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Acta Theriologica 53 (3): 193–216, 2008. PL ISSN 0001–7051

Morphometric variation of the skull during postnatal development in the Lowland European bison Bison bonasus bonasus Ma³gorzata KRASIÑSKA, Elwira SZUMA, Franciszek KOBRYÑCZUK and Tomasz SZARA

Krasiñska M., Szuma E., Kobryñczuk F. and Szara T. 2008. Morphometric variation of the skull during postnatal development in the Lowland European bison Bison bonasus bonasus. Acta Theriologica 53: 193–216. We studied the variation of linear measurements and skull capacity in Lowland European bison Bison bonasus bonasus (Linnaeus, 1758) during postnatal development, and the dependencies of the parameters in relation to sex, age, and body mass of the animals. Material consisted of 599 bison skulls (310 males and 289 females), within the age range of 1 month to 21 years (males) and to 27 years (females). In the group of calves to 1 year old, no sex connected differences in skull measurements were observed, whereas the skull capacity in older calves was significantly larger (0.01 > p > 0.001) in males than in females. From the third year of life, most skull measurements display characteristics of sexual dimorphism. Skull development in both sexes is most intensive during the first three years of life, and slows from the age of 5. In older individuals of both sexes (³ 6 years), orbital breadth continues growing and, in females, breadth of splanchnocranium continues increasing. Growth in a bison’s skull capacity is most intensive up to the third year of life and slows from the age of 5. During postnatal development, a bison skull grows proportionally except the neurocranium, which grows slightly slower in comparison with basal length and its development finishes earlier than that of splanchnocranium. In ontogenesis, a bison skull grows much slower compared to body mass. In relation to body mass, skull capacity and the height of neurocranium grow most slowly while orbital breadth grows most intensively. The results obtained were compared with data on skull sizes of bison born in 1930–1950 and bred in captivity and with skulls of the American bison Bison bison. Inbreeding is probably responsible for some types of phenotypic abnormalities in the skull which appear in modern European bison. Mammal Research Institute, Polish Academy of Sciences, 17-230 Bia³owie¿a, Poland, email: [email protected] (MK, ES); Department of Morphological Sciences, Faculty of Veterinary Medicine, Warsaw University of Life Sciences, Nowoursynowska str. 159, 02-776 Warsaw, Poland (FK, TS)

Key words: Bison bonasus bonasus, morphometric variation, postnatal development, skull

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194

M. Krasiñska et al.

Introduction The genus Bison H. Smith, 1827 is today represented by two species – the American bison Bison bison (L.), living in North America, and the European bison Bison bonasus (L.), living in Europe. The species Bison bison is divided into two subspecies – the prairie (plains) bison Bison bison bison (L.) and the wood bison Bison bison athabascae Rhoads 1898. At the turn of the 19th and 20th centuries, the species Bison bonasus also had two subspecies – the Lowland (Bia³owie¿a) European bison, Bison bonasus bonasus (L.), living in the Bia³owie¿a Forest, and the Caucasian European bison, Bison bonasus caucasicus Turkin et Satunin, 1904, present in Caucasus mountains (Corbet 1978). There were 727 European bison inhabiting the Bia³owie¿a Forest in the first years of the 20 Century. The population suddenly collapsed as a result of poaching during and after the First World War, and the last free-living individuals became extinct in the Bia³owie¿a Forest in 1919. The Caucasian bison survived in the Caucasus Mountains a little longer; becoming extinct in 1927 (Bashkirov 1940). In the beginning of the 20th Century, European bison survived only in captivity (54 Lowland European bison and one male Caucasian bison (named KAUKASUS). Thanks to those individuals, the restitution of the species was possible. Two breed lines are distinguished in modern European bison: the Pure Lowland European bison created the Lowland line, whereas descendants of Lowland bison and one bull KAUKASUS belong to LowlandCaucasian line form the second line and are bred separately (Olech 2006, Krasiñska and Krasiñski 2007). All contemporary living European bison are the descendants of 12 founders (Slatis 1960), while the Lowland European bison stems from only 7 founders (Olech 1987, 2006, Krasiñska and Krasiñski 2007). The consequence of so few founders is inbreeding. The world population of European bison is highly inbred, the average inbreeding coefficient for fully pedigreed actual population is equal to 44% for the Lowland line

and 26% for the Lowland-Caucasian line (Olech 2003, 2006). Inbreeding has been found to negatively influence the viability of young animals (Slatis 1960, Olech 1987, 2003, Belousova 1999). Some authors have suggested that inbreeding influences the susceptibility of the European bison to certain diseases and congenital abnormalities (Gill 1999, 2002, 2006, Matuszewska and Sysa 2001, 2002, Matuszewska et al. 2004, Olech 2006, Sysa and Matuszewska 2006, Krasiñska and Krasiñski 2007). Kobryñczuk (1985) stated that inbreeding has a depressive effect on growth of the skeleton of inbred European bison. Similarly McDonald (1981) suggested that inbreeding is probably responsible for several types of phenotypic abnormalities which appear in bison including abnormalities in the skull and limbs. Some inbred populations of genus Bison were probably more susceptible to pathologies than less inbred populations (McDonald 1981). An extensive collection of skulls of modern Lowland bison from the population in the Bia³owie¿a Forest (at present over 800 specimens), present in the scientific collection of the Mammal Research Institute PAS in Bia³owie¿a, enabled the creation of morphological documentation of this relict species. The European bison suffered a sudden bottleneck at the turn of the 19th and 20th Century. The aim of our research is, firstly, to study whether the high inbreeding of modern Lowland European bison caused phenotypic changes in skulls of contemporary living bison. Secondly, we aimed to make use of such extensive material to examine the variability of linear skull sizes and skull capacity during postnatal development in Lowland bison. With the data on body mass of a considerable number of bison at our disposal, it was possible to analyse the relation between linear measurements and skull capacity, and the body mass of these animals. Moreover, using the Szmalhauzen-Brodi formula (Nikitiuk 1972), we calculated the growth rate of skull capacity and body mass in bison ontogenesis, and the mutual relations of both these parameters. Apart from an assessment of the rate of development of morphometric skull characteristics and the morphological distance

Skull morphometry in the Lowland European bison

between bison age groups, we also attempted to estimate the sexual dimorphism variability in particular morphometric skull characteristics during postnatal development. An estimation of sexual dimorphism in bison skulls using method a discriminatory analysis and the morphological skull variability (polarisation, dichotomy) in adult individuals, and based on the same data as the present work, has been the subject of independent publications (Kobryñczuk et al. 2008a, b). History of morphometric studies of European bison skulls

Earlier researchers, namely Koch (1927) and Juœko (1953), studying the morphology of bison skulls based their work on rather scant material. A larger number of skulls (42) of both lines of bison were at the disposal of Empel (1962), who described their anatomy by recording and analysing their dimensions, proportions and indicators. The skulls came from European bison from captive breeding centres, born at the beginning of restitution (1939–1950). The subject of another study was an analysis of correlation of their measurements (Kobryñczuk and Roskosz 1980). These authors used the Szmalhauzen-Brodi formula (Nikitiuk 1972) to calculate the growth rate of skull parameters during postnatal development in the both lines of the European bison. Roskosz and Kobryñczuk (1983) established that in estimating skull capacity, it is best to use parameters like basal length (BP) and length of neurocranium (BSt). Kobryñczuk and Roskosz (1984) examined the relation between skull capacity and the capacity of the vertebral canal. According to Kobryñczuk (1985), the influence of inbreeding on skull shape and size in Lowland and Lowland-Caucasian lines is perceptible particularly in the latter, where it leads to a lengthening of the splanchnocranium. Roskosz and Kobryñczuk (1986) examined the correlations between the basal length and length of the neurocranium on the one hand, and measurements of length of subsequent parts of the vertebral column: cervical, thoracic, lumbar

