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Changes in the conservation status of Australian birds resulting from differences in taxonomy, knowledge and the definitions of threat
Biological Conservation 113 (2003) 269–276 www.elsevier.com/locate/biocon
Changes in the conservation status of Australian birds resulting from differences in taxonomy, knowledge and the definitions of threat S.T. Garnetta,b,c,*, G.M. Crowleya,b,c, A.J. Stattersfieldb a Queensland Parks and Wildlife Service, PO Box 2066, Cairns, 4870 Australia Conservation Biology Unit, Zoology Department, Cambridge University, Cambridge CB23EJ, UK c BirdLife International, Wellbrook Court, Girton CB30PS, UK
b
Received 5 September 2002; received in revised form 15 November 2002; accepted 16 November 2002
Abstract When the conservation status of Australian bird taxa in 1992 was retrospectively reassessed in 2000, the status of nearly 70% had to be changed. About 20% of the differences could be attributed to changes in the predictions of extinction probability. Most differences arose from refinement of ICUN Red List Categories and Criteria. Research showed that some populations were more threatened than realised and a few changes resulted from taxonomic revision. Funds might have been distributed differently had the adjusted analysis been available in 1992. Nevertheless, comparisons between either the original or the revised 1992 list and the 2000 list demonstrate degeneration in overall status of threatened birds in Australia. It is concluded that trends in conservation status are a valid long-term measure of the risk of biodiversity loss. Stabilisation of IUCN Red List definitions should mean that an increasing proportion of the status flux should be attributable to real changes in extinction probability. Crown Copyright # 2003 Published by Elsevier Science Ltd. All rights reserved. Keywords: Threatened; Australian; Birds; IUCN; Status
1. Introduction Since the IUCN started preparing lists of species that are threatened with extinction (see Collar, 1998; BirdLife International, 2000, for history) numerous assessments have been made of threatened species around the world. The number of taxa that have changed status from one time period to the next has then sometimes been used to determine trends in extinction probability over time (Smith et al., 1993) and will be used in the future ‘to develop indices of biodiversity trend’ (IUCN, 2001a). However, a comparison of global lists of threatened bird species between 1988 and 1994 found that only 3% of change in that time could be attributed to a genuine change in status (Crosby et al., 1994). The
* Corresponding author. Tel.: +61-7-4046-6601; fax: +61-7-40466643. E-mail address: [email protected] (S.T. Garnett).
remainder was attributed to changes in taxonomy (18%), increased knowledge (58%) and changes in IUCN Red List Categories and Criteria (20%). The imperiled nature of some Australian bird species was first mooted nearly a century ago (Campbell, 1915) but the first attempt to use standardized international criteria to assess the status of all Australia species did not occur until 1990 (Brouwer and Garnett, 1990). In 1992 this assessment was extended to include all species and subspecies of bird either breeding on Australian territory, including offshore islands, or for which > 5% of the global population was believed to visit regularly (Garnett, 1992, 1993). In 2000 the exercise was repeated (Garnett and Crowley, 2000). As with BirdLife International (2000), there were substantial differences between the two sets of assessments, only some of which can be attributed to real changes in the probability of extinction. This paper examines the nature of those differences, their implications for the assessment of trends in Australian threatened birds and for the funding of their conservation management.
0006-3207/03/$ - see front matter Crown Copyright # 2003 Published by Elsevier Science Ltd. All rights reserved. doi:10.1016/S0006-3207(02)00377-4
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2. Methods The status of all Australian taxa was assessed in 1992 and 2000 based on the accepted taxonomy, data on the biology of each taxon and the most recent IUCN Red List Criteria available at the time of the assessment (Garnett, 1992, 1993, Garnett and Crowley, 2000). In 2000 retrospective estimates were also made of the size and trend of population and distribution of each taxon in 1992 based on information available and taxonomy accepted in 2000. The status as it would have been in 1992 was then assessed using the IUCN Red List Criteria pertaining in 2000. Differences between 1992 and 2000 in assessment criteria, taxonomy and knowledge are summarised below. 2.1. Assessment criteria In 1992 the first quantitative assessment of the risk of threat had just become available (Mace and Lande, 1991). By 2000 Mace and Lande’s work had been refined and officially adopted by the IUCN (1994). The categories of Extinct, Critically Endangered, Endangered and Vulnerable were defined precisely, if slightly differently, in both publications (Table 1). Other categories used in 1992 and their 2000 equivalents were as follows: Rare: ‘taxa with small populations that are not at present ’Endangered’ or ’Vulnerable’, but are threatened. These taxa are usually localised within restricted geographical areas or habitats or are thinly scattered over a more extensive range’. In the 1992 assessment, most Rare taxa shared with the Vulnerable taxa a total population size believed to be less than 10,000 individuals. By 2000 this had effectively become the category Lower Risk (Near Threatened): ‘taxa. . . which are close to qualifying for Vulnerable’ (IUCN, 1994). For the purposes of the assessment Near Threatened taxa were considered to fall into one of the following categories based on Maxwell et al. (1996):
1. Reduced area of occupancy and/or extent of occurrence: taxa that have disappeared from over 50% of their former area of occupancy and/or extent of occurrence and are at risk of further decline. i.e. close to Vulnerable criterion B. 2. Decline in abundance: taxa that have experienced a significant and continuing decline in abundance in over 50% of their former area of occupancy and/or extent of occurrence. i.e. close to Vulnerable criterion A. 3. Small populations: taxa with populations smaller than 3000 mature individuals, or of unknown population size but suspected to be small. i.e. close to criterion D.
