Herpetologica Romanica Vol. 1, 2007, pp.

17-21

The trophic spectrum of a Bombina bombina (Linnaeus 1761) population

from the Cermei region (Arad County, Romania)

Nicoleta-Réka RADU1,*, Horia V. BOGDAN2,

Zsolt BATA2, Claudia POPA2, Eva G. OSVAT-SZABO2

1 Bsc student, University of Oradea, Faculty of Sciences, department of Biology, Oradea, Romania
1 Msc student, University of Oradea, Faculty of Sciences, department of Biology, Oradea, Romania
* Corresponding author e-mail address: reka_nicoleta_radu@yahoo.com

Abstract: Our study took place in May 2006 and consisted in two outings. For this study we analyzed 90
Bombina bombina specimens, out of which 47 were females and 43 were males. In the analyzed stomach contents
we managed to identify vegetal fragments, shad skin and animal preys. The animals preys that we manage to
determine summed a total of 1040 and were attributed to 36 categories. We observed that, along our study, both
the males and the females preferred aquatic Izopods, Coleopterans, Hymenoptera-Formicidas, Araneids,
Aphids and Diptera-Brahicerans. The diversity of the preys in the post-hibernating period presents high values
(females 2.39, males 2.35) due to the fact the fire-bellied toads seek to regain the energy lost while hibernating.
In the breeding period, a lower diversity is noted at the females (H=1.64) than the males (H=1.98), the latter
consuming a larger quantity of energy while searching for females and singing.

Key words: Bombina bombina, feeding, males, females

Introduction

Due to the fact that amphibians feed both in the water and on land they resort to feeding from
different sources. A diverse utilization of these sources by the population’s individuals, sexually different,
could be a consequence of the sexual dimorphism of the amphibians (Shine 1989). This is why some
differences can appear in matter of feeding (dissimilar preys). Studies about the feeding of other Bombina
bombina populations were undertaken both by foreign researchers (ex. Gocharenko et al. 1978, Tertyshnikov
& Goroyava 1982, Ščerbak & Ščerban 1980) as well as Romanian ones (ex. Cogălniceanu et al. 2000b, Sas et
al. 2003, 2004 a).
The objective of our study was to establish if there are any differences between the trophic spectrum of
males and females of a Bombina bombina population.

Material and Methods

Our study took place in May 2006 and consisted in two outings. In the months of April and June we also made several
trips to the area, but the presence of the red-bellied toads could not be noted because of the unfavorable temperatures. Thus, the
first time we took samples corresponds to the period the toads get out of their hibernation and the second sampling period
corresponds to their mating period. For this study we analyzed 90 Bombina bombina specimens, out of which 47 were females
and 43 were males (Tab.1).
The habitat of our population is represented by two semi-temporary ponds from near the Cermei locality, Arad County,
Romania. The first pond is a considerably bigger than the second one, measuring more than 300 m2 with a thick and tall
vegetation and with the water level reaching even over 1m in the deepest sections. We’ve observed the presence of both
invertebrates as well as vertebrates here (the latter being represented by fish). The second puddle is at about 25 m from the first
and it’s situated alongside the road. It’s a lot narrower, with rich vegetations on the side and with the water level notably lower
than in the big pond. Because of the increase in temperature in that period, at our second outing the water level dropped
significantly in both ponds.
The red-bellied toads were captured either with some square drags or simply by hand after which put in large buckets
filled with water from their own environment. The stomach contents were obtained using the stomach flushing method (see in:
Cogălniceanu 1997). We used a syringe on top of which we added a small plastic tube with the diameter of 2-4 mm and the
length of 6-10 cm. The water pressed by the syringe helps to eliminate the stomach contents which are them collected in Petri
dishes. The samples obtained were conserved with 4% formalin and stocked in air-tight test-tubes that were labeled with the
date and the sex of the toad. The collected samples were then analyzed in the laboratory, at a binocular microscope, thus
determining the preys with the help of the specialty literature (Moczar et al., 1950; Radu & Radu 1967; Ionescu & Mureşan
1971). The trophic diversity (H) was determined by calculating the Shannon Weaver index (1949) for both males and females.
Herpetol. Rom, 1,
2007, Romania
18 N.R. Radu et al.

