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A genetic background for reintroduction program of the European bison (Bison bonasus) in the Carpathians
Biological Conservation 108 (2002) 221–228 www.elsevier.com/locate/biocon
A genetic background for reintroduction program of the European bison (Bison bonasus) in the Carpathians Wanda Olecha, Kajetan Perzanowskib,* a Warsaw Agricultural University, Department of Animal Genetics, 02-786 Warsaw, Poland International Centre for Ecology, Polish Academy of Sciences, 38-700 Ustrzyki Dolne, Poland
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Received 20 September 2001; received in revised form 12 March 2002; accepted 13 March 2002
Abstract The European bison, extirpated from the Carpathian Mountains over 200 years ago, was reintroduced to the Bieszczady Mountains in the 1960/1970s in two small, isolated herds, and is now threatened by high inbreeding and low genetic variability. A new program of re-establishing viable populations in the Carpathians is based on the genetic analysis of formerly released animals, using the European Bison Pedigree Book. Calculating founder contributions, founder genome survival, founder genome equivalent, inbreeding coefficient and mean kinship allows the identification of under-represented or missing founders. Since genetic variability is much higher among bison in captivity and, in Poland, the Lowland–Caucasian line is represented only in those free-ranging herds, the reintroduction will be based on animals from foreign breeding centres. Bison will be released into existing herds, and planned new introduction sites, to facilitate natural gene exchange in the future. The same approach will be recommended for planned introductions in the Slovakian and Romanian Carpathians. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: European bison; Carpathians; Bieszczady; Genetics; Reintroduction
1. Introduction The European bison is among the few species known to be experiencing an extreme bottleneck (Erlich and Erlich, 1981). In the early twentieth century, only 54 individuals survived in the whole world population (Pucek, 1991). Genetic variation was very low because all these animals were descended from only 12 founders. During the subsequent recovery program, meticulous records (European Bison Pedigree Book) have been kept and updated for all animals in captivity, which allows precise tracking of the origin of the majority of currently living bison. At present, the species is separated into two genetic lines: a Lowland (or Bialowieza) line that is pure lowland subspecies (Bison bonasus bonasus) and a second Lowland–Caucasian line that is a mixture of two subspecies. The gene pool of the former contains genes from only seven founders: males Nos. 45, 87, 15 and 147 and females Nos. 42, 89 and 16. The Lowland– Caucasian line was derived from 12 founders, i.e. five * Corresponding author. E-mail address: [email protected] (K. Perzanowski).
more than the Lowland line. Among those additional five founders were male No. 100 ‘‘Kaukasus’’, originating from subspecies caucasicus and females Nos. 35, 46, 95 and 96 (see Slatis, 1960). According to the breeding strategy operated Poland and other European countries, those two lines should be maintained separately, especially in free-ranging herds. Cross mating between animals from these two lines should be prevented to save the genetic structure and originality in both groups. The present herd of bison in the Bieszczady Mountains are Lowland–Caucasian animals, and represent the only herd of this line in Poland (Pucek, 1984; Olech, 1999). At present, there are only a few free-ranging herds of bison in the Carpathians, originating from introductions during the 1960s and 1970s in Poland and Ukraine. None of these has reached the numbers that assure demographic and genetic stability. In many cases, man-made barriers such as the impenetrable state border, major highways and railroads separate adjacent herds. Under the project launched by WWF-Europe, aiming to reestablish the bison over its former natural range in the Carpathians, further reintroductions are planned to create connectivity between existing bison
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(02)00108-8
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ranges. This should ultimately allow natural gene exchange among the herds (Pererva et al., 1989; Perzanowski, 2000; Perzanowski and Kozak, 2000; Fig. 1). The initial introductions were undertaken without regard for the genetic composition of the herd. Therefore, the baseline for the present program is a genetic analysis of those herds presently living in the Carpathians, using Pedigree Book data to identify their genetic structure. Through the introduction of animals carefully chosen from captive herds, the composition of the gene pools should be improved through the equalisation of the contribution of all founders. This should reduce the present, very high, levels of inbreeding, improving the chances of establishing free ranging and self-sustaining populations. However, some doubts can be raised about the future of such highly inbred species; the case of the Chillingham cattle, a semi-wild breed remaining in isolation for over 300 years, indicates considerable potential among Bovidae for surviving even severe population bottlenecks (Hall, 1989; Visscher et al., 2001).
2. Methods 2.1. History The history of the European bison in Bieszczady (extirpated over 200 years ago) started again in 1963. Then, following the concept of spatially separating pure lowland animals from the descendants of mixed Lowland–Caucasian line, a decision was made to create a free-ranging bison population of the Lowland– Caucasian line in the Bieszczady (south-east Poland). The first area identified as most suitable comprised two forest districts (Stuposiany and Tarnawa, which no longer exists) in the south-eastern corner of Bieszczady, close to the state border with Ukraine. The area extended over ca. 20,000 ha, situated between 400 and 1300 m above sea level, with only a few human settlements. That habitat comprised mixed beech and fir (Fagus silvatica, Abies alba) forest, with many clearings as well as alpine meadow, :providing an excellent summer pasture for large grazers (Z abin´ski, 1968; Jaron´ski and Pepera, 1969).
Fig. 1. Present distribution of European bison herds in Bieszczady Mountains, Poland and the location of two, planned introduction sites. 1, Country border; 2, boundary of Bieszczady National Park; 3, boundary of Biosphere reserve; 4, boundary of forest districts; 5, home ranges of European bison herds; S, the planned re-introduction site in Slovakia; WM, Wola Michowa—the proposed place for reintroduction in Poland (after Perzanowski and Paszkiewicz, 2000, modified).
