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NORTH-WESTERN JOURNAL OF ZOOLOGY 12 (2): 299-303 ©NwjZ, Oradea, Romania, 2016 Article No.: e161503 http://biozoojournals.ro/nwjz/index.html

Food composition of alpine ( alpestris) in the post- terrestrial life stage

Oldřich KOPECKÝ1,*, Karel NOVÁK1, Jiří VOJAR2 and František ŠUSTA3

1. Department of Zoology and Fisheries, Faculty of Agrobiology, Food and Natural Resources, Czech University of Life Sciences Prague, Kamýcká 129, Praha 6 - Suchdol 165 21, Czech Republic. 2. Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 129, Praha 6 - Suchdol 165 21, Czech Republic. 3. Prague Zoological Garden, U Trojského zámku 3/120, Praha 7 - Troja 171 00, Czech Republic. *Corresponding author, O. Kopecký, E-mail: [email protected]

Received: 26. Juy 2015 / Accepted: 29. December 2015 / Available online: 09. January 2016 / Printed: December 2016

Abstract. in the temperate climatic zone, including European newt species, annually migrate to water for reproduction. While prey consumption and the composition of their diet during the breeding season have been explored relatively well, the opposite is true for the spring period before reproduction. Therefore, the primary of aim our study was to determine whether consumed food in the post- hibernation terrestrial life stage. We studied one population of alpine newts from the Czech Republic. The majority of the newts examined (65.30%) contained some food item. Repletion level was not connected with the newts’ body condition and also did not differ between males and females. In addition, the number of items consumed and the diversity of prey were not connected with an individual’s body condition or sex. Most numerous and frequent in the stomachs of both sexes were Collembola followed by Isopoda. Exploitation of other groups of prey was also almost the same, which resulted in a high niche overlap in the

prey of males and females (Ojk=0.888).

Key words: prey, diet, foraging, intersexual difference, body condition, Urodela.

Introduction (Roček et al. 2003). Alpine newts’ hibernation sites can be as much as 1,000 m distant from their Migration is an integral part of the life history breeding sites, and to overcome this distance can strategies of many taxa, including am- be time and energy consuming (Joly & Miaud phibians (Wells 2007). In the tropics, amphibians’ 1989). breeding migration to ponds is irregular and oc- In contrast to the explosive breeding of an- curs opportunistically after heavy rainfalls (Wat- urans, as in the cases of the common (Rana ling & Donnelly 2002). Conversely in the temper- temporaria) and (Bufo bufo), which do ate zone, breeding is circannual. The life cycle of not eat while breeding, newts are prolonged most temperate amphibians thus consists of terres- breeders (Griffiths 1996, Arntzen 2002) with bi- trial hibernation, a spring stage which includes phasic seasonal plasticity in prey capture behav- migration to water for reproduction, followed by a iour (Heiss et al. 2013, Heiss et al. 2015). Prey con- summer and autumn terrestrial stage (Griffiths sumption and the composition of the diet during 1996, Wells 2007). Environmental changes are ac- their breeding period (i.e. when the newts are in companied by great phenotypic changes (Warburg water) has been examined relatively well, includ- & Rosenberg 1997) along with changes in prey- ing resource partitioning between morphs (Denoël capture mechanics, which recently have been & Andreone 2003, Denoël & Schabetsberger 2003, studied in newts (Heiss et al. 2013, Heiss et al. Denoël et al. 2004), interspecific competition with 2015). other newts (Fasola & Canova 1992, Joly & Gia- Newts of the former are poly- coma 1992, Jehle et al. 2000), and intersexual vari- phagous opportunistic predators in the middle of ance (Kopecký et al. 2012a). On the other hand, trophic pyramids, but some of them, such as al- newts’ diet during the terrestrial phase, including pine newts (Ichthyosaura alpestris) from high alti- the post-hibernation period, has not been suffi- tude lakes, can assume the role of top predators ciently examined (Kuzmin 1990, Denoël 2004). (Schabetsberger & Jersabek 1995). The This is mainly because of newts’ well-concealed is a common species widely distributed across lifestyle during terrestrial phase (Verrell 1985, , where it occupies various while Schabetsberger et al. 2004). Inasmuch as gamete preferring woody, hilly, or mountainous regions production and behaviour associated with breed- 300 O. Kopecký et al. ing are energy-intensive processes (von Lindeiner repletion levels were compared using 2×2 contingency 2007), the level of energy reserves accumulated in tables. Differences between sexes in prey variables (num- the previous period (in our case, the post- ber of prey items, number of prey categories) were exam- ined using non-parametric Mann–Whitney U tests due to hibernation terrestrial life stage) can significantly imbalance in the samples’ sizes. Residuals from linear re- affect an individual’s breeding success. gression between the newts’ SVL and weight were com- The main aims of this study, therefore, were puted separately for males and females. In subsequent to: i) determine the food composition of alpine linear regression analysis, residuals were used as a body newts’ diet during the post-hibernation terrestrial condition variable (Denoël et al. 2002). Statistical signifi- life stage and identify their main prey; ii) ascertain cance was determined at the level α = 0.05. All tests were whether there are intersexual differences in reple- computed using Statistica 12.0 (Statsoft 2012). tion level and diversity and number of prey con- sumed; iii) quantify the niche overlap between Results sexes; and iv) identify the effect of body condition on prey variables. During our study, a total of 144 adult newts (58

