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NATURA MONTENEGRINA, PODGORICA, 6:101-109<br />

<strong>MORPHOLOGICAL</strong> <strong>TRAITS</strong> <strong>OF</strong> <strong>COMMON</strong> <strong>TOAD</strong> <strong>Bufo</strong> <strong>bufo</strong> (<strong>Bufo</strong>nidae) FROM<br />

BIOGRADSKO LAKE<br />

Natalija Č A Đ ENOVIĆ ¹, Tanja V U K O V ²<br />

¹ Natural History Museum of Montenegro, Podgorica, Crna Gora, E-mail: lazo@cg.yu<br />

² Institute for Biological Research “Siniša Stanković”, Beograd, Srbija<br />

Key words:<br />

<strong>Bufo</strong> <strong>bufo</strong>,<br />

morphometric,<br />

qualitative characters,<br />

differences between<br />

the sexes.<br />

SYNOPSIS<br />

In this paper we have presented the results of the<br />

analysis of morphological traits of Common Toad <strong>Bufo</strong> <strong>bufo</strong><br />

population, from Biogradsko Lake. On the samples taken<br />

from this locality univariant and multivariant statistical<br />

analyses have been performed. A large number of<br />

morphometric and qualitative characters have been done for<br />

the first time. For morphometric characters basic parameters<br />

of descriptive statistics have been calculated, and for<br />

qualitative characters three qualitative traits with three<br />

conditions at four body regions of Common Toad separately<br />

by sexes, have been treated. As for the morphometric<br />

characters it has been established that there is a significant<br />

statistical difference between the sexes.<br />

Ključne riječi:<br />

<strong>Bufo</strong> <strong>bufo</strong>,<br />

morfometrijski,<br />

kvalitativni karakteri,<br />

razlike među<br />

polovima.<br />

SINOPSIS<br />

MORFOLOŠKE KARAKTERISTIKE OBIČNE KRASTAVE ŽABE<br />

BUFO BUFO (BUFONIDAE) SA BIOGRADSKOG JEZERA<br />

U ovom radu su prikazani rezultati analize morfoloških<br />

odlika populacije krastave žabe <strong>Bufo</strong> <strong>bufo</strong>, sa Biogradskog<br />

jezera. Na uzorcima uzetim sa ovog lokaliteta urađene su<br />

univarijantne i multivarijantne statističke analize. Po prvi put<br />

je obrađen veliki broj morfometrijskih i kvalitativnih karaktera.<br />

Za morfometrijske karaktere izračunati su osnovni parametri<br />

deskriptivne statistike, a za kvalitativne karaktere obrađene<br />

su tri kvalitativne karakteristike sa tri stanja na četiri tjelesna<br />

regiona obične krastave žabe odvojeno po polovima. Što se<br />

tiče morfometrijskih karaktera utvrđena je statistički značajna<br />

razlika između polova.


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Natura Montenegrina, 6/2007<br />

INTRODUCTION<br />

Common Toad has a large distribution and popultes mainly the entire palearctic<br />

area. It populates almost the entire Europe, with the exception of far north, Ireland,<br />

Corsika, Sardinia, Balear's Islands, Malta, Crete, as well as some smaller<br />

islands (B o r k i n and V e i t h , 1997). It also populates the northwestern Africa<br />

(P a s t e u r and B o n s , 1959). Although common at lower altitudes, it may also be<br />

found also on altitudes exceedeing 2500 m and on Iberian Peninsula (A n g e l , 1946;<br />

B o r k i n and V e i t h , 1997). In Montenegro it is mainly widely distributed. Owing to<br />

wide distribution, climatic conditions in various parts of areal of distribution are very<br />

different. Thus, in northern part of the areal the winters are long, cold and humid, so<br />

that the period favorable for growth is rather short (J o h a n n e s s e n , 1970). On<br />

higher altitudes the conditions are even more extreme. On the other hand, southern<br />

populations of this species are exposed to much more favorable conditions of outer<br />

environment; therefore the period favorable for growth is much longer.<br />

Species <strong>Bufo</strong> <strong>bufo</strong> is a polytypic one. From the scope of this species a taxon<br />

from the Far East has been separated on the level of species <strong>Bufo</strong> gargarizans<br />