195

and sacral and its total length, on the other. Kobryñczuk et al. 1990 compared linear measurements (vertical and transversal) and the area of the foramen magnum in 103 skulls of the Lowland line, the Lowland-Caucasian line and the Caucasian bison with the height of the nuchal plane. None of the works mentioned above was based on material extensive enough to enable the analysis of morphometric variation of skulls of Lowland European bison during postnatal development. Moreover, it should be emphasized that earlier studies on skull morphometry were done by combining material from both breeding lines as an average for the species Bison bonasus. Besides the research on the linear measurements of the skull, Kobryñ and Cegie³ka (1994) described the sizes and shapes of bison cornual processes, and Krasiñska and Krasiñski (2002, 2007) variability of horn length and shape depending on sex and age. While Makowiecka (1994) differentiated the bison skulls of three breeding lines — Bia³owie¿a, Pszczyna and Lowland-Caucasian — based on the nonmetric characteristics of the skull. Papers concerning the morphometry of skull of the extinct subspecies Bison bonasus caucasicus (Turkin et Satunin, 1904) are not numerous. The authors of these papers claim that skulls of both subspecies of the European bison differ significantly in some skull characteristics (Bohlken 1967, Flerov 1965, 1979, Kobryñczuk 1985, Nemtsev et al. 2003). Data on the skull shape, in hybrids of the European and American bison (the so called ‘mountain bison’) presently living in the Caucasian Biosphere Reserve, and in the Lowland bison coming from the free ranging population in the Belarusian part of the Bia³owie¿a Forest can be found in the monograph ‘Wisent in Caucasia’ (Nemtsev et al. 2003). There are numerous papers on the systematics and evolution of the genus Bison based on the analyses of skull measurements. The authors of these papers discuss the differences in skull morphology between modern American and European bison (Flerov 1965, 1979, Bohlken 1967, Shackleton 1975, McDonald 1981, Zyll de Jong 1986).


196

Material and methods The material used in this research consisted of 599 bison skulls (310 male and 289 female) aged between 1 month and 21 years (males) and 27 years (females) housed in the museum of the Polish Academy of Science’s Mammal Research Institute in Bialowie¿a. These skulls came from 67 individuals from the enclosed Breeding Centre in Bia³owie¿a, along with 532 skulls from the free ranging bison population in the Polish part of the Bia³owie¿a Forest. These belonged to animals that died or were culled during the years 1967–2006. We divided the material into 7 age classes, sub-divided into males and females. Class I covered bison aged 1 to 12 months; II – from 1.5 to 2.5 years of age; III – from 2.5 to 3 years; IV – from 3.5 years to 4 years; V – about 5 years; VI – about 6 years, and group VII – individuals 7–22 years old (males) and 7–27 (females). For some of our statistical calculations, we combined classes V–VII, qualifying them as adult individuals. In order to establish the exact age to which skull growth is most intensive, and to make comparisons with the data from earlier material, we additionally divided the material into two age classes, separately for each sex: (1) individuals 1 month to 5 years old, and (2) bison ³ 6 years old. The age of the European bison from the free-ranging population of the Bia³owie¿a Forest was established by Z. A. Krasiñski according to sequence of tooth eruption, degree of tooth wear (Wêgrzyn and Serwatka 1984), body size, and horn size and shape. The age of those individuals from enclosed breeding centre was known. For comparative purposes, we used the skull measurements of the Lowland bison born at the beginning of the restoration project, as established by Empel (1962), and we calculated the mean values of the measurements. Addition-

ally, using the same material, we carried out measurements that were missing in the above-mentioned studies. The skulls came from the collection of the Department of Anatomy in Warsaw Agricultural University’s Veterinary Medicine Faculty. In our research, we explored only those skulls on which it was possible to take most of the measurements. The anatomical terms we used are in accordance with Nomina Anatomica Veterinaria (2005). Using the Duerst osteometric method (1926) and the indications included in the studies by Empel (1962) and Kobryñczuk (1985), we took seven linear measurements on each skull (Fig. 1): (1) basal length, Basion-Prosthion (BP) (2) length of splanchnocranium, Staphylion-Prosthion (StP) (3) length of neurocranium, Basion-Staphylion (BSt) (4) orbital breadth, Ectorbitale-Ectorbitale (EctEct) (5) breadth of splanchnocranium, Supramolare-Supramolare (SmSm) (6) height of splanchnocranium, Staphylion-Nasion (StN) (7) height of neurocranium, Sphenobasion-Bregma (SphBr). We additionally measured skull capacity, cavum cranii (SCap) filling each with dry pea grains of constant humidity. Estimation of the capacity was possible in 543 skulls (279 males and 264 females). Due to the considerable body and skull size differences between male and female bison (Krasiñska and Krasiñski 2002), sexes were kept separate for statistical analysis. The dimensions of a skull as a geometrical form grow in three directions and for this reason, we considered the parameters of length, width and height. In the same order of progression, we discussed the variability of these measurements during postnatal development. By means of the Scheffé test, we calculated the statistical significance of the differences between age groups in the case of each of the

B

Br

Ect

Ect

Sp Sph S ph ph

N St Sm

Sm

P Fig. 1. Measurement points on skull of the European bison Bison bonasus bonasus. Source: Kobryñczuk et al. 2008a. Measured points: B – Basion, Br – Bregma, Ect – Ectorbitale, N – nasion, P – Prosthion, Sm – Supramolare, St – Staphylion.


examined skull characteristics. The distance between age groups, in respect of morphometric skull variability, was estimated by means of multidimensional scaling (MDS) analysis. The MDS analysis was based on the Euclidean distances between age groups. The Euclidean distances were calculated on the basis of all seven metric characteristics, and skull capacity. In 362 cases (161 males and 201 females), the body mass of the bison was known. In relation to bison body mass as well as BP of a skull, an allometric analysis of size parameters of bison skull was carried out. Before a regression analysis, all metric variables and body mass were logarithmically transformed. The regression analysis of skull parameters in relation to body mass and of skull measurements in relation to BP length was carried out for males and females separately. Relationships among body mass, sex and metric characteristics were assessed using ANCOVA. Statistical significance between regression lines in both sexes was estimated using GLM analysis – the equal inclinations model. We plotted the dependence between the skull size and age of the animals on dispersion graphs, using the procedure of smoothing negatively (inversely) exponentially weighted (values). We calculated the coefficient of the Person correlation (r), for males and females, between their age and body mass, and their linear skull measurements. In addition, we investigated the dependence between skull capacity and skull linear measurements, and the age of the animals. The number of cases where both skull capacity and body mass of the animals were known was 336 (151 males and 185 females). The data on skull capacity in individuals whose body mass was known was analysed in the above mentioned age classes, estimating the relevance of the differences between them, as well as between males and females of the same age. We also defined the relation be3 tween size of skull cavity (cm ) and body mass (kg). The difference in skull cavity and body mass growth rate between the various age classes (S) was analysed separately for males and females using the Szmalhauzen-Brodi formula (Nikitiuk 1972): S=

logV1 - logV0 t ´ 0.4343

where V1 – the mean parameter value in the adjacent, older class, V0 – the mean parameter value in the adjacent, younger class, t – the difference between the mean of the age of the adjoining classes, 0.4343 – the scaling coefficient. The index of sexual dimorphism was calculated as a quotient of the mean measure of certain characters in males by the respective mean in females (Mm / Mf). Due to the strong correlation of all the linear measurements with age, these cannot be the only basis for sexual discrimination. The coefficients – the quotients of pairs of measurements that reflect proportions within the skull – are not burdened by such a dependency. Additionally, discriminant analysis makes it possible to estimate the co-agency of particular coefficients in sexual differentiation. For this reason, the quotients of linear measurements were applied for sexual discrimination attempts in particular age classes. Sexual dimorphism in particular age classes was established by means of a stepped discriminant analysis. The discriminatory power of the obtained functions was evalu-

197

ated on the basis of Lambda Wilks value, which keeps within the range of 0–1. Statistical analyses were carried out by means of Statistica.PL version 6.0, 1997.

