Food Composition of Some Low Altitude Lissotriton Montandoni (Amphibia, Caudata) Populations from North-Western Romania

Arch. Biol. Sci., Belgrade, 62 (2), 479-488, 2010 DOI:10.2298/ABS1002479C

FOOD COMPOSITION OF SOME LOW ALTITUDE LISSOTRITON MONTANDONI (AMPHIBIA, CAUDATA) POPULATIONS FROM NORTH-WESTERN ROMANIA

S. D. COVACIU-MARCOV1*, A. Ş. CICORT-LUCACIU1, I. SAS1, DIANA CUPŞA1, ÉVA H. KOVÁCS1 and SÁRA FERENŢI1

1 University of Oradea, Faculty of Sciences, Department of Biology, Oradea, 410087, Bihor County, Romania

Abstract – The diet of some populations of Lissotriton montandoni from north-western Romania is composed of prey belonging to 20 categories. The food components of the Carpathian newts are similar to those of other species of newts. Most of the prey are aquatic animals, but terrestrial prey also has a high percentage abundance. The consumed prey categories are common in the newts’ habitats as well, but in natural ponds the prey item with the highest abundance in the diet is not the most frequent one in the habitat. Thus, although the Carpathian newts are basically opportunistic predators, they still display a certain trophic selectivity.

Keywords: Lissotriton montandoni, low altitude, feeding, Romania

UDC 597.6 (498-16):591.526

INTRODUCTION between an animal and its environment (Kenett & Tory 1996). Quantitative information about the role Lissotriton montandoni is endemic in the Tatra of amphibians in ecosystems is extremely important Mountains and in some areas of the Carpathian in their capacity as consumers both in aquatic and Mountains (Cogălniceanu 1997). A large part of its terrestrial habitats (Whiles et al., 2006). In Romania distribution area is in Romania, the Carpathian newts there are no data about the feeding of Carpathian being present in the eastern Carpathians and in a very newts. A study on this subject was realized in Uk- small area of the southern Carpathians (Cogălniceanu raine but was only on a few individuals and at an et al., 2000, Covaciu-Marcov et al 2009). In Romania it ordinary altitude for the species (Kuzmin 1990). is present at altitudes higher than 500 m (Iftime 2005), Identification of the low altitude populations from but recently it has been recorded in the west of the north-western Romania raises the problem of the country at 200 m (Covaciu-Marcov et al., 2007). The manner in which the species can find the necessary species is considered vulnerable, being affected by the ecological conditions at those altitudes and if the deterioration of habitats (Iftime 2005). However, in trophic requirements are satisfied. Romania studies concerning the species’ biology and ecology are missing. Lack of such knowledge is likely The purpose of our study lies in establishing the to affect any program for the protection of the species diet composition of some low altitude populations of because understanding its habitat requirements and L. montandoni from north-western Romania. We will habitat use is a major challenge in conservationist address the following: 1) knowledge of food biology (Hartel et al., 2006) and Europe is still in need composition, 2) comparison between diet composi- of information about Romanian biodiversity (Hartel tion and prey availability, as was recently realized in a et al., 2008). study on the benthonic fauna from the habitats of the Feeding is an essential indicator of the position newts (Cupşa et al., 2007), and 3) establishing trophic of a species in an ecosystem as it is the primary link differences between the sexes, habitats and periods.

479 480 S. D. COVACIU-MARCOV ET AL.

Table 1. The percentage of empty stomachs, feeding intensity, origin of the preys, food diversity (Shannon Wiener index) and similarity (Sorensen index), and frequency of vegetal fragments, shed skin,eggs and minerals (M-males, F-females, IV-April, V-May)

Pond I Pond II

IV.09.2005 IV.23 2005 V.5.2005 IV.09.2005 IV.23 2005 V.5.2005

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

% empty stomachs 42.86 83.33 - 12.5 14.29 25 8.69 - - - 22.73 9.09

The maximum no. of 2 1 5 5 7 5 8 9 7 11 5 5 prey/individual

The average no. of prey 0.85 0.16 3.5 2 2.42 2.75 3.60 4.84 3.90 5.09 1.5 2

% Aquatic preys 66.66 100 80.95 93.75 88.24 81.82 100 98.42 80.48 85.05 87.87 81.82