Results

In the analyzed stomach contents we managed to identify vegetal fragments, shad skin and animal
preys (Tab.1, 2). The vegetal fragments were found in high ratios all along our study; thus, in the first period
the females consumed vegetation in amounts of 72.73% and the males 47.83% of the cases. In the second part
of our study, the differences are more or less insignificant: females – 52% and males – 55%. In what concerns
the frequency of the shad skin, in the first half of our study the differences between the sexes were very
small: 36.36% for the females and 34.78% for the males. We observed however a major dissimilarity towards
the end of our study when the females consumed only 8% while the males 35%.

Table no.1 The frequency of occurrence of stomachs with vegetal fragments and shed-skin
Number of frogs sampled is shown in parentheses. (F-females, M-males)

05.05 21.05
F (22) M (23) F (25) M (20)
% of vegetal fragments 72.73 47.83 52 55
% of shed skins 36.36 34.78 8 35

The animals preys that we manage to determine summed a total of 1040 and were attributed to 36
categories (Tab.2). We’ve separated the larvae from the adults at Coleopterans and Diptera-Brahicera as well
as the aquatic and terrestrial forms of the Gastropods and Isopods because we considered them to be
different in matter of their mobility and their environment of origin. We observed that, along our study, both
the males and the females preferred aquatic Izopods, Coleopterans, Hymenoptera-Formicidas, Araneids,
Aphids and Diptera-Brahicerans. Other categories of preys were consumed in lesser amounts.

Table no.2 The percent abundance of the most important prey categories.
Number of frogs sampled is shown in parentheses.
(F-females, M-males, aq-aquatic, t-terrestrial, L-larvae, ad-adults)

05.05 21.05
F (22) M (23) F (25) M (20)
Lumbricida 1.58 4.93 - -
Gasteropoda [aq] 1.58 - 4.83 5.26
Gasteropoda [t] 5.79 0.70 1.74 -
Araneida 7.37 4.93 1.35 5.26
Izopoda [aq] 40.00 23.94 43.82 18.42
Izopoda [t] 6.84 1.41 1.35 0.53
Colembole - 5.63 - -
Homoptera-Afidina 0.53 19.72 0.97 4.74
Heteroptera [t] 0.53 1.41 - 1.58
Coleoptera-Dytiscida [L] 1.05 3.52 0.39 1.58
Coleoptere [A] 7.89 9.15 27.03 38.95
Tricoptera [L] 1.58 4.23 - -
Nematocera [A] 5.79 9.86 - 2.11
Brahicera [L] 2.63 - - -
Brahicera [A] 3.16 2.82 0.97 2.11
Hymenoptera 0.53 - 0.77 3.68
Hymenoptera-Formicidae 6.84 4.23 15.06 13.68
Others 6.32 3.52 1.74 2.11

Herpetol. Rom, 1, 2007

The trophic spectrum of a Bombina bombina (Linnaeus 1761) population 19

The diversity of animal preys (Tab.3) is bigger in the first period at both males (2.55) and females
(2.39), stage that we’ve correlated with the end of their hibernation. In the second half of the study we
observed a smaller diversity at females (1.64) than at males (1.98), period considered to be their mating
season, when males need larger quantities of energy used in searching their females or in “singing”.

Table no.3 The feeding diversity. (F-females, M-males)

05.05 21.05
F (22) M (23) F (25) M (20)
Diversity (H-Shannon Weaver) 2.39 2.55 1.64 1.98

The amount of aquatic and terrestrial preys (Tab.4) revealed a relative balance when it comes to the
females, during the entire research (45.79% / 54.21%, and 49.42% / 50.58% respectively) while males stand
out a lot with their high amounts of terrestrial prey (66.20% and 73.16% respectively).

Table no.4 The percent abundance of aquatic and terrestrial preys (F-females, M-males)

05.05 21.05
F (22) M (23) F (25) M (20)
% aquatic preys 45.79 33.8 49.42 26.84
% terrestrial preys 54.21 66.2 50.58 73.16

The variation of the feeding intensity presented some differences (Tab.5). In the period correlated
with the end of their hibernation, the average number of preys/individual is bigger at females (8.64%) than
at males (6.17%), while the maximum number of preys/individual is of 18 at females and 28 at males.
During their mating season, the average number of preys/individual reached a staggering 20.7% at females,
more than twice the one of the males (9.5%). The females presented a maximum number of preys/individual
of 115 and the males only 15.

