Hermann s tortoise, for example, mostly concern. and Raducan, 1976; Hailey and Loumbourdis, 1988,

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1 Contributions Zoology, 7 (4) 16 (003) SPB Academic Publishing bv, The Hague Individual, local and subspecific variation in female Hermann s rise (Testudo hermanni) reproductive characters S. Longepierre 1, C. Grenot¹ & A. Hailey 3,4 l Ecole Normale Superieure, Laboraire d Ecologie, CNRSUMR 765, 46 rue d Ulm, F Paris, France; Present address: Laboraire EnvironnementMarin Litral, Gestion de la Biodiversite, E.A. Universite de Nice SophiaAntipolis, Parc Valrose, 06108NiceCedex France; department of Zoology, Aristelian University of Thessaloniki, Thessaloniki GR 54006, Greece; 4 Present address: School ofbiological Sciences, University of Brisl, WoodlandRoad, Brisl BS8 IUG, U.K. Keywords:: Egg production, characters, conservation, rise, Testudo hermanni Abstract Hermann s rise, for example, mostly concern the eastern form, Testudo hermanni boettgeri (Cruce We studied reproductive characters of a population ofthe rise Testudo h. hermanni in the Plaine des Maures (Var), and compared these another population in southern France and T. h. boettgeri in Greece. Clutch characters, which are measures of tal reproductive investment, showed no differences between subspecies or sites after size correction by AN COVA. Egg characters, which measure the division ofthis investment among offspring, did vary significantly among both and Raducan, 1976; Hailey and Loumbourdis, 1988, 1990) even though the western form, Testudo hermanni hermanni(bour, 1986), in France and Italy is more threatened. The few existing studies of T. h. hermanni have in addition been oriented more reproductive behaviourthan the ecophysiology of egg production (Cheylan, 1981; Swingland and subspecies and sites after correcting for. The presence ofsuch local variation should discouragerelocation ofthe threatened T. h. hermanni evenbetween populationsof the same subspecies. Contents Introduction 1 Material and methods Results Stubbs, 1985), as very low population densities make capture of gravid females difficult. A model of optimum size in Greece suggested that the dwarf T. h. hermanni that occur in southern Italy smaller than could be explained just by low adult survival rates, and that these therefore differed from T. h. boettgeri in reproduction or growth (Willemsen and Hailey, 001). One important question is whether such differences largely occur between the two subspecies, or at a more local Discussion 3 level among populations. This study therefore had Variation among populations 3 Variation individuals among 5 Conclusion 5 Acknowledgements 6 References 6 two aims. First, define the reproductive characteristics of threatened T. h. hermanni in the Plaine des Maures (France), and the relationships between investment in the egg and and female size and condition. Second, analyse data on reproduction of T. hermanni show whether there Introduction is significant variation among populations and/or subspecies. One possibly confounding facr in this Information on egg production is an important link between the study of population dynamics and the analysis, annual variation, is apparently not important in conservation of threatened rise species. Much T. hermanni. There no significant differences in or egg characters between 198 work already exists on species of Gopherus in the USA (Diemer and Moore, 1994; Hellgren et ail., and 1983 in France, or 1985 and 1986 in Greece, even though 1985 a drought year (Hailey and 000; Wallis et al., 1999), but data for European Loumbourdis, 1988). rises remain piecemeal. Reproductive data for

2 tall low Variation S. Longepierre et al. ofreproductive characters in Testudo hermanni Materialand methods ray source the film (F) 70 cm, so that the distance of the object (O) from the source 67. The study site Pardiguiere situated in the locality of Cannet des Maures, in the Plaine des Maures, cm (i.e., O/F 0.96). The centres of the eggs (in a horizontal plane with the width shown the X on department of Var, France. This area (43 11' N, ray) thus on average.8 cm above the film. 6 7' E) has a typical Mediterraneanclimate with mild winters and hot, dry summers. A stream (usually dry in parts) crossed the study site, forming a small valley flanked by arid eroded