4. Regionally secure populations: taxa with small or restricted populations in Australia (hence could qualify as Vulnerable: D1 or D2) that are genetically continuous with secure regional populations. Such taxa were downgraded to Near Threatened as per Ga¨rdenfors et al. (1999). Insufficiently Known: species suspected of being ’Endangered’, ’Rare’ or ’Vulnerable’ but whose true status cannot be determined without more information. In 2000 the nearest equivalent was the category Data Deficient: a taxon where there is inadequate information to make a direct, or indirect, assessment of its risk of extinction based on its distribution and/or population status. A taxon in this category may be well studied, and its biology well known, but appropriate data on abundance and/or distribution are lacking. The two categories are not directly equivalent: Insufficiently Known taxa were threatened but the level of threat is unknown, Data Deficient taxa are not necessarily threatened. In fact, in 2000, Data Deficient was not used for any Australian taxon. Special Concern: ‘An unofficial category adopted by the ICBP (N. Collar pers.comm.) for taxa that are often treated as threatened but, at this stage, do not appear to warrant classification as Endangered, Vulnerable, Rare or Insufficiently Known’ (Garnett, 1992, 1993). These taxa were categorised as follows: 1. Taxa with very small (< 5 pairs) and possibly temporary breeding populations in Australia but which are secure elsewhere. In 2000 such taxa were assessed as Critically Endangered unless there was evidence of continuing genetic interchange with extralimital populations in which case the status was downgraded to Endangered as per Ga¨rdenfors et al. (1999). 2. Taxa that have suffered population declines in the past but for which the population has since stabilized or is increasing. In 2000 these were classified as Least Concern unless the absolute population size was now small enough to fall within the D criterion of a threatened category. 3. Taxa which have declined in parts of their range but are secure in the remainder. In 2000 such taxa were classified as Least Concern unless the population fell within one of the Near Threatened criteria 1 or 2. 4. Taxa with large populations which may warrant more concern in the future. In 2000 these were classified as Least Concern unless the decline was sufficiently severe to approach the Near Threatened category 2. 5. Taxa that occur in remote areas for which there is good evidence to suggest their abundance has previously been underestimated. In 2000 all such
Table 1 Comparison of the criteria used to assess the status of Australian birds in 1992 (Garnett, 1992) and 2000 (IUCN, 1994) Criteria
1992 (based on Mace and Lande, 1991) Rate of population decline: > X%/year for Y year >Z% in last generation
Frequency and extent of catastrophes (subpopulations highly correlated in population fluctuations): > X% reduction in population/5–10 year or every 2–4 generations or >50% reduction in population/Y year or every Z
Threatened species category Endangered
Vulnerable
X=20 Y=2 Z=50
X=5 Y=5 Z=10 in 2 generations X=20
X=1 Y=10
X=10
Y=50
Y=20
Z=5-10 generations X=5
Z=50 year
X=50 Z=2-4 generations
Extent of fragmentation: X populations of < Y individuals or 2 populations of > Z individuals immigration of < 1 individual/ generation
X=2 Y=125
Total population: < X individuals Probability of extinction: X% probability of extinction in Y years or Z generations whichever is sooner
2000 (based on IUCN, 1994) A. Population reduction in the form of either of the following: (1) An observed, estimated, inferred or suspected reduction of at least X% over the last 10 years or three generations, whichever is the longer OR (2) A reduction of at least X% over the last 10 years or three generations, whichever is the longer, projected or suspected to be met within the next ten years or three generations, whichever is the longer. C. Population estimated to number less than X mature individuals and either (1) An estimated continuing decline of at least Y, whichever is longer, OR (2) A continuing decline, observed, projected, or inferred, in numbers of mature individuals and population structure in the form of either: (a) severely fragmented (i.e. no sub-population estimated to contain more than Z mature individuals) (b) all individuals are in a single sub-population.
B. Extent of occurrence estimated to be less than X km2 or area of occupancy estimated to be less than Y km2, and estimates indicating any two of the following: (1) Severely fragmented or known to exist at Z location. (2) Continuing decline, observed, inferred or projected, in any of the following: (a) extent of occurrence (b) area of occupancy (c) area, extent and/or quality of habitat (d) number of locations or sub-populations (e) number of mature individuals. (3) Extreme fluctuations in any of the following: (a) extent of occurrence (b) area of occupancy (c) number of locations or sub-populations (d) number of mature individuals.
D. Population estimated to number less than X mature individuals, OR (Vulnerable only) Population is characterised by an acute restriction in its area of occupancy (typically less than 100 km2) or in the number of locations (typically less than 5). Such a taxon would thus be prone to the effects of human activities (or stochastic events whose impact is increased by human activities) within a short period of time in an unforeseeable future, and is thus capable of becoming Critically Endangered or even Extinct in a short period. E. Quantitative analysis showing the probability of extinction in the wild is at least X% within Y years or Z generations, whichever is the longer
X=5 Y=2500 Z=5000 X=10,000 X=10 Y=100
X=80
X=50
X=20
X=250
X=2500
X=10,000
Y=25% within 3 years or 1 generation Z=50 X= < 100 km2
Y=25% within 3 years or 2 generations Z=250 X= < 5000 km2
Y=10% within 10 years or 3 generations Z=1000 X= < 20,000 km2
Y= < 10 km2 Z=1 X=50
Y= < 500 km2 Z= < 6 X=250
Y= < 2000 km2 Z= < 11 X=1000
X=50% within Y=10 years or Z=3
X=20
X=10
Y=20 Z=5
Y=100
271
X=250 X=50 Y=5 Z=2
Y=500 Z=1250 X=2500 X=20 Y=20 Z=10
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Critically endangered