males, 86 females) were examined. Mean body

Materials and Methods size of 52.3 mm (± SD: 5.0 mm, range: 34.3–60.9) was greater for females than it was for males at The study was conducted at a location known as “Trojka” 44.2 mm (± SD: 2.2 mm, range: 38.0–49.0 mm) (GPS: 50°30′89.0′′, 12°45′94.3′′), which lies in a spruce for- (Mann–Whitney U test, z=−8.64, p<0.001). The est at 750 m a.s.l. near the village of Kraslice in the west- (SDI) of our samples was de- ern Czech Republic. The location consists of three artifi- termined to be 0.185. Females were also heavier cial ponds lying close to each other. Their overall surface (mean: 4.00 g, ± SD: 1.14 g, range: 1.00–7.00 g,) area is about 30 m², and the distance between them does not exceed 0.3 m. Adult alpine newts were captured using than were males (mean: 2.08 g, ± SD: 0.37 g, range: drift fences and pitfall traps from 28 April to 6 May 1997. 1.25–3.25 g) (Mann–Whitney U test, z=−8.74, From an earlier observational study at this location (data p<0.001). not shown), we know that this date range takes in the Newts consumed Nematoda, Oligochaeta, peak of newt migration to the “Trojka” breeding site. The , Araneida, Acarina, Isopoda, Diplo- traps were controlled twice per day, in the morning and poda, Chilopoda, Collembola, Plecoptera, Psocop- in the evening. Each captured newt was sexed, measured tera, Heteroptera, Sternorrhyncha, Lepidoptera, (snout–vent length, SVL) to the nearest 0.1 mm and weighed using a Pesola scale to the nearest 0.05 g after Diptera, Hymenoptera, and Coleoptera. Females stomach flushing. Stomach contents were extracted using contained all prey categories except for Nematoda. the stomach flushing technique described by Opatrný Males’ food spectrum was less diverse than was (1980). The newts measured and flushed were not anaes- that of females. The stomachs of males did not thetized. They were released into the water immediately contain Plecoptera, Heteroptera, Sternorrhyncha, after these procedures. or Hymenoptera. The most numerous prey – and Stomach contents were stored individually in vials which also was consumed by the largest propor- and preserved in 4% formaldehyde. Prey items were then identified using a stereoscopic microscope and sorted into tion of newts of both sexes – consisted of the Col- 17 taxonomic categories plus a category of unidentified lembola, followed by Isopoda (Fig. 1). prey items. Two prey variables were determined for each Dominance according to the Berger & Parker individual: the number of prey items and the presence of index was higher in the diet of the males (d=0.292) particular prey categories in stomach. Because there were than it was in that of females (d=0.158). Collem- no other bodies of water in the vicinity of the location, we bola were found in higher frequencies in males could presume that the prey found in the newts’ stom- than in females, and so niche breadth was nar- achs was captured only in a terrestrial environment. The sex of the newts was determined according to rower in males (BA=0.465) than it was in females external sexual characteristics. Sexual size dimorphism (BA=0.577). Despite this difference, prey niche was determined using the sexual dimorphism index (SDI) overlap during the post-hibernation terrestrial life proposed by Lovich & Gibbons (1992). Niche overlap be- stage was high among the sexes (Ojk=0.888). tween sexes was evaluated by means of a modified ver- Not all newts contained prey. Of all the newts sion of Pianka’s niche overlap index (Christensen et al. examined, 39.65% of males and 31.39% of females 2005). Dominance of a particular prey category in the had empty stomachs, and there were no signifi- overall diet was computed using the Berger & Parker (1970) index. Niche breadth was determined via Levins’ cant differences in repletion level between sexes standardized niche breadth index (Levins 1968). (2×2 contingency table, χ²=1.04, p=0.31). Nor there Proportions of males and females according to their were apparent significant intersexual differences Newts’ food during spring migration 301

feed before but not during migration itself, which is common in many migrating vertebrates (Jenni- Eiermann & Jenni 1991). If this assumption is cor- rect, then the findings of replete migrating indi- viduals in pit-fall traps are due to slow gastric evacuation rates of ectothermic newts (Scha- betsberger 1994) which had taken food prior to migration. After hibernation and during migration, the time that newts spend on land is probably less than the time they spend in water. Additionally, the energy demands upon them during the repro- ductive period are cumulatively higher (von Lindeiner 2007). Newts may also endeavour to reach water as quickly as possible, because early arrival to the breeding waters is generally advan- tageous (Newman 1992, Arntzen 2002). Protandry (males arriving at breeding areas prior to females) has been described also for alpine newts (Scha- betsberger & Goldschmidt 1994, Kopecký 2008).

This suggests that early arrival is more crucial for Figure 1. Proportion (% n) and frequency (% f) of prey males, as is known for various other animal taxa categories in the diet of alpine newt during post- hibernation terrestrial life stage. Only prey categories (Morbey & Ydenberg 2001). Alpine newt females exceeding 5% are presented separately. do not select mates on the basis of such condition- dependent traits as body size (Garner & Schmidt 2003) and tail depth (Denoël et al. 2001), and so we when we compared the number of prey items and expected that males would hasten regardless of the prey categories between sexes (Table 1). nutrition to take advantage of the best reproduc- There were no significant differences in body tive opportunities at the beginning of the breeding condition between newts with and without prey season, when females are at their most receptive for males (Mann–Whitney U test: z=1.70, p=0.09) condition to mate (Hoeck & Garner 2007). or for females (z=−1.41, p=0.16). Body condition The ratio of individuals with prey to those did not have a significant effect on the number of without one (repletion level) was the same for prey items (linear regression: F=0.69, p=0.42) or both sexes. Males and females also did not differ the number of prey categories (F=0.58, p=0.45) for in relation to the quantity of studied prey vari- males. We found the same results for females ables (number of prey items and number of prey (prey items: F=2.24, p=0.14; prey categories: categories). These results from a terrestrial envi- F=2.52, p=0.12). ronment differ from those from an aquatic envi-

ronment, where females have been observed to

Discussion consume more prey items as well as more diverse and heavier prey (e.g. Kopecký et al. 2012a). This According to our results, it is apparent that the suggests that the higher nutritional requirements majority of newts (65.30%) captured food prior to of females are closely related to actual reproduc- entering water during their post-hibernation ter- tion. restrial life stage. The proportion of newts with Consumption of prey during the post- prey at this stage was lower than those that has hibernation terrestrial life stage was not influ- been found during the breeding phase, where enced by individuals’ body condition for either prey has been discovered in 73% (Covaciu-Marcov sex. The mode of alpine newts’ feeding behaviour et al. 2010), 84% (Kopecký et al. 2011), 92% (Bog- probably is primarily aquatic, and the terrestrial dan et al. 2011), and 100% (Dimancea et al. 2011) of feeding mode is derived from it (Heiss et al. 2013). individuals sampled. This could be a consequence The preparation of a newt’s organism to breed in of lower prey availability after the hibernation pe- water may vary among individuals (Kikuyama et riod. There might also be the possibility that newts al. 2000) due, for example, to the position and

302 O. Kopecký et al.

Table 1. Comparison of numbers of prey items and categories consumed by alpine newt males and females during post-hibernation terrestrial life stage.