areas of Permian sandy soil, with high diversity of xerophytic vegetation (Lavagne et al., but 1998) little shelter for rises. Scrub and forest (Quercus pubescens In France, F 84 cm and measurements from X rays corrected using the ratio O/F 0.97, equivalent the centres of the eggs being.5 cm above the film, because the rises slightly smaller than the T. h. All boettgeri. es from different individuals. We calculated volume 3 egg (EV, cm ) according and Pinus pinea) in surrounding areas alternated the equation: EV (p L w )/6000 (Coleman, with grassland and low maquis mixed with Cistus 1991). We calculated egg (EM, g) from the formations (Loisel, 1971). These provided large equation EM L w 14.7 grazing areas and shelter rises. Between the (Hailey and Loumbourdis, 1990). Mean size, shape dense vegetation and the eroded areas strips (L/w),, and volume of calcified eggs of shrubby vegetation belonging the Isoetion calculated for each female. The characters, (Aubert and Loisel, 1971; Barbero, 1965) and the size (CS), (CM), and Mediterranean Oleolentisc associations (Lavagne et al., 1998). Comparative data from T. h. boettgeri volume (CV) examined in relation straight carapace length (SCL), (), and from three sites in northern Greece (Willemsen condition index (Cl) of females. We calculated the and Hailey, 1989, 1999). Alyki coastal heath Cl as the residual from the length relation land on sandy soil with scattered Crataegus bushes and low thickets of Rubus, Artemisia and Cistus. ship: Cl (Y Y)/Y, where Y o o and Y are the observed and predicted es, respectively. Lichoron macquis of Quercus coccifera on Interrelationships between these parameters the lower slopes of Mount Olympus (altitude 450 analyzed m), with shorter garrigue of Q. coccifera and Cistus scrub around grassland and cultivated areas. Deskati using polynomial, exponential, and linear regressions (Sokal and Rohlf, 1994;Zar, 1984), and the model explaining most variation (in term open oak woodlandof Q. ilex on poor soil at an of R and probability) used. altitude of 650 m. Variation of egg,, and female characters We 3 captured wild female T. h. hermanni from among populations and subspecies of T. hermanni AprilJune 000. Each female Xray imaged in southern Europe investigated using analy (Hailey and Loumbourdis, 1988, 1990) using Po sis of variance (ANOVA) and analysis of covari laroid Cronex film in a cartridge (397 x 97 mrn; radiation 10 ma s" 1 for 0.06 s), measured, marked, ance (ANCOVA). Oneway ANOVA of subspecies compared T. h. hermanni in France with T. h. weighed (Stubbs et al, 1984), and released at the capture point. The number of calcified eggs recorded for each individual, and the length (L, mm) boettgeri in Greece. Oneway ANOVA of site compared three sites in Greece with rises of different size. The same analyses performed and width (w, mm) of the image of each egg measured from the film a precision of 0.5 mm. with ANCOVA, using SCL as covariate, thus correcting for differences in size. The image slightly magnified because the egg (within the female s ) raised above the film. Observations of T. h. boettgeri in which eggs Results measured on Xray films in similar cartridges and after laying showed that the true egg width The smallest female with eggs had a SCL of 148 mm, which considered as the size at maturity 96% (SD.8) of the image (A. Hailey, unpublished data). In that case the distance from the X in females; the largest female 169 mm. The

3 Contributions Zoology, 7 (4) shelled tive eggs period (between and the end of the that on emergence reproduc from hibernation laying period). This suggests females average the whole during 1.6:1 lay than more one because the interval between es is per year, about 0 only 1985), and Stubbs, visible in sizes days (Collins, 1980; Swingland and 13 ranged from of.6. Egg length and volume 0.64 strongly I. The males cording distribution frequency of Testudo hermanni period (April (%) hermanni white, May of in June grey, France volume ac and EV (R but shape, P an 1, average width egg 0.79). Egg related by the equation P < ). and volume related egg significantly for fe size southern 1), with related not 0.006, Clutch size, Fig. only be calcified and (figure females ( R among EM eggs will Xray images for part of this time. Clutch length, not egg egg, egg width (table I; equations given