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taxa were classified on the basis of whatever information could be assembled. 6. Taxa with relatively small populations (5000– 10,000 individuals) but for which no decline has been suggested and plausible threats are lacking. In 2000 such taxa were listed as Least Concern unless they approached Near Threatened criterion 3 or were geographically confined to the extent they approached Vulnerable criterion D. Secure: any taxon that did not fall into one of the above categories. In 2000 the equivalent category was Lower Risk (Least Concern). Such taxa were assessed but did not qualify for any other category. 2.2. Taxonomy In 1992 no widely accepted Australian taxonomy was available. The taxonomic scope of the assessment was therefore decided largely from consultation with leading Australian taxonomists: Richard Schodde and Les Christidis. By 2000 major taxonomic analyses had been completed; so for genera and species taxonomy followed Christidis and Boles (1994) except for albatrosses, some hawk-owls and grasswrens where Robertson and Nunn (1998), Norman et al. (1998), Christidis (1999) and Schodde and Mason (1999) were used at the species level and Marchant and Higgins (1990, 1993), Higgins and Davies (1996), Schodde and Mason (1997, 1999) and Higgins (1999) were followed at the subspecies level. 2.3. Knowledge Substantial support was provided for threatened species surveys and research during the 1990s (see Garnett and Crowley, 2000 for details on individual taxa). This increased knowledge of trends and rates of change in population size and distribution, as well as the nature and severity of threatening processes. Most of this knowledge is thought likely to have pertained to the threatened taxa at the time of the 1992 assessment. Its absence therefore resulted in a misapplication of status to some taxa. 2.4. Funding As part of the 2000 assessment, information was obtained on funding dedicated to the conservation of threatened bird taxa from 1992 and 1999 for all taxa listed in Garnett (1993), though excluding taxa listed as being of Special Concern in 1992 that were subsequently considered to have been Least Concern. Economic information was obtained primarily through personal communication from project officers and government managers responsible for threatened species programs
during the period, and was augmented by recovery plans when available. Gross figures only were obtained and covered salaries of dedicated project officers, project running costs (travel, accommodation, minor contracts, consumables etc.) and capital items (mostly vehicles). Most figures are estimates accurate to the nearest $1000 (Australian). Costs for which no estimate was made were the routine costs of protected area management which may have benefited threatened species, administrative costs incurred during proposal preparation and operation, unsalaried time donated by paid participants, opportunity costs of private landholders and travel costs of volunteers. A more detailed analysis of this information is in preparation (Garnett et al., in press), but the more restricted assessment is used here to compare expenditure on threatened taxa based on the 1992 classifications compared to the adjusted classifications and the classifications in 2000. Expenditure between categories was compared using the nonparametric Terpstra-Jonckhere test for independent samples (Neave and Worthington, 1988). Proportions were compared using w2.
3. Results Overall, a third of Critically Endangered and Endangered taxa and over half the taxa classified as Vulnerable in 1992 were given a different classification when re-assessed in 2000 (Table 2) as a result of changes in IUCN Red List criteria, rearrangements of taxonomy and new knowledge. Changes in the IUCN Red List Criteria, principally to provide greater precision to definitions, accounted for the majority of the differences, with surveys and research most of the remainder (Table 3). A few more taxa would have been listed in 1992 had recent taxonomic revisions been complete. Surveys and research allowed attribution of status to many taxa listed as Insufficiently Known in the first Action Plan. They also tended to show that taxa had smaller populations, were declining more quickly or were facing a greater threat than had been realised in 1992 (Table 4). The changes to the IUCN Red List Criteria that had most influence on changes in status were those relating to trends of small populations (criterion C) and those identifying the vulnerability of populations on islands (criterion D). Rates of population change were most important for identifying taxa meeting the criteria for the Near Threatened category Table 5). When the revised status in 1992 was compared with that in 2000, a total of 25 taxa changed status, a flux of 2.0%. Of these, the status of 18 taxa deteriorated (72.0%), 10 by two status levels; seven improved and there were no confirmed extinctions (Table 6). When the status as assessed in 1992 was compared with the status
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in 2000, 172 taxa had a worse status after eight years (75.4%), 135 declining by two or more status levels, and there were three extinctions; 56 taxa had an improved status including four that increased by two or more status levels. A total of 228 taxa would have changed status, a flux of 18.2%. Thus just 11% (25/228) of changes in taxa could be attributed to changes in the probability of extinction.
Based on the 1992 assessments, funding/taxon increased as status declined (W=208n=6,14,30, P < 0.01, Fig. 1). For the revised classifications, however, this relationship no longer held (W=1002n=15,33,50, P > 0.05). If the revised classifications had been used as a basis for funding, and the rate of funding of individual taxa in each status remained the same, then total funding would have increased by 10% for Critically Endangered
Table 2 Comparison of status between the Action Plan for Australian Birds (Garnett, 1992) using IUCN criteria, knowledge and taxonomy pertaining in 1992 and a retrospective analysis based on the criteria, knowledge and taxonomy current in 2000a
a Shaded cells enumerate the taxa assessed as having a similar extinction probability in 1992 regardless of assessment type. The 1992 assessment of extinction probability was excessively sanguine for taxa enumerated in cells below the diagonal but alarmist for those above it.
Table 3 Reasons for differences in status between the Action Plan for Australian Birds (Garnett, 1992) and a retrospective analysis using IUCN criteria, knowledge and taxonomy pertaining in 2000 Reason for change in status
No. of taxa
% Taxa
Further research Further surveys More rigorous IUCN criteria More rigorous IUCN criteria and taxonomic revision Taxonomic revision
39 22 140 11 19
16.9 9.5 60.6 4.8 8.2
Total
231
100.0
Table 4 Results of research and surveys on assessment of threatened taxon status Nature of study
Result of research
Trend
No. of taxa
Surveys
Population size/distribution area
Larger than anticipated Stable Smaller than anticipated Insufficient previous data
4 2 4 12
Increasing Stable Decreasing More severe No change Less severe Insufficient previous data
0 4 11 26 0 0 2
Investigation of insufficiently known taxa to enable status attribution Biological research
Trend in population/distribution
Severity of threatening process
Investigation of insufficiently known taxa to enable status attribution
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taxa and 82% for Endangered taxa, but decreased for Vulnerable taxa by 61%.
