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Reintroductions as a Management tool for European Ungulates

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... The main factors that shaped mtDNA genetic diversity and population structure of the species were the Quaternary climatic oscillations, postglacial recolonization, and hybridization with the Siberian Roe Deer (Matosiuk et al. 2014;Plis et al. 2022aPlis et al. , 2022b. Through hybridization during the Younger Dryas (10,800 to 10,000 BP)-when their ranges overlapped naturally over larger areas (Matosiuk et al. 2014)-as well as through translocations of Siberian Roe Deer into the range of C. capreolus by humans in the 19th and 20th centuries (Danilkin 1996(Danilkin , 2014Scandura et al. 2014;Plis 2023), many C. capreolus individuals inhabiting eastern and central Europe (mainly eastern Poland, Belarus, Baltic States, Slovakia, Hungary, Ukraine, and the European part of Russia) possess mtDNA of C. pygargus (Plis et al. 2022a(Plis et al. , 2022b. ...
... Similarly, hierarchical STRUCTURE analyses (performed using allele frequency-independent model) indicated an additional genetic cluster consisting of several specimens in site 12. Such distinctiveness of eastern European Roe Deer can be traced to past hybridization with the Siberian Roe Deer, which resulted from either overlap of the ranges of those species and/or translocation caused by humans (Danilkin 1996(Danilkin , 2014Matosiuk et al. 2014;Scandura et al. 2014;Plis 2023). Further genetic studies, including more nuclear markers (e.g. ...
Article
Although the European Roe Deer (Capreolus capreolus) is one of the most common and widespread ungulate species in Europe and inhabiting a variety of habitats, few studies have addressed its population structure at a large spatial scale using nuclear genetic data. The aims of our study were to: (i) investigate genetic diversity, level of admixture, and genetic structure across European Roe Deer populations; (ii) identify barriers to gene flow; and (iii) reveal factors that have impacted the observed pattern of population genetic structure. Using 12 microsatellite loci, we analyzed 920 European Roe Deer samples from 16 study sites from northern, southern, central, and eastern Europe. The highest genetic diversity was found in central and eastern sites, and lowest in the northern and southern sites. There were 2 main groups of genetically related populations in the study area—one inhabiting mainly Fennoscandia, and the second in the continental part of Europe. This second population was further divided into 3 to 5 spatially distributed genetic clusters. European Roe Deer belonging to the Siberian mitochondrial DNA clade, inhabiting large parts of eastern Europe, were not identified as a separate population in the analysis of microsatellite loci. No isolation by distance (IBD) was detected between roe deer from the fennoscandian and the continental study sites, but the Baltic Sea was inferred to be the main barrier to gene flow. Only weak IBD was revealed within the continental population. Three lower-level genetic barriers were detected in the western, southern, and eastern parts of the study area. The main factors inferred as shaping the observed genetic diversity and population structure of European Roe Deer were postglacial recolonization, admixture of different populations of the species originating from several Last Glacial Maximum refugial areas, and isolation of several study sites.
... In the last decades, various ungulate species have been restocked and reintroduced across Europe for conservation and hunting purposes, to reverse the decline they had experienced during the previous century (Apollonio et al., 2014(Apollonio et al., , 2010. Due to these management actions, native and exotic gene pools might have come into contact, leading to hybridisation, introgression and possible decline of local biodiversity (Linnel and Zachos, 2011). ...
... The roe deer is the most widespread ungulate species in Europe, inhabiting various ecosystems across many countries. After facing a great decline all over Europe during the last century, mainly due to overhunting and habitat loss, this species has been recently reintroduced and strongly managed throughout its range, as other ungulates (Apollonio et al., 2014(Apollonio et al., , 2010. Some fragmented relict populations are inhabiting Mediterranean habitats, in southern Spain and central/southern Italy (Gentile et al., 2008). ...
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After facing a great decline all over Europe during the past centuries, starting from the second half of the XX century the roe deer (Capreolus capreolus) was reintroduced and strongly managed throughout its range, as other ungulate species. Overhunting and habitat change were the main factors threatening roe deer populations in Italy, where small remnant populations of putatively native roe deer survived in a few localities of eastern Alps and central-southern Italy. We investigated the genetic variation of a roe deer population inhabiting the northern Apennines in the province of Massa-Carrara (Tuscany, Italy), analysing both mitochondrial DNA control region and a total of 11 autosomal microsatellite loci, to identify possible sources and recolonisation patterns, as well as the local prevalence of native Capreolus capreolus italicus gene pool. Analyses revealed an admixed nature of roe deer in this area, merging both native and non-native lineages, with a dominance of italicus haplotypes in the matriline and a majority of non-native genetic components in the autosomal markers. The high similarity with roe deer from neighbouring areas suggests a natural population origin by immigration. Two scenarios may explain the observed pattern of genetic variation: a colonisation by a limited number of immigrants from a single admixed source (either north or south-east), or a two-step recolonisation, firstly from the south, where the italicus ancestry was prevalent, and then from the north, mostly by individuals carrying C. c. capreolus genes. This study shows the genetic consequences of translocations even in populations not directly targeted by human interventions and highlight how investigating genetic variation might be essential in species management.
... One of the main project activities was the collection and analysis of data on previous reintroductions of red deer in Serbia and throughout Europe (e.g. Bojović, 1968;Tomić et al., 2010;Apollonio et al., 2014), with emphasis on errors and factors of the greatest significance for their success or failure. Thanks to that, measures were proposed to improve the ongoing reintroductions in Serbia, not only to improve the survival and reproduction of red deer, but also to make the reintroduction process as economical as possible. ...
... Habitat quality at the release site has a high impact on the success of reintroduction, if the number and origin of the inhabited breeding stock are favourable, which includes the degree to which the animals are dispersed from the release site (Griffith et al., 1989;Yott et al., 2011;Apollonio et al., 2014). The location of the acclimatisation enclosure Jezerine in the Tara area was determined with the participation of numerous experts (from Serbia, Slovenia and Italy) using landscape structure analyses and the common phytocoenological methodology (Gačić et al., 2018). ...
... One of the main project activities was the collection and analysis of data on previous reintroductions of red deer in Serbia and throughout Europe (e.g. Bojović, 1968;Tomić et al., 2010;Apollonio et al., 2014), with emphasis on errors and factors of the greatest significance for their success or failure. Thanks to that, measures were proposed to improve the ongoing reintroductions in Serbia, not only to improve the survival and reproduction of red deer, but also to make the reintroduction process as economical as possible. ...
... Habitat quality at the release site has a high impact on the success of reintroduction, if the number and origin of the inhabited breeding stock are favourable, which includes the degree to which the animals are dispersed from the release site (Griffith et al., 1989;Yott et al., 2011;Apollonio et al., 2014). The location of the acclimatisation enclosure Jezerine in the Tara area was determined with the participation of numerous experts (from Serbia, Slovenia and Italy) using landscape structure analyses and the common phytocoenological methodology (Gačić et al., 2018). ...
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The modern approach in the development of programs for the reintroduction of red deer was applied for the first time in Serbia. We compared the most important planned and implemented activities in the period 2018-2021, and assessed the results achieved in the Mt. Tara area. The plan was to hold the red deer (5♂ + 15♀) in the acclimatisation enclosure for several months and release them into the selected favourable area (150 km<sup>2</sup>) during three consecutive years. Bark stripping occurred mainly on thinner common hazel stems of coppice origin (≤ 9.9 cm). Total mortality among the 72 red deer that were transported to the acclimatisation enclosure was 8.3%. The longest movement of a 4-year-old female (held for 15 weeks) was 24 km. During the study period, no bark stripping was observed outside the acclimatization enclosure, nor were any deaths of the released red deer registered. In the period 2019-2021, 74 red deer were released from the acclimatization enclosure into the Mt. Tara area, which is about 60% of the estimated capacity of the selected favourable area.
... Krojerová-Prokešová et al., 2015;Zachos et al., 2016). The occurrence of admixture at contact zones is a natural phenomenon in many species (Taylor & Larson, 2019) but in the case of red deer, because of the economic interest of the species mainly for hunting purposes, human-mediated translocations may have been common with individuals moved from one lineage into the area of another (Apollonio et al., 2014). In eastern Europe, red deer translocations may have contributed to the overlapping of the original distribution ranges, mainly because of the introduction of individuals of the western lineage into areas in eastern Europe where the species became extinct in historical times (Niedziałkowska et al., 2011(Niedziałkowska et al., , 2012Szederjei & Szederjei, 1971). ...
Article
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Genome‐wide technologies open up new possibilities to clarify questions on genetic structure and phylogeographic history of taxa previously studied with microsatellite loci and mitochondrial sequences. Here, we used 736 individual red deer ( Cervus elaphus ) samples genotyped at 35,701 single nucleotide polymorphism loci (SNPs) to assess the population structure of the species throughout Europe. The results identified 28 populations, with higher degrees of genetic distinction in peripheral compared to mainland populations. Iberian red deer show high genetic differentiation, with lineages in Western and Central Iberia maintaining their distinctiveness, which supports separate refugial ranges within Iberia along with little recent connection between Iberian and the remaining Western European populations. The Norwegian population exhibited the lowest variability and the largest allele frequency differences from mainland European populations, compatible with a history of bottlenecks and drift during post‐glacial colonization from southern refugia. Scottish populations showed high genetic distance from the mainland but high levels of diversity. Hybrid zones were found between Eastern and Western European lineages in Central Europe as well as in the Pyrenees, where red deer from France are in close contact with Iberian red deer. Anthropogenic restocking has promoted the Pyrenean contact zone, admixture events in populations on the Isle of Rum and in the Netherlands, and at least partly the admixture of the two main lineages in central‐eastern Europe. Our analysis enabled detailed resolution of population structure of a large mammal widely distributed throughout Europe and contributes to resolving the evolutionary history, which can also inform conservation and management policies.
... After their extinction in mainland Europe, European mouflon (Ovis gmelini musimon) have been reintroduced since the eighteenth century in several European regions (Türcke and Tomiczek 1982;Apollonio et al. 2014;Guerrini et al. 2015). The species is now distributed in 21 European countries and lives both in enclosures, game reserves and in the wild, with population numbers varying greatly by country and region. ...
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In the early twentieth century, European mouflon was introduced in Croatia, while all introductions in Slovenia occurred in the 1950s and 1960s. Although majority of the introductions were historically documented, occasional cases involving individuals of unknown origin have likely contributed to a mixed genetic pool in established colonies. To understand the impact of past management and the potential founder effects on contemporary mouflon populations, we performed the first genetic study of the species in these two countries. Utilising next-generation sequencing of both mitochondrial control region (mtDNA CR) and major histocompatibility complex (MHC DRB exon 2), our study scrutinises the genetic diversity and structure of these populations. Additionally, the origins and genetic variability of mouflon in Croatia and Slovenia were compared with reference samples from Czech Republic, Sardinia (Italy), and Corsica (France). The mtDNA haplotype network showed that the majority of mouflon from Slovenia are closely related to mouflon from Sardinia, and only few shared the same haplotypes with mouflon from Croatia. Some mouflon from mainland Croatia share identical or closely related haplotypes with individuals from the initially established population in this country (on the Brijuni Archipelago), while others belong to a distinctly different cluster. We found five MHC alleles previously reported for mouflon in Europe, and genetic diversity was similar in both studied countries. We observed an excess of the Ovar-DRB1*07012/*07012 genotype, and only a few individuals exhibited the advantageous genotypes for parasite infection (Ovar-DRB1*0114 allele and Ovar-DRB1*0324/*0114 genotype). Genetic data showed that the population origins are generally in agreement with the written historical records, although we found signals of release of extra individuals into certain colonies.
... In order to describe and properly manage the remaining genetic diversity in sun bears molecular data are needed. For example, a phylogeographic approach can reveal management and evolutionary units (Avise, 1992;Moritz, 1994), help to identify conservation priorities (Goossens et al., 2013), and pinpoint suitable reintroduction locations (Apollonio et al., 2014). ...
Article
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The sun bear Helarctos malayanus is one of the most endangered ursids, and to date classification of sun bear populations has been based almost exclusively on geographic distribution and morphology. The very few molecular studies focussing on this species were limited in geographic scope. Using archival and non-invasively collected sample material, we have added a substantial number of complete or near-complete mitochondrial genome sequences from sun bears of several range countries of the species' distribution. We here report 32 new mitogenome sequences representing sun bears from Cambodia, Thailand, Peninsular Malaysia, Sumatra, and Borneo. Reconstruction of phylogenetic relationships revealed two matrilines that diverged ~295 thousand years ago: one restricted to portions of mainland Indochina (China, Cambodia, Thailand; "Mainland clade"), and one comprising bears from Borneo, Sumatra, Peninsular Malaysia but also Thailand ("Sunda clade"). Generally recent coalescence times in the mitochondrial phylogeny suggest that recent or historical demographic processes have resulted in a loss of mtDNA variation. Additionally, analysis of our data in conjunction with shorter mtDNA sequences revealed that the Bornean sun bear, classified as a distinct subspecies (H. m. euryspilus), does not harbor a distinctive matriline. Further molecular studies of H. malayanus are needed, which should ideally include data from nuclear loci.
