Introduction
Extinction is the inevitable end-point for all lifeforms (Koopowitz & Kaye, Reference Koopowitz and Kaye1990; Purvis et al., Reference Purvis, Jones and Mace2000), but the present rate of extinctions globally is estimated to be one thousand times the natural or background rate as a result of anthropogenic pressures on habitats and species (Barnosky et al., Reference Barnosky, Matzke, Tomiya, Wogan, Swartz and Quental2011; Pimm et al., Reference Pimm, Jenkins, Abell, Brooks, Gittleman and et al2014). Ignoring unproven re-creations, extinction of a species is irreversible and has biological, evolutionary and emotional consequences (Koopowitz & Kaye, Reference Koopowitz and Kaye1990; Ryan, Reference Ryan2009; Collen et al., Reference Collen, Purvis and Mace2010). With every global extinction, a unique evolutionary history is lost and the web of life irrevocably altered and diminished.
Yet despite the finality and magnitude of extinction, the actual event can be difficult to verify. Biology is replete with instances of so-called Romeo errors, in which species are declared or presumed extinct only to be rediscovered (Collar, Reference Collar1998). Prominent recent examples include the ivory-billed woodpecker Campophilus principalis of the Big Woods of Arkansas (Fitzpatrick et al., Reference Fitzpatrick, Lammertink, Luneau, Gallagher, Harrison and Sparling2005) and the enigmatic night parrot Pezeropus occidentalis of the Australian desert (Dooley, Reference Dooley2013). There have also been quieter rediscoveries amongst plants (Scott & Yeoh, Reference Scott and Yeoh1995; Wapstra et al., Reference Wapstra, Duncan, Buchanan and Schahinger2006; de Lírio et al., Reference de Lírio, Freitas, Negrão, Martinelli and Peixoto2017; Sochor et al., Reference Sochor, Egertova, Hrones and Dancak2018) and invertebrates (Bonham, Reference Bonham1997; Byk et al., Reference Byk, Bezdek, Gazurek, Kral and Tylkowski2018), and species whose continued existence remains the subject of intense debate, sometimes entering the realm of mythology, as for the Tasmanian tiger Thylacinus cynocephalus (Bailey, Reference Bailey2013).
The problem of verifying extinctions is a vexed issue for policy makers and scientists. IUCN guidelines state a species should be considered extinct when ‘there is no reasonable doubt that the last individual has died’ and that this is reliant on ‘exhaustive surveys in known and/or expected habitat, at appropriate times…throughout its historic range’ (IUCN, 2012). It has been argued that the IUCN criteria may not be an appropriate onus of proof when the aim is to assess extinctions accurately and consistently, and will severely underestimate extinctions (Butchart et al., Reference Butchart, Stattersfield and Brooks2006; Mace et al., Reference Mace, Collar, Gaston, Hilton-Taylor, Akcakaya and Leader-Williams2008). In response to these concerns, the latest Red List Guidelines have an additional tag of ‘Critically Endangered (Possibly Extinct)’ for taxa ‘that are, on the balance of evidence, likely to be extinct, but for which there is a small chance that they may be extant’ (IUCN Standards and Petitions Subcommittee, 2017, p. 79). These taxa should not be listed as Extinct until adequate surveys have been completed and unconfirmed reports investigated.
Statistical methods have also been developed for inferring extinction based on collection records and survey effort (Reed, Reference Reed1996; Solow, Reference Solow2005; Collen et al., Reference Collen, Purvis and Mace2010). These tend to be based on the distribution of sightings or collections through time, which can be used to calculate the expected rate of sightings if a species were extant. Although these formulae partially account for factors such as species abundance and detectability, they cannot account for life history traits (such as dormant or cryptic stages) and the potential complexity of a species’ ecology, particularly when it is poorly known. Moreover, they rely on an adequate sample size (typically considered to be > 5 records; Collen et al., Reference Collen, Purvis and Mace2010) and can seldom be applied to species with only one or two records, which is the case for many plants that are presumed extinct. Recent methodologies to estimate extinction probability have incorporated the timing and degree of threat, and a taxon's susceptibility (Keith et al., Reference Keith, Butchart, Regan, Harrison, Akcakaya, Solow and Burgman2017), and record reliability and survey data (Thompson et al., Reference Thompson, Koshkina, Burgman, Butchart and Stone2017).