4. Discussion In a similar global comparison of status change between two time periods, changes in taxonomy were Table 5 Relative importance of refinement of IUCN criteria Retrospective status
IUCN sub-criterion
Critically endangered
C D B C D C D A C D A B C D
1 4 2 1 8 4 38 16 22 18 2 1 18 2
0.7 2.9 1.5 0.7 5.9 2.9 27.2 11.8 16.2 13.2 1.5 0.7 13.2 1.5
A B C D
18 3 46 69
13.2 2.2 33.8 50.7
Endangered
Vulnerable Near threatened
Least concern
Subtotals
Total
No. taxa
136
% Taxa
100
the most important source of variation in status (Crosby et al., 1994). For Australia, however, taxonomy was relatively stable because the same taxonomic advisers were used in both Action Plans, and because all assessments were at the subspecies level. In those parts of the world where most threatened taxa occur there is rather more taxonomic uncertainty and inconsistency, especially at the species level. The level of knowledge about threatened birds is also relatively high in Australia allowing assessment of all bird taxa and the listing of none as Data Deficient. Globally 79 species are listed as Data Deficient (BirdLife International, 2000). The most important cause of status change was therefore changes to the IUCN Red List Criteria. In this analysis the two most important refinements to the criteria were the conditions under which criterion C, which describes trends in small populations, can be applied and the inclusion of criterion Vulnerable: D2 under which the vulnerability of populations on small islands and other restricted areas is recognised. Thus the revised list includes many island taxa that were excluded in the 1992 analysis. The comparison of the initial and revised statuses thus shows that great care must be taken in comparing trends in status over time, particularly if IUCN Red List trends are to become indicators of trends in biodiversity (IUCN, 2001a). Correct allocation of status is also important for its effect on conservation funding. While the Action Plan was only one of many influences on funding quantity and priority in Australia, the hypothetical results for the threatened taxa suggest that
Table 6 Comparison of the status of Australian bird taxa 1992–2000 based on assessment as undertaken in 1992 (upper table) and status as assessed retrospectively (lower table)a
a Highlighted cells are for taxa that retained the same status. Cells below the highlighted diagonal contain the number of taxa in each category assessed as having a higher risk of extinction in 2000, while the prospects for taxa enumerated in cells above the diagonal are assessed as having improved.
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Acknowledgements We are most grateful for help in collecting the original data from the broad suite of conservation biologists, both professional and amateur, who contributed to the two Action Plans for Australian Birds. The original data were collected by Stephen Garnett and Gabriel Crowley for Birds Australia under contract to Environment Australia and prepared for publication while Stephen Garnett was on sabbatical from the Queensland Parks and Wildlife Service at BirdLife International and the Conservation Biology Group in the Zoology Department of Cambridge University. Clive Cook made the writing possible and Nigel Collar commented on the manuscript. Fig. 1. Funds/taxon provided for Australian threatened birds 1993– 2000 based on status as assessed in 1992 (Garnett, 1992; clear box) compared to the amount/taxon provided based on a retrospective assessment (IUCN, 1994; shaded box). Dark points are medians, boxes are upper and lower quartiles, whiskers are maximum and minimum excluding outliers (winged circles).
funds could have been substantially reallocated had the revised allocations been possible in 1992. Some flux, however, is inevitable. Conservation science is a young discipline so it is likely that the IUCN Red List Categories will be adjusted again. Indeed there are small but important differences between criteria used for Australian birds in 2000 (IUCN, 1994) and those now being applied around the world (IUCN, 2001b). Similarly taxonomy is in a constant state of refinement, particularly as a result of increased use of molecular techniques. Technology is also allowing major improvements in the demographic studies needed to determine population sizes, ranges and trends. Reductions in the size of radio-transmitters, for instance, have allowed the study of many cryptic and mobile taxa while satellites enable increasingly accurate assessments of trends in tree cover. While Government may crave stability of status for the purposes of consistent policy and legislation, there has to be enough flexibility within legal instruments to accommodate status flux whatever its source. In particular status needs to be assessed frequently to keep abreast of changes and ensure annual funding allocations best reflect needs. Despite a high level of status flux, the comparison of status between periods can still be worthwhile. Although the flux in status between assessments was ten times greater for the direct comparison than the adjusted comparison, the trend was almost identical—75% of changes negative in the former compared to 72% in the latter. The 11% of variation in status that could be ascribed to real changes in the probability of extinction can thus become a useful long-term indicator of the risk of biodiversity loss (IUCN, 2001a).
References BirdLife International, 2000. Threatened Birds of the World. Lynx Edicions and BirdLife International, Barcelona and Cambridge. Brouwer, J., Garnett, S.T. (Eds.), 1990. Threatened Birds of Australia. RAOU, Melbourne. Campbell, A.J., 1915. Missing birds. Emu 14, 167–168. Christidis, L., 1999. Evolution and biogeography of the Australian grasswrens, Amytornis (Aves: Maluridae): biochemical perspectives. Aust. J. Zool. 47, 113–124. Christidis, L., Boles, W.E., 1994. The taxonomy and species of birds of Australia and its territories. RAOU Monograph 2, 1–112. Collar, N.J., 1998. Extinction by assumption; or, the Romeo Error on Cebu. Oryx 32, 239–244. Crosby, M.J., Stattersfield, A.J., Collar, N.J., Bibby, C.J., 1994. Predicting avian extinction rates. Biodiversity Letters 2, 182–185. Ga¨rdenfors, U., Rodrı´guez, J.P., Hilton-Taylor, C., Hyslop, C., Mace, G., Molur, S., Poss, S., 1999. Draft guidelines for the application of IUCN red list criteria at national and regional levels. Species 31-32, 58–70. Garnett, S.T., 1992. Action Plan for Australian Birds. Australian Nature Conservation Agency, Canberra. Garnett, S.T., 1993. Threatened and Extinct Birds of Australia. Royal Australasian Ornithologists Union, Melbourne. Garnett, S.T., Crowley, G.M., 2000. Action Plan for Australian Birds 2000. Environment Australia, Canberra. Garnett, S.T., Crowley, G.M., Balmford, A.P. Costs of conservation of Australian threatened birds. BioScience (in press). Higgins, P.J., 1999. Handbook of Australian, New Zealand and Antarctic Birds, vol. 4. Parrots to Dollarbird. Oxford University Press, Melbourne. Higgins, P.J., Davies, S.J.J.F. (Eds.), 1996. The Handbook of Australian, New Zealand and Antarctic Birds, vol. 3. Snipe–Pigeons. Oxford University Press, Oxford. IUCN, 1994. IUCN Red List Categories. IUCN Species Survival Commission, Gland, Switzerland. IUCN. 2001a., The IUCN Red list of Threatened SpeciesTM—a tool for monitoring biological diversity—implementation of Article 7 Identification and Monitoring. Recommendations from the Sixth Meeting of the Subsidiary Body on Scientific, Technical and Technological Advice (SBSTTA) to the Convention on Biological Diversity, Montreal, Canada, March 12–16 2001. Draft January 2001. IUCN, 2001b. IUCN Red List Categories and Criteria. Version 3.1 IUCN Species Survival Commission, Gland, Switzerland.
