POLISH JOURNAL OF ECOLOGY 56 2 289–297 2008 (Pol. J. Ecol.)

Regular research paper

Katarina LJUBISAVLJEVIĆ1, Georg DŽUKIĆ1, Miloš L. KALEZIĆ1,2

1 Department of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”, Bulevar Despota Stefana 142, 11060 Belgrade, e-mails: [email protected]; [email protected] 2 Institute of Zoology, Faculty of Biology, Studentski trg 16, 11000 Belgrade, Serbia e-mail: [email protected]

FEMALE REPRODUCTIVE LIFE HISTORY TRAITS OF THE MEADOW , PRATICOLA EVERSMANN, 1834 :  FROM THE WESTERNMOST BOUNDARY OF THE SPECIES RANGE

ABSTRACT: We presented the first data on and Porter 1993, Du et al. 2005, Ji and female reproductive traits of the meadow lizard Wang 2005). The meadow lizard (Darevskia Darevskia praticola from the westernmost bound- praticola Eversmann, 1834) (Fig. 1) appears ary of the species range (Peridanubian Serbia). to be a particularly suitable object for this Mating occurs during April and May, oviposition kind of study on the basis of its two in many period occurs in June, and hatching takes place in respects different characteristics. Firstly, as July. Females mature at body sizes of 49.5 mm of snout-vent length (SVL). One clutch is produced the meadow lizard is a species of the forest annually. The average clutch size of 5.7 eggs (range group of Darevskia genus (Arribas 4 – 8) represents the largest recorded for this spe- 1999), the knowledge of reproductive life cies. Clutch size and clutch mass increased signif- history traits of this species is of general in- icantly with the mother’s SVL. There was no evi- terest, considering the paucity of such stud- dence of the predicted trade-off between egg size ies dealing with small forest lacertids (e.g. and clutch size, as well as of variation in egg size Orlova 1969). Secondly, the meadow lizard associated with maternal SVL. The relative clutch provides a specific opportunity to study the mass (RCM) was rather high (0.60) for lacertid possible interrelation between complex dis- species and was not correlated with female size. junctive distribution patterns with different evolutionary lineages and differences in life KEY WORDS: oviposition period, clutch history traits. Namely, the current taxonomi- characteristics, Darevskia praticola, Serbia cal structure of the meadow lizard includes structuring at the subspecies level (e.g. 1. INTRODUCTION Darevsky 1997, Ljubisavljević et al. 2006, but see Arnold et al. 2007). A nomi- Recent studies of have accentuat- notypical subspecies (D. p. praticola) occurs ed the necessity of having independent data in northeastern Caucasus and Transcauca- sets from different populations and reptilian sus, while the D. p. pontica is distributed in taxa in order to understand both the general northwestern Caucasus and in southeastern patterns of covariation among life-history Europe. In southeastern Europe the meadow traits, and the relationships between these lizard inhabits southwestern and southeast- and environmental factors (e.g. Adolph ern Romania, Serbia, and Thrace in

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Fig. 1. Female Darevskia praticola from Vršački breg, Serbia.

Turkey and (Arnold and Ovenden 2. MATERIAL AND METHODS 2002). There it presents a patchy distribution connected to broad-leaved woodlands ex- 2.1. Localities and sampling posed to the influence of Submediterranean climate, restricted mainly to middle altitudes The analysis of female reproductive traits rarely exceeding 600 m (Stugren 1984). was carried out on samples collected from To date, there are several studies which three different localities in Peridanubian have yielded information on reproduction Serbia in 2002 and 2003: Vršački breg (340 of the meadow lizard in the eastern portion m above sea level, 45°08’N, 21°21’E); Avala of its range (Zhukov 1941, Orlova 1969, (250 m, 44°41’N, 20°31’E); Trešnja (250 m, Mushelishvili 1970, Orlova and Ter- 44°36’N, 20°34’E). tyshnikov 1979). Reproductive life history Because the preliminary analysis showed traits of southeastern European populations, no statistical differences in female snout-vent apart from the limited descriptive data for the length (SVL), clutch size and clutch and egg Romanian population (Méhely 1895, Fuhn characteristics between localities (ANOVA and Vancea 1961), are poorly known. for female SVL and ANCOVA with SVL as