Listing of a species as Extinct has significant conservation implications for allocation of resources and environmental reporting (Keith & Burgman, Reference Keith and Burgman2004). Thus it is important that lists of presumed and possibly extinct species are as accurate and transparent as possible. It has been estimated that Australia accounts for almost 20% of the world's flora that has been recently categorized as Extinct (Briggs & Leigh, Reference Briggs and Leigh1996), a fact that is usually explained by the continent's long isolation, high floristic endemism, and rapid and severe recent land-use changes (Lindenmayer, Reference Lindenmayer2007; Nipperess, Reference Nipperess, Stow, Maclean and Holwell2015). However, lists of Australia's extinct plants are characterized by high turn-over, low transparency of attribution and lack of consistency between jurisdictions (Keith & Burgman, Reference Keith and Burgman2004). The first assessment in Australia defined Presumed Extinct species as not found despite thorough searching or not collected for at least 50 years, and formerly known from areas now well-settled, and listed 78 species that met those criteria (Leigh et al., Reference Leigh, Briggs and Hartley1981). Between 1984 and 2004, 115 taxa were added to the list of extinct Australian plants, mostly as a result of new evaluations, and 167 were deleted, mostly as a result of rediscoveries, but also because of taxonomic changes or corrections (Keith & Burgman, Reference Keith and Burgman2004). This high turnover has continued, with numerous species discussed by Keith & Burgman (Reference Keith and Burgman2004) either rediscovered or synonymized, and numerous new species being added to national and state lists. The number of plant taxa that are actually likely to have become extinct in Australia is currently unknown, and without clearly defined criteria the issue will continue to be a point of confusion for plant conservation.
We present a transparent and uniform ecological framework for assessing plant extinctions, underpinned by expert knowledge of species and habitats. We provide an estimate of the current number of plant extinctions in Australia since 1788 and present a revised list of probably and possibly extinct species. This method can be used for vascular floras in other regions characterized by well-documented and curated floras and high levels of expert knowledge, and provides a coherent platform for assessing changes in the status of biodiversity.
Methods
We compiled a spreadsheet of taxa listed as Extinct according to the national Environment Protection and Biodiversity Conservation Act 1999 and lists of threatened species from individual states and territories. We also added unlisted taxa that are considered by experts, or noted in taxonomic treatments or state censuses, to be potentially or probably extinct. Taxa that are considered extinct in the wild but persist in translocated populations were included. Taxa that are not currently known from any living plants but are known to be extant in the soil seedbank or are considered extinct in one jurisdiction but still occur elsewhere in Australia were not included. Subspecies were included, but varieties, generally considered to be of lower taxonomic status, forms and hybrids are not considered here. We acknowledge that the distinction between subspecies and variety is unevenly applied by taxonomists, but have adopted this approach to filter out at least some trivial taxa. A separate list of taxa that have formerly been presumed to be globally extinct under national and/or state legislation was also compiled, to shed light on relevant factors behind extinction likelihood and assessment. Taxa listed as Extinct but that have been recently rediscovered were included.
For each taxon, data were compiled from Australian Virtual Herbarium records (CHAH, 2016), Conservation and Listing Advice, Recovery Plans, peer-reviewed literature, the assessments of Leigh et al. (Reference Leigh, Boden and Briggs1984) and Briggs & Leigh (Reference Briggs and Leigh1996), and consultation with experts with field knowledge of species and habitats. Variables included the last date collected, survey effort and adequacy (Thompson et al., Reference Thompson, Koshkina, Burgman, Butchart and Stone2017), degree of habitat modification, intensity and extent of threats (Keith et al., Reference Keith, Butchart, Regan, Harrison, Akcakaya, Solow and Burgman2017), detectability and life history of the species, and any taxonomic issues (Table 1). Taxa for which expert opinion or examination of specimens indicated they are morphologically close to co-occurring taxa and may not be taxonomically distinct were removed from further assessment, as were those whose occurrence in Australia is considered dubious. Species that also occur outside Australia were retained, but collecting dates and habitat notes relate only to Australian records.
Data compiled for each presumed extinct taxon in the Australian vascular flora.
To place some transparent and simple criteria around assignation of extinction likelihood, we devised a key containing relevant factors from Table 1. Through this key, each of the taxa currently listed as Extinct in Australia was assigned an extinction confidence/likelihood: (1) Almost certainly extinct, (2) Probably extinct, (3) Possibly extinct (on the balance of evidence, must be considered extinct but requires further surveys where possible to confirm its status), and (4) Possibly extant (surveys undertaken thus far have not been sufficient to consider the taxon extinct).