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Mace, G.M., Lande, R., 1991. Assessing extinction threats: towards a re-evaluation of IUCN threatened species categories. Cons. Biol. 5, 148–157. Marchant, S., Higgins, P.J. (Eds.), 1990. The Handbook of Australian, New Zealand and Antarctic Birds, vol. 1. Ratites–Ducks. Oxford University Press, Oxford. Marchant, S., Higgins, P.J. (Eds.), 1993. The Handbook of Australian, New Zealand and Antarctic Birds, vol. 2. Raptors–Lapwings. Oxford University Press, Oxford. Maxwell, S., Burbidge, A.A., Morris, K. (Eds.), 1996. The 1996 Action Plan for Australian Marsupials and Monotremes. Environment Australia, Canberra. Neave, H.R., Worthington, P.L., 1988. Distribution-free Tests. Unwin Hyman, London.
Norman, J.A., Christidis, L., Westerman, M., Hill, F.A.R., 1998. Molecular data confirms the species status of the Christmas Island Hawk-Owl Ninox natalis. Emu 98, 197–208. Robertson, C.J.R., Nunn, G.B., 1998. Towards a new taxonomy for albatrosses. In: Robertson, G., Gales, R. (Eds.), The Albatross: Biology and Conservation. Surrey Beatty and Sons, Chipping Norton, pp. 13–19. Schodde, R., Mason, I.J., 1997. Aves (Columbidae to Coraciidae), Zoological Catalogue of Australia, vol. 37.2. CSIRO Publishing, Melbourne. Schodde, R., Mason, I.J., 1999. The Directory of Australian Birds: Passerines. CSIRO, Collingwood. Smith, H.D.M., May, R.M., Pellew, R., Johnson, T.J., Walter, K.S., 1993. Estimating extinction rates. Nature 364, 494–496.
Changes in the conservation status of Australian birds resulting from differences in taxonomy, knowledge and the definitions of threat S.T. Garnetta,b,c,*, G.M. Crowleya,b,c, A.J. Stattersfieldb a Queensland Parks and Wildlife Service, PO Box 2066, Cairns, 4870 Australia Conservation Biology Unit, Zoology Department, Cambridge University, Cambridge CB23EJ, UK c BirdLife International, Wellbrook Court, Girton CB30PS, UK
b
Received 5 September 2002; received in revised form 15 November 2002; accepted 16 November 2002
Abstract When the conservation status of Australian bird taxa in 1992 was retrospectively reassessed in 2000, the status of nearly 70% had to be changed. About 20% of the differences could be attributed to changes in the predictions of extinction probability. Most differences arose from refinement of ICUN Red List Categories and Criteria. Research showed that some populations were more threatened than realised and a few changes resulted from taxonomic revision. Funds might have been distributed differently had the adjusted analysis been available in 1992. Nevertheless, comparisons between either the original or the revised 1992 list and the 2000 list demonstrate degeneration in overall status of threatened birds in Australia. It is concluded that trends in conservation status are a valid long-term measure of the risk of biodiversity loss. Stabilisation of IUCN Red List definitions should mean that an increasing proportion of the status flux should be attributable to real changes in extinction probability. Crown Copyright # 2003 Published by Elsevier Science Ltd. All rights reserved. Keywords: Threatened; Australian; Birds; IUCN; Status
1. Introduction Since the IUCN started preparing lists of species that are threatened with extinction (see Collar, 1998; BirdLife International, 2000, for history) numerous assessments have been made of threatened species around the world. The number of taxa that have changed status from one time period to the next has then sometimes been used to determine trends in extinction probability over time (Smith et al., 1993) and will be used in the future ‘to develop indices of biodiversity trend’ (IUCN, 2001a). However, a comparison of global lists of threatened bird species between 1988 and 1994 found that only 3% of change in that time could be attributed to a genuine change in status (Crosby et al., 1994). The
* Corresponding author. Tel.: +61-7-4046-6601; fax: +61-7-40466643. E-mail address: [email protected] (S.T. Garnett).
remainder was attributed to changes in taxonomy (18%), increased knowledge (58%) and changes in IUCN Red List Categories and Criteria (20%). The imperiled nature of some Australian bird species was first mooted nearly a century ago (Campbell, 1915) but the first attempt to use standardized international criteria to assess the status of all Australia species did not occur until 1990 (Brouwer and Garnett, 1990). In 1992 this assessment was extended to include all species and subspecies of bird either breeding on Australian territory, including offshore islands, or for which > 5% of the global population was believed to visit regularly (Garnett, 1992, 1993). In 2000 the exercise was repeated (Garnett and Crowley, 2000). As with BirdLife International (2000), there were substantial differences between the two sets of assessments, only some of which can be attributed to real changes in the probability of extinction. This paper examines the nature of those differences, their implications for the assessment of trends in Australian threatened birds and for the funding of their conservation management.