(A n a n j e v a et al. 1998, K u z m i n 1999a, 1999b), and the character of polytype is<br />

determined to it in addition to nominotype subspecies three other ones B. b.<br />

grediscola, B. b. verrucosissimus, B. b. spinosus. If we recognize the fact that<br />

Caucasus Toad (<strong>Bufo</strong> verrucosissimus) is a separate species (e.g. O r l o v a &<br />

T u n i y e v 1989, A n a n j e v a et al. 1998), than the taxonomic differentiation in scope<br />

of Common Toad is even more limited. Nominotype subspecies is the most widely<br />

distributed (Northern and Southern Europe). The two first subspecies have a limited<br />

geographical area (mountains Gredos and Caucasus), nominotype subspecies is the<br />

most widely distributed (Northern and Central Europe), whereas the areal of<br />

subspecies B. b. spinosus is limited to the region of Mediterranean (northwestern<br />

parts of Africa, southeast Europe, southern Switzerland, Italy as well as the southern<br />

parts of France and Spain).<br />

MATERIAL AND METHODS<br />

A total of 41 specimens has been analyzed, 26 males and 15 females. The<br />

largest part of the material has been collected in mating period. The material has<br />

mainly been manually collected and meredov (a net with a handle) has also been<br />

used.<br />

The samples belong to herpetological collection of the Natural History Museum<br />

of Montenegro; they are kept in 70 % alcohole.<br />

Morphometric analysis has been done on 21 traits which determine size and<br />

form of body and head of tailless amphibians. Measured traits are: L – longthe of body


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from the top of head to the opening of the cloaca; Lpa – length of front exstremity; F –<br />

length of femur measured fromxthe opening of cloaca to knee joint; T – lengthj of<br />

tibiofibula from knee joint to tibiotarsal joint; P – distance from tibiotarsal joint to the<br />

tip of the longest finger (IV); n – length of metatarsus from the internal metatarsal<br />

ridgelet to the tip of the longest finger (IV); DpPa – length of the first finger off front<br />

exstremity; DpPp – length of the first finger of back extremity; Cint – the biggest<br />

length of the internal metatarsal ridgelet; Lc – length of head from the top of head to<br />

jaw joint; Ltc – width of head measured between the jaw joints; Spp – betweeneyes<br />

space between the internal edges of eye lids; Lc – lengh of head from the top of head<br />

to jaw joint; Ltc – width of head measured between jaw joints; Spp – betweeneyes<br />

space between the internal edges of eye lids; Spi – distance betwnn the outer nasal<br />

openings; Spcr – distance between front angles of eye openings; Lo – the largest<br />

length of eyeball; Ltp – the largest width of upper eye lid; Dro – distance from the top<br />

of head to the eye edge; Dno- distance of nasal opening from eye; Lh - length of<br />

cutaneous folds on heels; Lg - length of partoid salivary glands; Wg - width of<br />

salivary glands and weight.<br />

Three qualitative traits (Table 1) with three conditions on four body regions of<br />

toad: head part - dorsal side, dorsal part-dorsal side, head part -ventral side,<br />

abdominal part-ventral side.<br />

The conditions of qualitative traits have been coded in the following manner:<br />

Dorsal side – head part:<br />

1a - round warts, 1b - oval warts, 1c – kidneylike warts; 2a – very protuberant<br />

warts, 2b – protuberant warts, 2c – drawn in warts; 3a – very marked thornlike ends of<br />

warts; 3b – medium marked thornlike ends of warts; 3c – weakly marked thornlike<br />

ends of warts;<br />

Dorsal side - dorsal part:<br />

4a - round warts, 4b - oval warts, 4c - kidneylike warts; 5a – very protuberant<br />

warts, 5b – protuberant warts, 5c – drawn in warts; 6a – very marked thornlike ends of<br />

warts; 6b – medium marked thornlike ends of warts; 6c – weakly marked thornlike<br />

ends of warts;<br />

Ventral side – head part:<br />

7a - round warts, 7b - oval warts, 7c - kidneylike warts; 8a – very protuberant<br />

warts, 8b – protuberant warts, 8c – drawn in warts; 9a – very marked thornlike ends of<br />

warts; 9b – medium marked thornlike ends of warts; 9c – weakly marked thornlike<br />

ends of warts;


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Ventral side – abdominal part:<br />

10a - round warts, 10b - oval warts, 10c - kidneylike warts; 11a – very<br />

protuberant warts, 11b – protuberant warts, 11c – drawn in warts; 12a – very marked<br />

thornlike ends of warts; 12b – medium marked thornlike ends of warts; 12c – weakly<br />

marked thornlike ends of warts;<br />

Trait<br />

Warts shape<br />

Condition<br />

a) round<br />

b) oval<br />

c) reniform<br />

a)very convex<br />

Warts convexity<br />

b) convex<br />

c) inverted<br />

Prominence of thornlike<br />

warts endings<br />

a)very prominent<br />

b)averagely prominent<br />

c)weakly prominent<br />

Table 1. Analysed qualitatie traits in <strong>Bufo</strong> <strong>bufo</strong><br />

Statistical Analysis<br />

Programme package STATISTICA (version 5.0) has been used for statistical<br />

analysis of data. For morphometric characters basic parameters of descriptive<br />

statistics have been separately calculated by genders: medium value ( x ), error of<br />

medium value (SE), standard deviation (SD), minimal (min) and maximal (max) values<br />

traits as well as coeficient of variation (CV). Analysis of sexual dimorphism has been<br />

performed on basic data (untransformed measures for every property), as well as on<br />

standardized residuals on eight traits (L, Lpa, F, T, P, n, Lc, Ltc). Regression of every<br />

property on body length (L) and use of standardized residuals from such a regression<br />

provides for the elimination of the impact of body size. Comparison of differences<br />

between the genders on basic data and on standardised residuals has been performed<br />

by the use of Tukey Test for the samples of uneven size.<br />

For the establishment of the significance of differences in respect of<br />

morphometric characters between the genders analysis of variance (ANOVA) has<br />

been used.<br />

Absolute and relative frequences (%) of the conditions of qualitative traits have<br />

been established. Qualitative traits have been analysed also through the<br />

corresponding analyses.


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RESULTS AND DISCUSSION<br />

Morphometric Characters<br />

Former data on values of morphometric characters of the species <strong>Bufo</strong> <strong>bufo</strong> are<br />

rather insufficient, or, some of them have been given only descriptively. That is why<br />

we have presented here the average values for a large number of characters that<br />

have not been previously analyzed and data about that do not exist in the literature.<br />

Basic parameters of morphometric characters descriptive statistics have been<br />

presented separately by sexes in the table 2. The smallest male of the sample of the<br />

population from Biogradsko Lake is 64.28, and the largest one 82.54 mm. The<br />

smallest female is 90.94 mm, and the largest 109.94 mm. Obtained values of body<br />

size of common toad from Biogradsko Lake are within the limits of the so far recorded<br />

values from other parts of areal of the species. (R a d o v a n o v i ć , 1951; A r n o l d and<br />

B u r t o n , 1978; Đ urović et al, 1979 etc).<br />

Sexual dimorphism has been analyzed in scope of population (localities) by<br />

application of Tukey test for samples of unequal size (“Unequal N HSD Tukey” test).<br />