In the key, a taxon can be found at any stage from step 5. This possibility is not included in the key, as it will of course lead to removal of the species from any extinction considerations. It is also possible to locate the target species with searching, but for taxonomic uncertainty to preclude definitive identification; this will mean returning to step 1. The amount of survey effort before assuming extinction has occurred increases with lack of spatial precision, low habitat modification/threat and cryptic lifeform stages/low detectability. It is impossible to get more certain than probably extinct unless precision of at least one record is < 5 km2, or > 90% or remaining habitat is surveyed, and detectability is high or surveys span multiple seasons and years. The cut-off for record accuracy is the approximate amount of habitat that can be confidently searched by a botanist in one day. This will vary between habitats and lifeforms, but 5 km2 is considered reasonable based on > 2,000 hours of our own searching for rare plants. The 90, 70 and 50% cut-offs for area of suitable habitat searched are intended as reasonable guiding estimates. Assessments of the level of understanding of a taxon's life history and optimum survey times relies upon expert opinion.
Key for assessing extinction likelihood in vascular floras
The number of taxa from the 71 presumed extinct Australian species is indicated at each couplet.
1. Subject to taxonomic uncertainty………Revise taxonomy (n=13)
1a. Reliable taxon or sufficient certainty to warrant further searching………2
2. Suspected identification or location error, and taxon unlikely to occur in Australia……… Discard unless further information available (n=7)
2a. Identification correct and record likely from Australia……… 3 (n=51)
3. At least one collection record able to be located to within 5 km2………4 (n=14)
3a. No records able to be located within 5 km2………11 (n=37)
4. Long-lived species, no cryptic lifeform stages………5 (n=5)
4a. Ephemeral species or geophyte, cryptic or dormant lifeform stage/s……… 8 (n=9)
5. Habitat highly modified or destroyed AND/OR well-known threatening process………6 (n=3)
5a. Habitat not or only lightly modified AND no well-defined threatening process………7 (n=2)
6. Thorough searching at site/s and > 90% of potential habitat………Almost certainly extinct (n=2)
6a. Thorough search effort at site/s and > 70% of potential habitat………Probably extinct (n=1)
6b. Search effort less than 6a………Possibly extinct; surveys needed to confirm (n=0)
7. Thorough searching at site/s and > 70% of other potential habitat………Probably extinct (n=0)
7a. < 70% of site and suitable habitat effort at site/s ………Possibly extinct; further surveys needed (n=2)
8. At least moderate understanding of life history/optimum survey times (e.g. seasonal conditions/disturbance events likely to have resulted in germination)………9 (n=1)
8a. Understanding of life history less than 8……… 10 (n=7)
9. Thorough searching at site/s and > 70% of suitable habitat at more than one optimum time/s AND habitat highly disturbed OR threatening process operating………Probably extinct (n=2)
9a. Thorough searching at site/s AND > 70% of suitable habitat at more than one optimum time/s; habitat not or lightly modified AND no well-defined threats………Possibly extinct (n=0)
9b. Search effort less than 9a………Possibly extant, surveys needed (n=0)
10. Site/s of historic collection + > 90% of other potential habitat searched across multiple seasons and conditions AND habitat highly modified……… Probably extinct (n=3)
10a. Site/s of historic collection + 50–90% of other potential habitat searched across multiple seasons and conditions AND habitat highly to moderately modified……… Possibly extinct (n=3)
10b. Site/s of historic collection not well-searched and/or < 50% of potential habitat searched across multiple seasons and conditions………Possibly extant; further surveys in various seasons needed (n=1)
11. Habitat not known from record labels; record precision > 100 km2……… 12 (n=4)
11a. Habitat able to be inferred, at least broadly……… 13 (n=33)
12. General area highly modified and well-surveyed……… Possibly extinct (n=4)
12a. General area not highly modified and no major threats identified……… Possibly extant (n=0)
13. Habitat highly modified AND/OR documented threatening process/es ……… 14 (n=8)
13a. Habitat not heavily modified, or at least large remnants remaining unaffected by major threatening processes ………19 (n=25)
14. Long-lived species, no cryptic lifeform stages ……… 15 (n=4)
14a. Ephemeral species or geophyte, cryptic or dormant lifeform stage/s………16 (n=4)
15. > 90% of potential habitat searched………Probably extinct (n=3)
15b. 50–90% of potential habitat searched……… Possibly extinct; further surveys needed (n=1)