0006-3207/03/$ - see front matter Crown Copyright # 2003 Published by Elsevier Science Ltd. All rights reserved. doi:10.1016/S0006-3207(02)00377-4
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2. Methods The status of all Australian taxa was assessed in 1992 and 2000 based on the accepted taxonomy, data on the biology of each taxon and the most recent IUCN Red List Criteria available at the time of the assessment (Garnett, 1992, 1993, Garnett and Crowley, 2000). In 2000 retrospective estimates were also made of the size and trend of population and distribution of each taxon in 1992 based on information available and taxonomy accepted in 2000. The status as it would have been in 1992 was then assessed using the IUCN Red List Criteria pertaining in 2000. Differences between 1992 and 2000 in assessment criteria, taxonomy and knowledge are summarised below. 2.1. Assessment criteria In 1992 the first quantitative assessment of the risk of threat had just become available (Mace and Lande, 1991). By 2000 Mace and Lande’s work had been refined and officially adopted by the IUCN (1994). The categories of Extinct, Critically Endangered, Endangered and Vulnerable were defined precisely, if slightly differently, in both publications (Table 1). Other categories used in 1992 and their 2000 equivalents were as follows: Rare: ‘taxa with small populations that are not at present ’Endangered’ or ’Vulnerable’, but are threatened. These taxa are usually localised within restricted geographical areas or habitats or are thinly scattered over a more extensive range’. In the 1992 assessment, most Rare taxa shared with the Vulnerable taxa a total population size believed to be less than 10,000 individuals. By 2000 this had effectively become the category Lower Risk (Near Threatened): ‘taxa. . . which are close to qualifying for Vulnerable’ (IUCN, 1994). For the purposes of the assessment Near Threatened taxa were considered to fall into one of the following categories based on Maxwell et al. (1996):
1. Reduced area of occupancy and/or extent of occurrence: taxa that have disappeared from over 50% of their former area of occupancy and/or extent of occurrence and are at risk of further decline. i.e. close to Vulnerable criterion B. 2. Decline in abundance: taxa that have experienced a significant and continuing decline in abundance in over 50% of their former area of occupancy and/or extent of occurrence. i.e. close to Vulnerable criterion A. 3. Small populations: taxa with populations smaller than 3000 mature individuals, or of unknown population size but suspected to be small. i.e. close to criterion D.
4. Regionally secure populations: taxa with small or restricted populations in Australia (hence could qualify as Vulnerable: D1 or D2) that are genetically continuous with secure regional populations. Such taxa were downgraded to Near Threatened as per Ga¨rdenfors et al. (1999). Insufficiently Known: species suspected of being ’Endangered’, ’Rare’ or ’Vulnerable’ but whose true status cannot be determined without more information. In 2000 the nearest equivalent was the category Data Deficient: a taxon where there is inadequate information to make a direct, or indirect, assessment of its risk of extinction based on its distribution and/or population status. A taxon in this category may be well studied, and its biology well known, but appropriate data on abundance and/or distribution are lacking. The two categories are not directly equivalent: Insufficiently Known taxa were threatened but the level of threat is unknown, Data Deficient taxa are not necessarily threatened. In fact, in 2000, Data Deficient was not used for any Australian taxon. Special Concern: ‘An unofficial category adopted by the ICBP (N. Collar pers.comm.) for taxa that are often treated as threatened but, at this stage, do not appear to warrant classification as Endangered, Vulnerable, Rare or Insufficiently Known’ (Garnett, 1992, 1993). These taxa were categorised as follows: 1. Taxa with very small (< 5 pairs) and possibly temporary breeding populations in Australia but which are secure elsewhere. In 2000 such taxa were assessed as Critically Endangered unless there was evidence of continuing genetic interchange with extralimital populations in which case the status was downgraded to Endangered as per Ga¨rdenfors et al. (1999). 2. Taxa that have suffered population declines in the past but for which the population has since stabilized or is increasing. In 2000 these were classified as Least Concern unless the absolute population size was now small enough to fall within the D criterion of a threatened category. 3. Taxa which have declined in parts of their range but are secure in the remainder. In 2000 such taxa were classified as Least Concern unless the population fell within one of the Near Threatened criteria 1 or 2. 4. Taxa with large populations which may warrant more concern in the future. In 2000 these were classified as Least Concern unless the decline was sufficiently severe to approach the Near Threatened category 2. 5. Taxa that occur in remote areas for which there is good evidence to suggest their abundance has previously been underestimated. In 2000 all such
Table 1 Comparison of the criteria used to assess the status of Australian birds in 1992 (Garnett, 1992) and 2000 (IUCN, 1994) Criteria
1992 (based on Mace and Lande, 1991) Rate of population decline: > X%/year for Y year >Z% in last generation
Frequency and extent of catastrophes (subpopulations highly correlated in population fluctuations): > X% reduction in population/5–10 year or every 2–4 generations or >50% reduction in population/Y year or every Z
Threatened species category Endangered
Vulnerable
X=20 Y=2 Z=50
X=5 Y=5 Z=10 in 2 generations X=20
X=1 Y=10
X=10
Y=50
Y=20
Z=5-10 generations X=5
Z=50 year
X=50 Z=2-4 generations
Extent of fragmentation: X populations of < Y individuals or 2 populations of > Z individuals immigration of < 1 individual/ generation
X=2 Y=125
Total population: < X individuals Probability of extinction: X% probability of extinction in Y years or Z generations whichever is sooner
2000 (based on IUCN, 1994) A. Population reduction in the form of either of the following: (1) An observed, estimated, inferred or suspected reduction of at least X% over the last 10 years or three generations, whichever is the longer OR (2) A reduction of at least X% over the last 10 years or three generations, whichever is the longer, projected or suspected to be met within the next ten years or three generations, whichever is the longer. C. Population estimated to number less than X mature individuals and either (1) An estimated continuing decline of at least Y, whichever is longer, OR (2) A continuing decline, observed, projected, or inferred, in numbers of mature individuals and population structure in the form of either: (a) severely fragmented (i.e. no sub-population estimated to contain more than Z mature individuals) (b) all individuals are in a single sub-population.
B. Extent of occurrence estimated to be less than X km2 or area of occupancy estimated to be less than Y km2, and estimates indicating any two of the following: (1) Severely fragmented or known to exist at Z location. (2) Continuing decline, observed, inferred or projected, in any of the following: (a) extent of occurrence (b) area of occupancy (c) area, extent and/or quality of habitat (d) number of locations or sub-populations (e) number of mature individuals. (3) Extreme fluctuations in any of the following: (a) extent of occurrence (b) area of occupancy (c) number of locations or sub-populations (d) number of mature individuals.
