Interpreting the IUCN Red List categories and criteria for cryptogams

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1 For. Snow Landsc. Res. 75, 3: (2000) 293 Interpreting the IUCN Red List categories and criteria for cryptogams Nick G. Hodgetts Joint Nature Conservation Committee, Monkstone House, City Road, Peterborough, PE1 1JY, UK Abstract In 1994 the World Conservation Union (IUCN) published revised Red List categories, with criteria and guidelines on how they should be used. While this a substantial improvement on the previous system, it was clear that it had to be interpreted in different ways for differernt taxonomic groups. In particular, assigning threat categories to lesser-known groups such as cryptogams and invertebrates required the criteria to be interpreted in an appropriate way. This led the European Committee for the Conservation of Bryophytes (ECCB) to produce guidelines on interpreting the categories specifically for bryophytes. The numerical thresholds in the IUCN publication apparently require much quantitative data. Since these sorts of data are rare for bryophytes, evaluation against the threat categories must often be done by inference from what data are available. The most relevant data that can be used for bryophytes are population decline, present distribution and total population size, number of sites, and estimated loss of habitats over a specified period of time. It is thought that the guidelines developed for bryophytes may be applicable to a wide range of cryptogams, including lichens, perhaps with some modification. The revised IUCN categories have been applied with some success to lichens in Great Britain. Keywords: IUCN, Red List, cryptogams, criteria, bryophytes, lichens 1 Introduction Red Data Books (RDBs) and Red Lists are very useful tools and sources of information for use in species conservation. The original system of threat categories proposed by the World Conservation Union (IUCN) has been used widely throughout the world. In 1994, the IUCN produced a revision of the Red List categories, along with criteria for assigning them to species (World Conservation Union 1994). This revised system provided the means to assess species status much more objectively than was possible before, using a series of numerical thresholds based on measurements of abundance and decline. PALMER et al. (1997) described how the revised system was being applied in Britain and HALLINGBÄCK et al. (1998) showed how it could be used for bryophytes.the latter paper has now been adopted semi-officially by IUCN as a recommendation for the use of the system for bryophytes.

2 294 Nick G. Hodgetts 2 The IUCN Red List categories and criteria The old IUCN categories have been fully explained elsewhere (IUCN Threatened Plants Committee Secretariat 1981; PALMER et al. 1997), so are not repeated here. In summary, the old Red List categories are Extinct, Endangered, Vulnerable and Rare, with the further categories Indeterminate, Insufficiently known, Out of danger, Not threatened and No information. Although used extensively, this system was subjective and non-quantitative. The revised IUCN categories (World Conservation Union 1994) seek to provide a more objective method for determining the degree of threat to species. The Red List categories are Extinct, Extinct in the Wild, Critically Endangered, Endangered and Vulnerable, with the further categories Lower Risk (divided into three subcategories: conservation dependent, near threatened and least concern), Data Deficient and Not Evaluated. These categories are summarised in Figure 1. The criteria used to place taxa within the categories are summarised in Table 1. Yes Evaluated? No Not evaluated (NE) Yes Adequate data? No Data deficient (DD) Yes Extinct? No Yes Threatened? No Extinct (EX) Extinct in the wild (EW) Critically endangered (CR) Endangered (EN) Vulnerable (VU) Threatened Conservation dependent (cd) Near threatened (nt) Nationally Scarce (ns) Least Concern (lc) Lower risk (LR) Fig. 1. Hierarchical relationships of the categories. IUCN definition of Extinct (EX): A taxon is Extinct when there is no reasonable doubt that the last individual has died. IUCN definition of Extinct in the Wild (EW): A taxon is Extinct in the Wild when it is known only to survive in cultivation, in captivity or as a naturalised population (or populations) well outside the past range. The application of this system to plants (including lichens) in Britain is explained by PALMER et al. (1997). The system is complex and offers a range of alternatives for identifying the status of threatened species.a species is required to fulfil a minimum of one criterion (of criteria A to E) to qualify for the Red List. Species are tested against all criteria, working downwards through the threat categories (starting with Extinct) until the appropriate category for that species is found.the species is allocated to the highest category that it fits. In other words, if a species is determined as Critically Endangered using criterion B but only Endangered using criterion C, its status is Critically Endangered. Decline may be measured directly as a reduction in the number of individuals observed or, in the absence of this information, inferred from habitat or distribution data.