% Terrestrial preys 33.33 - 19.05 6.25 11.76 18.18 - 1.58 19.52 14.95 12.13 18.18

Shannon Wiever index (H) 0.38 - 0.98 0.86 0.36 0.48 0.14 0.41 1.11 1.02 1.07 1.39

Sorrensen index 0.16 - 0.4 0.29 0.56 0.33 0.66 0.78 0.49 0.55 0.29 0.12

Vegetal fragments 71.43 66.67 66.67 87.50 100 50 52.17 46.15 61.90 50 72.73 72.73

Shed skin 28.57 100 16.67 37.50 14.29 50 21.74 15.38 9.52 10 22.73 9.09

Eggs - 16.67 - - - - - 7.69 - - 4.55 -

Minerals ------4.35 - - - 9.09 9.09

existence to the mines. It is an excavation made close MATERIALS AND METHODS to a pipe from the mine. It has a length of 2 m, a width The study was carried out during April-May 2005. of 1 m and a depth of 1.5 m, the water level is One hundred and seventy nine Carpathian newts (101 relatively constant and the turbidity high. The males and 78 females), captured from two habitats, vegetation is scruffy, consisting of a small amount of were analyzed.. The newts were captured from an area rushes on the shore. Near the habitat there is a located in the utmost north-western part of Romania, coniferous plantation and then a beech forest. Pond II on the territory of Turţ Village, 10 km from the is natural and permanent, situated at the edge of a border with Ukraine. Near the locality were the mines natural beech forest and at the base of a slope. It has a from Turţ (Turţ Băi) but at present the area has only a large surface, being a pooling area established at the few houses and abandoned mines. Thus, the current level of a brook. The pond is 13 m long and 2 m wide, anthropogenic impact is reduced, but the effects of but it is surrounded by marshy areas which extend in activities from the past are still evident. In the area rainy periods. The depth of the water is maximum there are buildings and abandoned equipment, heaps 0.75 m, the bottom is covered by dead leaves and the of barren rock and the brook is polluted even now due shore by amphibious vegetation. to the heaps of barren rock and decantation ponds. The newts’ habitats are at 250 m altitudes and at about The newts were captured with the help of nets 500 m from each other, near an asphalted road which attached to long metallic handles or with a square is little used. dredge. The stomach contents were collected using the stomach flushing method (Solé et al., 2005), and The analyzed habitats will be referred to as Pond I the newts subsequently released. Samples were and Pond II. Pond I is an artificial one that owes its stored in test tubes, preserved with formaldehyde FOOD COMPOSITION OF SOME LOW ALTITUDE LISSOTRITON MONTANDONI (AMPHIBIA, CAUDATA) 481 and examined in the laboratory. Food composition ning of the aquatic period, increasing subsequently was evaluated by percentage abundance (%A) and and decreasing again at the end. Of the 20 prey frequency of occurrence (%f). Dietary diversity was categories, 7 were consumed in both habitats (Table estimated with the Shannon-Wiener (1949) diversity 2). In Pond I none of the prey categories was con- index (H), and dietary similarity with the Sorensen stantly used in each period. However, in the third index (Chao et al., 2005). The Kruskal-Wallis and habitat, 3 prey categories (Gastropoda, Epheme- Mann Whitney U test was applied for comparison of roptera and Plecoptera larvae) occurred in all sam- the data sets (Kruskal & Wallis 1952). pling periods, plecopteran