Questioning current practice in brown bear , Ursus arctos , conservation in Europe that undervalues taxonomy

Questioning current practice in brown bear, Ursus arctos, conservation in Europe that undervalues taxonomy.— The present paper highlights problems associated with the currently–accepted taxonomy of brown bear, Ursus arctos, and their consequences for conservation at the European level. The enormous morphological variability within Ursus arctos is not acknowledged in current taxonomy and conservation practice. Seven major clades are recognized in Ursus arctos by molecular researchers, and although Western Europe maintains most of the populations belonging to the relict Clade 1 brown bear lineage, no reference to this is made in current conservation policy. Furthermore, the tiny population of Apennine brown bears, characterized by unique skull morphology, is not even recognized as a distinct Evolutionari Significant Unit (ESU) by current European legislation, nor is it included in the IUCN Red List. This may have serious consequences as brown bear conservation in Western Europe has been mainly based on restocking and reintroduction programs.


Introduction
More than 150 years since the publication of Darwin's 'Origin of Species' (Darwin, 1859), philosophical and biological issues regarding speciation and species boundaries are still debated (Hey, 2006;Naomi, 2011).In effect, conservation assessments usually include a review of what is deemed 'currently accepted taxonomy', with little understanding that taxonomy is in fact a specialist discipline, and that 'currently accepted' carries little or no scientific weight if not supported by updated taxonomic revisions (Gutierrez & Helgen, 2013).The conservation of biodiversity ultimately depends upon the work of taxonomists (McNeely, 2002).While it is clear that our knowledge is still limited for most tropical regions, it is often overlooked that, even in Europe, new assessments of the taxonomy of particular groups often lead to species descriptions (Fontaine et al., 2012).
Occasional conflicts between mammal taxonomists and conservationists have been observed in recent years (i.e., Isaac et al., 2004;Groves & Robovský, 2011;Shetty & Vidya, 2011;Cotterill et al., 2014).The case of the brown bear, Ursus arctos Linnaeus, 1758, represents a notable example of the neglect of taxonomic issues in the current approaches for the conservation of large mammals.
It is well established that the polar bear, Ursus maritimus, Phipps, 1774 is closely allied to Ursus arctos Linnaeus, 1758.However, patterns of mitochondrial DNA have failed to confirm the reciprocal monophyly of the two taxa (Talbot & Shields, 1996).
The species status of the polar bear has never been seriously questioned, and new data with other molecular markers appear to have reestablished the 'true relationship' between the two species (Cronin et al., 2013).Yet the hypothesis that polar bears originated from an island brown bear population, so that these brown bears are phylogenetically closer to polar bears than, for example, Gobi Desert brown bears, seems perfectly credible and merits further examination.
It is of interest that no studies to date have yet used molecular data to provide an alternative to the now classic 'one species' approach to Ursus arctos taxonomy, despite evidence of several deeply divergent mtDNA monophyletic clades within 'arctos' (Galbreath et al., 2007).
Furthermore, current awareness of the historical occurrence of hybridization and introgression between polar and brown bears (Edwards et al., 2011;Bidon et al., 2014) seems to support the need to adopt a different approach to species delimitation in the U. arctos complex away from the interbreeding criteria adopted as the fundamental pillar by the biological species concept.In the present paper we contend that the time is ripe for a taxonomic revision of the whole U. arctos complex, adopting an integrative coherent approach.
In the meantime, we here review available evidence with the aim of integrating the present conservation strategy for brown bear conservation within the European Union.
What are the consequences for brown bear conservation?