3 For. Snow Landsc. Res. 75, 3 (2000) 295 Table 1. Summary of the thresholds of the IUCN Criteria. criterion main thresholds Critically Endangered Endangered Vulnerable A. Rapid decline >80% over 10 yrs or >50% over 10 yrs or >20% over 10 yrs or 3 generations in past 3 generations in past 3 generations in past or future or future or future B. Small Range extent of occurrence extent of occurrence extent of occurrence fragmented, declining <100 km 2 or area <5000 km 2 or area km 2 or area of or fluctuating of occupancy <10 km 2 of occupancy <500 km 2 occupancy <2000 km 2 C. Small population <250 mature individuals, <2500 mature individuals, < mature and declining population declining population declining individuals, population declining D1. Very small <50 mature individuals <250 mature individuals <1000 mature individuals population D2. Very small range <100 km 2 or <5 locations E. Probability >50% within 5 years >20% within 20 years >10% within 100 years of extinction 3 Interpretation of the categories and criteria for cryptogams The revised IUCN system has now been used in Britain in published Red Data Books for lichens (CHURCH et al. 1996), vascular plants (WIGGINTON 1999) and bryophytes (CHURCH et al. 2001). With use, it is clear that the system can be used for these organisms and that it is a considerable improvement on the old system. However, it has to be interpreted appropriately according to the taxonomic group to which it is applied. The following guidelines give an indication of how the criteria may be interpreted for lichens, using as a basis the British lichen Red Data Book (RDB; CHURCH et al. 1996) and the guidelines produced by the European Committee for the Conservation of Bryophytes (ECCB), primarily for the purposes of making a European bryophyte Red List (HALLINGBÄCK et al. 1998). Note in particular that: the IUCN criteria need relatively little interpretation in order to work effectively; the concept of extent of occurrence is not used, as it is usually meanlingless for lichens and bryophytes in the present context; these guidelines must be used in conjunction with the official IUCN Red List categories (World Conservation Union 1994). Extinct (EX) Not having been seen in the wild in Britain during the last 50 years, despite searches having been made, and not maintained in cultivation (CHURCH et al. 1996). Taxa for which all known localities have been checked repeatedly in the last 30 years without success, or taxa listed as extinct or vanished in all available Red Lists, if the total area of distribution is covered by Red Lists (HALLINGBÄCK et al. 1998).

4 296 Nick G. Hodgetts Note: 1. No distinction has been made between EX and EW for cryptogams. As in the old system, the IUCN definition of Extinct is open to considerable interpretation. Critically Endangered (CR), Endangered (EN), Vulnerable (VU) (IUCN criteria A to D are indicated. Criterion E was not used, as it requires a population viability analysis, which is normally not available for lichens or bryophytes) A. Large decline Major population decline observed, estimated, inferred or suspected in the last 10 years, or three generations, whichever is the longer: 80% decline = CR 50% decline = EN 20% decline = VU Notes: 1. The subcriteria for this criterion listed in the IUCN guidelines allow decline to be inferred from distributional information, habitat degradation/decline or the effects of pollutants. 2. Generation time is a useful concept for cryptogams, as it enables decline over a longer time period than ten years to be used in assessing Red List status. However, it is an area that needs more work from lichenologists. Advice for bryologists (HALLINGBÄCK et al. 1998) has been to use a maximum of 25 years for one generation (i.e. for species that are not known to reproduce sexually), with a sliding scale of years for species that reproduce sexually only infrequently, down to 1 5 years for short-lived ephemeral colonists that reproduce frequently with small, highly mobile spores. In other words, a system of life strategies, such as that devised by DURING (1992) for bryophytes, needs to be adopted in order to obtain a broad estimate of generation time. B. Restricted area of occupancy, few localities, decline To qualify under this criterion, a species must occupy a restricted area and have few localities and have a continuing decline observed, inferred or projected. For lichens and bryophytes, the area of occupancy has been interpreted as the number of grid squares in which a species has been recorded. Extreme fluctuations, which are used in the IUCN criteria, have not been used here, as there is seldom any information on the dynamics of lichen and bryophyte populations. Recently recorded in only one hectad 1 or <10 1 x 1 km squares and found in only one locality/severely fragmented and in decline = CR Recently recorded in five or fewer hectads and found in two to five localities/severely fragmented and in decline = EN Recently recorded in six to twenty hectads and found in six to ten localities/severely fragmented and in decline = VU Notes: 1. Although there could be species occurring in, for example, three hectads and six localities, thus falling between two threat categories, this situation was not encountered in any of the Red List lichens in Britain. If it did arise, such a species would fall into the lower category (i.e. Vulnerable). 1 hectad = 10 km x 10 km square.