Here, we present the first basic study the covariate, F 2,7 = 0.05 – 16.74, P> 0.05 for on female reproductive characteristics of all variables), we pooled the data in order to the meadow lizard from the westernmost achieve a reasonable sample size. In the study boundary of its distribution range. Knowl- area, the meadow lizard occurs in hilly ter- edge of the reproductive potential of these rain in and around the open broad-leaved edge populations with a severely fragmented woods of the Hungarian and oak for- distribution is valuable for their conserva- est association Quercetum-frainetto-cerris tion and protection. (Radovanović 1951, Matvejev 1961).

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2.2. Data collection in the laboratory laboratory and additional oviductal clutches from five autopsied females. These individu- In the first half of June of 2002 and 2003, als were part of a larger sample of 41 females twelve late-pregnant females were collected which were examined for estimation of size from the study area and transported to the at sexual maturity based on the smallest in- laboratory. Individual females were housed dividual containing vitellogenic follicles or in individual terraria (30 × 20 cm) with a oviductal eggs. The mean maternal SVL was substrate of sand, while stones, pieces of calculated on 28 specimens from this sample bark and leaf litter were provided as shel- determined to be mature. The sample came tering sites. Food (mealworms and other in- from Georg Džukić’s herpetological collec- sects collected in the field) and water were tion of the Institute for Biological Research, available ad libitum. The lizards were main- Belgrade. tained under natural light and photoperiod We used multiple regression, analyses of conditions. The females were inspected al- variance (ANOVA) and covariance (ANCO- most every hour during daytime and once VA) to analyse the corresponding data. The during the night. Following oviposition, the analyses were carried out using the computer females were measured (snout-vent length, package Statistica® (STATISTICA for Win- SVL) and weighed. The eggs were dug up dows. StatSoft, Inc., Tulsa, OK). and carefully removed from the terraria, weighed and measured (maximum length 3. RESULTS and width), and their viability judged by the external characteristics of the eggshell. A 3.1. Sexual maturity digital calliper (0.01 mm precision) was used for the linear measurements, while mass Ovaries of immature females of the measurements were taken with an electronic meadow lizard consisted of transparent fol- balance (accuracy 0.001 g). The characteris- licles up to 1.6 mm in diameter. Somewhat tics of the eggs were, in all cases, determined larger follicles (>2 mm) showed signs of vi- within 8 h of laying. The estimate of egg vol- tellogenesis and were used as an indication of ume (V=4/3π a2b, a and b being half of the the first sign of reproductive activity of the fe- width and length of the egg, respectively) males. According to this criterion and on the was taken as an overall measure of egg size. basis of 41 collection specimens examined, In all cases each clutch was unequivocally the minimum size at which the females from assigned to an individual female, allowing us Serbia attained sexual maturity was 49.5 mm to calculate the relative clutch mass (RCM) in SVL, and all females larger than this size as the ratio of clutch mass to postparturition reproduced. Percentage of mature females in body mass. the analysed sample was 68%.

2.3. Statistical procedures 3.2. Oviposition and clutch frequency

Descriptive statistics (mean, standard er- The data obtained through fieldwork and ror, standard deviation, range) for all traits from specimens already preserved in collec- were calculated. For subsequent analyses all tion gathered in different years were pooled variables were log-transformed, to ensure together in order to give an overall descrip- data normality and to generate homoge- tion of the oviposition period in this species. neous variances (Sokal and Rohlf 1981). At the end of April the females bore small Since some previous studies (see e.g. Galán to medium vitellogenic follicles. Specimens 1997) revealed that the relationships between from all three study localities carried ovi- clutch characteristics and maternal SVL dif- ductal eggs during May, while in all cases the fer depending on whether oviductal or vi- clutches were laid during June in the labora- varium-laid eggs are taken into account, here tory. None of the examined females exhibited we considered only the vivarium-laid eggs. a simultaneous presence of enlarged vitello- Only the mean clutch size was estimated on genic follicles and oviductal eggs or corpora the basis of data for 12 clutches laid in the lutea. We neither found other indicators for

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Table 1. Egg and clutch characteristics of female Darevskia praticola from Serbia based on average values for each clutch. The mean ± SE, SD, range and number of adult females or clutches analysed (N) are shown. mean ± SE ± SD range N Female SVL (mm) 54.74 ± 0.60 3.16 49.49 – 60.51 28 Clutch size 5.71 ± 0.29 1.21 4 – 8 17 Clutch mass (g) 1.508 ± 0.090 0.311 1.184 – 2.220 12 Relative clutch mass (RCM) 0.601 ± 0.028 0.097 0.454 – 0.771 12 Egg mass (g) 0.264 ± 0.008 0.029 0.215 – 0.332 12 Egg length (mm) 10.67 ± 0.17 0.59 9.62 – 11.69 12 Egg width (mm) 6.61 ± 0.07 0.23 6.21 – 6.94 12 Egg volume (mm3) 244.76 ± 7.40 25.65 194.08 – 282.87 12

the production of more than one clutch per P> 0.05) and egg volume (r = –0.37, F 1,10 = season. 1.58, P> 0.05) which indicates that there was no significant egg size-clutch size trade-off 3.3. Clutch characteristics within individual clutches when holding fe- male SVL constant. Hence, larger clutches Reproductively active females had, on av- were not composed of significantly smaller erage, 54.7 ± 0.6 mm in SVL, and the clutch and lighter eggs and this relation is indepen- size of 4 to 8 eggs (mean ± SE = 5.7 ± 0.3). dent of female SVL. The laid eggs had a mean length of 10.7 ± 0.2 mm, a mean width of 6.6 ± 0.1 mm, and 4. DISCUSSION a mean mass of 0.26 ± 0.01 g. The relative clutch mass ranged from 0.45 to 0.77, with 4.1. Clutch frequency the mean value of 0.60 ± 0.03 (Table 1). The clutch size and clutch mass increased Populations of D. p. pontica are single significantly with female SVL (clutch size: r clutched, as indicated in our study and the

= 0.67, F 1,15 = 12.55, P <0.01, Fig. 2; clutch literature (Orlova 1969), while D. p. prati- mass: r = 0.58, F 1,10 = 4.97, P <0.05). No sig- cola appear to be able to lay two clutches per nificant relationship was found between the year in (Orlova 1969) and Geor- SVL and mean egg mass and sizes (egg mass: gia (Mushelishvili 1970). Production of

r = –0.08, F 1,10 = 0.07, egg length: r = –0.41, single or multiple clutches within the same F 1,10 = 1.99, egg width: r = 0.22, F 1,10 = 0.51, season is primarily related to female body egg volume: r = –0.07, F 1,10 = 0.05, P> 0.05 size and to the timing of oviposition (Galán in all cases). Hence, the mean egg sizes for 1997, Rúa and Galán 2003). Apart from a clutch remain constant with the increase this, generally in the small-sized lacertid spe- in female SVL, irrespective of the number cies a single annual clutch is conditioned by of eggs in the clutch. Also, the RCM was not the viviparous modality of reproduction (e.g. significantly related to the mother’s SVL (r = Z. vivipara, Heulin et al. 2000), or by the pe-

–0.04, F 1,10 = 0.02, P> 0.05). riod of annual and reproductive activity (e.g. We statistically removed the effects of Saint Girons and Duguy 1970, Arribas maternal SVL by calculating the residual and Galán 2005). In the case of D. p. pon- scores from separate regressions of egg vari- tica, production of a single clutch is probably ables and clutch size on female SVL, respec- the result of adoption of different life-history tively. Overall, the relative fecundity showed strategy, since, at least in South European a non-significant negative correlation with part of the range, the temperate climatic con-

the mean egg mass (r = –0.34, F 1,10 = 1.32, ditions are presumably more favorable than P> 0.05), egg length (r = –0.49, F 1,10 = 3.23, in the mountain regions of Armenia and P> 0.05), egg width (r = –0.21, F 1,10 = 0.50, where D. p. praticola occurs.

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Fig. 2. The relationship between clutch size and maternal snout-vent length (SVL) of Darevskia praticola from Serbia.

4.2. Clutch size and clutch characteristics (Ryabinina et al. 2002, Ljubisavljević et al. 2006). However, proximate factors that The mean clutch size (4–5.7– 8 eggs) re- apparently vary among localities (local con- corded in this study for the Serbian popu- ditions of weather and food supply) could lations of the meadow lizard represents the also be important determinants of the ob- largest recorded for this species (4–6 and 4 served life-history variation. – 5 eggs Méhely 1895, Fuhn and Vancea Our data showed that maternal size was 1961, respectively for the Romanian popu- the main determinant of reproductive in- lation; 2–4.4–6 eggs Orlova 1969, Orlova vestment in the meadow lizard, with larger and Tertyshnikov 1979, for the central females producing more offspring. A trade- Caucasian population of D. p. pontica; 3 eggs off between egg size and numbers (usually Mushelishvili 1970, for the Georgian pop- arises as a consequence of space constraints ulation of D. p. praticola). Since the present or limited food resources), although wide- study showed that clutch size was significant- spread in numerous lizard species (e.g. Bau- ly correlated with maternal size, geographi- wens and Díaz-Uriarte 1997, Dough- cal variation in reproductive output could ty and Shine 1997, Ji and Braña 2000, be linked to geographical variation in adult Castilla and Bauwens 2000, Arribas body size, as reported previously for other and Galán 2005), was not detected in this species (e.g. Ji and Wang 2005). study. However, trade-offs are not always ob- Different reproductive strategies for produc- served for a variety of reasons. For example, tion of one large or two small clutches gener- failure to take into account covariates, and ally found in D. p. pontica vs. D. p. praticola high variation in resource acquisition rela- are accompanied by considerable morpho- tive to variation in resource allocation, can logical and particular genetical differences obscure the underlying trade-off (Uller

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and Olsson 2005). Also, eggs may be well 4.3. Peculiarities in life-history optimised for size as a consequence of their strategy of the meadow lizard from the adaptive responses to local environments westernmost boundary of the range or influenced by maternal body volume but at some optimal rather than maximal level Some species in their patterns of geo- (Ji et al. 2002, Ljubisavljević et al. 2007). graphic variation and covariation in life-his- Finally, Bauwens and Díaz-Uriarte tory characters (see Bauwens and Thoen (1997) noted that the sample size and the 1981, Dunham et al. 1988, Bauwens and strength of the relationship between the re- Díaz-Uriarte 1997, Rúa and Galán siduals of two variables should be very large 2003, Ljubisavljević et al. 2007) do not to make that relation detectable. Therefore, conveniently fit the dichotomies in the the- the moderate sample size of this study may ory of r – and K – selection (Pianka 1970), impede the statistical detection of some re- the foraging mode (“sit-and-wait” vs. “active” lations among the size-free variables, given foragers, Vitt and Congdon 1978), the es- that some trade-offs between the egg size cape tactics (“cryptic” vs. “flight”, Vitt and and the clutch size were observable but not Price 1982) or time of maturation (“early” statistically significant. vs. “late maturing” Tinkle et al. 1970). The The mean RCM value recorded in the populations of D. praticola studied here ap- present study (0.6) was much higher than peared to adopt the strategy of large-sized has been reported previously for most of “sit and wait” lizards having a relatively large the small sized lacertids (Braña et al. 1991, (in comparison to other populations) single Bejaković et al. 1996, Galán 1997, Ar- clutch with the tendency to increase the ribas and Galán 2005). To our knowl- clutch size rather than the egg size and high edge, higher mean RCM values have been RCM value. In addition, they presumably recorded only in populations of Z. vivipara have a late-maturing reproductive strategy, (Bauwens and Thoen 1981, Pilorge et reaching sexual maturity after the second al. 1983). In reptiles, RCM has been inter- year of life (as it is documented in popula- preted as an adaptation for optimal repro- tions of the same subspecies in northwestern ductive expenditure and a constraint im- Caucasus by Smirina et al. 1984, and our posed by the maternal body shape (amount field observations). Adoption of this strat- of space available in the maternal abdominal egy, despite the fact that it actually belongs cavity) (e.g. Tinkle 1969, Vit and Con- to small “widely foraging” lacertids with the gdon 1978, Shine 1992). Species with a clutch consisting of less than ten eggs, may be lower number of clutches per season could interpreted as an adaptation to a particular be expected to increase their energetic in- habitat-type (more forested habitat instead vestment in each of them and variation in of more open areas in Caucasian region, RCM is mainly due to an increase in clutch Ljubisavljević 2004) or other environ- size (Braña et al. 1991). This may be one of mental factors affecting different predation the reasons for the higher RCM value found rates (Dunham et al. 1988). in the analysed single-clutched populations Relict populations close to the range of the meadow lizard with a large clutch boundary often exhibit relatively low rates size. Other reasons could be referred to of population increase and low densities specific characteristics related to escape tac- (e.g. Berlingd 2005). However, peripheral tics, vulnerability to predation, mobility and populations need not inevitably suffer lower foraging mode of this forest lizard. Certain fecundity with regard to central ones (e.g. limitations of the “widely foraging” strategy Carretero and Llorente 1995, Díaz et and the “flight” anti-predator tactic (sensu al. 2005) as shown in our study. Morpho- Vitt and Congdon 1978, Greene 1988) logical peculiarities of individuals within in densely vegetated areas as the structural the analysed edge populations have already habitat type of D. praticola (Van Damme been identified (Ljubisavljević et al. 2006, and Vanhooydonck 2002) and its cylin- authors unpublished data), which could be drical morphology could increase the RCM a reflection of intensive selection at the bor- value (Vitt 1981). der of the species range, while their genetic