Min−max Mean Median SD Mann–Whitney U test Males 1−11 2.71 2 2.78 z=−0.04 Prey items Females 1−8 2.27 2 1.73 p=0.97 Males 1−6 1.91 2 1.29 z=0.03 Prey categories Females 1−6 1.88 1 1.19 p=0.98

character of the place where they hibernate, and ground-dwelling are consumed by alpine consequently this process can affect their ability to newts in substantial numbers also in the terrestrial hunt prey. However, the small number of newts period of their life cycle (Kuzmin 1990). The nar- examined and the fact that this study was per- rower niche breadth and higher dominance index formed at only one location do not allow for any of males were the result of males’ focusing on this generalization of these findings. prey category. Studies conducted during the The number of identified prey categories (17), breeding period have found prey niche overlaps that is to say the prey diversity, is comparable to equal to 0.446 (Bogdan et al. 2011) and 0.660 the number of prey categories that newts consume (Kuzmin 1990). Alpine newts stay in water for in water during the breeding season (Bogdan et al. about one month (Kopecký et al. 2012b) or longer 2011, Kopecký et al. 2012a). Newts from the stud- (Fasola & Canova 1992, von Lindeiner 2007), and ied location consume the Acarina, Plecoptera, Ara- considerable changes in the availability and den- neida,Chilopoda, Lepidoptera, Coleoptera, Dip- sity of prey were observed during this long time tera, Hymenoptera, and Oligochaeta prey catego- (e.g. Denoël & Demars 2008). Based on data re- ries also in an aquatic environment (Kopecký et al. garding alpine newt homing (Joly & Miaud 1989), 2014). Completely terrestrial taxa had been con- we can approximate that the post-hibernation ter- sumed from the water surface or found dead on restrial life stage lasts at shorter time than does the the bottom after they had fallen into the water. breeding period. Therefore, the high prey niche Both sexes showed a mixed feeding strategy, overlap of sexes in the post-hibernation terrestrial with high variations among individuals. Female life stage (0.888) may be the result of limited prey alpine newts are bigger than males (Roček et al. availability during this period. 2003). In our study, females were 1.19 times larger than males. In our opinion, this slight difference in body size between males and females does not en- able females to catch larger prey categories that Acknowledgements. The study was carried out under are inaccessible to males. The genus Lumbricus permit number 8754/97-410/2453/97 from the Czech (from the Oligochaeta prey category) comprises Ministry of the Environment. This study was supported by project no. 20152007 (CIGA) of the Czech University of quite large prey, and it was consumed only by the Life Sciences Prague and by Research Project of the largest of the males even as were con- Faculty of Environmental Science, Czech University of sumed in substantial numbers and by a large pro- Life Sciences Prague, No. 20144247. The English was portion of females (Fig. 1). We have no data about corrected by Frederick Rooks (English Language Services, the dimensions of each consumed prey item, but Praha, Czech Republic) and Gale A. Kirking (English the case of the largest prey category (Lumbricus Editorial Services, Brno, Czech Republic). from Oligochaeta) and the high prey niche overlap (0.888) suggest that selectivity for different sizes is one of the important mechanisms reducing diet References similarity between alpine newt sexes (Joly & Gia- coma 1992). Selectivity for different prey sizes is Arntzen, J.W. (2002): Seasonal variation in sex ratio and probably more applicable in terrestrial environ- asynchronous presence at ponds of male and female Triturus newts. Journal of 36: 30-35. ments, where larger individuals consume also lar- Berger, W.H., Parker, F.L. (1970): Diversity of planktonic ger prey, as has been shown for juvenile alpine foraminifera in deep-sea sediments. Science 168: 1345-1347. newts (Denoël 2004). Bogdan, H.V., Ianc, R.M., Pop, A.N., Söllösi, R.S., Popovici, A.M., Pop, I.F. (2011): Food composition of an Ichthyosaura alpestris The prey category consumed in the highest (Amphibia) population from the Poiana Rusca Mountains, numbers and by the greatest portion of individu- Romania. Herpetologica Romanica 5: 7-25. als from both sexes was Collembola. These small Newts’ food during spring migration 303

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