5 For. Snow Landsc. Res. 75, 3 (2000) One of the most misunderstood aspects of the revised IUCN system is that of scale. Numerical thresholds for area of occupancy are provided and these are not related to the size of the area for which a Red List is made. As explained by GÄRDENFORS (1996) and HALLINGBÄCK et al. (1998), the size of the Red List region makes no difference, because the risk of a species recorded from, say, five isolated sites becoming extinct is the same in a small area as it is in a large area. Where a significant inflow of individuals or propagules occurs, or is thought to occur, from outside the area being considered (thus reducing the risk of extinction in that area), the species should be downgraded to the next appropriate threat category, as recommended by GÄRDENFORS (1996) and approved by IUCN at a meeting in 1997.The pre-downgrading category should, however, be given in parentheses. This situation is likely to arise more frequently in small countries surrounded by other countries (e.g. Luxembourg) than in larger countries or on islands (e.g. Great Britain). 3. In CHURCH et al. (1996), severe fragmentation was expressed simply in terms of the number of localities where a species is found (criterion B1) as, for lichens, information on the effects of isolation on subpopulations is more or less non-existent. Furthermore, because many species have very efficient dispersal mechanisms, resulting in many highly disjunct distribution patterns (but fewer narrowly endemic species), populations of cryptogams are often naturally fragmented, and so fragmentation does not in itself necessarily constitute a threat. On the other hand, species with less efficient distribution mechanisms (i.e. those with large diaspores, or those that reproduce infrequently) may be significantly more threatened when subpopulations are fragmented. Therefore HALLINGBÄCK et al. (1998) suggested that, in most circumstances, a minimum distance greater than 50 km between populations of species that are not known to reproduce with spores, or do so only very rarely, could indicate severe fragmentation; and a distance of km for species that do produce spores (shorter for species with low spore production and large spores, longer for those with high spore production and small spores). 4. The definition of a location (or locality, or site ) is one of the most difficult problems in any biological recording, but must not be allowed to get in the way of the application of Red List criteria.the only advice it is possible to offer on this matter is to choose locations that are sensible and appropriate for the data available. C. Small population and decline Small population: fewer than 250 mature individuals = CR fewer than 2,500 mature individuals = EN fewer than mature individuals = VU together with either: C1. Large decline: at least 25% in 3 years or 1 generation = CR at least 20% in 5 years or 2 generations = EN at least 10% in 10 years or 3 generations = VU or: C2. Continuing decline and restricted to a single population or continuing decline and subpopulations small: no subpopulation estimated to contain more than 50 mature individuals = CR no subpopulation estimated to contain more than 250 mature individuals = EN no subpopulation estimated to contain more than 1000 mature individuals = VU

6 298 Nick G. Hodgetts Note: 1. It is often very difficult to determine what constitutes an individual without detailed genetic studies. Even then, a very widespread species might be found to consist of genetically identical material, but it would clearly be nonsensical to call the entire population an individual. Therefore, a pragmatic definition of an individual must be used, and those producing Red Lists must record what they mean when talking about individuals of any particular species. In the case of lichens, for example, a single rosette of Parmelia or a reasonably discrete patch of Lepraria can be regarded as an individual. D. Very small or restricted populations Fewer than 50 mature individuals = CR Fewer than 250 mature individuals = EN Fewer than 1000 mature individuals (sub-criterion D1) or 4 or fewer localities (sub-criterion D2) = VU Data Deficient (DD) Species with insufficient data to categorise them but which are thought likely to qualify as Extinct, Critically Endangered, Endangered or Vulnerable when they are better known. The Data Deficient category includes recently discovered taxa and those which can be identified only by experts or by using complex techniques. It also includes species that have occurred apparently as chance ephemerals and several species that have not been seen for over 50 years but which cannot be regarded as extinct because insufficient attempts have been made to refind them. Data Deficient species are listed in Appendix C. Lower Risk (near threatened) Lower Risk (near threatened) species are close to qualifying for Vulnerable. As applied in Britain, this category includes species which occur in 15 or fewer hectads, but which do not qualify as Critically Endangered, Endangered or Vulnerable. This category does not include species thought to be significantly under-recorded. Lower Risk (conservation dependent) has not yet been applied to crypotogams. However, it is possible that it may be used in future if species are removed from Red Lists because of successful conservation action. Lower Risk (least concern) covers all other species except those that have not yet been assessed against the criteria (Not Evaluated). Nationally Scarce (NS) This is an additional domestic (non-iucn) category used in Britain, effectively a subdivision of Lower Risk (least concern). At present this category includes taxa recorded in hectads.