W. Olech, K. Perzanowski / Biological Conservation 108 (2002) 221–228
Between the autumn of 1963 and summer 1964, 15 bison including seven (three males, four females) adult and eight young (born in 1962, six males, two females) were translocated from breeding centres at Niepoomice and Pszczyna in Poland. In 1966, a further four individuals (two cows and two bulls) were brought from the same source. The animals were placed in an enclosure of 5 ha (60% a timber stand and 40% an forest opening) which was kept closed over winter. Subsequent movements of the herd, and its population dynamics were recorded by local forest rangers. At the beginning of 1967, the herd consisted of 21 animals (13 bulls and eight cows), including three calves born in the Bieszczady Mountains. This population has now spread into neighbouring districts, some crossing the state border with Ukraine. Their total number is estimated at > 100 animals (Fig. 1). In 1974, a group of six animals (four cows, one bull and one calf) was brought from Pszczyna and Cracov Zoo to a 18 ha enclosure, located in the village of Wola Michowa in the Koman˜cza Forest District. Over the next 5 years, the herd was supplemented with more animals, but two individuals from the first group were shot under suspicion of having serious pulmonary problems. In 1980, the whole group of 14 animals (Table 2) was finally released to the wild. For 4 years they stayed around the enclosure, but from 1991 they began to migrate into the neighbouring forest district of Baligro´d, where they have been permanently present since 1993. At present, this population is estimated at ca. 50 animals (Fig. 1). Complete records of population dynamics are available since 1985, at which time the total number of both groups of bison in Bieszczady reached 160. However, the period from the end of the 1980s through to the early 1990s witnessed a distinct decline to about 100 individuals. The most likely reason is migration across the Polish–Ukrainian border. By 1999, numbers in Bieszczady had again reached 160 animals. The group dwelling in Baligro´d district stays most of the time as one herd. The first herd (in Stuposiany district) however has fragmented into several smaller groups, in most cases migrating north, even as far as 50 km to the Brzegi Dolne district. At present bison are recorded there in three districts: Stuposiany, Lutowiska, Brzegi Dolne, and during summer within Bieszczady National Park. To date there is no evidence for any contact between bison originating from the Stuposiany and Koman´cza herds (Perzanowski and Paszkiewicz, 2000). The material for the present analysis was full pedigree (down to the founders) of all animals released in Bieszczady, comprising 19 individuals (11 bulls, eight cows) in Stuposiany region and 14 (six bulls, eight cows) in Koman´cza. The pedigrees of the ancestors of the Bieszczady herd were taken from European Bison Pedigree Book (issues 1924–1980).
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2.2. Genetic analysis The inbreeding coefficient and mean kinship within the group were calculated for each released animal in order to present the homogeneity of ancestors and show the relationship of each animal to the group. Subsequently, the founder contribution (in genomes) of every released animal was evaluated to assess the genetic structure of initial herds. All those parameters are widely used for comparisons of the various subsets of the European bison population (Belousova and Kudrjavatsev, 1996; Olech, 1989). Those parameters were computed using our own computer program, based on algorithms developed by Quass (1976). The pedigrees of the ancestors of the Bieszczady herd were also analysed using the gene drop method (Lacy, 1995) to determine the proportion of the genetic variability retained at the time of herd creation. For both introduced groups, the mean genetic retention was also calculated to determine the proportion of founder genes present at the moment of their release. Also, the founder genome equivalent (FGE), which provides information on the genetic variation, was computed. FGE can be explained as the number of equally contributing founders that would be required to obtain the level of genetic diversity that was observed in the group (Lacy, 1986). These parameters were calculated for both parts of the Bieszczady population, and compared with their relevant values in the contemporary captive population of Lowland–Caucasian line.
3. Results The values of the founder contribution to all released animals are given in Tables 1 and 2. Two founders (Nos. 147 and 46) are not represented in Stuposiany region at all. Five females in Stuposiany did not have genes from founder No. 35. In Koman´cza, only one founder (No. 46) was not represented but many others contributed an average of < 1%. Additionally, since five females (of eight) and three males in Koman´cza group came from the Pszczyna line, they only had genes from that pair of founders (Nos. 45 and 42). Only one male released in Koman´cza originated from the Lowland–Caucasian line; however, because the other five males belonged to Lowland subspecies, some hopefully had genes from founder No. 147. Fig. 2 gives a comparison of the founders’ contribution in both herds with the mean values for all contemporaries in a sample of captive Lowland–Caucasian line. In Stuposiany, the contribution of only two founders (Nos. 45 and 42) is over-represented, being higher than the average for contemporary animals. The contribution of the other founders is conversely smaller than the average for animals in captivity. The situation
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Table 1 The founder contribution [%] of 19 animals that gave origin to the Stuposiany herd EBPB No.
Sex
Founder numbers 45
42
89
87
16
15
28.12 37.50 12.50 12.50 12.50 32.81 32.81 32.81
28.12 28.12 12.50 12.50 12.50 23.44 23.44 23.44
12.50 7.81 26.56 26.56 26.56 10.16 10.16 10.16
12.50 7.81 14.06 14.06 14.06 10.16 10.16 10.16
4.69 4.69 5.47 5.47 5.47 5.86 5.86 5.86
4.69 4.69 5.47 5.47 5.47 5.86 5.86 5.86
25.195
20.508
16.309
11.621
5.420
5.420
9.37 18.75 32.81 12.50 12.50 32.81 12.50 35.94 14.06 12.50 23.44
9.37 18.75 23.44 12.50 12.50 23.44 12.50 26.56 14.06 12.50 23.44
26.56 17.19 10.16 25.78 25.00 10.16 26.56 7.81 25.00 26.56 18.75
14.06 17.19 10.15 13.28 12.50 10.16 14.06 7.81 12.50 14.06 12.50
7.03 7.03 5.86 5.86 6.25 5.86 5.47 5.47 5.47 5.47 3.91
7.03 7.03 5.86 5.86 6.25 5.86 5.47 5.47 5.47 5.47 3.91
Mean
19.745
17.188
19.958
12.571
5.788
5.788
0
5.664
1.847
0
3.818
7.635
Overall mean
22.470
18.848
18.133
12.096
5.604
5.604
0
5.066
1.510
0
3.557
7.114
973 1141 1300 1386 1466 1467 1566 1574
F F F F F F F F
Mean 1128 1287 1378 1453 1456 1458 1462 1468 1471 1563 1567
M M M M M M M M M M M
147
100 2.34 2.34 7.42 7.42 7.42 2.93 2.93 2.93
0
35
46
3.12 3.12 3.12
4.468
1.172
8.20 3.52 2.93 7.62 7.81 2.93 7.42 2.73 7.42 7.42 4.30
3.12
0
95 2.34 2.34 4.30 4.30 4.30 2.93 2.93 2.93
4.69 4.69 8.59 8.59 8.59 5.86 5.86 5.86
3.296
6.592
5.08 3.52 2.93 4.49 4.69 2.93 4.30 2.73 4.30 4.30 2.73
3.12 3.12 3.12 3.12 3.12 1.56
96
10.16 7.03 5.86 8.98 9.37 5.86 8.59 5.47 8.59 8.59 5.47
EBPB, European Bison Pedigree Book; F, Female; M, Male.
in Koman´cza is worse because genes from two founders (Nos. 42 and 45) over dominate the gene pool. The inbreeding coefficient (the animals’ own value of homogeneity) and the mean kinship (the average similarity to the herd) are presented in Tables 3 and 4. Mean kinship is especially useful in selecting the most valuable animals from a genetic point of view (e.g. male No. 1468 was the most unique in the group at Stuposiany because his mean kinship value is the smallest). The average inbreeding coefficient for the Stuposiany herd was 13.7%, i.e. lower than in Koman´cza (37.6%) where eight animals are descendants from only one pair of founders. In Stuposiany, eight founder animals had coefficients < 10%, and three > 20%, but in Koman´cza only two individuals were below 20%. The average mean kinship in the Stuposiany herd was 24.4% and in Koman´cza was distinctly higher (33.0%), confirming the inbreeding data in showing that the relationships within Koman´cza are much closer than at Stuposiany. The mean kinship among animals from Pszczyna line (with names starting with letters ‘‘PL’’) is very high, so the genetic value of those individuals to the herd is low (Table 4). Table 5 shows that the present captive population has a higher genetic variability than either of the two free-ranging herds of Bieszczady (Stuposiany and
Koman´cza), including the mean retention of founder genes, and the value of inbreeding coefficient.
4. Discussion At the time of first two releases into Bieszczady, no attention was paid to genetic aspects of the new populations. Consequently, we have assumed that the average value of founder contributions to the released males and females reflects the structure of the parent herd at the time. It can be disputed whether the significance of every animal included in the average should be the same, though because of lack of evidence on mating patterns after release, all males and females were equally taken into account. It might be expected that the social domination of some males will lead certain founders to be even more over-represented in contemporary populations, hence the actual level of genetic diversity within the wild would be lower than theoretically calculated. That however can only be determined using modern techniques like DNA analysis. In the case of European bison, where only 12 animals founded the present population, the lack (or serious under-representation) of some founders may lead to a critical level of inbreeding. In
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W. Olech, K. Perzanowski / Biological Conservation 108 (2002) 221–228 Table 2 The founder contribution [%] of 14 animals that gave origin to the Koman´cza herd EBPB No.
2127 3293 3530 3531 3533 3981 4274 4275
Sex
F F F F F F F F
Founder numbers 45
42
69.53 69.14 21.48 14.06 19.92 70.70 69.53 69.53
30.47 30.86 21.48 14.06 17.58 29.30 30.47 30.47 7.446
89
87
16
15
17.19 23.44 18.94
14.06 14.06 12.69
5.66 6.25 6.15
5.66 6.25 6.15
2.258
2.258
0
2.008
1.56 10.55
1.56 7.42
6.25 3.32
3.12 3.32
3.12
1.56
1.56
3.12
1.56
1.56
100
35
4.00 6.64 5.42
0.78 2.34 1.56
0.586
0
46
1.422
95
96
3.22 4.30 3.86
6.44 8.59 7.71
Mean
50.488
25.586
3063 3528 3538 3768 3978 3980
M M M M M M
52.15 42.77 69.14 69.92 60.16 70.31
Mean
60.742
29.362
2.279
1.758
2.116
1.335
0.781
0.720
0.130
0
0.342
0.684
Overall mean
55.615
27.474
4.863
3.431
2.187
1.797
0.391
1.240
0.358
0
0.882
1.764
32.23 22.85 30.86 30.08 30.47 29.69
5.103
147
4.10
2.844
2.05
EBPB, European Bison Pedigree Book; F, Female; M, Male.
Table 3 Inbreeding and mean kinship coefficients for animals released at Stuposiany Forest District EBPB No
Name
Sex
Father No
Mother No
Inbreeding coefficient
Mean Kinship
973 1141 1300 1386 1466 1467 1566 1574 1128 1287 1378 1453 1456 1458 1462 1468 1471 1563 1567
PULESNA PUJANKA PUCZAJA PUCELA PUCNOTA PUNINA PUMAJKA PUNICA PULON PULPIT PURLAN PUSTAN PURUS PURI PUSZCZAR PUREK PUJAR PUSZCZOT PUCZAJ
F F F F F F F F M M M M M M M M M M M
761 949 879 879 879 949 949 949 879 761 949 879 879 949 879 949 879 879 1207
724 973 790 1030 1030 1021 1021 941 823 979 979 903 795 941 790 725 973 790 1300
0.3086 0.2036 0.0769 0.0769 0.0769 0.1538 0.1538 0.1538 0.1008 0.2441 0.1538 0.0741 0.0791 0.1538 0.0769 0.1875 0.0691 0.0769 0.1821
0.2797 0.2595 0.2504 0.2399 0.2399 0.2450 0.2450 0.2450 0.2295 0.2498 0.2422 0.2303 0.2253 0.2450 0.2453 0.2118 0.2535 0.2453 0.2608
0.1370
0.2444
Average value EBPB, European Bison Pedigree Book.
fact, there was some speculation connecting the relatively low reproductive success and appearance of certain diseases in some free-ranging populations with the very low level of genetic variability (Gill, 1999). The negative influence of inbreeding on the viability of
calves was also reported (Olech, 1987; Belousova and Kudrjavtsev, 1996) Two founders (Nos. 45 and 42) are over represented in the gene pool, but the average value for animals in captivity is < 37% for both founders together. In some
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Fig. 2. The comparison of founder contribution in Stuposiany and Koman´cza herds with its average value for contemporary world captive population of Lowland–Caucasian line. Numbers of founders, according to European Bison Pedigree Book. VFC—values of founder contribution.
Table 4 Inbreeding and mean kinship coefficients for animals released at Koman´cza Forest District EBPB No.
Name
Sex
Father No.
Mother No.
Inbreeding coefficient
Mean kinship
2127 3293 3530 3531 3533 3981 4274 4275 3063 3528 3538 3768 3978 3980
PLIZA PLERKA PUGA PUHA II PUNA PLEREZA PLISHA PLANETOIDA POLCER PULAS PLOTKIR PLENNY POROS PLUSKAR
F F F F F F F F M M M M M M
1561 2267 2263 2263 2263 1866 2547 2547 1987 1997 2267 1561 2382 1866
1469 1357 2257 1205 2393 1994 2127 2678 2265 2542 1367 1994 2399 1357
0.4985 0.5090 0.2476 0.2276 0.1885 0.5170 0.6006 0.5557 0.2544 0.1016 0.5374 0.5232 0.3684 0.5156
0.4250 0.4151 0.2076 0.1862 0.2049 0.4172 0.4309 0.4231 0.3300 0.3018 0.4171 0.4181 0.3672 0.4031
0.3763
0.3298
Average value EBPB, European Bison Pedigree Book.
free herds of the Lowland–Caucasian line in Russia, the contribution of these founders is close to 65% (Belousova and Kudrjavatsev, 1996), but in Koman´cza region it is higher that 80%. All other founders make a smaller contribution, so it is interesting that in Stuposiany, the contribution of two founders (Nos. 87 and 89) is higher than average. In the best theoretical scenario, all founders should contribute equally (Ballou and Lacy, 1995). Further introductions can change the structure of gene pool towards this ‘‘best scenario’’, and the aim of
genetic reintroduction from captivity is one of most important reasons for this captive breeding (Kleiman, 1996). At the time that the Koman´cza and Stuposiany herds were established, they contained only 65.9 and 75.6% of the original genetic variation. This is not a bad scenario, however, for the captive population remains an excellent source for further reintroductions. The European bison presently in captivity have retained much more of their original genetic diversity than any of the bison
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Table 5 A comparison of genetic characteristics within Stuposiany and Koman´cza European bison herds compared with values for animals from Lowland– Caucasian line living at present in captivity
Number of founders Founder genome equivalent Fraction of gene diversity retained Mean inbreeding value
Stuposiany herd
Koman´cza herd
Present captive population
10 2.049 0.756 0.137
11 1.465 0.659 0.376
12 3.060 0.837 0.212
groups released into Bieszczady 20 years ago. Thus, further introductions of animals, selected from breeding centres, remains the simplest way of enhancing genetic variability and enriching the gene pool of the free ranging population (Mills and Allendorf, 1996). On the basis of pedigree analysis (European Bison Pedigree Book), it is possible to choose animals from the captive stock with above average contributions from absent or under-represented founders, and use these to enrich the gene pool of the wild herds. That opportunity can be especially important in planning large scale programs such as the restitution of the Carpathian population of European bison, based around the few, isolated free-ranging animals whose ancestors were introduced to Poland, Ukraine, Romania and Slovakia some 30 years ago. In this program, the enrichment of genetic structure of free-ranging herds will be one of the main aims. Hopefully, such an approach will become a standard in animal introduction programmes because, so far, little or no attention has been paid to genetic aspects in planning such projects (cf. Nievergeld, 1966; Ellenberg, 1976; Price, 1984; IUCN, 1985).
5. Conclusions The two introduced herds in Bieszczady are of very different origin. The one in Stuposiany represents the Lowland–Caucasian line, while the second in Koman´cza is genetically hybrid in origin because more ancestors were of pure Lowland subspecies. In the Stuposiany region genes of two founders (Nos. 147 and 46) are not represented. In Koman´cza there is a lack of genes from only one founder (No. 46) but representation of nine founders is at a very low level. All estimated population parameters show very low genetic variability in Bieszczady herds, especially in Koman´cza region. Therefore the enrichment of gene pool is very important there. Reintroduction, with the use of animals from captive herds in Europe, should take place as soon as possible.
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A genetic background for reintroduction program of the European bison (Bison bonasus) in the Carpathians Wanda Olecha, Kajetan Perzanowskib,* a Warsaw Agricultural University, Department of Animal Genetics, 02-786 Warsaw, Poland International Centre for Ecology, Polish Academy of Sciences, 38-700 Ustrzyki Dolne, Poland
b
Received 20 September 2001; received in revised form 12 March 2002; accepted 13 March 2002
Abstract The European bison, extirpated from the Carpathian Mountains over 200 years ago, was reintroduced to the Bieszczady Mountains in the 1960/1970s in two small, isolated herds, and is now threatened by high inbreeding and low genetic variability. A new program of re-establishing viable populations in the Carpathians is based on the genetic analysis of formerly released animals, using the European Bison Pedigree Book. Calculating founder contributions, founder genome survival, founder genome equivalent, inbreeding coefficient and mean kinship allows the identification of under-represented or missing founders. Since genetic variability is much higher among bison in captivity and, in Poland, the Lowland–Caucasian line is represented only in those free-ranging herds, the reintroduction will be based on animals from foreign breeding centres. Bison will be released into existing herds, and planned new introduction sites, to facilitate natural gene exchange in the future. The same approach will be recommended for planned introductions in the Slovakian and Romanian Carpathians. # 2002 Elsevier Science Ltd. All rights reserved. Keywords: European bison; Carpathians; Bieszczady; Genetics; Reintroduction
1. Introduction The European bison is among the few species known to be experiencing an extreme bottleneck (Erlich and Erlich, 1981). In the early twentieth century, only 54 individuals survived in the whole world population (Pucek, 1991). Genetic variation was very low because all these animals were descended from only 12 founders. During the subsequent recovery program, meticulous records (European Bison Pedigree Book) have been kept and updated for all animals in captivity, which allows precise tracking of the origin of the majority of currently living bison. At present, the species is separated into two genetic lines: a Lowland (or Bialowieza) line that is pure lowland subspecies (Bison bonasus bonasus) and a second Lowland–Caucasian line that is a mixture of two subspecies. The gene pool of the former contains genes from only seven founders: males Nos. 45, 87, 15 and 147 and females Nos. 42, 89 and 16. The Lowland– Caucasian line was derived from 12 founders, i.e. five * Corresponding author. E-mail address: [email protected] (K. Perzanowski).
more than the Lowland line. Among those additional five founders were male No. 100 ‘‘Kaukasus’’, originating from subspecies caucasicus and females Nos. 35, 46, 95 and 96 (see Slatis, 1960). According to the breeding strategy operated Poland and other European countries, those two lines should be maintained separately, especially in free-ranging herds. Cross mating between animals from these two lines should be prevented to save the genetic structure and originality in both groups. The present herd of bison in the Bieszczady Mountains are Lowland–Caucasian animals, and represent the only herd of this line in Poland (Pucek, 1984; Olech, 1999). At present, there are only a few free-ranging herds of bison in the Carpathians, originating from introductions during the 1960s and 1970s in Poland and Ukraine. None of these has reached the numbers that assure demographic and genetic stability. In many cases, man-made barriers such as the impenetrable state border, major highways and railroads separate adjacent herds. Under the project launched by WWF-Europe, aiming to reestablish the bison over its former natural range in the Carpathians, further reintroductions are planned to create connectivity between existing bison
0006-3207/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S0006-3207(02)00108-8
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ranges. This should ultimately allow natural gene exchange among the herds (Pererva et al., 1989; Perzanowski, 2000; Perzanowski and Kozak, 2000; Fig. 1). The initial introductions were undertaken without regard for the genetic composition of the herd. Therefore, the baseline for the present program is a genetic analysis of those herds presently living in the Carpathians, using Pedigree Book data to identify their genetic structure. Through the introduction of animals carefully chosen from captive herds, the composition of the gene pools should be improved through the equalisation of the contribution of all founders. This should reduce the present, very high, levels of inbreeding, improving the chances of establishing free ranging and self-sustaining populations. However, some doubts can be raised about the future of such highly inbred species; the case of the Chillingham cattle, a semi-wild breed remaining in isolation for over 300 years, indicates considerable potential among Bovidae for surviving even severe population bottlenecks (Hall, 1989; Visscher et al., 2001).
2. Methods 2.1. History The history of the European bison in Bieszczady (extirpated over 200 years ago) started again in 1963. Then, following the concept of spatially separating pure lowland animals from the descendants of mixed Lowland–Caucasian line, a decision was made to create a free-ranging bison population of the Lowland– Caucasian line in the Bieszczady (south-east Poland). The first area identified as most suitable comprised two forest districts (Stuposiany and Tarnawa, which no longer exists) in the south-eastern corner of Bieszczady, close to the state border with Ukraine. The area extended over ca. 20,000 ha, situated between 400 and 1300 m above sea level, with only a few human settlements. That habitat comprised mixed beech and fir (Fagus silvatica, Abies alba) forest, with many clearings as well as alpine meadow, :providing an excellent summer pasture for large grazers (Z abin´ski, 1968; Jaron´ski and Pepera, 1969).
Fig. 1. Present distribution of European bison herds in Bieszczady Mountains, Poland and the location of two, planned introduction sites. 1, Country border; 2, boundary of Bieszczady National Park; 3, boundary of Biosphere reserve; 4, boundary of forest districts; 5, home ranges of European bison herds; S, the planned re-introduction site in Slovakia; WM, Wola Michowa—the proposed place for reintroduction in Poland (after Perzanowski and Paszkiewicz, 2000, modified).
W. Olech, K. Perzanowski / Biological Conservation 108 (2002) 221–228
Between the autumn of 1963 and summer 1964, 15 bison including seven (three males, four females) adult and eight young (born in 1962, six males, two females) were translocated from breeding centres at Niepoomice and Pszczyna in Poland. In 1966, a further four individuals (two cows and two bulls) were brought from the same source. The animals were placed in an enclosure of 5 ha (60% a timber stand and 40% an forest opening) which was kept closed over winter. Subsequent movements of the herd, and its population dynamics were recorded by local forest rangers. At the beginning of 1967, the herd consisted of 21 animals (13 bulls and eight cows), including three calves born in the Bieszczady Mountains. This population has now spread into neighbouring districts, some crossing the state border with Ukraine. Their total number is estimated at > 100 animals (Fig. 1). In 1974, a group of six animals (four cows, one bull and one calf) was brought from Pszczyna and Cracov Zoo to a 18 ha enclosure, located in the village of Wola Michowa in the Koman˜cza Forest District. Over the next 5 years, the herd was supplemented with more animals, but two individuals from the first group were shot under suspicion of having serious pulmonary problems. In 1980, the whole group of 14 animals (Table 2) was finally released to the wild. For 4 years they stayed around the enclosure, but from 1991 they began to migrate into the neighbouring forest district of Baligro´d, where they have been permanently present since 1993. At present, this population is estimated at ca. 50 animals (Fig. 1). Complete records of population dynamics are available since 1985, at which time the total number of both groups of bison in Bieszczady reached 160. However, the period from the end of the 1980s through to the early 1990s witnessed a distinct decline to about 100 individuals. The most likely reason is migration across the Polish–Ukrainian border. By 1999, numbers in Bieszczady had again reached 160 animals. The group dwelling in Baligro´d district stays most of the time as one herd. The first herd (in Stuposiany district) however has fragmented into several smaller groups, in most cases migrating north, even as far as 50 km to the Brzegi Dolne district. At present bison are recorded there in three districts: Stuposiany, Lutowiska, Brzegi Dolne, and during summer within Bieszczady National Park. To date there is no evidence for any contact between bison originating from the Stuposiany and Koman´cza herds (Perzanowski and Paszkiewicz, 2000). The material for the present analysis was full pedigree (down to the founders) of all animals released in Bieszczady, comprising 19 individuals (11 bulls, eight cows) in Stuposiany region and 14 (six bulls, eight cows) in Koman´cza. The pedigrees of the ancestors of the Bieszczady herd were taken from European Bison Pedigree Book (issues 1924–1980).
223
2.2. Genetic analysis The inbreeding coefficient and mean kinship within the group were calculated for each released animal in order to present the homogeneity of ancestors and show the relationship of each animal to the group. Subsequently, the founder contribution (in genomes) of every released animal was evaluated to assess the genetic structure of initial herds. All those parameters are widely used for comparisons of the various subsets of the European bison population (Belousova and Kudrjavatsev, 1996; Olech, 1989). Those parameters were computed using our own computer program, based on algorithms developed by Quass (1976). The pedigrees of the ancestors of the Bieszczady herd were also analysed using the gene drop method (Lacy, 1995) to determine the proportion of the genetic variability retained at the time of herd creation. For both introduced groups, the mean genetic retention was also calculated to determine the proportion of founder genes present at the moment of their release. Also, the founder genome equivalent (FGE), which provides information on the genetic variation, was computed. FGE can be explained as the number of equally contributing founders that would be required to obtain the level of genetic diversity that was observed in the group (Lacy, 1986). These parameters were calculated for both parts of the Bieszczady population, and compared with their relevant values in the contemporary captive population of Lowland–Caucasian line.
3. Results The values of the founder contribution to all released animals are given in Tables 1 and 2. Two founders (Nos. 147 and 46) are not represented in Stuposiany region at all. Five females in Stuposiany did not have genes from founder No. 35. In Koman´cza, only one founder (No. 46) was not represented but many others contributed an average of < 1%. Additionally, since five females (of eight) and three males in Koman´cza group came from the Pszczyna line, they only had genes from that pair of founders (Nos. 45 and 42). Only one male released in Koman´cza originated from the Lowland–Caucasian line; however, because the other five males belonged to Lowland subspecies, some hopefully had genes from founder No. 147. Fig. 2 gives a comparison of the founders’ contribution in both herds with the mean values for all contemporaries in a sample of captive Lowland–Caucasian line. In Stuposiany, the contribution of only two founders (Nos. 45 and 42) is over-represented, being higher than the average for contemporary animals. The contribution of the other founders is conversely smaller than the average for animals in captivity. The situation
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Table 1 The founder contribution [%] of 19 animals that gave origin to the Stuposiany herd EBPB No.
Sex
Founder numbers 45
42
89
87
16
15
28.12 37.50 12.50 12.50 12.50 32.81 32.81 32.81
28.12 28.12 12.50 12.50 12.50 23.44 23.44 23.44
12.50 7.81 26.56 26.56 26.56 10.16 10.16 10.16
12.50 7.81 14.06 14.06 14.06 10.16 10.16 10.16
4.69 4.69 5.47 5.47 5.47 5.86 5.86 5.86
4.69 4.69 5.47 5.47 5.47 5.86 5.86 5.86
25.195
20.508
16.309
11.621
5.420
5.420
9.37 18.75 32.81 12.50 12.50 32.81 12.50 35.94 14.06 12.50 23.44
9.37 18.75 23.44 12.50 12.50 23.44 12.50 26.56 14.06 12.50 23.44
26.56 17.19 10.16 25.78 25.00 10.16 26.56 7.81 25.00 26.56 18.75
14.06 17.19 10.15 13.28 12.50 10.16 14.06 7.81 12.50 14.06 12.50
7.03 7.03 5.86 5.86 6.25 5.86 5.47 5.47 5.47 5.47 3.91
7.03 7.03 5.86 5.86 6.25 5.86 5.47 5.47 5.47 5.47 3.91
Mean
19.745
17.188
19.958
12.571
5.788
5.788
0
5.664
1.847
0
3.818
7.635
Overall mean
22.470
18.848
18.133
12.096
5.604
5.604
0
5.066
1.510
0
3.557
7.114
973 1141 1300 1386 1466 1467 1566 1574
F F F F F F F F
Mean 1128 1287 1378 1453 1456 1458 1462 1468 1471 1563 1567
M M M M M M M M M M M
147
100 2.34 2.34 7.42 7.42 7.42 2.93 2.93 2.93
0
35
46
3.12 3.12 3.12
4.468
1.172
8.20 3.52 2.93 7.62 7.81 2.93 7.42 2.73 7.42 7.42 4.30
3.12
0
95 2.34 2.34 4.30 4.30 4.30 2.93 2.93 2.93
4.69 4.69 8.59 8.59 8.59 5.86 5.86 5.86
3.296
6.592
5.08 3.52 2.93 4.49 4.69 2.93 4.30 2.73 4.30 4.30 2.73
3.12 3.12 3.12 3.12 3.12 1.56
96
10.16 7.03 5.86 8.98 9.37 5.86 8.59 5.47 8.59 8.59 5.47
EBPB, European Bison Pedigree Book; F, Female; M, Male.
in Koman´cza is worse because genes from two founders (Nos. 42 and 45) over dominate the gene pool. The inbreeding coefficient (the animals’ own value of homogeneity) and the mean kinship (the average similarity to the herd) are presented in Tables 3 and 4. Mean kinship is especially useful in selecting the most valuable animals from a genetic point of view (e.g. male No. 1468 was the most unique in the group at Stuposiany because his mean kinship value is the smallest). The average inbreeding coefficient for the Stuposiany herd was 13.7%, i.e. lower than in Koman´cza (37.6%) where eight animals are descendants from only one pair of founders. In Stuposiany, eight founder animals had coefficients < 10%, and three > 20%, but in Koman´cza only two individuals were below 20%. The average mean kinship in the Stuposiany herd was 24.4% and in Koman´cza was distinctly higher (33.0%), confirming the inbreeding data in showing that the relationships within Koman´cza are much closer than at Stuposiany. The mean kinship among animals from Pszczyna line (with names starting with letters ‘‘PL’’) is very high, so the genetic value of those individuals to the herd is low (Table 4). Table 5 shows that the present captive population has a higher genetic variability than either of the two free-ranging herds of Bieszczady (Stuposiany and
Koman´cza), including the mean retention of founder genes, and the value of inbreeding coefficient.
4. Discussion At the time of first two releases into Bieszczady, no attention was paid to genetic aspects of the new populations. Consequently, we have assumed that the average value of founder contributions to the released males and females reflects the structure of the parent herd at the time. It can be disputed whether the significance of every animal included in the average should be the same, though because of lack of evidence on mating patterns after release, all males and females were equally taken into account. It might be expected that the social domination of some males will lead certain founders to be even more over-represented in contemporary populations, hence the actual level of genetic diversity within the wild would be lower than theoretically calculated. That however can only be determined using modern techniques like DNA analysis. In the case of European bison, where only 12 animals founded the present population, the lack (or serious under-representation) of some founders may lead to a critical level of inbreeding. In
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W. Olech, K. Perzanowski / Biological Conservation 108 (2002) 221–228 Table 2 The founder contribution [%] of 14 animals that gave origin to the Koman´cza herd EBPB No.
2127 3293 3530 3531 3533 3981 4274 4275
Sex
F F F F F F F F
Founder numbers 45
42
69.53 69.14 21.48 14.06 19.92 70.70 69.53 69.53
30.47 30.86 21.48 14.06 17.58 29.30 30.47 30.47 7.446
89
87
16
15
17.19 23.44 18.94
14.06 14.06 12.69
5.66 6.25 6.15
5.66 6.25 6.15
2.258
2.258
0
2.008
1.56 10.55
1.56 7.42
6.25 3.32
3.12 3.32
3.12
1.56
1.56
3.12
1.56
1.56
100
35
4.00 6.64 5.42
0.78 2.34 1.56
0.586
0
46
1.422
95
96
3.22 4.30 3.86
6.44 8.59 7.71
Mean
50.488
25.586
3063 3528 3538 3768 3978 3980
M M M M M M
52.15 42.77 69.14 69.92 60.16 70.31
Mean
60.742
29.362
2.279
1.758
2.116
1.335
0.781
0.720
0.130
0
0.342
0.684
Overall mean
55.615
27.474
4.863
3.431
2.187
1.797
0.391
1.240
0.358
0
0.882
1.764
32.23 22.85 30.86 30.08 30.47 29.69
5.103
147
4.10
2.844
2.05
EBPB, European Bison Pedigree Book; F, Female; M, Male.
Table 3 Inbreeding and mean kinship coefficients for animals released at Stuposiany Forest District EBPB No
Name
Sex
Father No
Mother No
Inbreeding coefficient
Mean Kinship
973 1141 1300 1386 1466 1467 1566 1574 1128 1287 1378 1453 1456 1458 1462 1468 1471 1563 1567
PULESNA PUJANKA PUCZAJA PUCELA PUCNOTA PUNINA PUMAJKA PUNICA PULON PULPIT PURLAN PUSTAN PURUS PURI PUSZCZAR PUREK PUJAR PUSZCZOT PUCZAJ
F F F F F F F F M M M M M M M M M M M
761 949 879 879 879 949 949 949 879 761 949 879 879 949 879 949 879 879 1207
724 973 790 1030 1030 1021 1021 941 823 979 979 903 795 941 790 725 973 790 1300
0.3086 0.2036 0.0769 0.0769 0.0769 0.1538 0.1538 0.1538 0.1008 0.2441 0.1538 0.0741 0.0791 0.1538 0.0769 0.1875 0.0691 0.0769 0.1821
0.2797 0.2595 0.2504 0.2399 0.2399 0.2450 0.2450 0.2450 0.2295 0.2498 0.2422 0.2303 0.2253 0.2450 0.2453 0.2118 0.2535 0.2453 0.2608
0.1370
0.2444
Average value EBPB, European Bison Pedigree Book.
fact, there was some speculation connecting the relatively low reproductive success and appearance of certain diseases in some free-ranging populations with the very low level of genetic variability (Gill, 1999). The negative influence of inbreeding on the viability of
calves was also reported (Olech, 1987; Belousova and Kudrjavtsev, 1996) Two founders (Nos. 45 and 42) are over represented in the gene pool, but the average value for animals in captivity is < 37% for both founders together. In some
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Fig. 2. The comparison of founder contribution in Stuposiany and Koman´cza herds with its average value for contemporary world captive population of Lowland–Caucasian line. Numbers of founders, according to European Bison Pedigree Book. VFC—values of founder contribution.
Table 4 Inbreeding and mean kinship coefficients for animals released at Koman´cza Forest District EBPB No.
Name
Sex
Father No.
Mother No.
Inbreeding coefficient
Mean kinship
2127 3293 3530 3531 3533 3981 4274 4275 3063 3528 3538 3768 3978 3980
PLIZA PLERKA PUGA PUHA II PUNA PLEREZA PLISHA PLANETOIDA POLCER PULAS PLOTKIR PLENNY POROS PLUSKAR
F F F F F F F F M M M M M M
1561 2267 2263 2263 2263 1866 2547 2547 1987 1997 2267 1561 2382 1866
1469 1357 2257 1205 2393 1994 2127 2678 2265 2542 1367 1994 2399 1357
0.4985 0.5090 0.2476 0.2276 0.1885 0.5170 0.6006 0.5557 0.2544 0.1016 0.5374 0.5232 0.3684 0.5156
0.4250 0.4151 0.2076 0.1862 0.2049 0.4172 0.4309 0.4231 0.3300 0.3018 0.4171 0.4181 0.3672 0.4031
0.3763
0.3298
Average value EBPB, European Bison Pedigree Book.
free herds of the Lowland–Caucasian line in Russia, the contribution of these founders is close to 65% (Belousova and Kudrjavatsev, 1996), but in Koman´cza region it is higher that 80%. All other founders make a smaller contribution, so it is interesting that in Stuposiany, the contribution of two founders (Nos. 87 and 89) is higher than average. In the best theoretical scenario, all founders should contribute equally (Ballou and Lacy, 1995). Further introductions can change the structure of gene pool towards this ‘‘best scenario’’, and the aim of
genetic reintroduction from captivity is one of most important reasons for this captive breeding (Kleiman, 1996). At the time that the Koman´cza and Stuposiany herds were established, they contained only 65.9 and 75.6% of the original genetic variation. This is not a bad scenario, however, for the captive population remains an excellent source for further reintroductions. The European bison presently in captivity have retained much more of their original genetic diversity than any of the bison
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Table 5 A comparison of genetic characteristics within Stuposiany and Koman´cza European bison herds compared with values for animals from Lowland– Caucasian line living at present in captivity
Number of founders Founder genome equivalent Fraction of gene diversity retained Mean inbreeding value
Stuposiany herd
Koman´cza herd
Present captive population
10 2.049 0.756 0.137
11 1.465 0.659 0.376
12 3.060 0.837 0.212
groups released into Bieszczady 20 years ago. Thus, further introductions of animals, selected from breeding centres, remains the simplest way of enhancing genetic variability and enriching the gene pool of the free ranging population (Mills and Allendorf, 1996). On the basis of pedigree analysis (European Bison Pedigree Book), it is possible to choose animals from the captive stock with above average contributions from absent or under-represented founders, and use these to enrich the gene pool of the wild herds. That opportunity can be especially important in planning large scale programs such as the restitution of the Carpathian population of European bison, based around the few, isolated free-ranging animals whose ancestors were introduced to Poland, Ukraine, Romania and Slovakia some 30 years ago. In this program, the enrichment of genetic structure of free-ranging herds will be one of the main aims. Hopefully, such an approach will become a standard in animal introduction programmes because, so far, little or no attention has been paid to genetic aspects in planning such projects (cf. Nievergeld, 1966; Ellenberg, 1976; Price, 1984; IUCN, 1985).
5. Conclusions The two introduced herds in Bieszczady are of very different origin. The one in Stuposiany represents the Lowland–Caucasian line, while the second in Koman´cza is genetically hybrid in origin because more ancestors were of pure Lowland subspecies. In the Stuposiany region genes of two founders (Nos. 147 and 46) are not represented. In Koman´cza there is a lack of genes from only one founder (No. 46) but representation of nine founders is at a very low level. All estimated population parameters show very low genetic variability in Bieszczady herds, especially in Koman´cza region. Therefore the enrichment of gene pool is very important there. Reintroduction, with the use of animals from captive herds in Europe, should take place as soon as possible.
Acknowledgements We would like to thank the Large Herbivore Initiative and WWF-Europe for the support necessary to collect
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