Results Morphometry of linear skull measurements in males Length

The basal length (BP) in calves of age to 1 year amounts to an average 300 mm, while in three year old individuals this figure is about 40% higher (Table 1). Growth of BP length is most intensive in the period between birth and the age of 3 years. In 4-year-old males, this length is still considerably smaller than in the oldest group but it does not differ significantly from BP length in 5-year-old individuals (Table 2). This parameter is significantly correlated with age (n = 303, r = 0.73, p < 0.01, Fig. 2a.1) and increases proportionally to body mass (n = 159, r = 0.91, p < 0.01, Fig. 3a). During postnatal development, the measurements for length of splanchnocranium (StP) and length of neurocranium (BSt) behave similarly to BP lengths (Table 1) and present similar dependencies in relation to age (Figs 2b.1, 2c.1) and body mass (Figs 3b, 3c). Breadth

Orbital breadth (EctEct) in calves amounts to an average 175 mm, while in 4-year-old males it increases by an average 67%. The breadth of EctEct grows most intensively up to the age of 4 (Fig. 2d.1). The broadest skulls occur in individuals 7–21 years old (Table 1). The breadth of EctEct in the oldest group reaches 322 mm but does not differ significantly from that for 5–6 year old individuals (Table 2). This measurement is significantly correlated with age (n = 303, r = 0.77, p < 0.01, Fig. 2d.1) and body mass (n = 161, r = 0.93, p < 0.01, Fig. 3d). The breadth of the splanchnocranium (SmSm) in calves amounts to an average 111 mm and in 5-year-old males is 59% broader. Bulls 7–21 years old have the broadest faces, though not significantly broader than in 6 year old males


198

Table 1. Measurements (in mm) of skulls of European bison males and females and skull capacity (in ml). For determination of age classes, measurement abbreviations see Material and methods. t-tests were used for comparison measurements of males and females in each age class. p – statistical significance: *** – p < 0.001, ** – 0.01 > p > 0.001, * – 0.05 > p > 0.01, ns – p > 0.05, M – males, F – females Age class

Sex

n

Mean

M F M F M F M F M F M F M F

61 75 52 29 19 18 24 15 22 17 19 10 110 125

299.9 300.5 378.6 368.4 420.5 403.2 451.3 435.0 459.5 436.5 473.7 443.0 473.9 448.8

Min

Max

SD

200 227 338 330 390 383 400 420 430 410 460 430 440 410

380 400 460 430 450 430 500 455 500 450 500 470 510 480

32.7 27.3 24.4 21.9 19.8 13.1 21.7 11.2 18.1 11.7 10.1 14.2 12.9 11.8

100 135 200 190 230 237 240 250 270 250 270 260 270 260

240 270 280 270 270 265 300 280 300 280 300 290 310 300

22.2 21.9 16.6 18.5 12.6 8.7 14.4 8.1 9.2 8.3 8.2 8.4 8.1 8.4

p

BP I II III IV V VI VII

ns ns ** * *** *** ***

StP I II III IV V VI VII


61 74 52 29 19 18 24 15 22 17 19 10 109 125

173.2 179.1 226.7 223.2 253.7 249.6 276.3 263.7 281.1 272.4 289.7 276.0 290.6 280.4


61 74 52 29 19 18 24 15 22 17 19 10 109 125

125.9 123.3 152.1 149.5 164.5 154.5 175.6 170.7 180.2 164.1 184.5 169.0 186.2 170.0

100 97 130 130 150 140 160 160 150 150 170 160 170 150

160 156 190 170 180 180 200 185 210 180 210 180 210 190

13.0 16.9 11.2 9.7 11.4 12.0 9.7 7.3 13.5 7.1 11.2 8.8 8.9 9.1

61 75 52 29 19 18 24 15 22 17 19 10 113 125

EctEct 175.1 130 169.1 131 227.0 189 213.3 180 261.6 240 240.0 230 291.5 250 262.0 240 305.9 280 264.1 240 317.9 290 269.0 350 321.6 270 276.4 240

240 200 290 270 300 270 330 280 340 280 330 290 360 300

24.1 15.2 23.9 18.3 18.9 12.4 20.6 11.5 15.3 10.6 12.7 12.0 14.4 11.7

ns ns ns ** ** *** ***

BSt I II III IV V VI VII

I II III IV V VI VII


ns ns * ns *** *** ***

ns ** *** *** *** *** ***


199

Table 1 – continued. Age class

Sex

n

Mean

I


61 75 52 29 19 18 24 15 22 17 19 10 113 125

110.9 107.9 136.6 132.7 150.3 144.9 167.5 159.7 175.7 162.3 184.7 164.0 187.1 172.8

Min

Max

SD

90 90 116 120 135 134 150 150 160 150 170 150 160 140

140 134 175 160 160 160 190 180 190 180 200 180 210 190

12.2 10.3 11.0 7.7 7.5 6.9 12.5 7.9 9.9 7.5 8.4 8.4 9.7 8.9

70 80 100 90 130 130 150 140 150 140 160 150 150 140

135 140 160 150 150 140 180 160 180 160 180 160 190 187

13.2 8.5 12.6 11.8 6.3 4.3 9.0 6.5 8.4 5.3 7.4 5.3 7.6 7.8

80 80 100 90 130 130 140 140 140 140 150 140 140 140

140 140 150 150 150 150 160 150 175 150 180 150 180 160

12.3 8.7 10.7 10.6 6.3 5.4 5.3 4.8 9.1 3.3 5.8 4.2 7.5 5.1

210 333 500 470 520 520 600 570 640 570 660 600 600 580

640 600 680 690 700 690 750 680 760 680 800 720 820 750

73.1 50.4 40.1 50.5 54.7 40.7 42.4 36.5 38.4 35.4 42.9 41.4 45.6 40.7

p

SmSm

II III IV V VI VII

ns ns * * *** *** ***

StN I II III IV V VI VII


61 75 52 29 19 18 24 15 22 17 19 10 110 125

99.7 96.9 128.8 122.9 142.6 137.5 157.5 150.0 166.4 151.8 170.0 155.0 172.5 158.4


61 74 52 29 19 18 24 15 22 17 19 10 110 124

100.9 99.3 129.4 125.2 142.6 139.4 152.5 146.3 158.0 148.8 160.0 148.0 161.4 149.0

ns * ** ** *** *** ***

SphBr I II III IV V VI VII

ns ns ns *** *** *** ***

SCap I II III IV V VI VII


46 60 52 27 18 16 24 12 21 17 17 9 101 123

496.1 467.2 595.9 566.3 633.3 592.5 680.4 617.5 692.9 625.9 710.6 648.9 707.1 658.2

** *** * *** *** ** ***


200

Table 2. Differences between mixed-age groups of the European bison males and females in relation to mean skull measurements determined by ANOVA and Scheffe test statistic. ** – p < 0.001, * – 0.001 < p < 0.05, ns – p > 0.05. Age classes of males I

Age classes of females

II

III

IV

V

VI

VII

I II III IV V VI

**

** **

** ** *

** ** ** ns

** ** ** ns ns

** ** ** * ns ns

I II III IV V VI

**

** **

** ** **

** ** ** ns

** ** ** ns ns

** ** ** ** ns ns

I II III IV V VI

**

** **

** ** ns

** ** ns ns

** ** * ns ns

I II III IV V VI

**

** **

** ** **

** ** ** ns

I II III IV V VI

**

** **

** ** **

I II III IV V VI

**

** **

I II III IV V VI

**

I II III IV V VI

**

I

II

III

IV

V

VI

VII

I II III IV V VI

**

** **

** ** **

** ** ** ns

** ** ** ns ns

** ** ** ns ns ns

I II III IV V VI

**

** **

** ** ns

** ** * ns

** ** * ns ns

** ** * * ns ns

** ** * ns ns ns

I II III IV V VI

**

** ns

** ** *

** ** ns ns

** ** * ns ns

** ** * ns ns ns

** ** ** * ns

** ** ** ** ns ns

EctEct I II III IV V VI

**

** **

** ** *

** ** * ns

** ** * ns ns

** ** * * ns ns

** ** ** ns

** ** ** ** ns

** ** ** ** ** ns

SmSm I II III IV V VI

**

** *

** * *

** * * *

** * * ns ns

** * * ns ns ns

** ** *

** ** ** ns

** ** ** * ns

** ** ** ** ns ns

I II III IV V VI

**

** **

** ** *

** ** * ns

** ** * ns ns

** ** * * ns ns

** **

** ** ns

** ** ** ns

** ** ** ns ns

** ** ** * ns ns

I II III IV V VI

**

** **

** ** ns

** ** * ns

** ** ns ns ns

** ** ** ns ns ns

** ns

** ** ns

** ** * ns

** ** * ns ns

** ** ** ns ns ns

I II III IV V VI

**

** ns

** * ns

** ** ns ns

** ** ns ns ns

** ** ** ns ns ns

BP

StP

BSt

StN

Sphr

SCap


(Table 1, 2). The SmSm breadth is significantly correlated with age (n = 303, r = 0.79, p < 0.01, Fig. 2e.1) and body mass (n = 161, r = 0.93, p < 0.01, Fig. 3e). Height