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status still needs to be checked. Channell Arribas O.J., Galán P. 2005 – Reproductive and Lomolino (2000) showed that pe- characteristics of the Pyrenean high-Moun- ripheral populations are no more “doomed tain Lizards: Iberolacerta aranica (Arribas, to extinction” than populations in the centre 1993), I. aurelioi (Arribas, 1994) and I. bon- of a species’ range, and in fact often less so. nali (Lantz, 1927) – Anim. Biol. 55: 163–190. Bauwens D., Thoen C. 1981 – Escape tactics They often exhibit unique genetic character- and vulnerability to predation associated with istics (e.g. in lizards Gullberg et al. 1998, reproduction in the lizard Lacerta vivipara – J. Böhme et al. 2007) that make them espe- Anim. Ecol. 50: 733–743. cially valuable for the evolutionary potential Bauwens D., Díaz-Uriarte R. 1997 – Co- of the species and biodiversity conservation variation of life-history traits in lacertid liz- (Lesica and Allendorf 1995). In the ana- ards: a comparative study – Amer. Natur. 149: lysed populations of the meadow lizard the 91–111. threatening factors are likely to be extrinsic Bejaković D., Aleksić I., Tarasjev A., (habitat loss and degradation) and this is ac- Crnobrnja-Isailović J., Džukić G., cording to Araujo and Williams (2001) Kalezić M.L. 1996 – Life-history variation a strong reason for directing conservation in a community of lacertid lizards from the Lake Skadar region (Montenegro) – Herpetol. management priorities towards these kinds J. 6: 125–132. of populations. Berlingd S.A. 2005 – Population dynamics and conservation of the sand lizard (Lacerta agilis) ACKNOWLEDGEMENTS: We thank Valen- on the edge of its range – Acta Universitatis tina Orlova for making the literature in Russian Upsaliensis, Digital comprehensive summa- available to us and Ljiljana Tomović for her help ries of Uppsala Dissertations from the Faculty in the field. We are also very grateful to Gordana of Science and Techology 41, 42 pp. Šokorac for the correction of the English version Böhme M.U., Schneeweiß N., Fritz U., of the manuscript. Comments and suggestions of Schlegel M., Berendonk T.U. 2007 – prof. dr. Anna Hillbricht-Ilkowska and an anony- Small edge populations at risk: genetic diver- mous reviewer greatly improved the final version sity of the green lizard (Lacerta viridis viridis) of the manuscript. This study was supported by in Germany and implications for conservation the Serbian Ministry of Science (grant no. 143052, management – Conserv. Genet. 8: 555–563. “Patterns of amphibian and reptile diversity on Braña F., Bea A., Arrayago M.J. 1991 – the Balkan Peninsula”). Egg retention in lacertid lizards: relationships with reproductive ecology and the evolution of viviparity – Herpetologica 47: 218–226. 5. REFERENCES Carretero M.A., Llorente G.A. 1995 – Re- production of Acanthodactylus erythrurus in Adolph S.C., Porter W.P. 1993 − Tempera- its Northern boundary – Russ. J. Herpetol. 2: ture, activity, and lizard life histories − Amer. 10–17. Natur. 142: 273–295. Castilla A.M., Bauwens D. 2000 – Repro- Araujo M.B., Williams P.H. 2001 − The bias ductive characteristics of the lacertid lizard of complementarity hotspots toward marginal Podarcis atrata – Copeia 2000: 748–756. populations − Conserv. Biol. 15: 1710–1720. Channell R., Lomolino M. 2000 – Dynamic Arnold E.N., Ovenden D. 2002 – A field biogeography and conservation of endan- guide to the reptiles and amphibians of Brit- gered species – Nature 403: 84–86. ain and Europe. 2nd ed. – Harper Collins Darevsky I.S. 1997 – Lacerta praticola Ever- Publishers, London, 288 pp. smann, 1834 (In: Atlas of amphibians and Arnold E.N., Arribas O., Carranza S. reptiles in Europe, Eds: J.P. Gasc, A. Cabela, J. 2007 – Systematics of the Palaearctic and Ori- Crnobrnja-Isailović, D.Dolmen, K. Grossen- ental lizard tribe Lacertini (Squamata: Lacer- bacher, P. Haffner, J. Lescure, H. Martens, J.P. tidae: Lacertinae), with descriptions of eight Martinez Rica, H. Maurin, M.E. Oliveira, T.S. new genera – Zootaxa 1430: 1–86. Sofianidou, M. Veith, A. Zuiderwijk) – Socie- Arribas O.J. 1999 – Phylogeny and relation- tas Europea Herpetologica, Museum National ships of the mountain lizards of Europe and d’Histoire Naturelle, Paris, pp. 254–255. near east (Archaeolacerta Mertens, 1921, s.l.) Díaz J.A., Pérez-Tris J., Tellería J.L., Car- and their relationships among the Eurasian bonell R., Santos T. 2005 – Reproductive lacertid radiation – Russ. J. Herpetol. 6: 1–22. investment of a lacertid lizard in fragmented habitat – Conserv. Biol. 19: 1578–1585.

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Received after revising November 2007

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