Table no.5 The number of preys, the average and maxim number of preys / individual
(F-females, M-males)

05.05 21.05
F (22) M (23) F (25) M (20)
No. of preys 190 142 518 190
Average 8.64 6.17 20.7 9.5
Maxim 18 28 115 15

Discussions

Generally the food of amphibians consists in different invertebrate groups. The consumption of
vegetal fragments in the amphibian’s case is considered by many authors to be involuntary, being
swallowed together with the prey (Whitaker et al., 1977). This aspect is also suggested by their presence
throughout all our study, their ingestion being in direct correlation with the abundance of the preys in the
habitat. The post-hibernation period (the first sampling) revealed higher vegetation consumption by the
females (72.73%) than the males (47.83%) because of the need to accumulate energy in a relatively short
amount of time. These also have implications in the breeding period and during spawning (the second
sampling). During their breeding period, there were little dissimilarities between the sexes in means of
vegetation consumption (52% for females and 55% for males). Vegetal remains were frequently encountered

Herpetol. Rom, 1, 2007

20 N.R. Radu et al.

in the stomach contents of other amphibian species as Rana arvalis (Covaciu-Marcov et al., 2001, 2002a), Rana
ridibunda (Covaciu-Marcov et al., 2000) and Lyciasalamandra luschani fazilae (Çiçek et al. 2007) or at the
Bombina hybrids (Sas et al. 2005).
The shad skin fragments were present with about constant frequencies between the two sexes
during the entire study, with the exception of the breeding period when they represent 8% of the female’s
diet. These shad skin represent a source of proteins and therefore their consumption contributes to the
growth of the overall protein level of the amphibian’s organisms. Thus we considered them to be ingested
intentionally. In the specialty literature, there are also other similar cases described at the Rana dalmatina
(Aszalos et al. 2005), Rana arvalis (Sas et al., 2003b), Bombina bombina (Sas et al., 2003a) and Triturus cristatus
(Cicort-Lucaciu et al. 2005) species, where some shad skin comes from other individuals from the same
population as well.
The most important category from the stomach contents is obviously represented by animal preys,
knowing that adult amphibians are predators (Cogălniceanu et al., 2000). The number of the prey taxa from a
period is in direct correlation with the environment’s conditions, the thermal variations having a negative
effect on both the preys and the predators, influencing the trophic offer and therefore the toad’s trophic
spectrum. The most important categories preferred by the investigated Bombina bombina population are
represented by the aquatic Izopoda, Coleoptera, Araneida and Hymenoptera-Fomicida taxa. These are
present along the entire study in large amounts. The aquatic Izopoda and the Formicida having a very small
size and a gregarious way of life are very accessible for feeding. The Coleopterans also represent an
important part of the diet of other species of amphibians, too, like: Rana arvalis (Covaciu Marcov et al., 2003),
Rana temporaria (Houston 1973), Bombina bombina (Kovacs & Torok, 1997; Medvedev 1974; Goncharenko et
al., 1978) or Bombina variegata (Kuzmin 1990).
As a preferential particularity especially for the females some other taxa appear but in smaller
amounts: aquatic and terrestrial Gastropods, terrestrial Izopoda and Brahicera larvae. The males preferred
Colembolans, Aphids, Heteroptera, Dytiscida larvae and Trichoptera and Nematocera larvae. Gamarida,
Miriapoda, Efemeroptera, Odonata larvae, Cicada and Lepidoptera were identified with lower amounts,
probably consumed auxiliary, with little importance to the overall trophic spectrum of the fire-bellied toads.
The high diversity of the preys in the post-hibernating period presents high values (females 2.39,
males 2.35) due to the fact the fire-bellied toads seek to regain the energy lost while hibernating. In the
breeding, a lower diversity is noted at the females (H=1.64) than the males (H=1.98), the latter consuming a
larger quantity of energy while searching for females and singing. The females, because of their need to
conserve the energy, consumed both aquatic and terrestrial preys in an almost balanced way (aquatic 49.42 /
terrestrial 50.58). The males preferred the terrestrial sources of energy in amounts of double or even triple
higher than the aquatic ones (66.20% and 73.16% respectively).
The feeding intensity presented some variations during our study. Thus, in the first period the
maximum number of preys/individual at males is of 28 while in the second part, 15. When it comes to the
females, the first period recorded a maximum number of preys/individual of 15 and a staggering 115 in the
second. This value is due to the presence of the aquatic Izopoda in that period. The average number of
preys/individual rises at females from one period to the other (8.67 to 20.7) because of the necessity to
accumulate energy in a short amount of time, essential for the spawning as well as biologically. This value
rises at males, too, from 6.17 to 9.5 during the mating season. The obtained values of the average number of
preys/individual are closer to the ones resulted in the case of the “sister-species” Bombina variegata (Kuzmin
1990).