The taxonomic history of brown bears has been complicated owing to the great deal of phenotypic variation found both locally and regionally (Kitchener, 2010).Most modern researchers therefore simply choose to ignore the issue.Despite the availability of a wealth of genetic data in recent years (Swenson et al., 2011), its taxonomic significance has not been investigated (Kitchener, 2010; see below), or only rarely (Galbreath et al., 2007).In the specific IUCN/SSC Action Plan, the presence of possible taxonomically divergent populations in such a widespread species is simply overlooked (Servheen et al., 1998) with the consequence that the whole species is not considered as threatened (Least Concern;McLellan et al., 2008).Such treatment is prone to type 2 and 3 taxonomic errors (Cotterill et al., 2014), and one or more cryptic lineages may be at unnoticed risk of becoming extinct (Calvignac et al., 2009).In Europe, the species is included in Annex II of the Habitat Directive, but no attention is given to conservation below the species level.A major finding of genetic research, never fully translated into taxonomy and conservation strategy, is that the U. arctos complex can be separated into seven major geographically structured mitochondrial DNA clades and a small number of subclades (Hirata et al., 2013;Ashrafzadeh et al., 2016).Current EU bear conservation strategies (i.e., Boitani et al., 2015) seem to completely overlook that some of the Western European populations belong to the relict mtDNA lineage Clade 1, mainly restricted to the Iberian, Italian, Balkan and Southern Scandinavian Peninsulas (Davison et al., 2011;Hirata et al., 2013;fig. 1), and recently discovered in Western Turkey (fig.1; Çilingir et al., 2015).The value of recognized clades as conservation management units has been challenged in Europe by Valdiosera et al. (2007), who found Clade 3 mtDNA in ancient bear samples from within the current Clade 1 range in Northern Spain.These results have been interpreted as suggesting that present brown bear lineages are more the result of range fragmentation by humans than of evolutionary significant units (Valdiosera et al., 2008).The issue deserves further study as it is highly probable that with changing environmental conditions (i.e., glacials), Europe was colonized by mammal lineages of Eastern origin that retreated during interglacial periods, while Mediterranean lineages survived in southern refugia.For instance, during the Late Glacial, both Lynx lynx (Linnaeus, 1758) and L. pardinus (Temminck, 1827) occurred on the Iberian peninsula (Sommer & Benecke, 2006) and even in the northern Italian peninsula (Rodríguez-Varela et al., 2015), confirming their evolutionary species status.The size of the populations belonging to U. arctos Clade 1, wholly restricted to Europe, is difficult to estimate from available data because some of the 'populations' considered by EU experts (Scandinavian, Carpathian) are centered in the contact area where Clade 1 meets the worldwide Clade 3 (Zachos et al., 2008;Xenikoudarkis et al., 2015).It seems that so far no study has addressed the question of whether the two clades are also distinguishable morphologically, as has been attempted elsewhere (e.g., Baryshnikov et al., 2004).
Bear conservation in the EU and the overlooked demise of the Apennine bear Large carnivore populations, including brown bears, have recently been described as flourishing in EU states (Chapron et al., 2014).Attempts have been made to reestablish almost extinct brown bear populations (Alps, Pyrenees) through the translocation of bears from viable populations elsewhere.As in the rest of the world, no intraspecific taxonomic units have been accepted by bear experts in Europe (Swenson et al., 2000;Swenson et al., 2011).Accordingly, it has been emphasized that the Croatian bear population would appear to satisfy all criteria to serve as a source population for future reintroduction projects in Western Europe (Kocijan et al., 2011).This approach to brown bear conservation in Europe has been challenged with specific reference to the small, isolated Apennine brown bear population whose only breeding nucleus is found in the National Park of Abruzzo, Lazio and Molise, in Italy (Guacci et al., 2013).The original description of U. arctos marsicanus Altobello, 1921, based on limited materials, was rightly dismissed by Pocock (1932) who was aware of the considerable morphological variability found in U. arctos.Yet this view has been shared without any further study of new materials throughout the 20th Century, a period of taxonomic inertia for European mammalogy (Gippoliti & Groves, 2013).
According to early genetic studies (Randi et al., 1994;Taberlet & Buvet, 1994), this population, together with the Balkan populations, is considered to belong to the western brown bear clade 1b and shows negligible differentiation.But more recently, both Randi (2003) and Lorenzini et al. (2004) have indicated that differences in mitochondrial DNA and microsatellites suggest a distinct management unit.Furthermore, evidence is mounting that Apennine brown bears have a considerable phenotypic distinctiveness -specifically regarding the skull (Conti, 1954;Loy et al., 2008;Colangelo et al., 2012), to the extent that all these authors accepted U. arctos marsicanus as a valid taxon.Capasso Barbato et al. (1993), while discussing the cranial characters of extant U. arctos populations and U spelaeus Rosenmuller, 1784, confirmed that U. arctos marsicanus share some peculiarities with U. spelaeus, as previously evidenced by Conti (1954).This unusual situation can hardly be explained simply as the result of 'genetic drift' due to isolation from the main continental bear population in the last 400-700 years (cfr.Ministry of the Environment, 2011; Colangelo et al., 2012).The stability of a suture zone in Scandinavia in the last

Clade 3a
Clade 1 150 years, with the two clades only a few kilometers apart (Xenikoudarkis et al., 2015), demands that historical connectivity between the Apennine and Alps populations be verified and not merely automatically inferred.It seems reasonable at this stage to consider the Apennine brown bear as a southern endemic survivor, like the Apennine chamois Rupicapra ornata Neumann, 1899(Vigna-Taglianti, 2003).