by Longepierre, 001). Egg length, black). and egg volume (but not egg width egg, shape) of females the also significantly according length or related quadratic conditionof females size, with strong characters by quadratic length not, among these Longepierre, 001). also but largely explained by correlations characters (table I; (table I; Longe pierre, 001). The variation of volume, and RCM curves, or significantly curves The related (figure ) but not the condition of females (table I). or Discussion Variation. The variation Fig. hermanni gles; R CV 0.60, RCM with 0.66, p p reproductive characters of Testudo. Clutch (a, open 0.006), 0,003) + of (). relative and size (c, volume trian ; Females in the Plaine des Maures had calcified eggs from (b, circles; 510.7; R CS 0.58, p April squares; 63.7 fdled open among populations h. l;r ). June, a similar 1981; Swingland boettgeri and in Greece some and 1.7 mm, (range with a mean g). The of 81 est in May no females with calcified eggs ing July. (77%), ± ± 18 g proportion of adult females with shelled eggs varied with month, then 158 April being high and June (both 50%); captured dur The overall ratio of females with : without season manni in southern Maures. that of T. populations Europe (table II). previously Torises T. h. 1988,, and female The of adult females in the Plaine des Maures similar Loumbourdis, egg, characters did vary among size of females with eggs (± S.E.) 1985) and Stubbs, (Hailey 1990). Nevertheless mean reproductive T. h. hermanni in the Massif des Maures (Cheylan, her size very found in the Massif des from Greece larger, and ANOVAs showed significant variation of size both between countries, and among sites in Greece. The larger size of these rises from Greece re

4 q j S. Longepierre et al. Variation ofreproductive characters in Testudo hermanni Table I. Reproductive characters of female Testudo hermanni hermanni 14) with calcified eggs, in the Plaine des Maures, and matrix ofrevalues between egg,, and female characters (S.E, 3 standard error; P<0.05, / <0.01, P< 0.001; all other values are not significant P > 0.05). Clutches Females Mean ± S.E. Range minmax CS CM CV SCL Cl Egg length (L, mm) 35.6 ± Egg width (w, mm) 7.8 ± Egg (EM, g) 16.5 ± Egg volume (EV, cm 3 ) 14.4 ± Egg shape, L/w 1.8 ± Clutch size (CS).64 ± q Clutch (CM, g) 44.1 ± , Clutch volume (CV, cm 3) 38.6 ± Q Relative (RCM, %) 5.77 ± q 93 q 93 q Table. Comparison of Testudo h. hermanni at two sites in southern France, and with T. h. boettgeri in Greece. Notes: For France, (1) is the Plaine des Maures (this study) and () is the Massif des Maures (from Swingland and Stubbs, 1985). For Greece, (3) is the mean ofthree sites (from Flailey and Loumbourdis, 1988, 1990) and (4) is the predicted value at 158 mm SCL. / values are shown for oneway ANOVAs of country (France versus Greece), and ofsite in Greece (Alyki, Deskati and Lichoron), and for ANCOVAs of and country ofsite with SCL as covariates. France Greece ANOVA ANCOVA (1) () (3) (4) Country Site Country SCL Site SCL SCL (mm) P< P< EM (g) P P P 0.19 P< P P< L (mm) P P 0.86 P P P P w (mm) P P< P P< P< P <0.001 Shape P P< P P P< P CS (eggs) P P< P P< 0,001 P P< CM (g) P P< P 0,71 P< P P< RCM (%) P 0,83 P P P P P fleets the particular populations in which reproduc size among populations; ANCOVAs showed tion has been studied (Hailey and Loumbourdis, no significant effects of country or site after ad 1988). Body size varies widely in Greece, and tqrises from the Peloponnese have even smaller bocly size than French populations (Willemsen and Hailey, justing for the highly significant size covariate (table II). Mean size and thus higher in Greece than in France, but the val 1999). No general size distinction can thus ues predicted for T. h. boettgeri of 158 mm be made between T. h. hermanni and T. h. boettgeri. The most fundamental reproductive character, similar those observed in France. Clutch size and in the Plaine des Maures also very similar those previously reported at the relative (RCM) did not vary significantly with country, site, or size, with a mean value close 6% in all areas (table II). This value is low compared squamate reptiles, probably due Massif des Maures (table II). We conclude that characters, which are measures of tal reproductive investment, show no differences between the restriction of volume and by the carapace (Hailey and Loumbourdis, 1988). The characters size and did subspecies or among sites after has been taken in account. Mean egg varied significantly size variation with site but vary significantly with both country and site in not country in both ANOVA and ANCOVA, and ANOVA. This variation due differences of with size covariate. Egg in the Massif