7 For. Snow Landsc. Res. 75, 3 (2000) Worked examples from the British lichen Red Data Book The examples below give the reasons why species do or do not qualify for their status under each of the criteria A to D. Hypogymnia intestiniformis. Status: CR. A. Not applicable. Last recorded in 1964, so no major population decline in last 10 years. B. Applicable. Declined from seven localities in seven hectads to a single locality in a single hectad (and a single 1 km x 1 km square): Critically Endangered. C. Not applicable. No detailed information available on population size. D. Applicable.Anecdotal evidence suggests that the single locality supported only a very small number of individuals (<50): Critically Endangered. Lecidea erythrophaea. Status: VU. A. Not applicable. Insufficient information exists to determine the percentage decline in the last 10 years. B. Applicable. Declined from 13 localities in 13 hectads to six localities in six hectads: Vulnerable. C. Not applicable. No detailed information available on population size. D. Not applicable. Number of individuals cannot be estimated with sufficient accuracy to assign it to a category on this basis (D1). Occurs in more than four localities (D2). Parmelia quercina. Status: VU. A. Applicable. Although recorded in 21 hectads since 1960, survey work suggests a serious decline more recently: Vulnerable. B. Not applicable. Occurs in more than ten localities. C. Applicable. The total population certainly comprises fewer than individuals, and there has been a recent serious decline (C1): Vulnerable. D. Not applicable. Number of individuals cannot be estimated with sufficient accuracy to assign it to a category on this basis (D1). Occurs in more than four localities (D2). Peltigera malacea. Status: EN. A. Not applicable. Insufficient information exists to determine the percentage decline in the last 10 years. B. Applicable. Declined from nine localities in eleven hectads to three localities in five hectads: Endangered. C. Not applicable. No detailed information available on population size. D. Not applicable. No information on number of individuals (D1). Occurs in fewer than four localities (D2), but this would only be relevant in assigning the species to the category Vulnerable if it had not already been determined as Endangered under criterion B. Usnea subscabrosa. Status: VU. A. Not applicable. No decline observed. B. Not applicable. No decline observed. C. Not applicable. No decline observed. D. Applicable. No information on number of individuals (D1), but occurs in fewer than four localities (D2): Vulnerable.

8 300 Nick G. Hodgetts Table 2. Numbers of lichen species in the British Red List and the Data Deficient and Near Threatened categories. Extinct (EX) 29 Critically Endangered (CR) 27 Endangered (EN) 30 Vulnerable (VU) 91 Data Deficient (DD) 96 Lower Risk (near threatened) (LR (nt)) 91 Total Discussion Common criticisms of the revised IUCN system are that the criteria were invented only with large mammals (e.g. rhinoceros) in mind, and they will not work for my group, as we have insufficient information: all species will end up as Data Deficient!. However, remarks of this kind rather miss the point of the revised system, which has to be studied very carefully (including the introductory sections of the IUCN booklet) in order to be interpreted correctly. It is allowed to use the criteria and categories as a framework to be interpreted in a suitable way for each taxonomic group. In fact, as demonstrated above, little radical interpretation is needed in order to use the system effectively for lichens. One concern with the revised system is that the Red List itself (i.e. species with a status of Extinct, Extinct in the Wild, Critically Endangered, Endangered and Vulnerable) can be severely reduced, with a large number of species dropping out into the Lower Risk (near threatened) category, and many species being forgotten or sidelined in Data Deficient.This is an important point and needs to be addressed. Firstly, many species formerly on Red Lists as Rare undoubtedly do end up in the new Lower Risk (near threatened) category. This is because Rare is not really a threat category but merely an expression of frequency. In the British list, many arctic-alpine species that have been recorded from only a small number of mountains and were thus Rare in the old system are now Lower Risk (near threatened) because no threat had been established. For example, applying the revised guidelines revealed that Cetraria delisei was known from only nine hectads (so would previously have qualified as Rare), but there was no evidence of decline or fragmentation, and it was estimated that the population was more than 1000 individuals. Therefore the new category had to be Lower Risk (near threatened). This does not mean that it is forgotten as a conservation issue. Listing a rare species as Lower Risk (near threatened) is not a cause for complacency, but merely a more realistic assessment of its status. Similarly, a large number of British lichens now have a status of Data Deficient. Again, this does not imply that they are consigned to some lichenological dustbin. Indeed, if a species is listed as Data Deficient, new survey work should be a high priority for that species.although merely listed in the British lichen RDB, Data Deficient species will receive full species accounts in the bryophyte RDB in order to emphasise their importance. It should be emphasised that Red Lists are merely expressions of what is threatened in any given area and are only a part, though a vitally important one, of the process of assigning conservation priorities. In Britain, they contribute to the biodiversity lists, which also include non-red List species that are giving cause for concern because they are declining, and species