This test has shown an expressed sexual dimorphism, where the females have higher<br />

average values of analyzed traits (Table 2). On basis of calculated parameters of<br />

descriptive statistics, separately by sexes and on basis of compared differences<br />

between the sexes, it has been established that the females have statistically higher<br />

values of all the characters, especially when the word is about L – body length, Lpa –<br />

length of front extremity, Lc – head length, Ltc – head width, Lg – length of salivary<br />

glands, weigth.<br />

With the population of Biogradsko Lake a great number of traits that have been<br />

demonstrating sexual dimorphism by the analysis of basic data where the size has<br />

been included, indicate the absence of sexual dimorphism for the largest number of<br />

characters when body size is excluded. The charactereistics which demonstrate the<br />

presence of sexual dimorphism also after the eliminating body size are T- length of<br />

tibiofibula and F – length of femur.<br />

Females are bigger than males in a large number of amphibian species<br />

(S h i n e , 1979; M i a u d et al., 1999; K h o n s u e et al.., 2001a, 2002b; M o n n e t and<br />

C h e r r y , 2002). That has been especially expressed with tailless amphibians in<br />

which females are bigger than males with 90% of species (S h i n e , 1979). This has<br />

also been established in this paper for studied population from Biogradsko Lake, as<br />

well as for the populations of the remaining part of the areal of distribution of this<br />

species (G i t t i n s et al., 1980; H e m e l a a r , 1988). The most common explanation of<br />

sexual dimorphism in body size is the advantge the females have in respect of eggs<br />

production (H a l l i d a y and V e r r e l l , 1986; C v e t k o v i ć et al., 2003). Namely,<br />

there is a positive correlation in many groups between body length and fecundity<br />

(C u m m i n s , 1986; B e r v e n , 1988; S i n s c h , 1998; G i b b o n s and M c C a r t h y ,<br />

1986). Assumption is that the selection, owing to a pointed correlation of body length


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Natura Montenegrina, 6/2007<br />

Males Females sexual dimorphism<br />

Unequal N HSD (Tukey)<br />

Trait N Means SD SE Min Max N Means SD SE Min Max basic data/standard results<br />

L 26 73.71 4.1447 0.8128 64.28 82.54 15 100.64 5.0865 1.3133 90.94 109.94 ***<br />

Lpa 26 54.62 3.6473 0.7153 46.68 63.17 15 71.64 3.7562 0.9699 62.23 77.60 ***/ns<br />

F 26 32.53 3.1809 0.6238 25.32 38.86 15 40.67 4.9746 1.2844 31.98 46.95 ***/***<br />

T 26 24.10 2.0556 0.4031 20.52 27.25 15 28.82 2.4023 0.6203 25.55 34.46 ***/**<br />

P 26 36.65 4.2990 0.8431 27.03 42.91 15 42.98 2.8349 0.7320 37.06 47.03 **/ns<br />

n 26 51.90 4.6742 0.9167 43.30 60.54 15 62.52 4.8611 1.2551 56.26 72.83 ***/ns<br />

n-P 26 15.25 4.0443 0.7931 7.26 22.45 15 19.54 4.4970 1.1611 12.24 27.70 **<br />

DpPa 26 6.58 0.7584 0.1487 5.10 7.99 15 10.44 1.5234 0.3933 7.48 13.45 ***<br />

DpPp 26 6.74 0.8867 0.1739 5.29 8.63 15 8.46 1.2908 0.3333 5.85 10.79 ***<br />

Cint 26 4.53 0.5892 0.1155 3.37 5.56 15 6.34 0.9030 0.2331 4.51 7.74 ***<br />

Lc 26 17.50 1.1857 0.2325 14.28 19.46 15 24.69 1.6894 0.4362 22.04 27.83 ***/ns<br />

Ltc 26 22.41 1.5435 0.3027 19.67 24.73 15 31.19 2.0888 0.5393 28.09 36.37 ***/ns<br />

Spp 26 8.75 0.9524 0.1868 6.72 10.92 15 12.55 1.6316 0.4213 9.75 15.07 ***<br />

Spi 26 4.03 0.5097 0.1000 2.85 4.92 15 5.32 0.6099 0.1575 4.39 6.47 ***<br />

Spcr 26 7.49 0.5751 0.1128 6.28 8.62 15 11.82 0.9789 0.2528 10.28 14.21 ***<br />

Lo 26 6.25 0.6112 0.1199 4.95 7.43 15 9.28 0.7010 0.1810 7.61 10.27 ***<br />

Ltp 26 5.88 0.6321 0.1240 4.32 6.71 15 7.80 0.8845 0.2284 5.72 9.61 ***<br />

Dro 26 7.54 0.5957 0.1168 6.27 8.75 15 10.72 0.8648 0.2233 9.42 12.33 ***<br />

Dno 26 3.22 0.3864 0.0758 2.59 4.08 15 4.49 0.5739 0.1482 3.54 5.41 ***<br />

Lh 26 3.56 0.5723 0.1122 2.65 4.77 15 5.09 0.3795 0.0980 4.49 5.81 ***<br />

Lg 26 14.86 1.7528 0.3438 11.78 18.10 15 20.77 2.2236 0.5741 17.04 24.34 ***<br />

Wg 26 5.80 0.7387 0.1449 4.53 7.50 15 8.20 1.0614 0.2741 6.48 10.06 ***<br />

Weight 26 44.50 6.4576 1.2664 33.00 56.00 15 141.07 31.1367 8.0395 97.00 230.00 ***<br />

Table 2. Basic parameters of descriptive statistics of males and females of Biogradsko Lake and Tukey (HSD) test with gender factor


107<br />

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and fecundiy, favorises several values for body length of females. Greater eggs<br />

production on the other hand is explained by larger internal space for their storage,<br />

which larger females have (A n d e r s o n , 1994).<br />

The direction and magnitude of dimorphism in body length depend of various<br />

selective pressures the specimens of male and female sex are exposed to. D a r w i n<br />

(1871) assumed that sexual selection (though the competition among the specimens<br />

of the same sex or through an active selection of partner), may lead to sexual<br />

dimorphism. For instance, in species with pointed struggles among the males, males<br />

are frequently bigger than females.<br />

However, it is important to underline that common toad is one of rare secies in<br />

which males are a smaller sex, although there are struggles for females among them<br />

(H a l l i d a y and V e r r e l l , 1986; A r a k , 1988).<br />

Qualitative Analysis<br />

By a comparison of rerlative frequency of condition of monitored qualitative traits<br />

it has been noted that the same conditions, as a rule, have the greatest frequency<br />

both in the sample of males and in the sample of females (Tabele 3). The exception is<br />

the convexity of of warts in head region (in males the largest relative frequency have<br />

the warts which are indented, and with females warts are very protuberant) and the<br />

appearance of thornlike endings of ventral side of head region (most frequently weakly<br />

expressed in males and averagely expressed in females). The table of relative<br />

frequency of the conditions indicates that with females the variability of condition is<br />

higher than with males.<br />

By a correspondant analysis we have monitored the impact of qualitative traits<br />

on ordination of specimens of both sexes. The first corresponding axis has separated<br />

24.69% of variability, and the other one 17.03%. There is no clear sex separation<br />

(Figure 1). The sample of males indicates an uniformity in respect of monitored traits.<br />

Only one male has been separated during the second coresponding axis from the<br />

„main cloud” of male specimens on basis of two traits (11b and 12b) (Figure 2). One<br />

may observe a higher variability in scope of the sample of females. Traits 1c, 4b and<br />

5a separate two females along the first correspoding axis from other females, where it<br />

should be mentioned that these two traits as well as the traits 2a, 3b and 6b influence<br />

separating of females from males (Figures 1 and 2).<br />

The significance of this paper is in presenting for the first time the analysis of a<br />

larger number of morphometric and qualitative characters of population of the species<br />

<strong>Bufo</strong> <strong>bufo</strong> from Biogradsko Lake. These data make the grounds for further<br />

investigations of the populations of the species <strong>Bufo</strong> <strong>bufo</strong> both from Biogradsko Lake<br />

and the populations of this species from the territory of entire ontenegro.


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Natura Montenegrina, 6/2007<br />

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Natura Montenegrina, 6/2007

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