5 003 Contributions Zoology, 7 (4) 5 des Maures similar that predicted for a Greek rise of the same size. Variation in egg populations. Egg length showed more individual variation, and thus less likely differ significantly among populations. therefore local rather than between the subspecies. Egg length varied significantly with country Egg and characters not related in ANOVA, due a significant effect of size; the length or condition of females, but they there no significant effect of country in AN related their according quadratic COVA. There no significant effect of site on egg length in ANOVA or ANCOVA. Egg width relationships (figure ). The lack of effect of condition is expected if the carapace limits the tal and shape both varied significantly with country, volume of the (Hailey and Loumbourdis, site, and size in ANCOVA and with site in 1988), so that increase in eggs reduces the volume ANOVA; shape but not width varied significantly of the gut rather than increasing tal (Hailey with country in ANOVA. Eggs from the Plaine des and Loumbourdis, 1990). The lack of effect of Maures wider than predicted for Greek rises of equal size; conversely their values length is counter the pattern found among populations (table II) where larger females had more of the shape index (egg length/egg width) lower. Thus, in contrast characters, egg eggs and higher. Clutch size usually characters did vary with country increases with length within populations, although fecundity may decrease again in the largest and site after adjusting for differences in size. Egg is a individuals (Hailey and Loumbourdis, 1988, 1990), measure of the division of reproductive investment perhaps because of old age. among individual offspring (Lack, 1968; Smith and Fretwell, 1974; Lloyd, 1987), and could vary due genetic adaptation, phenotypic plasticity, or genetic drift. Egg width and shape are more likely reflect nonadaptive effects such as morphological The curved relationships'of reproduction found here could also be due reproductive senility, suggesting that this is a general phenomenon in populations of longlived T. hermanni. Some decrease of reproduction with age indeed in necessary the model of constraints of the pelvic canal width in females optimum adult female size, which otherwise pre (Congdon and Gibbons, 1987). We conclude that dicted sizes much larger than observed (Willemsen and Hailey, 001). the ecology of hatchlings ( resources and survival rates) and female morphology could vary among sites and subspecies in T. hermanni, while tal reproductive investment by females does not. Conclusion Reproductive characters of Testudo hermanni vary Variation among individuals among populations after correcting for differences in size. Differences among sites as large Egg length, egg, egg volume, and shape significantly related size,, volume, and female, but egg width as those between France and Greece, showing that showed no significant relationships (table II). These withinpopulation relationships opposite amongpopulation comparisons, where egg width local variation is as large as any subspecific differences. Such local variation should discourage relocation of the threatened T. h. hermanni, even between populations within the same region. This suggests that rises should be conserved in situ, showed significant variation with country, site, and rather thanrelocated as has been practised in France size while egg length did not (table II). This (Devaux 1990). More than 6000 rises contrast can be explained by noting that egg width released from in the Plaine des Maures, may be constrained by the pelvic canal width, while the Levant islands, the Esterel region and other egg length is not. Egg width thus much less variable in the Plaine des Maures (range 6.94 (unpublished) areas, without considering the possibility of local variation. Fortunately mm) than egg length (range mm), and so more likely show significant differences other these individuals permanently marked and those recovered excluded from this study. There

