Ana səhifə

Genetic diversity and landscape genetic structure of otter (Lutra lutra) populations in Europe


Yüklə 1.4 Mb.
səhifə4/4
tarix24.06.2016
ölçüsü1.4 Mb.
1   2   3   4

Discussion


Lack of phylogeographic structure and origin of the

European otter populations


The otter is one of the few mammalian species that, despite being globally abundant and widely distributed throughout the Eurasian continents, displays very low diversity at the mtDNA CR, and no apparent phylogeographic structure (Randi et al. 2005). Results from previous studies, obtained by partial (300 bp) or complete (1,100 bp) sequencing of the mtDNA CR, showed that a single haplotype is pre- dominantly distributed in almost all the otter populations sampled across Europe, from the Iberian Peninsula to Scandinavia and Russia. Most of the other haplotypes are restricted to single or few localities and the major part of the sampled localities showed just one or a few haplotypes. In this study we obtained extended sequences, including the 30 end of the CYB, the entire CR and the initial 50 region of the 12S RNA, which confirm the published results. The vast majority of otter mtDNA haplotypes differ by 1–2 mutations across more than 1,500 nucleotides, and most of the population groups host just a few haplotypes. The mtDNA sequences showed a star-shaped phylogeny that makes the identification of putative sources of colo- nization events impossible, and that cannot be used to describe any phylogeographic pattern. The otter popula- tions are not reciprocally monophyletic and hence it is not possible to use mtDNA information to design Evolutionary Significant Units (ESU, sensu Moritz 1994), with the exception of the population from southern Italy, which, congruent also with the microsatellite results, might rep- resent an ESU.

The CYB gene (Koepfli and Wayne 1998) and complete mitochondrial genome sequences (Ki et al. 2009) were used in phylogenetic studies of the subfamily Lutrinae, and showed that otters speciated recently. Koepfli et al. (2008) sequenced the CYB and NADH5 genes (1,832 bp in total) in otters from Eurasian localities, showing again that a single very frequent haplotype was widespread, and that most of the haplotypes found in Europe differed just by one or a few mutations. However, three haplotypes sampled

from South Korea were more divergent (1.15% uncorrected distance) and joined into a distinct phylogeographic clade (bootstrap support from maximum-likelihood trees =

100%). Although a recent selective sweep cannot be excluded, these findings suggest that extant European otters originated recently, and that western Europe was colonized by the expansion of a single refugial population. The observed average sequence divergence (0.16% uncorrected distance) could have been generated in ca. 100,000–

150,000 years of evolution from a common ancestral mtDNA genome. This result fits well with recent assess- ments of the European sub-fossil record. The only known Pleistocene otter bones were discovered in northern Italy (Fiore et al. 2004), dated early Weichselian (the Wuerm glaciation). All the other 473 known otter sub-fossil remains were collected only in Holocene deposits (Sommer and Benecke 2004; Sommer and Nadachowski 2006). Otters became frequent and geographically widespread only from 5500 BC, and reached north Europe and the British islands only around 3000 BC. Otter remains are absent from both western and eastern Europe since Mid Holocene (during the Atlantic and Sub Boreal periods,

5500–3000 BC). Hence, sub-fossil and mtDNA data con- sistently indicate that otters colonized central Europe dur- ing the Holocene, most probably from a single refugial population that survived in isolation during the entire last glaciation. Although neither the sub-fossil record nor the mtDNA data can be used to locate the refuge area, it has been hypothesized that otters survived only in the Italian Peninsula (Sommer and Nadachowski 2006), although eastern refugia have also been indicated (Ferrando et al.

2004).

Landscape genetic structure of otter populations


Microsatellite allelic diversity and heterozygosity were moderate in the European otter populations, concordant with other published studies (Dallas et al. 1999, 2002; Pertoldi et al. 2001; Arrendal et al. 2004; Hajkova et al.