15c. < 50% of potential habitat searched………Possibly extant; further surveys needed (n=0)
16. Good understanding of species, life history/optimum survey times ………17 (n=0)
16a. Poor understanding of species, life history……… 18 (n=4)
17. > 90% of potential habitat searched repeatedly at optimum times………Probably extinct (n=0)
17a. 50–90% of potential habitat searched at optimum times………Possibly extinct (n=0)
17b. < 50% of potential habitat searched at optimum times ………Possibly extant (n=0)
18. > 90% of potential habitat searched repeatedly in multiple seasons………Probably extinct (n=1)
18a. > 70% of potential habitat searched repeatedly in multiple seasons……… Possibly extinct (n=3)
18b. < 70% of potential habitat searched……… Possibly extant; surveys in various seasons needed (n=0)
19. At least moderately detectable taxon with no cryptic lifeform stages………20 (n=16)
19a. Low detectability, complex disturbance response and/or cryptic lifeform stages……… 21 (n=9)
20. > 70% of potential habitat searched……… Possibly extinct (n=5)
20a. < 70% potential habitat searched ……… Possibly extant; further surveys needed (n=12)
21. Good understanding of species life history/optimum survey times……… 22 (n=1)
21a. Poor understanding of species life history……… 23 (n=7)
22. > 70% of potential habitat searched repeatedly at suitable times………Possibly extinct (n=0)
22a. < 70% of potential habitat searched repeatedly at suitable times……… Possibly extant; further surveys recommended (n=1)
23. > 70% of potential habitat searched across numerous seasons……… Possibly extinct (n=4)
23a. < 70% of potential habitat searched………Possibly extant; further surveys in various seasons recommended (n=3)
Results
Overview of presumed extinct plants
Of the 71 Australian plant taxa currently listed as or presumed to be extinct, 13 (18%) are considered to be taxonomically suspect (Supplementary Table 1). Nine of these are known only from the type specimen, which often comprises incomplete fragments, and the other four are known from 2–5 collections. Seven have not been collected for the past 100 years. All are very close morphologically to other co-occurring species, and belong in groups regarded as taxonomically ill-defined and difficult, for example Frankenia L., Hemigenia R.Br. and the Orchidaceae genera Caladenia, Diuris and Prasophyllum.
The occurrence in Australia of a further seven presumed extinct taxa, all ferns from the Wet Tropics of north-eastern Australia, is dubious (Supplementary Table 1). All are relatively widespread tropical ferns and their extinction in Australia would represent local extinctions, but their apparent occurrences in Australia represent highly disjunct, and sometimes biogeographically unlikely, populations. Three are known only from collections by Czech botanist Karel Domin in 1909, and two from Domin's published descriptions without specimens. There are large areas of intact rainforest habitat where they occurred and there has been extensive survey effort in these areas. Where specimens are available, they have been verified as being correctly identified, however a labelling error on this batch of specimens cannot be ruled out, as Domin also visited areas outside Australia on the same expedition where the ferns in question do occur.
There are 51 taxa with sound taxonomy and unambiguous occurrences in Australia that are currently considered extinct (Supplementary Table 2). Although experts consider them all reliable taxa, there has been some degree of taxonomic confusion with closely-related species in the past for 19, and hybrid origins of four cannot be discounted without further material. Eighteen of the 51 taxa are listed as Extinct under both the national Environment Protection and Biodiversity Conservation Act and state legislation, and a further 14 are listed only under state legislation. Fourteen are listed as either Critically Endangered, Endangered, Vulnerable or Priority Flora (Western Australia) under the Environment Protection and Biodiversity Conservation Act and/or state legislation, and five are unlisted, but recent publications, taxonomic treatments, state censuses and/or expert opinion consider them potentially extinct. Most families are represented by one or two taxa, but Asteraceae stands out with nine species and Fabaceae and Proteaceae with five and four, respectively. Western Australia has the highest number of presumed extinct taxa (16, all bar one from the south-west), followed by New South Wales (15) and Queensland (13). The Northern Territory and Australian Capital Territory have no presumed extinct plants. Three presumed extinct taxa come from islands. Shrubs are the most represented life form, with 22 presumed extinct taxa, followed by mostly short-lived forbs (18).