... Species reintroductions, i.e., human-mediated attempts to re-establish extirpated species within parts of their former range, have become a common practice in conservation efforts (Armstrong and Seddon, 2008;Ottewell et al., 2014;Scandura et al., 2014;Boitani and Linnell, 2015). As the primary purpose of any reintroduction is to establish a self-sustaining population (IUCN/SSC, 2013), not only the establishment but also the long-term persistence of reintroduced population should be assessed to evaluate the success of such effort (Armstrong and Seddon, 2008). ...
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Where reintroduced wildlife populations are considered as vulnerable this is generally due to limited founder size and isolation. While many of these populations show low levels of genetic diversity, little is known about the temporal patterns of genetic diversity loss and the role of initial founder effects vs. ongoing genetic drift. Here we analysed genotype data from 582 Eurasian lynx samples from the reintroduced Bohemian-Bavarian-Austrian population (BBA) over a time span of 35 years, representing approximately 13 generations. Two-wave reintroduction of lynx from at least two distinct West-Carpathian areas resulted in relatively high start-up of genetic diversity. After the initial decline when the population lost about a quarter of its genetic diversity compared to the Carpathian source population, the genetic diversity and effective population size remained almost unchanged over the next 20 years. Despite confirmed isolation of BBA and thus absence of gene flow, we detected relatively low inbreeding during the two recent decades within the slightly increasing population size, which may have prevented ongoing loss of genetic diversity. Given the current status of BBA, we do not support genetic reinforcement to maintain its long-term viability; but urge the importance of facilitating gene flow with neighbouring lynx populations through an improvement of landscape connectivity and by strengthening law enforcement as well as the prevention of illegal killings. A sound genetic monitoring alongside regular camera trap-based monitoring of population size, health status and reproduction is pivotal to decide on future conservation interventions.
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In mainland Europe, mouflon were first introduced in the 18th and 19th centuries, mainly in Germany, Austria, the Czech Republic, Slovakia, and Hungary. In the early 20th century, mouflon were introduced in Croatia, while all introductions in Slovenia occurred in the 1950s and 1960s. Since the introduction, populations in both countries have remained largely stable, with occasional declines and increases in some areas. Due to several up-following introduction events, also using individuals with unknown origin, the genetic pool of the species might be very admixed; however, no genetic study has been made to date. Therefore, our aim was to: i) determine the origin of introduced mouflon in Slovenia and Croatia, ii) compare the neutral and adaptive genetic make-up of introduced populations. In genetic analyses, which were performed at neutral loci (partial fragment of mitochondrial control region, mtDNA CR) and adaptive major histocompatibility complex (MHC; DRB exon 2) using the next generation sequencing approach, we also included individuals from Germany, France (Corsica), Italy (Sardinia), and the Czech Republic. The haplotype network based on mtDNA CR showed that most analysed mouflon from Slovenia shared the same haplotypes or were closely related to mouflon from Germany and Sardinia, and a few shared the same haplotypes as most mouflon from Croatia. Croatian mouflon from all studied populations shared the same or close haplotypes with individuals from the first Croatian population established in Brijuni Island National Park (northern Adriatic Sea) in the early 20th century. Similar results for populations in both countries were revealed by MHC genes. According to the genetic data, the population origins are generally in agreement with the written historical records, although there are indications of the introduction or release of extra individuals into certain colonies where historical data is lacking. Furthermore, our findings validate that both mitochondrial and MHC genetic diversity are useful tools for investigating the paths of translocation.
Chapter
This comprehensive species-specific chapter covers all aspects of the mammalian biology, including paleontology, physiology, genetics, reproduction and development, ecology, habitat, diet, mortality, and behavior. The economic significance and management of mammals and future challenges for research and conservation are addressed as well. The chapter includes a distribution map, a photograph of the animal, and a list of key literature.
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