Potentially threatened: a Data Deficient flag for conservation management

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DOI 10.1007/s10531-016-1164-0 COMMENTARY Potentially threatened: a Data Deficient flag for conservation management Ivan Jarić 1,2 Franck Courchamp 3 Jörn Gessner 1 David L. Roberts 4 Received: 12 May 2016 / Revised: 3 June 2016 / Accepted: 20 June 2016 Springer Science+Business Media Dordrecht 2016 Abstract Data Deficient (DD) comprise a significant portion of the total number of listed within the IUCN Red List. Although they are not classified within one of the threat categories, they may still face high extinction risks. However, due to limited data available to infer their extinction risk reliably, it is unlikely that the assessment of the true status of Data Deficient would be possible before many decline to extinction. An appropriate measure to resolve these problems would be to introduce a flag of potentially threatened within the Data Deficient category [i.e., DD(PT)]. Such a flag would represent a temporary Red List status for listed Data Deficient that are, based on the available direct evidence and/or indirect indices, likely to be assigned to one of the threat categories, but where current data remains insufficient for a complete classification. The use of such a flag could increase the focus of the scientific community and conservation decision-makers on such, thus avoiding the risk that necessary conservation measures are implemented too late. As such, establishment of the DD(PT) category as a kind of alarm for priority could be beneficial. Communicated by David Hawksworth. & Ivan Jarić jaric@igb-berlin.de 1 2 3 4 Leibniz-Institute of Freshwater Ecology and Inland Fisheries, Müggelseedamm 310, 12587 Berlin, Germany Institute for Multidisciplinary Research, University of Belgrade, Kneza Viseslava 1, 11000 Belgrade, Serbia Ecologie, Systématique and Evolution, Univ. Paris-Sud, CNRS, AgroParisTech, Université Paris- Saclay, 91400 Orsay, France Durrell Institute of Conservation and Ecology, School of Anthropology and Conservation, University of Kent, Marlowe Building, Canterbury CT2 7NR, Kent, UK

Keywords Data Deficient Endangered Extinction risk IUCN Red List Threatened The IUCN Red List of threatened is considered as one of the most relevant information sources and decision-making support tools for conservation management (Rodrigues et al. 2006; IUCN 2015). However, for many, limited or insufficient data are available on their geographic distribution, abundance, population trends and threats to infer their extinction risk reliably. This leaves those conducting assessments in a dilemma: based on available data and acknowledging the associated uncertainties, can a classification other than Data Deficient (DD; IUCN 2001) be made? How assessors incorporate and handle the uncertainties associated with poorly known can result in the difference between a being listed as Data Deficient or as threatened. Data Deficient represent as much as 16 % of the total number of listed within the IUCN Red List (i.e., approximately 13,000 out of the 80,000 assessed so far are classified as Data Deficient; IUCN 2015). Although they are not classified within the threat categories, Data Deficient may still face high extinction risks, and may actually be more frequently threatened than successfully evaluated (Howard and Bickford 2014; Bland et al. 2015; Jetz and Freckleton 2015; Roberts et al. 2016). This problem was also illustrated by recent population declines reported in some Data Deficient (Morais et al. 2013). Many of these may in fact be perilously close to extinction (Schipper et al. 2008). At the same time, such may be neglected by research and conservation programs, with funding rarely being directed to address specifically the problem of Data Deficient (Morais et al. 2013; Bland et al. 2015). Lack of conservation focus is mainly driven by their uncertain conservation status (Bland et al. 2015), as well as by the tendency of conservation managers to prioritize well-studied (Sitas et al. 2009). The Data Deficient category is essentially different from the other categories, since its listing does not imply that a taxon is not threatened, but represents an expression of necessity for additional efforts by researchers. Assessment of the true status of Data Deficient could be achieved through focused field surveys (Bland et al. 2015). However, given the necessary time, man-power and monetary implications in collecting baseline data on all Data Deficient, it is unlikely that this would be possible before populations of many decline, potentially to extinction (Howard and Bickford 2014; Bland et al. 2015). Given the very large number of classified as Data Deficient, there is a need to prioritize those that should be studied first and removed from this category, with prioritization primarily on the grounds of potential threat. We suggest that one of the appropriate measures to resolve this problem would be to introduce a flag of Potentially Threatened within the Data Deficient category [i.e., DD(PT)], as a temporary Red List status that would warn that such are potentially threatened and that monitoring, research and conservation attention are required. The idea behind such a flag follows the establishment of the flag of potentially extinct within the Critically Endangered category [CR(PE); Butchart et al. (2006)], as both flags represent temporary classifications until more detailed information are made available to confirm suspected status. We define Potentially Threatened Data Deficient as those that are, based on available direct evidence and/or indirect indices, likely to be assigned to one of the threat categories (i.e., VU, EN or CR), but where current data remains insufficient for a complete

classification. It is important to emphasize that the liberal use of the Data Deficient category should be discouraged, and all with sufficient information for their inclusion within one of the threat categories should be classified as such (IUCN 2001). Furthermore, we advise against the direct use of DD(PT) flag for newly assessed, to avoid further inflation of the Data Deficient category; it should be preferably applied only to the current Data Deficient, i.e. those that have been classified as such within previous assessments. Although Data Deficient lack information needed for a Red List classification, large amounts of life-history, ecological, and phylogenetic information may be available for many of these (Bland et al. 2015). While these data alone can be technically insufficient for making a standardized decision on classifying a into one of the data-sufficient categories, they can be nevertheless used for indirect threat assessments. In recent years, a number of indirect assessment methods have been applied to Data Deficient within different groups, mainly mammals and amphibians, to infer their likely threat level (Table 1). Most frequently used approaches were machine-learning methods, largely based on information related to geographic range, life-history and ecological data, phylogeny, environmental data and threat intensity (Howard and Bickford 2014; Bland et al. 2015). The general characteristic of all the methods was their attempt to model the relationship between different types of information related to data-sufficient and their Red List classification, and to apply it thereafter to Data Deficient based on the available information. Such methods should be considered as sufficient evidence for classifying assessed within the DD(PT) category. The proportion of Data Deficient considered to be potentially threatened varied between studies; for instance, predictions for Data Deficient mammal ranged from 35 (Jones and Safi 2011) to 69 % (Jetz and Freckleton 2015; Table 1). However, in accordance with the precautionary principle, each identified as potentially threatened with extinction by one or several of the applied methods should be a candidate for the DD(PT) category. From a conservation perspective, it would be more problematic to incorrectly deny the DD(PT) status to a than to incorrectly attribute it. Conversely, identified by all the methods as likely to be not-threatened would remain within the general Data Deficient category until sufficient data and analyses can identify their adequate threat category. Beside the methods listed in Table 1, other methods designed for extinction risk assessment of data-poor could also be applied, based on the type and the amount of available data. For instance, for many Data Deficient, biological collections or sighting records represent the only available data (Roberts et al. 2016). In such situations, application of methods that infer threat based on the observation records would be appropriate (e.g. Burgman et al. 1995, 2000; McCarthy 1998; Regan et al. 2000; McInerny et al. 2006; Robbirt et al. 2006). The recognition of DD(PT) flag for already in the Data Deficient category would contribute to the better research and conservation prioritization of those for which a sound classification other than Data Deficient cannot be made. The use of such a flag would reduce the risk of these being neglected by the scientific community and conservation decision-makers, to the point when postponed conservation measures are implemented too late. Establishment of the DD(PT) flag could be highly beneficial as a temporary measure, designed to highlight the status of such. Research efforts are expected to be more effective and yield more critical knowledge if they are directed to the least known (de Lima et al. 2011). Given that they are also likely to be threatened with extinction, classified as DD(PT) should be recognised as a major research priority.

Table 1 Examples of studies that involved indirect estimation of extinction threat for Data Deficient Reference Assessed DD Method Used data Results Davidson et al. (2009) Jones and Safi (2011) Morais et al. (2013) Howard and Bickford (2014) Quintero et al. (2014) Bland et al. (2015) Jetz and Freckleton (2015) Mammals Mammals Brazilian anuran Amphibians Mexican amphibians Terrestrial mammals Mammals Decision-tree modelling, classification tree and random forest modelling Combination of spatial eigenvector estimation and phylogenetic eigenvectors Quantile regression to model a relationship between the time since discovery and range-size Machine-learning method, random forest models Machine-learning method, random forest models Seven machine learning methods: classification tree, random forest, boosted tree, k nearest neighbours, support vector machine, neural network, and decision stumps Spatial-phylogenetic statistical framework, generalized linear models, generalized least-squares approach 11 explanatory variables; geographic range, density, group size, mass-specific production, home range, body mass, habitat mode and activity period identified as relevant predictors Phylogenetic, distribution and environmental data Time since description and current distribution Extinction risk data and distribution ranges 14 15 explanatory variables, including data on life history and population trends, environmental data and negative impacts 29 36 explanatory variables, including data on life history and ecology, environmental data and measures of threat intensity Body mass, distribution and encroachment (anthropogenic habitat transformation) data 28 out of 341 assessed (8 %) determined to be at high extinction risk 35 % of 481 assessed determined to be threatened with extinction 37 of 231 assessed (16 %) threatened with extinction, overall rate likely 57 % 63 % of 1249 assessed probably threatened with extinction 18 out of 24 assessed (75 %) declining 313 of 493 assessed (63 %) threatened with extinction 331 of 483 assessed (69 %) threatened with extinction

Table 1 continued Reference Assessed DD Method Used data Results Luiz et al. (2016) Groupers (Teleostei: Epinephelidae) Ordinal analytical approach, cumulative link mixed-effects modelling Body-size, maximum depth of occurrence, breadth of habitat use, geographic range size, aggregative spawning behaviour, and biogeographical region 6 of 50 assessed (12 %) endangered or vulnerable Classification of DD(PT) could also serve as a platform to instigate and enhance communication within the scientific community on the true status of such. One of the primary roles of the IUCN Red List is to contribute to conservation efforts, as a communication tool for decision-makers, funding sources, scientific community and the general public. Establishment of the DD(PT) category as a kind of alarm for potential priority would fit this purpose and likely prove to be a highly beneficial tool, with the scientific community and managers involved in monitoring programs as its major endusers. Acknowledgments The authors acknowledge the sponsorship provided by the Alexander von Humboldt Foundation and the Federal German Ministry for Education and Research, as well as the support by the Invacost research program, and by the Project No. 173045, funded by the Ministry of Education, Science and Technological Development of the Republic of Serbia. References Bland LM, Collen B, Orme DL, Bielby J (2015) Predicting the conservation status of data-deficient. Conserv Biol 29(1):250 259 Burgman MA, Grimson RC, Ferson S (1995) Inferring threat from scientific collections. Conserv Biol 9:923 928 Burgman MA, Maslin BR, Andrewartha D, Keatley MR, Boek C, McCarthy MA (2000) Inferring threat from scientific collections: power tests and an application to Western Australian Acacia. In: Ferson S, Burgman MA (eds) Quantitative methods for conservation biology. Springer, New York, pp 7 26 Butchart SHM, Stattersfield AJ, Brooks TM (2006) Going or gone: defining Possibly Extinct to give a truer picture of recent extinctions. Bull BOC 126:7 24 Davidson AD, Hamilton MJ, Boyer AG, Brown JH, Ceballos G (2009) Multiple ecological pathways to extinction in mammals. Proc Natl Acad Sci USA 106(26):10702 10705 de Lima RF, Bird JP, Barlow J (2011) Research effort allocation and the conservation of restricted-range island bird. Biol Conserv 144:627 632 Howard SD, Bickford DP (2014) Amphibians over the edge: silent extinction risk of Data deficient. Divers Distrib 20(7):837 846 IUCN (2001) IUCN Red List Categories and Criteria. Version 3.1. http://www.iucnredlist.org. Accessed 10 May 2016 IUCN (2015) The IUCN Red List of Threatened Species. Version 2015-4. http://www.iucnredlist.org Accessed 10 May 2016

Jetz W, Freckleton RP (2015) Towards a general framework for predicting threat status of data-deficient from phylogenetic, spatial and environmental information. Philos Trans R Soc Lond B Biol Sci 370(1662):20140016 Jones KE, Safi K (2011) Ecology and evolution of mammalian biodiversity. Philos Trans R Soc Lond B Biol Sci 366(1577):2451 2461 Luiz OJ, Woods RM, Madin EMP, Madin JS (2016) Predicting IUCN extinction risk categories for the world s Data deficient groupers (Teleostei: Epinephelidae). Conserv Lett. doi:10.1111/conl.12230 McCarthy MA (1998) Identifying declining and threatened with museum data. Biol Conserv 83:9 17 McInerny GJ, Roberts DL, Davy AJ, Cribb PJ (2006) Significance of sighting rate in inferring extinction and threat. Conserv Biol 20:562 567 Morais AR, Siqueira MN, Lemes P, Maciel NM, De Marco P, Brito D (2013) Unraveling the conservation status of Data deficient. Biol Conserv 166:98 102 Quintero E, Thessen AE, Arias-Caballero P, Ayala-Orozco B (2014) A statistical assessment of population trends for data deficient Mexican amphibians. PeerJ 2:e703 Regan HM, Colyvan M, Burgman MA (2000) A proposal for fuzzy International Union for the Conservation of Nature (IUCN) categories and criteria. Biol Conserv 92:101 108 Robbirt KM, Roberts DL, Hawkins JA (2006) Comparing IUCN and probabilistic assessments of threat: do IUCN Red List criteria conflate rarity and threat? Biodivers Conserv 15:1903 1912 Roberts DL, Taylor L, Joppa LN (2016) Threatened or data deficient: assessing the conservation status of poorly known. Divers Distrib 22(5):558 565 Rodrigues ASL, Pilgrim JD, Lamoreux JF, Hoffmann M, Brooks TM (2006) The value of the IUCN Red List for conservation. Trends Ecol Evol 21(2):71 76 Schipper J et al (2008) The status of the world s land and marine mammals: diversity, threat, and knowledge. Science 322(5899):225 230 Sitas N, Baillie JEM, Isaac NJB (2009) What are we saving? Developing a standardized approach for conservation action. Anim Conserv 12:231 237