larvae being present in the stomach contents of both sexes in every period. RESULTS The percentage abundance and frequency of occurrence of prey exhibit variations usually both bet- Not all of the studied Carpathian newts had sto- ween periods and sexes. mach contents (Table 1). The individuals that did Generally, the prey categories with high percen- not feed make up a relatively important part of the tage abundance also had a significant frequency of total populations and were especially numerous in occurrence. In Pond I the most important prey ca- the artificial habitat (Pond I). The highest number tegories are different comparing the three periods, of newts without stomach content was caught at the but in Pond II plecopteran larvae exhibit very high beginning and at the end of the aquatic period. In values both for percentage abundance and frequency the middle of the period such individuals were mis- of occurrence in all sampling events (Table 2 and 3). sing or were very rare. The number of prey/individuals exhibits great differences both between habi- The plant materials and molted skins of tats and between periods and sexes. The lowest va- amphibians were constantly consumed in both habitats lues, both for the maximum and average number of and by both sexes. Eggs were identified in the stomach prey/individual were recorded in the artificial ha- contents of a few newts from both habitats but only in bitat (Pond I). The same was true of the occurrence certain periods. Inorganic fragments occur accidentally of empty stomachs: the least prey was consumed at and exclusively in Pond II and only in some of the the beginning of the period of study. The number of periods. Dietary diversity is variable between sexes and prey rose towards the middle of the aquatic period habitats, but these variations follow the pattern and then decreased again (Table 1). indicated by the empty stomachs and the number of prey/individuals. Thus, food diversity is lower for Pond Five categories of stomach contents were iden- I than for Pond II, as well as at the beginning of the stu- tified in the case of the Carpathian newts that had dy (Table 1). fed: 1) prey of animal type, 2) remains of plant materials, 3) fragments of molted skin, 4) amphi- The results of the Mann Whitney U test show bian eggs and 5) inorganic particles. The two popu- that the differences between the two sexes and the lations of L. montandoni had consumed a total two habitats are not significant (P>0.05). For number of 462 prey belonging to 20 prey categories. analyzing the differences between the periods we From the stomach contents of the newts captured used the Kruskal Wallis test, its results showing in Pond I only 72 prey items were identified and the insignificant variations between different months remaining 390 prey items were collected from the (H=5.67, df.=2, P>0.05). newts from Pond II. The diet of the population from Pond I consisted of 11 prey categories and DISCUSSION that from Pond II comprised 16 prey categories. In both habitats the number of the consumed prey ca- L. montandoni feeds less intensely than other species tegories displayed the same evolution as the num- of newts found in Romania (David et al., 2008a, b, ber of prey/individuals, and was lowest at the begin- Dobre et al., 2007, Ovlachi et al., 2007). The 482 S. D. COVACIU-MARCOV ET AL.

Table 2. The amount of prey taxa (M-males, F-females, IV-April, V-May, t-terrestrial, aq-aquatic, ad-adult, L-larvae)

Pond I Pond II

IV.09.2005 IV.23 2005 V.5.2005 IV.09.2005 IV.23 2005 V.5.2005

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

Annelida-Oligochaeta - - - 6.25 - - - 1.58 8.53 6.54 - -

Gasteropods- snail ------9.52 6.09 3.73 3.03 4.54

Lamellibranchiata ------13.63

Crustaceans-Gammarida - - 9.52 6.25 ------

Crustaceans-Isopods (t) ------6.09 3.73 3.03 4.54

Arachnida-Araneida - - - - - 9.09 - - 1.21 - - -

Arachnida-Pseudoscorpionida - - 19.04 ------

Epfemeroptera L (aq) ------1.58 2.43 1.86 9.09 9.09

Plecoptera L(aq) ------96.38 87.3 67.07 71.93 60.60 36.36

Plecoptera-ad. - - - - 5.88 - - - 2.43 - 9.09 -

Trichoptera L (aq) ------3.61 - - 0.93 3.03 -

Dermaptera-Blattoidea ------0.93 - -

Homoptera-Afidina ------1.21 0.93 - -

Coleoptera-ad. ------4.54

Coleoptera L. Dytiscida (aq) 66.66 100 ------

Diptera-Nematocerans-L (aq) - - 52.38 43.75 - - - - - 6.54 3.03 -

Diptera-Nematocerans-ad. - - - - 5.88 ------4.54

Diptera-Brachyicera-ad. - - - - 88.23 81.81 - - 4.87 1.86 - 4.54

Hymenoptera-Formicida 33.33 - - - - 9.09 ------

Anuran tadpoles - - 19.04 43.75 - - - - - 0.93 9.09 18.18 number of empty stomachs is very high and they et al., 2007) due to unfavorable weather conditions - are present during almost the entire aquatic period, mainly low temperatures which affect both the and the number of prey/individuals is low. The predators and especially the prey (Guidali et al., feeding intensity of newts is lower at both the 1999; Covaciu-Marcov et al., 2003). This explains beginning and the end of the aquatic period the feeding rate from the first period when indeed (Covaciu-Marcov et al., 2003, Cicort-Lucaciu et al., the temperatures were low. 2006) due to the adaptation to this environment and then to the loss of it. Usually, amphibians had a Generally, it is considered that the situations in low rate of feeding intensity at the beginning of which the entire population had fed indicate opti- their activity period (Hirai & Matsui 2000; Kovács mal feeding conditions (Sas et al., 2009). Thus it FOOD COMPOSITION OF SOME LOW ALTITUDE LISSOTRITON MONTANDONI (AMPHIBIA, CAUDATA) 483

Table 3. The frequency of the prey taxa (M-males, F-females, IV-April, V-May, t-terrestrial, aq-aquatic, ad-adult, L-larvae)

Pond I Pond II

IV.09.2005 IV.23 2005 V.5.2005 IV.09.2005 IV.23 2005 V.5.2005

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

Annelida-Oligochaeta - - - 12.50 - - - 7.69 23.81 25.00 - -

Gasteropods- snail ------23.08 23.81 15.00 4.55 9.09

Lamellibranchiata ------9.09

Crustaceans-Gammarida - - 16.67 12.50 ------

Crustaceans-Isopods (t) ------23.81 15.00 4.55 9.09

Arachnida-Araneida - - - - - 25.00 - - 4.76 - - -

Arachnida-Pseudoscorpionida - - 50.00 ------

Epfemeroptera L (aq) ------7.69 9.52 10.00 9.09 18.18

Plecoptera L(aq) ------82.61 100.00 90.48 100.00 59.09 45.45

Plecoptera-ad. - - - - 14.29 - - - 9.52 - 4.55 -

Trichoptera L (aq) ------13.04 - - 5.00 4.55 -

Dermaptera-Blattoidea ------5.00 - -

Homoptera-Afidina ------4.76 5.00 - -

Coleoptera-ad. ------9.09

Coleoptera L. Dytiscida (aq) 42.86 16.67 ------

Diptera-Nematocerans-L (aq) - - 66.67 37.50 - - - - - 15.00 4.55 -

Diptera-Nematocerans-ad. - - - - 14.29 ------9.09

Diptera-Brachyicera-ad. - - - - 85.71 75.00 - - 14.29 10.00 - 9.09

Hymenoptera-Formicida 14.29 - - - - 25.00 ------

Anuran tadpoles - - 50.00 62.50 - - - - - 5.00 9.09 18.18 seems that in the habitats from Turţ the Carpathian at lower altitudes than in other areas from Romania newts do not have favorable feeding conditions or (Covaciu-Marcov et al., 2008, Gherghel et al., 2008). are possibly less adapted to forage in the aquatic environment compared to other newt species. This In Pond I the feeding conditions are even more might be a consequence of its adaptation to higher difficult due to the anthropogenic impact on the areas where difficult conditions lead to the shor- habitat. As this pond is artificial it does not have a tening of the aquatic period and influence feeding well-defined zoocenosis, and thereby no potential in this environment. Nevertheless, the above-men- preys. This fact is also supported by the benthonic tioned suppositions cannot be stated without reser- fauna of the two habitats, there being only 2 taxa in vations because at Turţ L. montandoni is recorded Pond 1 compared to 9 in Pond II (Cupşa et al., 484 S. D. COVACIU-MARCOV ET AL.