At this point, one would surely have expected a revision of conservation policies both nationally and at the EU level.Nothing of the kind happened.Guacci et al. (2013) called for a more pressing conservation strategy for this endemic Italian taxon, including, if necessary, captive breeding and a bank of biomaterials -an aspect that is not considered in the National Action Plan (Ministry of the Environment, 2011), but is pursued elsewhere through semen collection from live individuals or post-mortem recovery of epididymal spermatozoa (Fickel et al., 2007;Anel et al., 2011).At present, it seems that conservation authorities and bear researchers continue to emphasize ecological connectivity between Apennine protected areas to create new breeding nuclei and reduction of human-induced mortality.If such an approach does not lead to positive results (for instance, due to female brown bear philopatry and thus dispersal avoidance outside their natal range), no alternative strategy seems to exist -or, better, the only available way to maintain genetic variability and increase range size in the future would be to bolster this population with individuals from the closest viable wild population, as done elsewhere (Chapron et al., 2009).Even if this intervention vigorously followed the IUCN Guidelines for reintroductions and other conservation translocations, given the unique status of U. arctos marsicanus among brown bears, it is clear that no candidate population exists.In 2008 it was stated that: 'The reconsideration and acceptance of the Apennine population as a distinct taxon will have a strong effect on any action to be undertaken for the conservation of the species in Italy' (Loy et al., 2008).As Randi (2003) also stressed: 'there should be distinct conservation managements for the Alpine and Apennine brown bear populations, and Apennine brown bears should be managed as an evolutionary significant unit (ESU)' (Loy et al., 2008).It should be emphasized that although the small population size (about 50 individuals, including circa 13 breeding females; cfr.Ciucci et al., 2015) is obviously a cause for concern, so far, no obvious effects of inbreeding have been reported.Although captive-breeding is not generally considered a viable option for brown bear conservation (Huber, 2010), Guacci et al. (2013) stressed that release of orphan bears is a common practice in several parts of the world (cfr.Beecham et al., 2015).Thus, if it is necessary to save a threatened taxon, captive-bred cubs could be released adopting a similar approach.Although starting a captive breeding program is a considerable risk with this current population status, since the 1990s, four Apennine brown bears have been kept in captivity (roughly 10% of the wild adult population).No serious attempts have been made to breed these bears, however, because it is assumed that captive-bred bears would not be successfully released back to the wild.Apart from captive breeding, however, it is time to recognize that our goal in Central Italy is the conservation of U. arctos marsicanus -an endemic taxon-and not simply that of the Apennine brown bear population.

Moving ahead in the conservation of brown bear diversity
Only today are we beginning to appreciate how decades of game management and wildlife translocations, without adequate backup from zoology and especially from taxonomy, has led us to overlook the fate of native Italian endemic taxa of ungulates (such as wild boars, Sus scrofa majori De Beaux & Festa, 1927 and roe deer, Capreolus capreolus italicus Festa, 1925), to the point where their re-establishment is near impossible given the presence of introduced alien stocks (Gippoliti & Amori, 2002;Champagnon et al., 2012).Even with carnivores such as the Eurasian otter Lutra lutra, awareness of the presence of a distinctive ESU in southern Italy (Panzacchi et al., 2010) came just in time to block some reintroduction programs.The Southern European Peninsulas of Iberia, Italy and the Balkans are known today to maintain a number of endemic lineages that make them a conservation priority; these lineages include the most threatened cat species in the world, Lynx pardina, considered a subspecies of Lynx lynx until 20 years ago (Beltrán et al., 1996).
The European Union needs to re-evaluate its conservation policy.A premium must be assigned to the conservation of populations that have not been altered by human-assisted genetic introgression.Only in this way can we effectively increase awareness of European biodiversity heritage.
As regards the conservation of brown bear in Europe, it has been suggested that an integrative approach to taxonomic research should be adopted.In the meantime, no measure should be proposed to encourage gene flow in the contact zone between Clade 1 and Clade 3. In the case of relict Clade 1 populations, such as the Apennine marsicanus, immediate action, as recognized by current conservation plans (Boitani et al., 2015;Ministry of the Environment, 2011), must be integrated by a long-term approach to secure genetic materials for future use, as has been done for the Cantabrian population (Nicolas et al., 2010).The precautionary principle and available scientific evidence demand that we manage U. arctos marsicanus as a distinct ESU.As such, future re-stocking with individuals from other populations is clearly not recommended.
Augmentation of the Apennine bear population has never been officially proposed.Any such project would raise serious safety concerns among local communities, who have never reported incidents with Apennine bears.Furthermore, such a project would lead to a hybrid swarm or substitution of a unique brown bear taxon before we fully understand the origin, history and significance of U. arctos marsicanus.