D. Population estimated to number less than X mature individuals, OR (Vulnerable only) Population is characterised by an acute restriction in its area of occupancy (typically less than 100 km2) or in the number of locations (typically less than 5). Such a taxon would thus be prone to the effects of human activities (or stochastic events whose impact is increased by human activities) within a short period of time in an unforeseeable future, and is thus capable of becoming Critically Endangered or even Extinct in a short period. E. Quantitative analysis showing the probability of extinction in the wild is at least X% within Y years or Z generations, whichever is the longer
X=5 Y=2500 Z=5000 X=10,000 X=10 Y=100
X=80
X=50
X=20
X=250
X=2500
X=10,000
Y=25% within 3 years or 1 generation Z=50 X= < 100 km2
Y=25% within 3 years or 2 generations Z=250 X= < 5000 km2
Y=10% within 10 years or 3 generations Z=1000 X= < 20,000 km2
Y= < 10 km2 Z=1 X=50
Y= < 500 km2 Z= < 6 X=250
Y= < 2000 km2 Z= < 11 X=1000
X=50% within Y=10 years or Z=3
X=20
X=10
Y=20 Z=5
Y=100
271
X=250 X=50 Y=5 Z=2
Y=500 Z=1250 X=2500 X=20 Y=20 Z=10
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Critically endangered
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taxa were classified on the basis of whatever information could be assembled. 6. Taxa with relatively small populations (5000– 10,000 individuals) but for which no decline has been suggested and plausible threats are lacking. In 2000 such taxa were listed as Least Concern unless they approached Near Threatened criterion 3 or were geographically confined to the extent they approached Vulnerable criterion D. Secure: any taxon that did not fall into one of the above categories. In 2000 the equivalent category was Lower Risk (Least Concern). Such taxa were assessed but did not qualify for any other category. 2.2. Taxonomy In 1992 no widely accepted Australian taxonomy was available. The taxonomic scope of the assessment was therefore decided largely from consultation with leading Australian taxonomists: Richard Schodde and Les Christidis. By 2000 major taxonomic analyses had been completed; so for genera and species taxonomy followed Christidis and Boles (1994) except for albatrosses, some hawk-owls and grasswrens where Robertson and Nunn (1998), Norman et al. (1998), Christidis (1999) and Schodde and Mason (1999) were used at the species level and Marchant and Higgins (1990, 1993), Higgins and Davies (1996), Schodde and Mason (1997, 1999) and Higgins (1999) were followed at the subspecies level. 2.3. Knowledge Substantial support was provided for threatened species surveys and research during the 1990s (see Garnett and Crowley, 2000 for details on individual taxa). This increased knowledge of trends and rates of change in population size and distribution, as well as the nature and severity of threatening processes. Most of this knowledge is thought likely to have pertained to the threatened taxa at the time of the 1992 assessment. Its absence therefore resulted in a misapplication of status to some taxa. 2.4. Funding As part of the 2000 assessment, information was obtained on funding dedicated to the conservation of threatened bird taxa from 1992 and 1999 for all taxa listed in Garnett (1993), though excluding taxa listed as being of Special Concern in 1992 that were subsequently considered to have been Least Concern. Economic information was obtained primarily through personal communication from project officers and government managers responsible for threatened species programs
during the period, and was augmented by recovery plans when available. Gross figures only were obtained and covered salaries of dedicated project officers, project running costs (travel, accommodation, minor contracts, consumables etc.) and capital items (mostly vehicles). Most figures are estimates accurate to the nearest $1000 (Australian). Costs for which no estimate was made were the routine costs of protected area management which may have benefited threatened species, administrative costs incurred during proposal preparation and operation, unsalaried time donated by paid participants, opportunity costs of private landholders and travel costs of volunteers. A more detailed analysis of this information is in preparation (Garnett et al., in press), but the more restricted assessment is used here to compare expenditure on threatened taxa based on the 1992 classifications compared to the adjusted classifications and the classifications in 2000. Expenditure between categories was compared using the nonparametric Terpstra-Jonckhere test for independent samples (Neave and Worthington, 1988). Proportions were compared using w2.
3. Results Overall, a third of Critically Endangered and Endangered taxa and over half the taxa classified as Vulnerable in 1992 were given a different classification when re-assessed in 2000 (Table 2) as a result of changes in IUCN Red List criteria, rearrangements of taxonomy and new knowledge. Changes in the IUCN Red List Criteria, principally to provide greater precision to definitions, accounted for the majority of the differences, with surveys and research most of the remainder (Table 3). A few more taxa would have been listed in 1992 had recent taxonomic revisions been complete. Surveys and research allowed attribution of status to many taxa listed as Insufficiently Known in the first Action Plan. They also tended to show that taxa had smaller populations, were declining more quickly or were facing a greater threat than had been realised in 1992 (Table 4). The changes to the IUCN Red List Criteria that had most influence on changes in status were those relating to trends of small populations (criterion C) and those identifying the vulnerability of populations on islands (criterion D). Rates of population change were most important for identifying taxa meeting the criteria for the Near Threatened category Table 5). When the revised status in 1992 was compared with that in 2000, a total of 25 taxa changed status, a flux of 2.0%. Of these, the status of 18 taxa deteriorated (72.0%), 10 by two status levels; seven improved and there were no confirmed extinctions (Table 6). When the status as assessed in 1992 was compared with the status
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in 2000, 172 taxa had a worse status after eight years (75.4%), 135 declining by two or more status levels, and there were three extinctions; 56 taxa had an improved status including four that increased by two or more status levels. A total of 228 taxa would have changed status, a flux of 18.2%. Thus just 11% (25/228) of changes in taxa could be attributed to changes in the probability of extinction.
