threats leading to habitat loss have been less effectively addressed relative to that of invasive alien species: For every 10 species deteriorating as a result of agricultural expansion, fewer than 1 improved because of mitigation of this threat. Protected areas are an essential tool to safeguard biodiversity from habitat loss, but the protected areas network remains incomplete and nonstrategic relative to Threatened species (17), and reserve management can be ineffective (36). Numerous Threatened species are restricted to single sites, many still unprotected (37), and these present key opportunities to slow rates of extinction. In the broader matrix of unprotected land, agri-environmental schemes could offer important biodiversity benefits, provided that management policies are sufficient to enhance populations of Threatened species (38).

Hunting has been relatively poorly addressed in mammals (62 deteriorations, 6 improvements) when compared with birds (31 deteriorations, 9 improvements). In birds, successes have resulted mainly from targeted protection [e.g., Lear’s macaw (Anodorhynchus leari) changed from Critically Endangered to Endangered as a result of active protection of the Toca Velha/Serra Branca cliffs in Brazil], but also from enforcement of legislation (e.g., hunting bans) and harvest management measures. Many mammals subject to hunting occur at low densities, have large home ranges, and/or are large-bodied. Although active site-based protection has contributed to an improvement in the status of some of these species, site protection alone is often insufficient if not complemented by appropriate legislation, biological management, and effective enforcement (39). For example, a combination of the Convention on International Trade in Endangered Species of Wild Flora and Fauna (CITES) and enactment of the Vicuña Convention, which prohibited domestic exploitation and mandated the establishment of protected areas, has helped to improve the status of the vicuña (Vicugna vicugna) from Near Threatened to Least Concern.

The threat of fisheries has been mitigated relatively more effectively for marine mammals (4 deteriorations, 2 improvements) than for birds (10 deteriorations, 0 improvements), reflecting both the time when drivers first emerged and the past influence of supranational conservation policy. Among historically exploited, long-lived mammals, for example, the humpback whale (Megaptera novaeangliae) has benefited from protection from commercial whaling (since 1955) and has improved from Vulnerable to Least Concern. Declines among slow-breeding seabirds (particularly albatrosses and petrels; fig. S9) are mainly a consequence of increasing incidental by-catch resulting from the growth of commercial fisheries, primarily those that use long-line and trawling methods. Legislative tools, such as the recently enacted multilateral Agreement on the Conservation of Albatrosses and Petrels (40), may yet deliver dividends by coordinating international action to reduce fisheries mortality of these highly migratory species. Binding legislation and harvest management strategies also are urgently needed to address the disproportionate impact of fisheries on cartilaginous fishes (fig. S10).

We have no data on the relationship between expenditure on biodiversity and conservation success. A disproportionate percentage of annual conservation funding is spent in economically wealthy countries (41), where there are generally fewer Threatened species (Fig. 2 and fig. S4B) and the disparity between success and failure appears less evident (Fig. 4). Southeast Asia, by contrast, has the greatest imbalance between improving and deteriorating trends, emphasizing the need there for greater investment of resources and effort.

Conclusions. Our study confirms previous reports of continued biodiversity losses. We also find evidence of notable conservation successes illustrating that targeted, strategic conservation action can reduce the rate of loss relative to that anticipated without such efforts. Nonetheless, the current level of action is outweighed by the magnitude of threat, and conservation responses will need to be substantially scaled up to combat the extinction crisis. Even with recoveries, many species remain conservation-dependent, requiring sustained, long-term investment (42); for example, actions have been under way for 30 years for the golden lion tamarin (Leontopithecus rosalia), 70 years for the whooping crane (Grus americana), and 115 years for the white rhinoceros (Ceratotherium simum).

Halting biodiversity loss will require coordinated efforts to safeguard and effectively manage critical sites, complemented by broad-scale action to minimize further destruction, degradation, and fragmentation of habitats (37, 39) and to promote sustainable use of productive lands and waters in a way that is supportive to biodiversity. Effective implementation and enforcement of appropriate legislation could deliver quick successes; for example, by-catch mitigation measures, shark-finning bans, and meaningful catch limits have considerable potential to reduce declines in marine species (19). The 2010 biodiversity target may not have been met, but conservation efforts have not been a failure. The challenge is to remedy the current shortfall in conservation action to halt the attrition of global biodiversity.

Supporting Online Material

www.sciencemag.org/cgi/content/full/science.1194442/DC1

Materials and Methods

Figs. S1 to S10

Tables S1 to S9

References

Acknowledgments

References and Notes

  1. See supporting material on Science Online.
  2. We are indebted to the more than 3000 species experts who devoted their knowledge, intellect, and time to the compilation of vertebrate data on the IUCN Red List. Full acknowledgments are provided in the supporting online material.
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