Acknowledgements. At this way we would like to thank to dr. S.D. Covaciu-Marcov (University of Oradea, Romania) for reviewing of the
manuscript. We would like to thank to Istvan Sas (University of Oradea, Romania) for helpful comments on an early version of the manuscript.
We'd also like to thank D. Cupşa (University of Oradea) for the assistance in prey animals determination. We would also like to thank to
Annamaria Toth, Marius Groza and to other students from Herpetological Club - Oradea for their priceless help in the field.

References

Aszalós, L., Bogdan, H.V., Kovács, É.H., Peter, V.I. (2005): Food composition of two Rana species on a forest habitat (Livada Plain,
Romania). North-Western Journal of Zoology 1: 25-30.
Çiçek, K., Tok, C.V., Mermer, A., Tosunoğlu, M., Ayaz, D. (2007): Food Habits of the Lycian Salamander, Lyciasalamandra luschani
fazilae Başoğlu and Atatür, 1974: Preliminary data on Dalyan Population. North-Western Journal of Zoology, 3:1-8

Herpetol. Rom, 1, 2007

The trophic spectrum of a Bombina bombina (Linnaeus 1761) population 21

Cicort-Lucaciu, A.Şt., Ardeleanu, A., Cupşa, D., Naghi, N., Dalea, A. (2005):The trophic spectrum of a Triturus cristatus (Laurentus
1768) population from Plopiş Mountains area (Bihor County, Romania). North-Western Journal of Zoology 1: 31-39.
Cogălniceanu, D. (1997): Practicum of Amphibian ecology – methods and technics for studying the Amphibians ecology. Ed.
Universităţii din Bucureşti, Bucharest. (in Romanian)
Cogălniceanu, D., Palmer, M., W., Ciubuc, C. (2000a): Feeding in Anuran communities on islands in the Danube foodplain.
Amphibia – Reptilia, 22: 1–19.
Cogălniceanu, D., Aioanei, F., Bogdan, M. (2000b): Amfibienii din România. Determinator. Ed. Ars Docendi, Bucuresti: 1-99
Covaciu–Marcov, S.D., Cupşa, D., Ghira, I. (2000): Trophical spectrum of a Rana ridibunda Pallas 1771 population from Cefa (jud.
Bihor, Romania). Universitatea din Bacău, Studii şi Cercetări, Biologie, 5: 107–113.
Covaciu–Marcov, S.D., Cupşa, D., Sas, I. (2001): The study of the trophic spectrum of two populations of Rana arvalis Nills 1842
from the north of Bihor county. Analele Univ. ”Al. I. Cuza” Iaşi: 160–171
Covaciu–Marcov, S. D., Cupşa, D., Sas, I. (2002): The study of the trophic spectrum of two populations of Rana arvalis Nills 1842
from the north of Bihor county. Analele Ştiinţifice ale Univ. ”Al. I. Cuza” (serie nouă), Iaşi, Secţiunea I, Biologie Animală, Tomul
XLVIII: 160–171
Covaciu–Marcov, S. D., Cupşa, D., Sas, I., Telcean, I. (2003): Trophical spectrum of a Rana arvalis Bihor County, Romania. Studii şi
Comunicări, Seria Ştiinţele Naturale, I – II, 2001 – 2002: 170–181. (in Romanian)
Goncharenko, A., E., Koval, N., F., Tkachenko, A., K. (1978): Data on the ecology of the red - spotted fire-belied toad Bombina
bombina in the central part of the Yuzhiny Bug River Basin – Vestn. Zool., 2: 46–50 (in Russian)
Guidali, F., Scali, S., Carettoni, A., Fontaneto, D. (1999): Feeding habits, niche breadth and seasonal dietary shift of Rana dalmatina
in northern Italy. Current studies in Herpetology, Miaud C. & Guyetant R. (eds), Le Bourget du Lac / France, S. E. H.: (161–166)