Based on the 1992 assessments, funding/taxon increased as status declined (W=208n=6,14,30, P < 0.01, Fig. 1). For the revised classifications, however, this relationship no longer held (W=1002n=15,33,50, P > 0.05). If the revised classifications had been used as a basis for funding, and the rate of funding of individual taxa in each status remained the same, then total funding would have increased by 10% for Critically Endangered
Table 2 Comparison of status between the Action Plan for Australian Birds (Garnett, 1992) using IUCN criteria, knowledge and taxonomy pertaining in 1992 and a retrospective analysis based on the criteria, knowledge and taxonomy current in 2000a
a Shaded cells enumerate the taxa assessed as having a similar extinction probability in 1992 regardless of assessment type. The 1992 assessment of extinction probability was excessively sanguine for taxa enumerated in cells below the diagonal but alarmist for those above it.
Table 3 Reasons for differences in status between the Action Plan for Australian Birds (Garnett, 1992) and a retrospective analysis using IUCN criteria, knowledge and taxonomy pertaining in 2000 Reason for change in status
No. of taxa
% Taxa
Further research Further surveys More rigorous IUCN criteria More rigorous IUCN criteria and taxonomic revision Taxonomic revision
39 22 140 11 19
16.9 9.5 60.6 4.8 8.2
Total
231
100.0
Table 4 Results of research and surveys on assessment of threatened taxon status Nature of study
Result of research
Trend
No. of taxa
Surveys
Population size/distribution area
Larger than anticipated Stable Smaller than anticipated Insufficient previous data
4 2 4 12
Increasing Stable Decreasing More severe No change Less severe Insufficient previous data
0 4 11 26 0 0 2
Investigation of insufficiently known taxa to enable status attribution Biological research
Trend in population/distribution
Severity of threatening process
Investigation of insufficiently known taxa to enable status attribution
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taxa and 82% for Endangered taxa, but decreased for Vulnerable taxa by 61%.
4. Discussion In a similar global comparison of status change between two time periods, changes in taxonomy were Table 5 Relative importance of refinement of IUCN criteria Retrospective status
IUCN sub-criterion
Critically endangered
C D B C D C D A C D A B C D
1 4 2 1 8 4 38 16 22 18 2 1 18 2
0.7 2.9 1.5 0.7 5.9 2.9 27.2 11.8 16.2 13.2 1.5 0.7 13.2 1.5
A B C D
18 3 46 69
13.2 2.2 33.8 50.7
Endangered
Vulnerable Near threatened
Least concern
Subtotals
Total
No. taxa
136
% Taxa
100
the most important source of variation in status (Crosby et al., 1994). For Australia, however, taxonomy was relatively stable because the same taxonomic advisers were used in both Action Plans, and because all assessments were at the subspecies level. In those parts of the world where most threatened taxa occur there is rather more taxonomic uncertainty and inconsistency, especially at the species level. The level of knowledge about threatened birds is also relatively high in Australia allowing assessment of all bird taxa and the listing of none as Data Deficient. Globally 79 species are listed as Data Deficient (BirdLife International, 2000). The most important cause of status change was therefore changes to the IUCN Red List Criteria. In this analysis the two most important refinements to the criteria were the conditions under which criterion C, which describes trends in small populations, can be applied and the inclusion of criterion Vulnerable: D2 under which the vulnerability of populations on small islands and other restricted areas is recognised. Thus the revised list includes many island taxa that were excluded in the 1992 analysis. The comparison of the initial and revised statuses thus shows that great care must be taken in comparing trends in status over time, particularly if IUCN Red List trends are to become indicators of trends in biodiversity (IUCN, 2001a). Correct allocation of status is also important for its effect on conservation funding. While the Action Plan was only one of many influences on funding quantity and priority in Australia, the hypothetical results for the threatened taxa suggest that
Table 6 Comparison of the status of Australian bird taxa 1992–2000 based on assessment as undertaken in 1992 (upper table) and status as assessed retrospectively (lower table)a
a Highlighted cells are for taxa that retained the same status. Cells below the highlighted diagonal contain the number of taxa in each category assessed as having a higher risk of extinction in 2000, while the prospects for taxa enumerated in cells above the diagonal are assessed as having improved.
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Acknowledgements We are most grateful for help in collecting the original data from the broad suite of conservation biologists, both professional and amateur, who contributed to the two Action Plans for Australian Birds. The original data were collected by Stephen Garnett and Gabriel Crowley for Birds Australia under contract to Environment Australia and prepared for publication while Stephen Garnett was on sabbatical from the Queensland Parks and Wildlife Service at BirdLife International and the Conservation Biology Group in the Zoology Department of Cambridge University. Clive Cook made the writing possible and Nigel Collar commented on the manuscript. Fig. 1. Funds/taxon provided for Australian threatened birds 1993– 2000 based on status as assessed in 1992 (Garnett, 1992; clear box) compared to the amount/taxon provided based on a retrospective assessment (IUCN, 1994; shaded box). Dark points are medians, boxes are upper and lower quartiles, whiskers are maximum and minimum excluding outliers (winged circles).
funds could have been substantially reallocated had the revised allocations been possible in 1992. Some flux, however, is inevitable. Conservation science is a young discipline so it is likely that the IUCN Red List Categories will be adjusted again. Indeed there are small but important differences between criteria used for Australian birds in 2000 (IUCN, 1994) and those now being applied around the world (IUCN, 2001b). Similarly taxonomy is in a constant state of refinement, particularly as a result of increased use of molecular techniques. Technology is also allowing major improvements in the demographic studies needed to determine population sizes, ranges and trends. Reductions in the size of radio-transmitters, for instance, have allowed the study of many cryptic and mobile taxa while satellites enable increasingly accurate assessments of trends in tree cover. While Government may crave stability of status for the purposes of consistent policy and legislation, there has to be enough flexibility within legal instruments to accommodate status flux whatever its source. In particular status needs to be assessed frequently to keep abreast of changes and ensure annual funding allocations best reflect needs. Despite a high level of status flux, the comparison of status between periods can still be worthwhile. Although the flux in status between assessments was ten times greater for the direct comparison than the adjusted comparison, the trend was almost identical—75% of changes negative in the former compared to 72% in the latter. The 11% of variation in status that could be ascribed to real changes in the probability of extinction can thus become a useful long-term indicator of the risk of biodiversity loss (IUCN, 2001a).
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