The height of the splanchnocranium (StN) in calves amounts to an average 100 mm and in 4-year-old individuals is 58% greater (Table 1). The StN height increases most distinctly during the first 4 years of life. Seven to 21 year-old males have the highest splanchnocranium, measuring an average 173 mm. In the oldest age class, this size does not differ significantly from the size of StN in 5–6 year old individuals (Table 2). The height of StN is significantly correlated with age (n = 303, r = 0.75, p < 0.01, Fig. 2f.1) and increases proportionally to body mass (n = 161, r = 0.91, p < 0.01, Fig. 3f). The height of the neurocranium (SphBr) in calves averages 101 mm, while in 3-year-old males it is 42% larger (Table 1). The height increases most intensively during the first 3 years of life (Fig. 2g.1). In males at the age of 7–21, it averages 161 mm. The height of SphBr in males from the oldest age class does not differ significantly from that in the classes of 5–6 year-olds (Table 2). As with other measurements, the height of SphBr increases proportionally to age (n = 303, r = 0.71, p < 0.01, Fig. 2g.1) and body mass (n = 159, r = 0.87, p < 0.01, Fig. 3g). Morphometry of linear measurements in skulls of females

201

During postnatal development, the length measurements for the splanchnocranium (StP) and neurocranium (BSt) behave similarly as the basal length (BP) (Table 1, 2) and display similar dependencies to age (Figs 2b.2, 2c.2) and body mass (Figs 3b, c). Breadth

Orbital breadth (EctEct) in calves averages 169 mm, while in 4-year old individuals it increases by 55% and this is significantly larger than the EctEct value in both younger and older age classes (Table 2). The most intensive increase in skull breadth occurs during the first 4 years of life (Fig. 2d.2). Females in the age class 7–27 have the broadest forehead (276 mm). This dimension does not differ significantly from the data on females at the age of 5–6 years (Table 2). The breadth of EctEct is significantly correlated with age (n = 286, r = 0.74, p < 0.01, Fig. 2d.2) and body mass (n = 201, r = 0.94, p < 0.01, Fig. 3d). The breadth of the splanchnocranium (SmSm) in calves averages 108 mm, while in 4-year old females it averages 166 mm (Table 1). The breadth increases most intensively up to the age of 4, and in 4-year-old females differs significantly from all the younger classes, as well as from the oldest (Table 2). The SmSm breadth in the oldest female bison averages 173 mm and does not differ significantly from the mean SmSm in females from the 4 and 6-year old age classes (Table 2). The breadth of SmSm is significantly correlated with age (n = 286, r = 0.77, p < 0.01, Fig. 2e.2) and body mass (n = 201, r = 0.95, p < 0.01, Fig. 3e).

Length

The skull’s basal length (BP) in calves averages 301 mm, while in 3-year old individuals, it increases by 34%. Female skulls at the age of 7–27 attain an average 449 mm and do not differ significantly from skulls of individuals from 4–6 year old classes (Table 1, 2). The length of the female’s skull grows most intensively during the first 3 years of life. This length grows proportionally to age (n = 286, r = 0.72, p < 0.01, Fig. 2a.2) and body mass (n = 201, r = 0.94, p < 0.01, Fig. 3a).

Height

The height of the splanchnocranium (StN) grows most intensively during the first 4 years of life, after which growth is slower (Table 2). In calves it amounts to an average of 97 mm, while in 4-year old females the figure is 150 mm (a 55% increase; Table 1, 2). The mean value of the height under discussion in 4-year-old females does not differ significantly from that in the 5–6 years age class (Table 2). The StN height is significantly correlated with age (n = 286, r = 0.73,


202

550 500

(a.1)

480 440

BP (mm)

BP (mm)

450 400 350 300

r = 0.73, p < 0.001

200

220

0

2

4

6

8

320

(b.1)

r = 0.73, p < 0.001 0

2

4

6

8

10 12 14 16 18 20

BSt (mm)

BSt (mm)

140 120 100

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(b.2)

r = 0.72, p < 0.001 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(c.2)

0

2

4

6

8

160 140 120 100

r = 0.70, p < 0.001

80

10 12 14 16 18 20

320

(d.1)

r = 0.65, p < 0.001 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(d.2)

280

320

EctEct (mm)

EctEct (mm)

r = 0.72, p < 0.001

180

160

280 240 200 r = 0.77, p < 0.001

160 120

300 280 260 240 220 200 180 160 140 120 200

(c.1)

180

360

320

200

10 12 14 16 18 20

200

80

360

240

StP (mm)

StP (mm)

320 300 280 260 240 220 200 180 160 140 120 100 80

400

280

250

150

(a.2)

0

2

4

6

8

10 12 14 16 18 20

Age (in years)

240 200 160 120

r = 0.74, p < 0.001 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

Age (in years)

Fig. 2. Relationships between basion-prosthion length (BP) and age classes in males (a.1) and females (a.2), staphylon-prosthion length (StP) and age classes in males (b.1) and females (b.2), basion-staphylon length (BSt) and age classes in males (c.1) and females (c.2), ectorbitale-ectorbitale width (Ect-Ect) and age classes in males (d.1) and females (d.2),


220

200

(e.1)

180 160 140 120

0

2

4

6

8

StN (mm)

StN (mm)

180

140 120 100 80

r = 0.75, p < 0.001 0

2

4

6

SphBr (mm)

120 100 80

r = 0.71, p < 0.001

60

2

0

Skull capacity (ml)

900 800

4

6

8

10 12 14 16 18 20

(h.1)

700 600 500 400 300 r = 0.62, p < 0.001

200 100

0

2

4

6

8

10 12 14 16 18 20

Age (in years)

Skull capacity (ml)

SphBr (mm)

(g.1)

140

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(f.2)

160 140 120 100

60

8 10 12 14 16 18 20

160

r = 0.77, p < 0.001

r = 0.73, p < 0.001

80

200 180

120

200

(f.1)

160

60

140

80

10 12 14 16 18 20

200 180

160

100

r = 0.79, p < 0.001

100 80

(e.2)

180

SmSm (mm)

SmSm (mm)

200

203

170 160 150 140 130 120 110 100 90 80 60 800 750 700 650 600 550 500 450 400 350 300

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(g.2)

r = 0.68, p < 0.001 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

(h.2)

r = 0.67, p < 0.001 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28

Age (in years)

Fig. 2 – continued: supramolare-supramolare width (SmSm) and age classes in males (e.1) and females (e.2), staphylon-nasion higth (StN) and age classes in males (f.1) and females (f.2), sphenobasion-bregma height (SphBr) and age classes in males (g.1) and females (g.2), between skull capacity (SCap) and age classes in males (h.1) and females (h.2) in the European bison Bison bonasus bonasus.