Gunzburger, S. M. (1999): Diet of the Red Hills Salamander Phaeognatus hubrichi. Copeia, 1992(2): 523–525.
Houston, W. W. K. (1973): The food of common frog, Rana temporaria, on high moorland on northern England. J. Zool. Lond. 171:
153–165
Ionescu, M. A., Lăcătuşu, M. (1971): Entomologie, Bucureşti – Ed. Didactică şi Pedagogică.
Kovacs, T., Torok, J. (1997): Detemination of minimum sample size to estimate diet diversity in Anuran species. Herpetological
Journal, Vol. 7: 43–47.
Kuzmin, S. L. (1990): Trophiv nivhe overlap in syntopic postmetamorphic amphibians of the Carpathian Mountains (Ukraina :
Soviet Union) – Herpetozoa, 3 : 13–24
Medvedev, S. I. (1974): Data on study of amphibian food in the region of the middle flow of the Seversky Donets River USSR –
Vest. Zool., 1: 50–59 (in Russian with English summary)
Moczar, L., Balogh, J., Dudich, E., Ehik, Gy., Fejervary, G., Gyorfi, J., Loksa, I., Soos, A., Stohl, G., Warga, K., Woynarovich, E.
(1950): Allathatarozo. Vol. I, Vol. II, Kozoktatasugyi kiadovalalat, Budapest.
Radu, G. V., Radu, V. V. (1967): Zoologia nevertebratelor, vol. 2. Ed. Didactică şi Pedagogică: 1-708
Sas, I., Covaciu–Marcov, S. D., Cupşa, D., Schirchanici, A., Aszalos, L. (2003a): Research upon the trophical spectrum of a Bombina
bombina (L. 1761) population from Resighea region (county of Satu – Mare, Romania). Muzeul Olteniei Craiova, Oltenia, Studii şi
Comunicări Ştiinţele Naturii, 19 : 183–188. (in Romanian with English abstract)
Sas, I., Covaciu–Marcov, S. D., Cupşa, D., Schirchanici, A., Peter, V. I. (2004a): The study of the trophic spectrum of Bombina
bombina (Linnaeus 1761) populations in the Ier Valley area (county of Bihor, Romania). Nymphaea, Folia naturae Bihariae,
Oradea, 31 : 91–109.
Sas, I., Covaciu–Marcov, S. D., Cupşa, D., Aszalos, L., Kovacs, E. H., Telcean, I. (2003b): Data about the trophic spectrum of a
population of Rana arvalis of the Andrid Area (Satu – Mare, Romania). Studii şi Cercetări, Biologie 8, Bacău: 216 – 223
Sas, I., Covaciu–Marcov, S. D., Cupşa, D., Schirchanici, A., Aszalos, L. (2003a): Research of the trophical spectrum of a Bombina
bombina population from Satu – Mare County. Muzeul Olteniei Craiova, Oltenia, Studii şi Comunicări Ştiinţele Naturii, Vol.
XIX: 183 – 188. (in Romanian)
Sas, I., Covaciu-Marcov, S.D., Pop, M., Ile, R.D., Szeibel, N., Duma, C. (2005): About a closed hybrid population between Bombina
bombina and Bombina variegata from Oradea (Bihor county, Romania). North-Western Journal of Zoology, Vol.1: 41-60
Scerbak, N. N., Scerban, N. I. (1980): Amphibians and Reptiles of Ukranian Charpatians. Kiev, Ed. Nankova Dunka: 1-266. (in
Russian)
Shine R., 1979. Sexual selection and sexual dimorphism in the Amphibians. Copeia, 2, p: 297 – 306.
Tertyshnikov, M. F., Gorovaya, V. I. (1982): New data on the occurrence and ecology of the red – spotted fire – bellied toad Bombina
bombina in the Central Ciscuacasia USSR. – Vestn. Zool., 1: 80–83 (in Russian)
Whitaker, J., Rubin, O. D., Munsee, J. R. (1977): Observation on food habits of four species of Spadefoot toads, genus Scaphiopus.
Herpetologica 33 : 468–47

Herpetol. Rom, 1, 2007