All taxa presumed extinct seem to have been rare and/or restricted throughout their historic range, with 22 known from a single collection and all bar five known from < 5 collections. Only three are known from ≥ 5 populations. Twenty-four have not been collected in the last 100 years and 41 in the past 50 years. Those with more recent collections have been searched for repeatedly at sites where they formerly occurred and not found, or the habitat has been destroyed. At least 23 are regarded as difficult to detect, having tiny growth habits, cryptic life forms and/or complex seed bank or disturbance dynamics. More than half are known or strongly suspected to respond positively to disturbance.
Assessing extinction likelihood
Applying our key of ecological and survey factors, only two species are considered almost certainly extinct in the wild (although one persists in a translocated population), 10 are considered probably extinct and 21 possibly extinct (Table 2). The remaining 18 taxa are classified as possibly extant, primarily because of lack of adequate surveys to inform their status.
Presumed extinct taxa in the Australian vascular flora, and their extinction likelihood as assessed using the methodology described here. Taxa from different regions are separated by semi-colons.
To be assigned to the almost certainly extinct category, a species must have a record with high locational precision (< 5 km2), which has been searched at an appropriate time/s by expert botanists. A high proportion of other suitable habitat in the vicinity will also have been searched. There will usually, although not always, be a demonstrable threat from destruction or major modification of habitat. This condition was met for just two species, Allocasuarina portuensis, which is almost certainly extinct in the wild but persists as translocated plants at a number of locations (Office of Environment & Heritage, 2017) and Streblorrhiza speciosa, a scrambling shrub known from the highly modified Phillip Island in the Norfolk group that has not been seen since 1830 despite targeted surveys (Schrire, Reference Schrire2007).
The 10 taxa considered probably extinct come from highly modified agricultural and urban areas with little remnant vegetation, including four from south-western Australia and three from the Greater Sydney area. All have at least one record that could be located to within 50 km2 (with the exception of Acacia kingiana, the record only being accurate to within 200 km2 but with a clear habitat description) and have had > 70% of remaining habitat searched (> 90% for seven taxa). Five are considered to have low detectability, and most probably respond to disturbance. Paradoxically, species with more recent records are more likely to be assessed as probably extinct, as these more recent records are known from precise localities, whereas older records often have very low precision, rendering targeted survey difficult.
Although records could be located within 5 km2 for only 14 taxa, habitat could be inferred, at least broadly, for all except four taxa (Supplementary Tables 1 & 3). All four are James Drummond collections from south-western Western Australia, collected in the 1840s–1850s from an area that is now both heavily modified and well-surveyed botanically. Thus despite lack of location precision, three are assigned as possibly extinct. A further 10 Western Australian taxa were assessed as possibly extinct, as well as six from south-eastern Australia and three from the north-east of New South Wales (Table 2). Location precision and detectability vary, but nearly all have had at least > 70% of potential habitat searched (repeatedly for taxa with cryptic life forms stages and seasonal fluctuations in abundance). The habitat of seven is highly modified. Two species, the short-lived disturbance-responsive forb Corchorus thozetii from central Queensland and the shrub Pomaderris sericea from mountainous terrain in Victoria and New South Wales, have had < 70% of remaining potential habitat searched at appropriate times but are known from at least one accurate record that has been revisited without the species being relocated. In the case of the former, the site where it was collected in the 1990s has now been cropped, but other suitable habitat remains unsurveyed. The main reason for possibly extinct taxa not being assessed as probably extinct was that their habitats were not highly modified and there were no threats affecting the entire range of the species. This often occurred in concert with low detectability and/or complex and poorly-understood disturbance dynamics.
The remaining 18 taxa assessed as possibly extant have had < 70% of their potential habitat searched, and in some cases much less, combined with large areas of remnant suitable habitat and few severe threats. The exception is Genoplesium sp. (Raby Bay), which would have been ranked as probably extinct as a result of the high level of habitat modification, until a possible collection of an infertile specimen in 2017 (Lui Weber, pers. comm., February 2018). Twelve of these taxa are known or strongly considered to be responsive to disturbance, with large temporal fluctuations further increasing the demands for repeated surveys to reliably infer extinction. Five are from the rainforests of north Queensland, and another five from the sub-coastal and coastal areas of Queensland.