2007). These data confirm that the trophic diversity sition according to the abundance of prey from the depends on the quality of the habitat inhabited by habitat. amphibians (Kovács et al., 2007). The anthropogenic impact on the population of the artificial habitat The differences between the two sexes are not becomes obvious, knowledge about feeding being significant, but these differences affect the feeding crucial for understanding the effects of habitat mo- intensity as well as the number, percentage abun- dification on amphibians (Anderson et al., 1999). dance and frequency of occurrence of prey items. In Pond III the feeding intensity is always higher in The changes in time of the feeding intensity females; they consume more prey categories (Table follow the evolution of climatic conditions. The 2). This was predictable since in the breeding increase of temperature increases feeding intensity period the males, even hungry, are more interested and the newts consume more prey. A similar ten- in the nuptial parade than in feeding compared to dency was previously reported for other species of the females (Ranta et al., 1987). In other amphibian newts (Covaciu-Marcov et al., 2003), the differences species the feeding of females in the breeding pe- being determined by the variation of prey abun- riod was also more intense and they consumed mo- dance between different periods (Fasola & Canova re large sized prey than the males (Juncá & 1992, Denoël & Andreone 2003). However, the Eterovick 2007). Nevertheless, in Pond I, apart from maximum number of prey/individuals (only 11 the last period, the situation is reversed, probably as items) is significantly lower than for other species a further consequence of the artificiality of the pond of newts (Cicort-Lucaciu et al., 2007, David et al., which alters the results due to the reduced prey 2008b, 2009). This is a consequence of the con- availability. sumption of relatively large sized prey. From the diet composition of the L. montandoni populations Although apparent, not even the differences small prey (eg. Crustacea: Copepoda, Ostracoda or between habitats are statistically significant. It is Cladocera) which are responsible for the high num- clear that Pond I does not provide optimal trophic ber of prey in the case of other species of newts, are conditions for newts. Their feeding is deficient, absent. But this situation is an outcome of the con- which is evident from the lower percentage abun- ditions from the two habitats from which the mic- dance of aquatic prey which reflects the lack of the rocrustaceans are missing (Cupşa et al., 2007). Pro- proper trophic resources of the pond (Table 1). The bably their absence is a consequence of the colder trophic diversity is lower in this habitat. Thus, for microclimate which is obvious in the case of Pond the population of L. montandoni, breeding in the II which is shaded and situated at the edge of a fo- artificial habitat is probably a solution of the crisis rest. caused by the lack of trophic resources. Neverthe- less, the habitat is permanent and free from pre- If there are microcrustaceans in the water, they datory invertebrates (Cupşa et al., 2007), a fact that are consumed in large quantities by the Carpathian probably favors the newts, which have been re- newts (Kuzmin 1990) as well as by the other species corded in this habitat for many years, despite the of newts (Joly 1987, Schabetsberger et al., 1995, fact that the natural pond is only at an altitude of Kutrup et al., 2005, David et al., 2007). At Turţ, this 500 m and in other species of newts migrations up is the case of a pond which was not taken into to 2000 m have been registered (Schmidt et al., account because it had dried up by the end of April, 2006). where newts had massively consumed microcrustaceans which formed important agglomerations in In the aquatic period, the newts mainly feed on some sectors of the pond. In that pond the maxi- aquatic prey (Kutrup et al., 2005, Dobre et al., mum number of prey/newt was 96, much higher 2007). Nonetheless, in our study the terrestrial prey than in the other two habitats. These data prove have relatively high values, higher than those that the Carpathian newts change their diet compo- achieved by many other populations of newts. The FOOD COMPOSITION OF SOME LOW ALTITUDE LISSOTRITON MONTANDONI (AMPHIBIA, CAUDATA) 485 differences between habitats are maintained rally with much lower frequencies (David et al., concerning the origin of prey as well; in Pond I the 2007, Ovlachi et al., 2007). The high frequency of terrestrial prey is more numerous. Thus, the trophic the occurrence of molted skins, especially in Pond I, scarcity in Pond I that forces newts to forage in the strengthens the idea of the existence of inadequate terrestrial environment in order to complete dietary feeding conditions in this habitat. requirements is highlighted. This situation, where a habitat with low trophic offer forces the newts to Amphibian eggs have been consumed in both forage massively in the terrestrial environment, has habitats, with higher frequency in Pond I at the first been observed in other species such as Triturus sampling event. At that time there was an agglo- cristatus (Covaciu-Marcov et al., 2002a, 2003). meration