2007). In this study, we could not find evidence for any clear global trend in the geographical distribution of genetic diversity. Otters in central Europe (Germany) and Fennoscandia showed the highest numbers of alleles per locus and average heterozygosity. In contrast, other north European populations (e.g. Denmark) showed the lowest genetic diversity values, probably due to post-Pleistocene bottlenecks (Pertoldi et al. 2001; Randi et al. 2005). Con- sequently, the microsatellite data did not indicate any clear phylogeographic patterns. For instance, genetic diversity does not decline northwards as it is expected from serial bottlenecks during colonization waves, or it does not increase in central European regions as expected by






post-glacial admixtures of expanding differentiated popu- lations (Hewitt 2000). These scenarios are not supported perhaps because the historical phylogeographic patterns have been disrupted by the consequences of more recent climate change or anthropogenic population declines and fragmentation. Randi et al. (2003) using Beaumont’s (1999) MSVAR procedure (http://www.rubic.rdg.ac.uk/

*mab/software.html) suggested that otter populations in

Europe suffered two strong demographic declines ca.

4700–4900 and 2000-2600 years ago, respectively. A sudden otter population decline in Denmark, probably caused by human disturbance ca. 2000–3000 years ago, was described by Pertoldi et al. (2001). Hajkova et al. (2007) detected signals of a recent decline (during the last century) that affected the genetic composition of otter populations in the Czech and Slovak republics.

In summary, genetic data indicates that the Holocene history of European otters has been dominated by a global expansion wave followed by local demographic fluctua- tions, which left detectable signals in the genetic make-up of the populations. Most of the groups, corresponding to the sampled countries, that we used in the global popula- tion genetic analyses were not in mutation-drift equilib- rium, showing significant departure from HWE and suggesting that they do not represent random breeding populations, but rather artificial admixture of populations which are at least partially isolated (Wahlund 1928). These artificial groups were split, through Bayesian clustering and landscape genetic analyses, in a number of clusters that represent more natural sub-populations. In this way, otters distributed in Iberia were split into two sub-populations, genetically distinct, which are currently in contact in regions (Coimbra and Portalegre) that are not characterized by obvious physical or habitat barriers. Otters distributed along the western Atlantic French coast and in eastern Germany were sampled through apparently continuous ranges, which however included respectively three and two cryptic sub-populations. We could not identify any obvious extrinsic barrier separating these sub-populations. Otters from Fennoscandia were also subdivided into at least three sub-populations, not delimited by any obvious geographi- cal barrier. Most of the inferred sub-groups were more close to HWE and showed less IBD than their corre- sponding geographical aggregations. The assignment tests also showed that almost all the individuals could be assigned to their respective sub-population of origin. Thus, local otter populations in Europe are genetically subdi- vided, and their cryptic structure is discovered using mul- tilocus markers and landscape genetics methods.

Genetic sub-structure might be maintained by restric- ted contemporary gene flow (Dallas et al. 2002). Signif- icant patterns of IBD are evident at the widest geographical scales covered by this study (e.g. ca.

600 km in Iberia, 600 km in France, 400 km in Germany,

2000 km in Fennoscandia), but they are partially reduced at the smaller geographical scales defined by the cryptic sub-group subdivisions (ranging from 140 to 1600 km; ca. 260 and 410 km in the populations 1 and 2 of Iberia; ca.120, 200 and 180 km in populations 1, 2 and 3 of France; ca. 200 and 200 km in the populations 1 and 2 of Germany; ca. 140, 1600 and 1600 km in the populations

1, 2 and 3 of Fennoscandia). This findings mean that local populations mate randomly and are connected by gene flow at distances not wider than a few hundred km, in agreement with results of Dallas et al. (2002). Despite the potential for high dispersal (Durbin 1996), intrinsic factors, such as natal philopatry and polygyny, or extrinsic habitat barriers (e.g. topography and watershed structure, regions of unsuitable habitats) can hamper gene flow and dispersal. Alternatively, those local populations which are currently expanding after recent declines and fragmentation events, like the otter populations in Ger- many, might have had no time enough to admix and reach stable genetic equilibria.

Conclusions: population genetics and otter conservation


This study generalizes at a continental scale early findings showing that European otters do not present any obvious phylogeographic pattern, but that extant local populations are isolated by distance and deviate from HWE. Concor- dantly with results described by Dallas et al. (2002) in British otters, also the populations sampled in south Iberia, central Europe and Fennoscandia showed cryptic sub- structuring, which could have not been predicted simply by their spatial distributions. A continent-wide lack of phy- logeographic structure did not prevent the onset of fine- grained population sub-structuring. Consequently, otters in Europe are currently subdivided in a mosaic of sub-popu- lations generated by both historical (fragmentation) and current (limited dispersal) factors.

Conservation strategies, either if based on habitat restoration or animal translocations, should take into account these information. Habitat restoration programs are aimed at facilitating the expansion of extant natural populations. However, evidences of IBD, detectable at a scale of a few hundred km, and limited gene flow indi- cate that effective otter dispersal distances are spatially restricted. It follows that source populations should not be geographically too distant from putative colonization areas (Dallas et al. 2002). Many otter distribution areas remain to be better sampled, and detailed landscape genetic analyses need to be performed case-by-case, to identify those critical landscape features that can limit






otter dispersal within and between river basins (Janssens et al. 2008).

In areas in which natural colonization is not possible or

natural connections are not available, reintroduction pro- grams are considered a viable alternative. In Europe rein- troduction programs were based on the release of wild- captured or captive-reproduced otters. In these cases, pre- liminary assessments of the genetic structure of the foun- ders, are mandatory, in order to avoid the release: (1) of animals that originated from crossings between European and Asian otters (Wayre 1991), which are known to bear mtDNA haplotypes of non-European origin (Mucci et al.

1999; Randi et al. 2003; Ferrando et al. 2004); (2) of highly inbred otters with low genetic variability. The dynamics of reintroduced populations should be carefully monitored, also using non-invasive genetic methods. The outcome of reintroduction projects can vary if evaluated at local or more widespread geographic scales. Released otters might survive and reproduce successfully locally, but the genetic structure of more distant population might be not affected (Arrendal et al. 2004).

Both habitat restoration and animal translocations could lead to admixture of populations that have been historically isolated and genetically differentiated. Admixture would increase genetic diversity and reduce inbreeding, or, in contrast, results in a loss of local adaptation and increases the risk of outbreeding depression (Edmands 2007), depending on the past demographic history of the admixing populations. Local adaptations could originate rapidly also in large and mobile carnivores and generate genetically differentiated ecotypes (Musiani et al. 2007). The adaptive consequences of otter isolation in different habitats types are, at the moment, unknown. More detailed landscape genetic analyses and monitoring of ongoing translocation projects, could eventually lead to identify populations that are better suited to survive, for instances, in poor versus rich food resource areas, or in coastal versus inland eco- systems. For these reason, waiting for better identification of eventual genotype-habitat covariance, we suggest cau- tions in planning translocation of otters among very dif- ferent habitat types.

Finally, results in this study offer, for the first time at a continental scale, a collection of allele frequencies that can be used as a guideline to design non-invasive genetic projects, suited to monitor the dynamics of reintroduced populations, including apparent survival, sex ratios, dis- persal and effective gene flow (Jansman et al. 2001; Ar- rendal et al. 2004; Hajkova et al. 2007). In particular, this data set identifies baseline populations that can be used to detect the presence of contemporary migration from neighboring populations, or the presence of alien genotypes that could derive from the release of captive bred otters of non-European origins.

Acknowledgments This study has been partly supported by the Italian Ministry of Environment, Department of Nature Conservation. We wish to thank the ConGen program (funded by the European Science Foundation) and the Danish Natural Science Research Council for financial support to C. Pertoldi (grant number: #21-01-

0526, #21-03-0125 and 95095995). P. Hajkova was supported by the Grant Agency of the Academy of Sciences of the Czech Republic, grant no. KJB600930804 and by the Ministry of the Environment of the Czech Republic, grant no. VaV-SP/2d4/16/08. VaV-SP/2d4/16/

08. We thank everybody who helped in sampling collection. In par- ticular, for France, L. Lafontaine wishes to acknowledge all people who provided otter samples for this study, and/or belonging to the following networks : SFEPM, LPO, ONCFS (DRD CNERA-PAD, F. Le´ger, P. Migot, D. Serre), ONEMA, FDAPPMA, Parcs Naturels Re´gionaux de Brie`re (X. Moyon), du Morvan, MNHN (G. Ve´ron) and Muse´ums d’Histoire Naturelle of La Rochelle, Orle´ans, Toulouse, ENV Nantes, ADEV, GMB, Syndicat du Bassin du Scorff, Station INRA Moulin des Princes, APPMA Plouay, Base du Douron, EDENN, AREMIP, LPO Marais Breton, Fe´de´rations De´partemen- tales des Chasseurs and officers from the Office National de la Chasse et de la Faune Sauvage SD12, SD17, SD22, SD29, SD33, SD35, SD40, SD44, SD56, SD85. The careful revisions done by three anonymous referees, and additional comments by the Associated Editor, greatly aided us to improve early versions of this paper.

References


Arrendal J, Walker CW, Sundqvist AK et al (2004) Genetic evaluation of an otter translocation program. Conserv Genet

5:79–88


Avise JC (1986) Mitochondrial DNA and evolutionary genetics of higher animals. Phil Trans R Soc Lond B 312:325–342

Bandelt HL, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

Beaumont M (1999) Detecting population expansion and decline

using microsatellites. Genetics 153:2013–2029

Belkhir K, Borsa P, Chikhi L et al. (2001) GENETIX 4.02, logiciel sous Windows TM pour la ge´ne´tique des populations. Laboratoire Ge´nome, Populations, Interactions, CNRS UMR 5000, Univer- site´ de Montpellier II, Montpellier, France. http://www.genetix. univ-montp2.fr/genetix/genetix.htm

Benzecri JP (1973) L’Analyse des donnees. Vol 2, L’Analyse des correspondances. Dunod, Paris

Bifolchi A, Lode` T (2005) Efficiency of conservation shortcuts: an

investigation with otters as umbrella species. Biol Conserv

126:523–527

Cassens I, Tiedemann R, Suchentrunk F, Hartl G (2000) Mitochon- drial DNA variation in the European otter (Lutra lutra) and the use of spatial autocorrelation analysis in conservation. J Hered

91:31–35

Dallas JF, Piertney SB (1998) Microsatellite primers for the Eurasian otter. Mol Ecol 7:1247–1251

Dallas JF, Bacon PJ, Carss DN et al (1999) Genetic diversity in the

Eurasian otter, Lutra lutra, in Scotland. Evidence from micro- satellite polymorphism. Biol J Linn Soc 68:73–86

Dallas JF, Marshall F, Piertney SB et al (2002) Spatially restricted gene flow and reduced microsatellite polymorphism in the Eurasian otter Lutra lutra in Britain. Conserv Genet 3:15–29

Durbin LS (1996) Individual differences in spatial utilization of a river system by otters Lutra lutra. Acta Theriol 41:137–147

Edmands S (2007) Between a rock and a hard place: evaluating the

relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475






Effenberger S, Suchentrunk F (1999) RFLP analysis of mitochondrial DNA of otters (Lutra lutra) from Europe. Implications for the conservation of a flagship species. Biol Conserv 90:229–234

Excoffier L, Laval G, Schneider S (2005) ARLEQUIN ver. 3.0: an integrated software package for population genetics data anal- ysis. Evolut Bioinform Online 1:47–50

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

Ferrando A, Ponsa` M, Marmi J, Domingo-Roura X (2004) Eurasian

otters, Lutra lutra, have a dominant mtDNA haplotype from the

Iberian Peninsula to Scandinavia. J Hered 95:430–435

Finnegan LA, Ne´ill LO´ (2009) Mitochondrial DNA diversity of the

Irish otter, Lutra lutra, population. Conserv Genet. doi:

10.1007/s10592-009-9955-4

Fiore I, Gala M, Tagliacozzo A (2004) Ecology and subsistence strategies in the eastern Italian Alps during the Middle Palae- olithic. Int J Osteoarchaeol 14:273–286

Foster-Turley P, Santiapillai C (1990) Action plan for Asian otters.

In: Foster-Turley P, Macdonald SM, Mason CF (eds) Otters: an action plan for their conservation. IUCN, Gland, Switzerland

Garnier S, Alibert P, Audiot P et al (2004) Isolation by distance and sharp discontinuities in gene frequencies: implications for the phylogeography of an alpine insect species, Carabus somieri. Mol Ecol 13:1883–1897

Gerloff U, Schlotterer C, Rassmann K et al (1995) Amplification of hypervariable simple sequence repeats (microsatellites) from excremental DNA of wild living Bonobos (Pan paniscus). Mol Ecol 4:515–518

Guillot G, Mortier F, Estoup A (2005) GENELAND: a computer package for landscape genetics. Mol Ecol Notes 5:712–715

Hajkova P, Pertoldi C, Zemanova B et al (2007) Genetic structure and evidence for recent population decline in Eurasian otter popu- lations in the Czech and Slovak Republics: implications for conservation. J Zool 272:1–9

Hewitt G (2000) The genetic legacy of the Quaternary ice ages.

Nature 405:907–913

IUCN (1998) Guidelines for re-introductions. Prepared by the IUCN/ SSC re-introduction specialist group. IUCN, Gland and Cambridge

Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics

23:1801–1806

Jansman HAH, Chanin PRF, Dallas JF (2001) Monitoring otter populations by DNA typing of spraints. IUCN Otter Spec Group Bull 18:12–19

Janssens X, Fontaine MC, Michaux JR et al (2008) Genetic pattern of the recent recovery of European otters in southern France. Ecography 31(2):176–186

Jefferies DJ, Wayre P, Jessop RM, Mitchell-Jones AJ (1986) Reinforcing the native otter Lutra lutra population in East Anglia: an analysis of the behavior and range development of the first release group. Mamm Rev 16:65–79

Ketmaier V, Bernardini C (2005) Structure of the mitochondrial control-region of the Eurasian Otter (Lutra lutra; Carnivora, Mustelidae): patterns of genetic heterogeneity and implications for conservation of the species in Italy. J Hered 96:318–328

Ki JS, Hwang DS, Park TJ et al (2009) A comparative analysis of the complete mitochondrial genome of the Eurasian otter, Lutra lutra (Carnivora; Mustelidae) Mol Biol Rep. doi:10.1007/ s11033-009-9641-0

Koelewijn HP, Jansman HAH (2007) The Dutch otter reintroduction project: what non-invasive genetic sampling told us about social structure and behaviour in a low density population. In:

Proceedings of V European congress of mammalogy, Siena, Italy. Hystrix It J Mamm, 2:524, 21–26 September 2007

Koepfli KP, Wayne RK (1998) Phylogenetic relationships of otters (Carnivora: Mustelidae) based on mitochondrial Cytochrome b sequences. J Zool 246:401–416

Koepfli KP, Kanchanasaka B, Sasaki H, Jacques H, Louie KDY, Hoai T, Xuan Dang N, Geffen E, Gutleb A, Han S, Heggberget TM, Lionel LaFontaine L, Lee H, Roland Melisch R, Ruiz-Olmo J, Santos-Reis M, Sidorovich VE, Stubbe M, Wayne RK (2008) Establishing the foundation for an applied molecular taxonomy of otters in Southeast Asia. Conserv Genet 9:1589–1604

Kruuk H (2006) Otters ecology, behaviour and conservation. Oxford

University Press, Oxford

Longmire JL, Maltbie M, Baker RJ (1997) Use of ‘‘lysis buffer’’ in DNA isolation and its implication for museum collections. Occasional Papers, Museum of Texas Tech University 163:1–4

Macdonald SM, Mason CF (1994) Status and conservation needs of

the otter (Lutra lutra) in the western Palaearctic. Nat Environ

67:1–54

Madsen AB (1996) Otter (Lutra lutra) mortality in relation to traffic and experience with using stop-grids in Denmark. In: Proceedings of the Vth International Otter Colloquium. Habitat 6:237–241



Moritz C (1994) Defining ‘evolutionarily significant units’ for conservation. Trends Ecol Evol 9:273–375

Mucci N, Pertoldi C, Madsen AB et al (1999) Extremely low mitochondrial DNA control-region sequence variation in the otter (Lutra lutra) population of Denmark. Hereditas 130:331–336

Musiani M, Leonard JA, Cluff HD et al (2007) Differentiation of

tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. Mol Ecol

16:4149–4170

Paetkau D, Slade R, Burdens M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol

13:55–65

Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in excel.

Population genetic software for teaching and research. Mol Ecol

Notes 6:288–295

Pe´rez-Haro M, Vin˜ as J, Man˜ as F et al (2005) Genetic variability in the complete mitochondrial control-region of the Eurasian otter (Lutra lutra) in the Iberian Peninsula. Biol J Linn Soc 86:397–

403


Pertoldi C, Hansen MM, Loeschcke V et al (2001) Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993. Proc R Soc Lond B Biol Sci 268:1775–

1781


Prigioni C, Remonti L, Balestrieri A et al (2006) Estimation of European otter (Lutra lutra) population size by fecal DNA typing in southern Italy. J Mammal 87:855–858

Pritchard JK, Stephens M, Donnelly PJ (2000) Inference of popula- tion structure using multilocus genotype data. Genetics 155:945–

959

Randi E, Davoli F, Pierpaoli M et al (2003) Genetic structure in otter (Lutra lutra) populations in Europe: implications for conserva- tion. Anim Conserv 6:1–10



Randi E, Mucci N, Arrendal J et al (2005) Assessing the patterns of

genetic diversity in otter populations in Europe. In: European

Otter Workshop, Padula (Salerno), Italy, 20–23 October 2005

Reuther C (1994) European otter habitat network. In: Seminar on the conservation of the European otter (Lutra lutra), Environmental Encounters 24, Strasbourg, Leeuwarden, Council of Europe

Reuther C, Roy A (2001) Some results of the 1991 and 1999 otter (Lutra lutra) surveys in the River Ise catchment, Lower-Saxony, Germany. IUCN Otter Spec Group Bull 18:28–40




Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

Rozas J, Sanchez-DelBarrio JC et al (2003) DNASP, DNA polymor- phism analyses by the coalescent and other methods. Bioinfor- matics 19:2496–2497

Ruiz-Olmo J, Lo´ pez-Mart´ın JM, Palazo´ n S (2001) The influence of

fish abundance on the otter (Lutra lutra) populations in Iberian

Mediterranean habitats. J Zool 254:325–336

Saavedra D, Sargatal J (1998) Reintroduction of the otter (Lutra lutra)

in northeast Spain (Girona Province). Galemys 10:191–199

Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites. Application to human mitochondrial DNA. Genetics 152:1079–1089

Sjo¨ a˚sen T (1996) Survivorship of captive-bred and wild-caught

reintroduced European otters Lutra lutra in Sweden. Biol

Conserv 76:161–165

Sommer R, Benecke N (2004) Late- and Post-Glacial history of the

Mustelidae in Europe. Mamm Rev 34:249–284

Sommer RS, Nadachowski A (2006) Glacial refugia of mammals in

Europe: evidence from fossil records. Mamm Rev 36:251–265

Stanton DWG, Hobbs GI, Chadwick EA et al (2009) Mitochondrial genetic diversity and structure of the European otter (Lutra lutra) in Britain. Cons Genet 10:733–737

Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

Van Ewijk KY, Knol AP, De Jong RCCM (1997) An otter PVA as a preparation of a reintroduction experiment in the Netherlands. Z Saugetier 62:238–242

Wahlund S (1928) Zusammensetzung von Populationen und Korre- lationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11:65–106

Wayre J (1991) The Otter Trust’s reintroduction programme using

captive-bred otters. In: Reuther C, Rochert C, Hankensbiattel R (eds) Proceedings of international Otter Colloquium. Habitat

6:219–222

Weber D, Weber JM, Mu¨ ller HU (1991) Fischotter (Lutra lutra L.) in Schwarzwasser-sensegebiet; dokumentation eines gescheiterten Wiedereinbu¨ rgerungsversuches. [Otters in the Schwarzwasser- Sense-catchment; documentation of an unsuccessful re-intro- duction project.] Mitteilungen der Naturforschenden Gesell- schaft in Bern. (In German with English summary)

Wright S (1969) Evolution and the genetics of populations. Vol 2, the theory of gene frequencies. University of Chicago Press, Chicago




123


1   2   3   4


Verilənlər bazası müəlliflik hüququ ilə müdafiə olunur ©atelim.com 2016
rəhbərliyinə müraciət