9 For. Snow Landsc. Res. 75, 3 (2000) 301 for which Britain has an international responsibility, such as oceanic lichens. Thus, although there are few oceanic lichens on the British Red List (since most of them are relatively frequent on the west coast), many appear on the biodiversity lists, as it is recognised that they have a very restricted world distribution and so Britain has a special responsibility for their conservation. The Joint Nature Conservation Committee has recently started work on a project to rationalise the process of species status assessment. Up to now, assigning conservation status to species has been a somewhat ad hoc affair, but the revised IUCN system allows the application of a single standard across the whole taxonomic spectrum. The principal behind the species status project is to provide a framework whereby species status can be assessed using a standard methodology by the appropriate experts. In the case of lichens in Britain, this means engaging members of the British Lichen Society to produce an agreed Red List (and also lists of Lower Risk (near threatened) species and Nationally Scarce species).the structure of the project will be a steering group overseeing a number of specialist expert groups. Each expert group will use the revised IUCN system (interpreting it in an appropriate way) to construct a draft Red List for their taxonomic specialism, which will then be widely advertised among the relevant specialist community and posted on a website for a timelimited consultation period. Following this, the expert group will send an amended list to the steering group and the final, agreed list will be published on a website, along with lists for the other taxonomic groups covered. This will be the official species status list. The list for each taxonomic specialism will be reviewed at regular intervals, as appropriate to the level of information available. The revised IUCN system therefore offers a standard means of assessing species status and can be used both globally and regionally. Generally speaking, the larger the area covered by a Red List, the more meaningful it is. It is to be hoped that those involved in producing lichen Red Lists for their own countries will adopt the system and also co-operate to produce European and global Red Lists as more information becomes available. Acknowledgements I would like to thank Tomas Hallingbäck and all the other members of the European Committee for the Conservation of Bryophytes, on whose hard work much of this paper is based. 6 References CHURCH, J.M.; COPPINS, B.J.; GILBERT, O.L.; JAMES, P.W.; STEWART, N.F., 1996: Red Data Books of Britain and Ireland: Lichens. Volume 1, Britain. Peterborough, Joint Nature Conservation Committee. CHURCH, J.M.; HODGETTS, N.G.; PRESTON, C.D.; STEWART, N.F., British Red Data Books. Mosses and liverworts. Peterborough. Joint Nature Conservation Committee. DURING, H.J., 1992: Ecological classification of bryophytes and lichens. In: BATES, J.W.; FARMER, A.M. (eds) Bryophytes and lichens in a changing environment Oxford, Clarendon Press. GÄRDENFORS, U., 1996: Application of IUCN Red List categories on a regional scale. In: BAILLIE, J.; GROOMBRIDGE, B. (eds) 1996 IUCN Red List of threatened animals. Cambridge. HALLINGBÄCK, T.; HODGETTS, N.G.; RAEYMAEKERS, G.; SCHUMACKER, R.; SÉRGIO, C.; SÖDERSTRÖM, L.; STEWART, N.F.; VÁNA, J., 1998: Guidelines for the application of the revised IUCN threat categories to bryophytes. Lindbergia 23, 1: 6 12.

10 302 Nick G. Hodgetts IUCN Threatened Plants Committee Secretariat 1981: How to use the IUCN Red Data Book categories. IUCN Threatened Plants Committee, Kew, UK. PALMER, M.A.; HODGETTS, N.G.; WIGGINTON, M.J.; ING, B.; STEWART, N.F., 1997: The application to the British flora of the World Conservation Union s revised Red List criteria and the significance of Red Lists for species conservation. Biol. Conserv. 82: WIGGINTON, M.J., 1999: Red Data Books of Britain and Ireland: Vascular Plants. Peterborough, Joint Nature Conservation Committee. World Conservation Union 1994: IUCN Red List categories. Gland, IUCN.