Formerly extinct plants
More than 120 taxa previously presumed extinct (i.e. listed under state and/or federal legislation and/or Leigh et al. (Reference Leigh, Boden and Briggs1984) or Briggs & Leigh (Reference Briggs and Leigh1996), or identified as such in published sources such as taxonomic treatments) have been rediscovered in Australia, mostly since the 1980s (Supplementary Table 3). Over half of these (67) have been straightforward rediscoveries in the field, but 36 have involved rediscoveries of specimens collected decades earlier that had not been correctly identified at the time of their collection. In many cases, taxonomic revisions or apparent field rediscoveries trigger re-examination of collections. Conversely, specimen rediscoveries sometimes result in renewed targeted surveys, which in turn locate further populations. Only five of the 36 specimen rediscoveries have occurred in isolation from field rediscoveries. The remaining 24 taxa presumed extinct have been removed because of taxonomic revision revealing them as synonyms of more widespread taxa (in 19 cases), of hybrid origin or more widespread than previously thought as a result of revision of the species’ concept. Seven of these taxa are still listed on extinct lists, including five under the Environment Protection and Biodiversity Conservation Act.
The average time that these rediscovered plant species have been apparently lost (excluding those with taxonomic issues) was 93 years, and 42 had not been seen for > 100 years before they were rediscovered. Western Australia accounts for > 60% of rediscoveries (n = 74), with 21 from Queensland. One-third are known from highly modified habitats, a factor that contributed to their being considered extinct, but 40 are known from habitats that mostly remain in remnant condition, with few threats present. Fifty-six are shrubs, 41 annual or perennial forbs, nine grasses and sedges, and eight ground orchids. More than 50 were known from a single recognized collection prior to their rediscovery, while only six had been known from > 5 collections. Over half of formerly presumed extinct plants are now known to be abundant or at least locally common, although > 45% of these respond to fire or other disturbance and thus exhibit large temporal fluctuations. Although 19 remain known from a single rediscovered population and are categorized as Endangered or Critically Endangered, 44 are now known from at least 10 populations. Eighty-two per cent of rediscoveries and specimen rediscoveries have occurred since 1980, with over half of these occurring in the 1990s. There has been an average of one rediscovery per year over the past decade across Australia, the latest being the ferns Oreogrammitis leonardii and Hymenophyllum whitei, both collected for the first time in 70 years in 2018 on remote mountain tops in far north Queensland, and the shrub Acacia prismifolia, collected beside a busy highway in south-western Australia in 2018, having not been seen since 1933.
Discussion
The systematic assessment of extinction likelihood amongst the Australian vascular flora reveals that the true extinction toll is far less than previous assessments, in sharp contrast to the general perception that the number of identified extinctions languishes behind the true number that have occurred (Butchart et al., Reference Butchart, Stattersfield and Brooks2006; Collen et al., Reference Collen, Purvis and Mace2010). This is partly a result of the listing of many plant species that are now considered taxonomically dubious or that never occurred in Australia, and partly a result of the vastness and inaccessibility of some largely unmodified habitat types, the tiny proportion able to be feasibly surveyed, and the cryptic life form stages of many species (a response to Australia's variable climatic conditions). The history of rediscoveries and taxonomic changes reinforces the fact that taxonomic assessment and adequate surveys must precede any declarations of extinction, especially if large swathes of habitat are still intact and threatening processes cannot be identified.
Species with unresolved taxonomy, and those with dubious Australian occurrences, should be prioritized for taxonomic revision and specimen re-examination to clarify their status (Wege et al., Reference Wege, Thiele, Shephard, Butcher, Macfarlane and Coates2014). The species assigned possibly extant and possibly extinct should be searched for where possible, with a focus on accurate recording of search effort, and seasonal and habitat condition (Keith, Reference Keith2000; Silcock et al., Reference Silcock, Healy and Fensham2014). We suggest that taxa assessed as possibly extinct should be retained on lists, or added where necessary, and those that are listed as possibly extant should be removed pending further survey. This treatment would leave 33 taxa as presumed extinct in Australia, albeit with two-thirds ranked as possibly rather than probably extinct. Two-thirds occur in highly modified habitats with well-documented threats, particularly where habitat clearing for agriculture and urbanization coincides with high levels of narrow-range endemism (Burgman et al., Reference Burgman, Keith, Hopper, Widyatmoko and Drill2007). Grazing and hydrological modification seem to have played a part for numerous taxa. The remainder occur in habitats that are not substantially modified, including four that seem to have become extinct in the absence of any known or suspected threat. Extinction is a natural process and the possibility exists that some taxa may have become extinct independent of human activities (Richman et al., Reference Richman, Case and Schwaner1988; Williamson, Reference Williamson1989), although undoubtedly most extinctions are anthropogenic (Regan et al., Reference Regan, Lupia, Drinnan and Burgman2001; Barnosky et al., Reference Barnosky, Matzke, Tomiya, Wogan, Swartz and Quental2011).
More than 120 species formerly considered extinct have been rediscovered in Australia since the mid 1970s, many of which eluded detection for more than a century (Supplementary Table 3). This cautions against declaring species extinct, particularly for those that may be ephemeral in response to disturbance (Kirkpatrick & Gilfedder, Reference Kirkpatrick and Gilfedder1998; Duretto et al., Reference Duretto, Orme, Rodd, Stables and Toelken2017). Most species listed as Presumed Extinct in Leigh et al. (Reference Leigh, Boden and Briggs1984) were known from single or few, low-precision pre-1900 records, and were not rediscovered until concerted flora survey and taxonomic studies since the 1970s. Many of these were initially assessed as having a slim chance of being rediscovered, primarily because of severe habitat loss and modification (Leigh et al., Reference Leigh, Boden and Briggs1984). Even species that occur in close proximity to well-collected urban centres can remain undetected for many years, as demonstrated by recent rediscoveries in the Perth and Sydney metropolitan areas (Davis, Reference Davis2012; Duretto et al., Reference Duretto, Orme, Rodd, Stables and Toelken2017).
Rediscovery of presumed extinct taxa, particularly those that are considered to have always been rare, could be considered parallel to the continuing discovery of new species. Between 1990 and 2009, an estimated mean of > 250 taxa of flowering plants per annum have been described as new (Chapman, Reference Chapman2009). Some of these are mere formalizations of long-known or suspected informal taxa, but many represent genuine new discoveries. The discovery of a new species is closely akin to the rediscovery of a species known by only one or few historic collections. In this light, we should not be surprised or suspicious of rediscoveries of presumed extinct species.
Our review highlights the differences in assessing flora compared to fauna extinctions (Boyd & Stanfield, Reference Boyd and Stanfield1998; Collen et al., Reference Collen, Purvis and Mace2010). Plants often have persistent seedbanks, increasing the effective generation time and making it difficult to confirm extinction on the basis of the species’ absence in the above-ground plant community (Silcock et al., Reference Silcock, Healy and Fensham2014). There are usually fewer records for plants, often only the type specimen. This makes it difficult to be confident of taxonomic status, as well as rendering it impossible to infer declines. However, most plant sightings are reinforced by collections, thus removing the issue of assessing the veracity of sightings, which is a vexed issue for inferring animal extinction (Boyd & Stanfield, Reference Boyd and Stanfield1998; Solow, Reference Solow2005). The task of assessing extinction likelihood has been made more streamlined by the digitization of many herbarium collections, including the Australian Virtual Herbarium (CHAH, 2016).
Despite our analysis pointing to fewer extinctions than previously thought, there may also be undocumented extinctions, where species disappeared before they were collected. The relatively small number of botanical collectors in Australia prior to broad-scale habitat modification would not have collected a comprehensive sample of the entire vascular flora (Keith & Burgman, Reference Keith and Burgman2004). Undocumented extinctions are especially likely to have occurred in rapidly modified habitats that were not well-surveyed prior to modification, especially those that contain endemic and restricted species, for example Great Artesian Basin springs (Rossini et al., Reference Rossini, Fensham, Stewart-Koster, Gotch and Kennard2018) and the Western Australian Wheatbelt. There are also numerous taxa that are not listed as extinct but have not been seen for many years (Gibson, Reference Gibson2016). Some occur in highly modified habitats, and surveys are urgently required to assess their status.