204


p < 0.01, Fig. 2f.2) and body mass (n = 201, r = 0.94, p < 0.01, Fig. 3f). The height of the neurocranium (SphBr) grows most intensively during the first 3 years of life, after which growth is slower (Fig. 2g.2). It was on average 99 mm in calves, and 139 mm in 3-year-old females (Table 1). SphBr height in 3-year-old females is significantly larger in comparison with the two youngest age classes and the oldest class, and is essentially imperceptibly lower than in the age class of 5 years (Table 2). The height of SphBr in female bison skulls at the age of 4–27 years does not differ significantly (Table 2). The height of SphBr is significantly correlated with age (n = 286, r = 0.68, p < 0.01, Fig. 2g.2) and body mass (n = 185, r = 0.91, p < 0.01, Fig. 3g).

III (0.0519). Between the youngest and oldest class it amounts to 0.0268, and so corresponds approximately with the rate between classes IV and V (Table 4). The growth rate of male body mass between classes I and II amounts to 0.8423, while between VI and VII it attains 0.0090. This rate decreases unsteadily and in male ontogeny is characterised by a slight slowing in the period between IV and V, and acceleration between classes V and VI (Table 4). The growth rate of body mass is larger than growth rate of skull capacity and the quotient of these two parameters between the consecutive age classes amounts to 3, 9, 3, 6, 22, and 4 times. The very large difference of these rates (22) in males from the age of 5–6 years, is intriguing.

Skull capacity in postnatal development

Females

Males

The female calf skull capacity amounts to an average 467 ml. In 3-year old females it attains the value 592 ml and differs significantly only in comparison with calves and the oldest individuals (Table 1, 2). Skull capacity increases most distinctly during the first 3 years of life. In 4-year-old females, it does not differ significantly in comparison with the values in 3-year-old or older individuals. In cows aged 7–27, skull capacity attains an average 658 ml but does not differ significantly from the value of skull capacity in females 4–6 years old (Table 2). This feature is significantly correlated with age (n = 264, r = 0.67, p < 0.01, Fig. 2h.2) and body mass (n = 185, r = 0.90, p < 0.01, Fig. 3h). In females from the youngest age class, similarly to the males, the quotient of skull capacity and body mass amounts to 1:0.24, while in class V this attains the ultimate value of 1:0.62. In females from age classes V to VII, the quotient of both these parameters remains constant, while for males in class V it amounts to 1:0.68 and continually increases, attaining in class VII the value – 1:0.89. Thus 1 ml of encephalon in female calves, as in males, operates 240 g of body mass, whereas in the three oldest age classes – 620 g, ie 270 g less than in the case of males (Table 3). The growth rate of skull capacity between the youngest and oldest classes amounts to

The skull capacity in calves up to one-year old amounts to an average 496 ml, while in 3-year-olds attains 633.3 ml. This feature grows most intensively during the first 3 years of life (Table 1). The skull capacity in 4-year old males does not differ significantly from either 3-year-old individuals or older individuals (Table 2). Male skull capacity attains its largest dimensions (an average 707 ml) at the age of 7–21 years, but is only significantly larger than the skull capacity in males from the first three age classes (Table 2). The skull capacity is significantly correlated with age (n = 279, r = 0.62, p < 0.01, Fig. 2h.1) and body mass (n = 151, r = 0.84, p < 0.01, Fig. 3h). The skull capacity and body mass quotient in males from the youngest age class amounts to 1:0.24 and from the oldest age class this figure is 1:0.89. Therefore one can assume that 1 ml of male encephalon in age class I operates 240 g of body mass, while in age class VII it operates 890 g (Table 3). The growth rate of skull capacity in males totals 0.2822 between age classes I and II and decreases to 0.0020 between subsequent age classes. This rate would be steadily decreasing if it were not greater between age classes III and IV (0.0737) than that between age classes II and


2.75 2.70

(a)

female: r = 0.97; y = 1.916 + 0.280x male: r = 0.97; y = 1.949 + 0.264x

2.65

logStP

logBP

2.60 2.55 2.50 2.45 2.40 female male

2.35 2.30 1.6 2.35 2.30

1.8

2.0

2.2

2.4

2.6

2.8

2.55 2.50 2.45 2.40 2.35


2.30 2.25 2.20 2.15 2.10 2.05

3.0

(b)

205

female male 1.6

1.4

1.8

2.2

2.0

2.6

2.4

2.8

3.0

2.60

(c)

(d)


2.50


logEctEct

logBSt

2.25 2.20 2.15 2.10

2.40 2.30 2.20

2.05 2.10

female male

2.00 1.95

2.00 1.4

1.6

1.8

2.2

2.0

2.4

2.6

2.8

3.0

(e) female: r = 0.96; y = 1.384 + 0.322x

2.25

male: r = 0.96; y = 1.446 + 0.294x

2.25 2.20 2.15 2.10 2.05 2.00 1.95 1.90

2.0

2.2

2.4

2.6

2.8

3.0

(f)


2.20 2.10 2.05 2.00 1.95

1.6

1.8

2.0

2.2

2.4

2.6

2.8

female male

1.90

female male 1.4

1.85 1.4

3.0

1.6

1.8

2.0

2.2

2.6

2.4

2.8

3.0

2.95

2.30

(g) female: r = 0.94; y = 1.458 + 0.272x

2.90

male: r = 0.94; y = 1.472 + 0.266x

(h)


2.85

2.20 2.15

logSCap

logSphBr

1.8

2.15

1.85

2.25

1.6

1.4 2.30

logStN

logSmSm

2.35 2.30

female male

2.10 2.05 2.00

2.80 2.75 2.70 2.65 2.60

1.95

2.55

female male

1.90 1.4

1.6

1.8

2.0

2.2

logM

2.4

2.6

2.8

female male

2.50

1.85 3.0

1.6

1.8

2.0

2.2

2.4

2.6

2.8

3.0

logM

Fig. 3. Comparison of linear relationships in males and females between logarithmically transformed: (a) basion-prosthion length (BP), (b) staphylon-prosthion length (StP), (c) basion-staphylon length (BSt), (d) ectorbitale-ectorbitale width (Ect-Ect), (e) supramolare-supramolare width (Sm-Sm), (f) staphylon-nasion higth (StN), (g) sphenobasion-bregma higth (SphBr), (h) skull capacity (SCap) and body mass (M) in the European bison Bison bonasus bonasus.


206

Table 3. Mean values of skull capacity (SCap) in ml and body mass (M) in kg and their relationship in subsequent age classes; v – coeficient of variation. Skull capacity (SCap) Age class

n

Body mass (M) SCap:M

Mean

SD

v

510 596 626 679 691 699 708

67.2 43.8 55.3 46.0 31.4 32.4 53.6

13.2 7.4 8.8 6.8 4.5 4.6 7.6

Mean

SD

v

124 199 318 406 474 591 628

43.2 82.4 60.3 55.6 60.0 88.3 107.3

34.7 51.5 19.0 13.7 12.7 15.0 17.1

1:0.24 1:0.33 1:0.51 1:0.60 1:0.68 1:0.84 1:0.89

112 198 261 357 390 410 411

33.2 47.6 30.5 58.7 49.2 53.6 86.2

30.0 24.1 7.9 16.4 12.6 13.1 21.0

1:0.24 1:0.36 1:0.45 1:0.58 1:0.62 1:0.62 1:0.62

Males I II III IV V VI VII

40 34 12 16 8 7 34

Females I II III IV V VI VII

51 22 10 10 9 8 75

465 555 581 613 629 655 659

51.1 42.9 27.7 35.9 41.4 39.4 39.9

11.1 7.1 4.8 5.9 6.6 6.1 6.1

0.0234 and, as with males, corresponds to the rate between classes IV and V (Table 4). It is only in females up to the age of 5 years that the growth rate of body mass is greater than the growth rate of skull capacity. Between the consecutive age classes, the quotient of the parameters amounts to 3, 8, 6, 3, and 4 times (Table 4). The greatest difference in the values for these rates (8) occurs in females between the 2nd and 3rd year of life. The growth rate of body mass between classes I and II equals 0.3745, and between classes VI and VII attains a mere 0.0002. In contrast to males, in females the growth rate of body mass during ontogeny gradually decreases (Table 4).