of egg clutches of Rana temporaria. These have provided a consistent trophic basis for an The consumption of terrestrial prey by newts in important number of newts, a fact which is under- the aquatic period is considered to be a conse- standable in a small habitat, and this kind of trophic quence of the fortuitous presence of these prey element is probably identified on an olfactory basis items in the aquatic habitat where the newts capture (Joly 1981). Nonetheless, the consumption of eggs them from the water surface (Denoël et al., 1999, did not reach comparable values with those Denoël & Joly 2001). This is acceptable especially in recorded in other species (Covaciu-Marcov et al., the case of flying prey like flies. The consumption of 2002b, 2003, Cicort-Lucaciu et al., 2006). Perhaps, other terrestrial prey (ants and pseudoscorpions) at that time some newts foraged in the terrestrial seems to indicate that some individuals of L. mon- environment and the others, due to the low tempe- tandoni leave the water and forage in the terrestrial rature. were less active and stayed hidden under the environment. This is plausible, considering that vegetation near the shores. Eggs were consumed in after the breeding period, the newts feed in the the first period in Pond II, but by a smaller number terrestrial environment. It is hard to believe that of newts. Due to the larger area of the pond, the ants, or indeed pseudoscorpions which have low newts had more difficulty in finding the eggs of mobility and spend a lot of time in hiding, enter the Rana temporaria, as these are laid on the shores in water accidentally in large numbers. Pseudoscor- sectors with little water. In the last period, eggs (in pions represent a primary prey item in the diet of this case newt eggs) were consumed only in Pond newts from Romania and are sometimes identified II. The intake of amphibian eggs is beneficial for in the food composition of other amphibians several reasons one of which is the low energy (Groza et al., 2008). Thus, due to the low trophic consumption needed for a large volume of food offer, the newts, at least those from Pond I, some- (Denoël & Demars 2008). Ranid larvae were con- times forage in terrestrial environment. Feeding sumed in both habitats, but display high percentage escapades into the terrestrial environment have abundance in Pond I in the middle of the aquatic been suspected for other newt species as well, e. g. period of newts. The larvae proceeded from Rana Messotriton alpestris (Kuzmin 1990). temporaria spawns. Being abundant in a small habitat, the larvae comprised a quantitatively im- Plant materials in the stomach content is con- portant resource which is very useful in this artifi- stantly encountered in amphibians (Santos et al., cial habitat. 2004), their consumption being considered accidentally (Gunzburger 1999, Kovács et al., 2007). Despite the reduced feeding compared to other Vegetal remains have a relatively high frequency of newt species, the Carpathian newts from Turţ occurrence in both sexes in each period. Similar to consumed twice as many prey categories as those plant materials, the remains of molted skin are fre- from Ukraine (Kuzmin 1990). This has several ex- quently consumed by a significant proportion of planations. Firstly, the 10 newts from Ukraine were the Carpathian newts. These items are regularly too few to provide an adequate estimation. Secon- present in the stomach content of newts, but gene- dly, the samples were taken only once, toward the 486 S. D. COVACIU-MARCOV ET AL. end of the aquatic period (Kuzmin 1990). The that although newts are opportunistic predators additional prey categories from Turţ are represen- (Covaciu-Marcov et al., 2003, Ferenţi et al., 2008) ted by aquatic mollusks (gastropods and lamelli- they still exhibit a certain level of trophic selectivity branchiates), but most important by terrestrial prey as revealed by previously recorded cases where (spiders and ants) which customize the habitat with newts did not always consume the most abundant reduced prey availability. Also, there are great prey in the environment (Covaciu-Marcov et al., differences between the percentage abundance and 2002b). There is a form of selection according to the frequency of occurrence of prey compared to accessibility, size and utility of prey (Joly & the previous study (Kuzmin 1990). In Ukraine, Giacoma 1992) but also a selection made of the most of the prey were microcrustaceans which were most numerous prey (Cicort-Lucaciu et al., 2005, missing in the case of the populations studied by us. 2007). Our results support this point of view, and though L. montandoni is an opportunistic predator, Comparing the prey availability from habitats it still performs a certain selection between the most (Cupşa et al., 2007) with the diet of newts it can be accessible prey from a habitat, hence a kind of observed that generally the prey consumed controlled opportunism. intensively by newts are important elements of the pools. The situation is even more obvious in Pond I, where the dominant categories from the habitat are REFERENCES prevailing in the diet too. This is once again a Anderson, A. M., Haukos, D. A. and J. T. Anderson (1999). 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