Even accounting for possible undocumented extinctions, almost 60 times as many taxa are listed as being at risk of global extinction (i.e. Critically Endangered or Endangered under federal and/or state legislation) than have become extinct since 1788. This could be a result of the inherent resilience of the flora, whereby species can become extremely reduced in range and abundance but are able to persist. In some ancient landscapes such as south-western Australia, long-term landscape stability has resulted in a propensity for flora to occur in small disjunct populations and have genetic systems to cope with this (Byrne & Hopper, Reference Byrne and Hopper2008; Hopper et al., Reference Hopper, Silveira and Fiedler2016). The relative resilience of Australia's flora in comparison to its fauna is highlighted by total extinction rates. Over 10% of Australia's terrestrial mammals (Woinarski et al., Reference Woinarski, Burbidge and Harrison2015) and 3.5% of its birds (Szabo et al., Reference Szabo, Khwaja, Garnett and Butchart2012) have become extinct in the past 200 years, compared to 0.15% of its flora.
Alternatively, the discrepancy between the extinct and threatened lists could highlight a looming extinction debt (Vellend et al., Reference Vellend, Verheyen, Jacquemyn, Kolb, Van Calster, Peterken and Hermy2006; Kolk & Naaf, Reference Kolk and Naaf2015; Halley et al., Reference Halley, Monokrousos, Mazaris and Vokou2017). Under this scenario many plants listed as threatened are functionally extinct, having fallen below the critical number to sustain their populations in the long term, or with populations dominated by mature individuals with minimal recruitment. Of the 660 species listed as Critically Endangered or Endangered at a national level, 62 are known from < 50 individuals, and 300 from < 250, well below numbers considered to represent long-term viable populations (Traill et al., Reference Traill, Brook, Frankham and Bradshaw2010). Many of these are now restricted to tiny remnants that are inherently vulnerable to degradation and within which ecological processes, particularly those driving recruitment, no longer operate.
The list and accompanying data presented here provide a baseline for tracking plant extinctions in Australia. The reasons for assigning a species to each extinction likelihood category are explicit, through assembling the best available information on species biology, ecology and search effort, and working each species through the key. This avoids the uncertainties and biases that tend to plague decisions on assigning extinction status (Keith et al., Reference Keith, Butchart, Regan, Harrison, Akcakaya, Solow and Burgman2017). It will now be clear whether additions or removals from the presumed extinct list are a result of taxonomic revisions, specimen rediscoveries or real changes to status (i.e. documented extinctions or rediscoveries). The use of multiple explicitly evaluated extinction likelihood categories provides a more meaningful measure for reporting on changes over time and between regions than the variable and changeable presumed extinct lists, as they are currently compiled. By accurately evaluating, understanding and acknowledging extinctions, we come closer to preventing more species being added to the list of the lost.
Acknowledgements
We acknowledge the many botanists who shared their knowledge of presumed and possibly extinct species, and their efforts to find them, and who delved into herbarium specimens and often murky taxonomies: Greg Keighery, Mike Hislop, Kevin Thiele, Neil Gibson, Barbara Rye, Dave Coates, Sarah Barrett, Barbara Rye, Andrew Webb, Bree Phillips, Anne Harris and Carolyn Wilkins (Western Australia); Lachlan Copeland, Peter Weston, Bob Makinson, Amanda Jowett, Liz Tasker, Mark Clements, Tony Auld, John Briggs, Steve Douglas, Keith McDougall, Lachlan Willmott (New South Wales); Rigel Jensen, Bob Jago, John Thompson, John Neldner, Bill McDonald, Lui Weber, Bill O'Donnell, Keith McDonald, Paul Forster (Queensland); Bob Bates, Doug Bickerton, Peter Lang, Dan Duval, Greg Guerin (South Australia); Paul Foreman, Jeff Jeanes, Gary Backhouse, Neville Scarlett (Victoria); Richard Schahinger, Jamie Kirkpatrick (Tasmania). Neil Gibson commented on the text and checked Appendices for Western Australia. John Woinarski alerted us to numerous additional species that are or have been considered extinct. This work was funded by the National Environmental Science Program's Threatened Species Recovery Hub. ARF's examination of material in European and US herbaria was supported by an IPID4all Germany Academic Exchange, Technische Universität Dresden Graduate Academy Project 2015_43 and a Queensland Smithsonian Fellowship 2017.
Author contributions
Research design, data collation, writing: JLS; discussion of ideas and writing: RJF; data contribution, discussion of ideas and writing: ARF, NGW.
Conflicts of interest
None.
Ethical standards
This research abided by the Oryx guidelines on ethical standards.