Table 4. Comparison of pace of growth of cavum cranium capacity and body mass in males and females. The pace of growth of capacity and body mass was determined using pattern of Szmalhauzen-Brodi (Nikitiuk 1972, see chapter Material and methods). Age classes as in Table 3. Age classes

Body mass

Males I to II II to III III to IV IV to V V to VI VI to VII I to VII

Morphological distance between age classes

MDS analysis based on the Euclidean distances between bison age classes using all the examined linear characteristics and skull capacity indicates that in both males and females the greatest deviations in skull size occur in age classes I to III (Figs 4, 5). The distance between groups III and IV is significant, in addition to

Skull capacity

0.2822 0.0519 0.0737 0.0224 0.0097 0.0020 0.0268

0.8423 0.4605 0.2463 0.1405 0.2187 0.0090 0.1319

Females I to II II to III III to IV IV to V V to VI VI to VII I to VII

0.1272 0.0461 0.0504 0.0241 0.0414 0.0007 0.0234

0.3745 0.3661 0.3004 0.0855 0.0506 0.0002 0.0888


207

1.0 I

I

0.8

0.2

VIIVI V

Dimension 2

Dimension 2

0.6

IV

-0.2 III

-0.6

0.4 0.0

VII VI V IV

III

-0.4 -0.8

II

II -1.0 -1.0

-0.6

-0.2

0.6

0.2

1.0

1.4

1.8

-1.2 -1.0

-0.6

-0.2

0.2

0.6

1.0

1.4

1.8

Dimension 1

Dimension 1 Fig. 4. Dispersion of the age classes of males of the European bison Bison bonasus bonasus based on the Euclidean distances in respect to size and capacity of the skull.

Fig. 5. Dispersion of the age classes of females of the European bison Bison bonasus bonasus based on the Euclidean distances in respect to size and capacity of the skull.

which it seems to be greater in males. However, in both males and females the age classes IV to VII remain very close to each other. The above is also confirmed by the results of the Scheffé test obtained for particular skull measurements (Table 2).

Analogical regression of skull parameters in relation to the factors of sex and body mass indicates weaker influence of these factors on the size of a bison skull (Table 6). Body mass and sex explain the variation in EctEct to the highest extent (86.9%). Also as much as 85.6% of the variation in SmSm is explained by the regression. Similarly to independent variables BP and sex, and the regression of skull variables to body mass and sex, the variation in SCap (74.4%) is explained by the model to the lowest degree. Dimensions of a bison skull are very closely correlated among themselves (within the skull) as well as with body mass. However, the regression of separate skull measurements in relation to BP length and body mass shows different inclination angles b. Skull dimensions grow pro-

Allometric analysis

The regression of metric characteristics of skull in relation to the factors of sex and BP showed that variation in separate skull characteristics is highly significantly explained by both variables (Table 5). In the case of StP, as much as 96.3% of variation is explained by the regression, and to a lowest degree (83.7%) the regression explains the variation in SCap.

Table 5. Skull measurements and skull capacity variance in European bison explained by sexual factor and basion-prostion length (BP). SS – sums of squares, SSrest – residual (error) variance, df – degrees of freedom. Measurement StP BSt EctEct SmSm StN SphBr SCap

R

2

0.963 0.903 0.934 0.912 0.920 0.910 0.836

SS

df

SSrest

df

F

p

991 724 263 107 1 451 520 415 509 380 150 251 707 3 917 329

2 2 2 2 2 2 2

37 880 28 119 102 057 39 982 32 824 24 871 764 197

536 536 536 536 536 536 536

7016 2507 3811 2785 3103 2712 1374

0.00 0.00 0.00 0.00 0.00 0.00 0.00


208

Table 6. Skull measurements and skull capacity variance in European bison explained by sexual factor and body mass (M). SS – sums of squares, SSrest – residual (error) variance, df – degrees of freedom. Measurement

R

BP StP BSt EctEct SmSm StN SphBr SCap

2

0.829 0.805 0.778 0.869 0.856 0.831 0.768 0.744

SS

df

SSrest

df

F

p

1 218 210 545 819 139 356 817 973 242 255 209 778 135 214 3 917 329

2 2 2 2 2 2 2 2

252 033 131 904 39 676 122 984 40 825 42 657 40 807 758 974

331 331 331 331 331 331 331 331

800 685 581 1101 982 814 548 480

0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00

portionally to the increase in BP, since the index b oscillates between 0.803 and 1.314 (Table 7). The lowest value of b was found for BSt and SCap, and the highest for EctEct. The increase in skull dimensions is much slower compared to the growth of bison body mass. The index b in regression equations of the increase in metric characteristics of a skull in relation to body mass ranges from 0.214 to 0.355. In relation to body mass, values of SCap and SphBr increase most slowly. EctEct has the highest value of b in relation to body mass. Regression of separate skull measurements in relation to body mass of males and females in-

Table 7. Indices b from regression equations that defined relationship between skull dimensions and BP length (A) and body weight (B) in females and males of European bison. Explanation of skull indexes see chapter Material and methods.

Measurement

A Female

B Male

Female

Male

BP

–

–

0.280

0.264

StP

1.114

1.110

0.310

0.292

BSt

0.803

0.850

0.231

0.224

EctEct

1.182

1.314

0.335

0.355

SmSm

1.119

1.108

0.322

0.294

StN

1.174

1.172

0.328

0.309

SphBr

0.981

0.998

0.272

0.266

SCap

0.877

0.847

0.254

0.214

dicates that in some characteristics there are differences between the sexes (Fig. 3a–h, Table 8). Highly significant sex difference (p < 0.001) was found for the regression of SCap in relation to body mass (Table 8, Fig. 3h). The increase in SCap is significantly more proportional to the growth of body mass in females than in males. Significant sex differences (p < 0.05) in the regression line in relation to body mass were found for skull measurements: SmSm, EctEct and BP (Table 8). For all characteristics, except EctEct, the skull size grew faster in females than in males along with the growth of body mass. In the case of breadth EctEct, the value grew faster in males than in females along with the growth of body mass (Table 8). Sexual dimorphism

With regard to linear skull measurements in calves in age class I, no significant differences between sexes were observed (Table 1). Only male skull capacity is significantly greater than in females, just after birth (t = 2.522, p < 0.02; Table 1, Fig. 6). The greatest differences among linear measurements concern orbital breadth EctEct (p = 0.077). In males from all the age classes, orbits are set wider, and from the 3rd year of life these differences are highly significant (Table 1, Fig. 6). In the 2nd year of life, two features distinguish male skulls from the female ones. These are EctEct (t = 2.002, p < 0.01) and StN (t = 2.051, p < 0.05). By the 3rd year of life as many as five measurements are significantly larger in


209

Table 8. Sex and body weight, and interaction of both the factors in allometric growth of skull size in European bison. Explanation of skull indexes see chapter Material and methods. SS – sums of squares.

BP StP BSt EctEct SmSm StN SphBr SCap

Body weight (logM)

Sex

Measurement

Interaction sex/body weight (logM)

SS

F

p

SS

F

p

SS

F

p

0.001 0.001 0.001 0.002 0.005 0.002 0.000 0.013

3.5 1.1 0.8 2.5 7.0 2.8 0.3 15.9

0.061 0.288 0.374 0.118 0.009 0.096 0.598 0.000

2.239 2.730 1.549 3.646 2.912 3.107 2.197 1.411

5508.2 3300.9 2429.3 5194.8 4101.0 3744.3 2551.3 1686.5

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

0.002 0.003 0.000 0.003 0.006 0.003 0.000 0.010

5.3 3.1 0.6 4.4 8.5 3.1 0.3 12.4

0.022 0.078 0.438 0.036 0.004 0.079 0.597 0.000

males than in females. Apart from the dimorphic characteristics in age class II, in age class III significant differences are displayed in BP, BSt and SmSm measurements (Table 1). At the age of 4, a significant level of sexual dimorphism is displayed by all the linear skull characteristics except for BSt (Table 1, Fig. 6). In adult (³ 5 years) individuals, all linear measurements as well as skull capacity display

strong sexual variation (t = 9.726 – 15.980, p < 0.001). The greatest variation concerns EctEct (p < 0.001; Table 1, Fig. 6). In age class I, the strongest discriminatory power is displayed by the indices EctEct/StP and SmSm/BP (Table 9). In age class II, none of the indices meet the criteria necessary for discrimination. Skulls of 3-year-old bison are best differentiated by the EctEct/StP quotient. In age class

1.18 1.16 StN 1.14 EctEct

Dimorphism index

1.12 1.10

SphBr

1.08

SCap

1.06

StP

1.04

BP

1.02 BSt 1.00 SmSm 0.98 0.96 I

II

III

IV

V

Age groups Fig. 6. Sexual dimorphism indices of some skull characteristics through the age classes in the European bison Bison bonasus bonasus.


210

Table 9. Discriminative functions based on skull indexes to determination of sexual dimorphism in different age classes of the European bison. Explanation of skull indexes see chapter Material and methods. For age classe II none of the indices meet the criteria necessary for discrimination. Age classes I III IV V VI VII

Wilks’ lambda statistic

Discriminative function

19.041 SmSm/BP + 8.606 EctEct/StP – 15.384 14.927 EctEct/StP – 14.757 42.041 EctEct/BP – 26.440 22.426 EctEct/StP – 10.527 SphBr/StN – 13.105 24.018 EctEct/StP 53.165 EctEct/StP – 54.507 StN/StP + 65.834 StN/EctEct – 60.547

IV, dimorphism is determined by the EctEct/BP index. Above the 4th year of life, the EctEct/StP ratio is again responsible for discrimination, while in age class V this is accompanied by the SphBr/StN ratio and in class VII the two ratios StN/StP and StN/EctEct. On the basis of the Wilks lambda statistic for particular discriminative functions, sexual dimorphism in bison skulls increases with age, attaining its peak in about the 5th year of life. Analysing the proportions in the shaping of bison skulls, the skulls of adult bulls are longer, broader and higher than in female bison.

Discussion The previous analyses of smaller sample sizes and undifferentiated lines of European bison, showed that, in adult females particularly, the correlation of skull measurements with age remains high throughout their lifetime (Kobryñczuk and Roskosz 1980). In Lowland European bison, the coefficient of the correlation between skull measurements and age ranges from 0.62 to 0.79 in males and from 0.65 to 0.77 in females. Both in males and females the lowest values of the correlation were noted in skull capacity. Additionally, in females lower correlation with age was found for the length and height of neurocranium. The strongest correlation was noted between age and orbital breadth, and between age and splanchnocranium breadth.

0.858 0.752 0.549 0.305 0.329 0.425

The most intensive development of a bison skull lasts up to the 5th year of life. An increase in skull dimensions in older individuals (³ 6 years) is very slow; however, it still happens in many cases. Generally the largest skull sizes occur in the oldest bison. Exceptionally, in oldest males this growth is not followed by both skull height of splanchnocranium and the length of the splanchnocranium, while in oldest females by height of splanchnocranium. As with linear skull measurements, skull capacity in bison of both sexes increases significantly up to the 3rd year of life, after which the increase is not so distinctive, and ceases in individuals aged 5 years. Skull cavity and body mass growth rate is marked by uniform deceleration, where this growth within a unit of time has negative values. Similar observations were made in the growth of selected linear parameters of bison skulls (Kobryñczuk and Kobryñ 1980). The skull capacity in both sexes, is more dependant on body mass than on age. It should be added that this relationship is larger in females (r = 0.90 – body mass, and r = 0.67 – age) than in males (r = 0.84 and 0.62). From the analysis of the growth rate in neurocranium height and skull capacity, together with the earlier results of research by Kobryñczuk and Roskosz (1984), it can be concluded that encephalon of the European bison grows mostly during the first three years of life and its growth is slightly faster than that of medulla spinali. McDonald (1981) indicated that horn core characters show the greatest allomorphosis among


taxa, whereas occipital-frontal-facial characters show considerably less allomorphosis. The highly significant correlation of all the measurements (length, breadth and height) proves that the skull develops proportionally during postnatal development. The slope b of the regression line of skull dimensions in relation to basal length oscillates between 0.803 and 1.314. For the American and European bison, Bohlken (1967) noted that regression of skull metric characteristics in relation to basal length varied between 0.86 and 1.54, with palate length growing most slowly, and face breadth and orbital breadth most intensively. In the European bison, the height of splanchocranium increases evenly along with the growth of basal length. Only skull capacity and the length of neurocranium increase more slowly than basal length; other skull dimensions grow faster. Skull dimensions and body mass are strongly correlated (r ranges from 0.90 to 0.97). However, the increase in skull size is much slower compared to the speed of the growth of body mass (b oscillates between 0.214 and 0.355) than compared to the basal length of a skull. Similarly to relationships within the skull, capacity grows most slowly also in relation to body mass (b = 0.254 in females, b = 0.214 in males). Orbital breadth increases most intensively along with the growth of body mass (b = 0.335 in females, b = 0.355 in males). Body mass influences all studied skull dimensions highly significantly (p < 0.001). Sex significantly influences such parameters of skull size as the breadth of splanchnocranium (p = 0.009) and skull capacity (p < 0.001). In females, skull size increases slightly more intensively compared to body mass than in males. Only orbital breadth grew more proportionally to body mass in ontogenesis of males. Differences in allometric development of a skull in males and females are significant in the case of basal length, orbital breadth, breadth of splanchnocranium, and skull capacity. Earlier McDonald (1981) indicated that males and females exhibit similar patterns of skull allometry. Significantly smaller mean length of the neurocranium, resulting in shorter basal length of skull, as well as smaller skull capacity both in average and maximal values (Table 10), was

211

found for contemporary males compared to the ones born in 1930–1950 analyzed by Empel (1962). These differences may be a result of an increase in inbreeding level expressed in that way in modern males of Lowland European bison. It may be caused by the fact that all the males of the Lowland line have copies of the same chromosome Y, originating from the same founder M 45 PLEBEJER (Olech 2006). Differences in skull morphometry of modern females of the Lowland line and the ones born in 1930–1950 are different than in males. Significantly larger orbital breadth and the height of splanchnocranium were found in the skulls of modern females than in females from the old data (Table 11) while other skull measurements did not differ significantly. It is difficult to decide whether these changes are also a result of an increase in inbreeding. Kobryñczuk (1985) observed in individuals of the Lowland-Caucasian line the elongation of pars basialis of skull and the splanchnocranium was accompanied by simultaneous narrowing of the splanchnocranium, shortening of the scapula and elongation of the bones of the free part of limb, which could be the result of inbreeding. Changes in phenotypic skull characteristics of contemporary European bison observed by us, as well as in the data of Kobryñczuk (1985), show that an increase of inbreeding influences phenotypic characteristics of skull and may differ between the two breeding lines as well as between the sexes. Size and shape of Lowland European bison skull from the population of the Belarusian part of the Bia³owie¿a Forest (Nemtsev et al. 2003) fall within the range of variability of our own measurements (Table 10, 11). Analyses of morphometric variation in the skull of the American bison were carried out based on skull measurements different from those used by most authors dealing with the European bison. In studies on craniometry of the American bison, only three measurements – basal length (FP), orbital breadth (GPW) and breadth of splanchnocranium (WMP) (Bohlken 1967, Shackleton et al. 1975, McDonald 1981, Zyll de Jong 1986) could be compared with the Lowland European bison. Average values of basal length, orbital breadth and breadth of


212

Table 10. Comparison of skull measurements of adult males (5–22 yrs) of European bison from other studies. Student t-test was used for comparison measurements of two chronologically different populations (present study and old material). Statistical significance t statistic: *** – p < 0.001, ** – 0.01 > p > 0.001, * – 0.05 > p > 0.01, ns – p > 0.05. Old material – skulls of males, born between 1930 and 1950 of the 20th century, living in captivity, partly worked out by Empel 1962. Other literature data: Belaruss – males from Belarussian part of Bia³owie¿a Forest (Nemtsev et al. 2003), B. bison athabascae Zyll de Jong 1986, Nyarling River herd derived from B. bison athabascae Zyll de Jong 1986, B. bison bison Shackleton et al. 1975, B. bison bison McDonald 1981. Nyarling B. b. bison B. b. bison B. bison Belaruss athabascae River herd, Shackleton McDonald Zyll de et al. 1975 1981 Zyll de Jong 1986 Jong 1986

Present study

Old material

mean min max SD n

471.8 430 510 14.3 151

485.3 452 522 17.6 22

StP

mean min max SD n

289.1 270 310 8.9 150

287.1 201 309 21.0 22

ns

BSt

mean min max SD n

185.1 150 210 10.1 150

194.0 170 240 15.1 22

3.96***

EctEct

mean min max SD n

318.9 270 360 15.3 154

318.6 291 339 12.5 22

SmSm

mean min max SD n

185.6 160 210 9.6 154

191.2 180 200 5.8 8

StN

mean min max SD n

171.3 150 190 8.0 153

166.3 156 175 6.6 10

ns

SphBr

mean min max SD n

160.7 140 180 7.6 151

163.8 160 170 4.4 8

ns

SCap

mean min max SD n

705.4 600 820 44.3 139

742.4 600 840 50.29 21

3.50***

BP

470.5

24

310

54

531.3 512 555 13.8 12

518.3 487 543 16.0 18

486.6 450 520 12.2 77

358 341 385 11.1 13

346.9 324 364 10.8 19

318.1 282 352 12.2 81

196.8 180 221 7.5 13

197.6 184 212 8.2 19

189.8 160 206 9.1 83

t

4.00***

324.6 288 356 1.2 117

ns

ns


213

Table 11. Comparison of skull measurements of adult females (5–27 yrs) of European bison from other studies. Student t-test was used for comparison measurements of two chronologically different populations (present study and old material). Statistical significance t statistic: *** – p < 0.001, ** – 0.01 > p > 0.001, * – 0.05 > p > 0.01, ns – p > 0.05. Old material – skulls of females, born between 1930 and 1950 of the 20th century, living in captivity, partly worked out by Empel 1962. Other literature data: Belaruss – males from Belarussian part of Bia³owie¿a Forest (Nemtsev et al. 2003), B. bison athabascae Zyll de Jong 1986, Nyarling River herd derived from B. bison athabascae, Zyll de Jong 1986, B. bison bison Shackleton et al. 1975, B. bison bison McDonald 1981. Nyarling B. b. bison B. b. bison B. bison Belaruss athabascae River herd, Shackleton McDonald Zyll de et al. 1975 1981 Zyll de Jong 1986 Jong 1986

Present study

Old material

mean min max SD n

447.0 410 480 12.6 152

447 428 477 13.8 22

StP

mean min max SD n

279.3 250 300 8.7 152

278.4 267 295 8.3 22

ns

BSt

mean min max SD n

169.3 150 190 9.0 152

169.5 154 182 8.3 22

ns

EctEct

mean min max SD n

274.6 240 300 12.2 152

267.4 251 286 9.3 22

mean min max SD n

171.1 140 190 9.4 152

170.5 160 180 5.8 10

StN

mean min max SD n

157.5 140 187 7.7 152

149.9 140 160 5.1 14

SphBr

mean min max SD n

148.9 140 169 4.9 151

147.0 140 160 4.8 10

ns

SCap

mean min max SD n

653.9 570 750 41.2 149

645.9 620 750 49.1 22

ns

BP

SmSm

450.1

24

263.7

47

467

1

284

1 177

1

460.7 441 485 13.2 11

443 415 468 11.8 25

280.8 262 309 14.9 16

257 237 275 10.1 35

170.4 155 186 8.5 16

164 153 179 6.8 36

t

ns

267.5 248 291 2.0 25

2.64**

ns

–3.57***

214


splanchnocranium in skull of modern males of Lowland European bison are distinctly smaller than in Bison b. athabascae, and similar or slightly smaller than in Bison b. bison (Table 10). In the female skull, the modern Lowland European bison average values of basal length and breadth of splanchnocranium were similar to Bison b. bison, but distinctly smaller than in Bison b. athabascae, while orbital breadth was distinctly larger than in bison, and smaller than in athabascae (Table 11). It may be stated that fundamental differences between skulls of modern American and European bison are connected with the length and breadth of the skull. This corresponds with the results of the discriminant analysis of morphological relationships of crania of modern American and European bison (Zyll de Jong 1985), which found that contribution to the discrimination between athabascae, and bonasus comes mainly from basal length, orbital breadth and several other measurements as GWA, AOW and OC, while discrimination between athabascae and bison is contributed to mainly by orbital breadth, basal length, breadth of splanchnocranium and GWA. Results of our research confirm the opinion of Zyll de Jong (1986) that the closer craniometrical proximity of “Bison b. bison and Bison bonasus bonasus to one another than that of either to Bison b. athabascae is difficult to harmonize with the view that the European bison is specifically distinct”. The authors agree with the opinion of Bohlken (1967), among others, that differences in morphometry of skulls of American and European bison might have the nature of intraspecific variation and that American and European bison could be subspecies or one species. Variation in skull parameters in the group including Lowland and Lowland Caucasian line is considerably larger in comparison with Caucasian bison and North American bison. For example, the variation in skull length of the contemporary European bison is 3–4 times greater then in B. caucasicus or B. b. athabascae. Interorbital breadth differs to an even greater extent in this respect. An exception is formed by the skulls of B. latifrons and B. alaskensis, in which variation is very great (McDonald 1981).

In follows from this that skull phenotype of the Lowland European bison has not as yet stabilised (Kobryñczuk 1985). Results of this study and the results of Kobryñczuk et al. (2008a, b) in modern Lowland European bison, showed relatively large variation in the shape of skulls of males and females. Skulls of physically mature males generally have male features, while among adult females skulls with male features form 10% of all studied skulls. In Lowland European bison, skulls of adult bulls are longer, wider and higher than those of females. Empel (1962) found the biggest differences between the sexes in the measurements of the breadth of calvaria cavum cranii and planum nuchale. While McDonald (1981) state that in various taxa of Bison absolute dimorphism in linear skull characters is generally greatest among horn core characters, less among facial and frontal characters. Discriminant analysis in Lowland European bison indicates that together with an increase in age, the number of skull indices of statistically significant sexual discriminatory power also increases. From among the analysed indices the highest discriminatory power in various bison age classes involved EctEct indices (EctEct/StP, StN/EctEct). This is linked to the fact that from the day of birth, EctEct breadth displays the highest sexual dimorphism in all the examined skull characteristics. Comparing the variability of bison skull sizes and capacity with variations of body sizes during the postnatal development (Krasiñska and Krasiñski 2002), a high degree of similarity is observed. The measurements of body and skull are significantly correlated with age, as well as with body mass. The largest body mass is associated with the largest skull and body sizes in bison. Sex-related differences in body mass and measurements were most pronounced in bison ³ 3 years old. Sexual dimorphism in terms of skull sizes also increases with age, peaking at about the age of 5. Development of the bison skull basically ceases at the age of 5. In older individuals of both sexes, only the orbital breadth increases slightly, as well as the breadth of the splanchnocranium in females, as was similarly proved by Empel (1962) and Kobryñczuk and


Roskosz (1980). Similarly, physical development (measurements and body mass) of females ends at the age of 5, while in males at the age of 7 (Krasiñska and Krasiñski 2002). Acknowledgments: We thank Prof M. Konarzewski and Dr K. Zub for creative support in statistic work. The authors wish to thank A. Arasim for technical support in collecting data process. We are very grateful Prof P. D. Polly improved English language in the last version of the manuscript, and also him and two anonymous referees provided helpful comments and criticism.

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Received 4 October 2007, accepted 29 April 2008. Associate editor was O. David Polly.