6 Variation de la France. Thesis, Ecole Normale Superieure de Paris 6 S. Longepierre et al. ofreproductive characters in Testudo hermanni insufficient time for ofthose released any offspring in the study area have become mature; any reproduction of relocated individuals will complicate future studies, which will thus need include genetic analysis. Hailey A, Loumbourdis NS Population ecology and conservation of rises; demographic aspects of reproduction in Testudo hermanni. Herpel. J. 1: Hellgren EC, Kazmaicr RT, Ruthvcn DC, Synatzske DR Variation in rise life hisry: demography of Gopherus berlandieri. Ecology. 81: Lack D Ecological Adaptations for Breeding in Birds, (ed. Chapman and Hall), London, U.K. Acknowledgements Lavagne A, Marino ML, Rebuffel G Commune de Vidauban, site N 6 Commune du Cannet des Maures la Pardiguiere nord. (ed. S.l.V.O.M. du Centre Var), Le Luc We thank the collective of the Cannet des Maures and society Meilland for their help during this work, and two referees for helpful comments. This study supportedby the grant DGAD/ SRAE No form the ministere de TAmenagement du en Provence, France. Lloyd DG Selection of offspring size at independence and other sizeversusnumber strategies. Am. Nat. 19: Terriire et de FEnvironnement. Loisel R Les cistaies calcifuges de Provence. Ann. Fac. Sci. Mars. 46: Longepierre S, 001. Ecophysiologie de Testudo hermanni References hermanni Gmelin, 1789: Evaluation des contraintes environnementales et alimentaires en milieu nature! dans le Sud Au bcrt G, Loisel R Etude des des Isoegroupements Nanojuncetea et des Helianthemetea annuadans le sudest MediterraneanFrangais. Ann. Fac. Sci. Mars. 45:0341. Barbcro M Groupements hygrophiles de 1 Isoetion dans les Maures. Bull. Soc. Bol. Fr. 11; UCBL I. (Ed. ANRT, Grenoble). France. Longcpicrre S, Hailey A, Grcnot C Home range area in the rise Testudo hermanni in relation habitat complexity: implications for conservation of biodiversity. Biodivers. Conserv. 10: Hour R L identite des rtues terrestres europeennes: Specimenstypes et localitestypes. Rev. Fr. Aquar : 111 CheylanM Biologieet Ecologiedelartued Hermann Testudo hermanni Gmelin, Contribution de I espece a la connaissance des climats quaternaires de la France. Ecole Pratique des hauls Etudes, Montpellier, France. Coleman G Measuring parental investment in nonspherical eggs. Copeia Collins P.W.P The captive breeding of Mediterranean rises in Britain. In: The care and breeding of captive reptiles.lawman S, Millichamp NJ, Lucas DGD & Millwood, AJ (Eds), Brit. Herp. Soc., London, U.K., 136. Congdon JD, Gibbons JW Morphological constraint on egg size: a challenge optimal egg size theory. Proc. Nat. Acad. Sci., USA. 84: Cruce M, Raducan I Reproducerea la broasca tesasa de uscat (Testudo hermanni hermanni Gmelin). Stud. Cer. Bio. Buc. Ser. Biol. Anim. 0: Devaux B Reintroduction de rues d Hermann ( Testudo hermanni hermanni) Ecol. Terre Vie. 5: dans le if des Maures. Rev. Diemcr JE, Moore CT Reproduction of gopher rises in northcentral Florida. Fish and Wildl. Res. 13: Smith CC, Fretwell SD The optimal balance between the size and number of offspring. Am. Nat. 108: Sokal RR, Rohlf FJ Statistical Tables. 3 rd edn. Freeman and Company, New York, U.S.A. Stubbs D, Hailey A, Pulford E, Tyler W Population ecology of European rises: review of field techniques. AmphibiaReptilia. 5: Swingland IR, Stubbs D The ecology of a Mediterraneanrise ( Testudo hermanni ): reproduction. JZool. Land. 05: Wallis IR, Hencn BT, Nagy KA Egg size and annual and annual egg production by female desert rise ( Gopherus agassizii ): the importance offood abundance, size and date of egg shelling. J. Herpel. 33; Willcmscn RE, Hailey A Status and conservation ot rises in Greece. Herpel. J. 1: Willemsen RE, Hailey A Variation of adult size ofthe rise Testudo hermanni in Greece: proximate and ultimate causes. J. Zool. Land. 48: Willemsen RE, Hailey A Variation in adult survival rate of the rise Testudo hermanni in Greece: implications for evolution of size. J. Zool. Land. 55: Zar JH Biostatistical Analysis, nd edn. PrenticeHall International, Englewood Cliffs, New Jersey, U.S.A. Hailey A, Loumbourdis NS Egg size and shape, dynamics and reproductive effort in European rises. Can. Received: 15 November 00 J. Zool. 66: