HERPETOLOGICAL JOURNAL, Vol. 12, pp. 115-121 (2002)

BODY MASS CONDITION AND MANAGEMENT OF CAPTIVE EUROPEAN TORTOISES

1 2 3 3 R. E. WILLEMSEN , A. HAILEY , S. LONGEPIERRE AND C. GRENOT

1 MonteCassinostraat 35, 7002 ER Doetinchem, The Netherlands

"Department of Zoology, Aristotelian University of Th essaloniki, GR-540 06 Th essaloniki, Greece

1Ecole Normale Superieure, Laboratoire d'Ecologie, CNR S- UMR 7625, 46 rue d 'Ulm, F- 75005 Paris, France

The condition index (Cl) of the tortoises Testudo graeca, T. hermanni hermanni, T. h. boettgeri and T. marginata was examined in captivity in southern and northern Europe. The CJ was calculated using mass-length relationships ofwild tortoises: log (MIM '), where Mis observed mass and M' is mass predicted fr om length. The mass-length relationships diffe red slightly between the subspecies of T. hermanni. Captive tortoises at the Centro Carapax (Italy) and the Oosterbeek Tortoise Study Centre (The Netherlands) had Cl within the same range as wild tortoises, so there was no general effect of captivity on body mass condition even at densities ten times the highest observed in the wild. However, the seasonal pattern of CJ at Oosterbeek diffe red significantly from that of wild tortoises, with a peak in late summer rather than in spring. Low Cl of tortoises in some enclosures at the Centro Carapax prompted supplementary fe eding before their health was affected. Tortoises at SOPTOM (France) during a period of disease had significantly lower Cl than wild tortoises, with mean CJ of -0.04 and mean relative mass (MIM ') of 91 %. The Cl offe rs a useful guide to the health and management of captive Mediterranean tortoises, although further data are required on those kept in different circumstances, such as outdoor-only enclosures in northern Europe.

Key words: captivity, condition index, management, Testudo, tortoise

INTRODUCTION or inadequate food) or obesity (e.g. from inactivity or excessively rich diet). There are many possible measures of condition in animals, the simplest of which is the body mass condi­ This paper deals with body mass condition in three large collections of captive tortoises, two in southern tion that compares mass with size (reviewed in Hailey, Europe and one in northern Europe. The two southern 2000; Willemsen & Hailey, 2002). A useful condition collections were in enclosed natural vegetation near to index (Cl) for tortoises is log (M/M'), where Mis ob­ wild populations, permitting a good test of the effects of served mass, M' is mass predicted from length (L), and captivity (including all the conditions associated with MIM ' is relative mass (usually expressed as a percent­ captivity such as social stresses or disease transmission age). Log (MIM') is equal to a residual from a regression from crowding, diet, and food supply) separate from of log Mon log L. A value of CI=O indicates that ob­ those of climate and other aspects of habitat. The sea­ served mass = predicted mass (i.e. MIM'= l.O or 100%), sonal variation of the Cl in northern Europe, where the whereas a negative value of the Cl indicates that ob­ climate is less suitable for tortoise activity (Lambert served mass is lower than predicted mass. Previous 1981, 1983), was also of interest. We also examine the studies have shown that the Cl in wild tortoises varies mass-length relationship in Testudo hermanni hermanni among species and areas with characteristic seasonal (formerly T. h. robertmertensi; Bour, 1986). This west­ patterns (Willemsen & Hailey, 2002). Veterinary stud­ ern subspecies is vulnerable (IUCN, 2000) and ies have also shown that body mass varies with health susceptible to habitat fragmentation (Longepierre, (Jackson, 1978, 1980, 1985): a relative mass less than Hailey Grenot, 2001) and loss of habitat (Guyot about 80% is an indication of poor health (Hailey, & & Clobert, 1997), while the eastern subspecies, h. 2000). The veterinary studies cited above used data T. from captive tortoises to calculate M'. It is not clear boettgeri, is more widespread and abundant (Willemsen Hailey, 1989) and not currently listed as threatened whether mass-length relationships of wild tortoises are & (IUCN, 2000). Measurement of condition in h. applicable to captive animals, or whether the latter gen­ T. hermanni is particularly important in view of controver­ erally suffer from chronic underweight (e.g. from stress sial collection and release programmes (Devaux, 1990) in which large numbers of wild tortoises pass through Correspondence: A. Hailey, School of Biological Sciences, captivity before relocation. T. h. hermanni is thought to University of Bristol, Woodland Road, Bristol, BS8 1 UG. E­ differ slightly in shape from T. h. boettgeri (Ernst & mail: [email protected] Barbour, 1989); if the mass-length relationships differ 116 R. E. WILLEMSEN ET AL.

TABLE 1. Details of enclosures, stocking densities and subspecies used to compare body mass condition for captive European tortoises in different study centres: Carapax (Italy); Oosterbeek (The Netherlands); SOPTOM (France).

Centre Species No. enclosures Area (ha) Density (ha-1) Date of measurements

Carapax T. h. hermanni 2 0.7 170-2 10 April-May 2000 Carapax T. h. boettgeri 0.025 600 April-May 2000 Carapax T. marginata 1 0.7 60 April-May 2000 Carapax T. graeca 2 0.015-0.15 400- 1000 April-May 2000

Oosterbeek T. h. boettgeri 0.03 1100 April-Oct. 1980, 1985

SOPTOM T. h. hermanni 3 0.03 2000-3300 July-Oct. 1996

significantly, then separate reference equations would different enclosures according to their origin, in vegeta­ be required to calculate M' and the Cl in the two subspe­ tion similar to that for T. h. hermanni. Natural food cies. plants such as Medicago, Trifolium, Rumex, Plantago METHODS and various Compositae were reduced in the enclosures due to tortoise grazing. All food plants had been elimi­ Wild tortoises were measured in the field as de­ nated from the T. h. boettgeri enclosure, which scribed by Stubbs et al. ( 1984) and released contained only grass; these tortoises were fe d with fruits immediately afterwards at the point of capture. Straight and sometimes vegetables (mostly Lactuca sativa and carapace length was measured to the nearest 1 mm on a Cichorium andivia). Captive individuals of T. h. flat-bed scale. The body mass of most tortoises was hermanni, T. h. boettgeri, T. graeca and T. marginata measured to the nearest 5 g with 2 kg or 3 kg Soehnle were measured and weighed in the last week of April spring balances. Small individuals were measured to 1 g and the first week of May 2000. Captive T. h. hermanni with a 250 g Soehnle spring balance. Tortoises in France were compared with 159 female and 109 male T. h. were measured to 0.01 g on an electronic balance. Sex hermanni froma local, wild population, measured in the was determined by plastral concavity and relative tail same season between 1990 and 1995; several years ' data size; only tortoises larger than 10 cm straight carapace were used to reduce the effect of variation of the Cl length are considered here. Data were analysed with among years. Each tortoise was considered only once. SPSS and Minitab for regression, analysis of variance Further details of Carapax can be found at the web site (ANOVA) and covariance (AN COY A), and compari­ http://www.novars.it/carapax/. son of a sample mean against an expected value (i.e. CI=O, when mean observed mass = predicted mass) us­ THE TORTOISE STUDY CENTRE, THE NETHERLANDS ing single-sample t-tests. In AN COYA we used log Mas the dependent variable, log Las the covariate, and sex or Tortoises were kept out of doors in a large garden at subspecies as a fixed factor. The variability of Cl values Oosterbeek, with plexiglass domes and a small glass­ was compared using Bartlett's test of homogeneity of house to which the animals had free access for variance (Sokal & Rohlf, 1981 ). Data on captive tor­ thermoregulation. Their food was growing plants, sup­ toises were from three sites and the stocking densities at plemented with vegetables, fruit and bread. Almost all each site are shown in Table 1. food plants were natural, or closely related to those eaten in the wild, such as Trifolium, Sedum, Ta raxacum THE CENTRO CARAPAX, ITALY and Plantago species. Tortoises hibernatedout of doors, either in natural refuges or in boxes filled with dead Tortoises were housed in enclosures containing their leaves or straw. Captive T. h. boettgeri were measured normal habitat of grassland, scrub and open woodland, and weighed monthly between April and October in on a hill slope. Cl measurements of T. h. hermanni were 1980 and 1985. A total of 26 tortoises (15 females and made in two enclosures with stocking densities of about 11 males) were measured at different times; each tor­ 200 ha-I (the highest population density found in wild toise is considered only once in each month. Further Testudo is about 100 ha-I; Stubbs et al., 1985). One en­ details of the Tortoise Study Centre can be found at the closure was based on an open field with encroachment web site http:// www.phys.uu.nl/-eendebak/schild/ of Rubus, coarse grasses, and macchia of the oaks schild.htrnl. Quercus cerris and Q. ilex, while the other was a former olive grove with Rubus scrub . The T. h. boettgeri meas­ THE STATION D'OBSERVATION ET DE PROTECTION DES ured here were kept in a grassland enclosure. T. TORTUES DES MAURES (SOPTOM), FRANCE marginata were in an enclosure of which a third was oak wood and the rest was olive trees and Rubus scrub; this Tortoises were kept in outdoor enclosures with low enclosure had been occupied for 10 years and food scrub of Cistus and Erica, but fewfood plants, and were plants were scarce and even the grass (not usually eaten fed vegetables and fruits. Captive T. h. hermanni were by Testudo) was cropped short. T. graeca were kept in measured from July to October 1996. Comparative data CONDITION INDEX IN CAPTIVE TORTOISES 117

TABLE 2. Condition index (Cl) of captive European tortoises. n is the number of individuals, except at Oosterbeek where this is the number of individual x month observations. t is the result of a single sample t test with the probability (P) that mean CI=O. Females (f) and males (m) are shown separately where there was a significant diffe rence in CJ between the sexes.

Group Location mean Cl n SD p

T. h. hermanni Carapax -0.0005 99 0.0443 0. 12 0.90 T. h. boettgeri Carapax 0.0177 14 0.0800 0.68 0.5 1 T. graeca ( f) Carapax -0.0547 15 0.0407 5.04 <0.001 T. graeca (m) Carapax 0.0018 9 0.0535 0.09 0.93 T. marginata Carapax -0.0229 20 0.0476 2.10 0.047 T. h. boettgeri Oosterbeek 0.0057 175 0.0391 1.91 0.057 T. h. hermanni SOPTOM -0.042 1 43 0.0462 5.98 <0.001

from wildtorto ises were from Vidauban and Cannet des not significantly different fromthe mean Cl of wild T. h. Maures, Var, France (described by Longepierre & hermanni in Italy {F1 =0.024, P=0.97). Most Cl val­ •362 Grenot, 1997) measured from July to October 1997- ues of captive T. h. hermanni at the Centro Carapax 1999. Each individual was considered only once. were between -0. 1 and +0.1 (Fig. 1 a), and the variability Further details of SOPTOM can be found at the web site of Cl was similar to that of wild tortoises in Italy 2 http ://www.tortues.com/index_ uk. html. (Bartlett's test, x =3.82, df=l, P>0.05).

RESULTS 14 SUBSPECIFIC DIFFERENCES IN T. HERMANN!

The mass-length relationships of wild T. h. hermanni 12 a Carapax in Italy and T. h. boettgeri in Greece were compared by 10 ANCOV A of log M by subspecies with log L as covariate. There was a significant diffe rence between 8 the two subspecies for fe males (F1 1 309=10. 14, P=0.001) � but not for males (Fl.2054=1.66, P 0.197), with females 6 being about 3% heavier in Italy than in Greece at the same length. The Cl of T. h. hermanni was calculated 4 using the mass-length relationships for wild tortoises fromItaly. An ANCOVA of log M by sex with log Las 2 covariate showed a significant difference between the O -+-r-r+-+-r-1-1-1-1-1-1-1-1-1-1f-!-f-l-f-l-f-l-1-+1f-l-1--r-i� sexes (F1 •262=14.99, P<0.001). Separate reference equa­ -0.15 -0.10 -0.05 0 0.05 0.10 0.15 tions were therefore used for females and males as follows: Condition index (log M/M') Females, Log M=-3.161 +2.767 log l - 0.04 (SE intercept=0. 108, SEb=0 .050, n=156, r2=95.2%) -� b � Ma les, Log M = -3.610 + 2,967 log L C) 0.02 0 (SE intercept=0.238, SEh=0.1 14, n=109, r2=86.3%). >< Q) The overall standard deviation of the Cl was 0.03 8 "C 0.00 (n=265). The variability of the Cl in wild T. h. hermanni c: was thus identical to that of T. h. boettgeri in Greece, c: 0 which also had SD=0.038 (Willemsen & Hailey, 2002). ;e -0.02 "C c: Oosterbeek CENTRO CARAPAX 0 (.) -0.04 �T---�--.--�---.-----.----,,- The Cl of captive T. h. hermanni at the Centro A M J J A s 0 Carapax was calculated using the mass-length equations for wild tortoises fromItaly (above). The Cl did not dif­ Month fer significantly between females and males FIG. 1. (a) Frequency distribution of condition index in (F1 97=0.009, P=0.997). The mean Cl for captive tor­ • captive T. hermanni hermanni at the Centro Carapax, Italy. toises was not significantly different from 0 (Table 2) (b) Seasonal variation of condition index in T. hermanni (this mean is not necessarily equal to 0 because the Cl boettgeri; captive tortoises in Oosterbeek, the Netherlands was calculated using the regression for wild, not captive, (solid circles) and wild tortoises in Greece (open circles, from tortoises). The mean Cl for captive tortoises was also Willemsen & Hailey, 2002). Bars show ± SE. 118 R. E. WILLEMSEN ETAL.

20 (F1 1 8=1.45, P=0.244); mean Cl was just significantly 18 a France different from 0 (Table 2), with tortoises having slightly lower mass than predicted. 16 (wild) - � 14 OOSTERBEEK - >. 12 The Cl of T. h. boettgeri in northern Europe was ex­ CJ c: amined in relation to season. A two-way ANOVA of Cl Cl) 10 ::I with sex and month showed no significant sex x month C" 8 interaction (F6 161=0 .21, P=0 .973), indicating that the Cl) • ... LL 6 seasonal pattern of Cl did not differ between females 4 and males. The seasonal pattern (Fig. 1 b) was, however, significantly different fromthat of wild T. h. boettgeri in 2 Greece (Willemsen & Hailey, 2002); two-way ANOVA 0 of Cl with status (wild/captive) and month showed a sig­

-0.15 -0.10 -0.05 0 0.05 0.10 0.15 nificant interaction of status x month (F6 6185=5.82, • 20 P<0.001 ). The Cl of the captive tortoises was lower than T. h. boettgeri 18 b that of wild in April and May, but in­ SOPTOM creased until September, while that of wild tortoises 16 - declined after June. Although seasonal patterns of Cl

0� 14 differed between wild and captive tortoises, the range of - seasonal variation (fromabout -0.02 to 0.02) was small >. 12 CJ compared to the total variation. The mean Cl at c: 10 Cl) Oosterbeek was not significantly different from 0 (Table ::I C" 8 2), and the variability was very similar to that of wild T. Cl) ... h. boettgeri in Greece (SD=0.039 and 0.038, respec­ LL 6 4 tively). 2 SOPTOM

0 The Cl of wild T. h. hermanni in France was calcu­ -0.15 -0.10 -0.05 0 0.05 0.10 0.15 lated using the mass-length equations for wild T. h. hermanni Condition index (log M/M') in Italy (above). The Cl did not differ signifi­ cantly between the sexes (F1 55=3 .64, P=0.062). The , mean Cl was 0.0026 (n=57, SD=0.0437), not signifi­ FIG. 2. Frequency distributions of condition index in (a) wild T. hermanni hermanni in France, (b) captive T. h. hermanni cantly diffe rent from 0 (t=0.44, df=56, P=0 .66), and at SOPTOM, France. most values were between -0. 1 and +0. 1 (Fig. 2a). The Cl of captive T. h. hermanni at SOPTOM calculated us­ There were similar results for captive T. h. boettgeri ing the same equations also did not differ between the at the Centro Carapax, with Cl calculated fromthe mass­ sexes (F1 41 =0.51, P=0.480). However, the mean Cl at M length equations for wild T. h. boettgeri from Greece. SOPTO was low, and diffe red significantly from 0 There was no significant difference between females (Table 2) and from that of wild T. h. hermanni in France and males (F1 1 =0.494, P=0.622), and the mean was not (F1 98=24.4, P<0.001). The frequency distribution of the 2 • significantly different from 0 (Table 2). The variability Cl was shifted towards lower values (Fig. 2b), with 10% of Cl of captive T. h. boettgeri at the Centro Carapax of observations being below -0.1 compared to about 1 % was, however, significantly greater than that of the cap­ being below -0.1 in other samples (Fig la; Hailey, 2000; 2 tive T. h. hermanni (x =10.69, df=l, P<0.01). The Willemsen & Hailey, 2002). Nevertheless, the variabil­ greater variability may have resulted from the diverse ity of the Cl at SOPTOM was similar to that of wild T. h. 2 sources and histories of the non-native tortoises at the hermanni in France (x =0. 15, df=l, P>0.05). Centro Carapax, which were acquired as donations and The variability of Cl (as measured forexample by the customs seizures, usually of unknown provenance. SD) is of interest because some putative causes of low The Cl of captive T. graeca at the Centro Carapax, mean Cl, such as interference competition for food or calculated using the mass-length equations of wild T. stress from high aggression, might be expected to in­ graeca (Willemsen & Hailey, 2002), varied signifi­ crease variation among individuals (with the losers cantly with sex having particularly low values). The variability of Cl (F1 22=7 .80, P=0.01 1). The mean Cl was • o significantly different from 0 in females, which had differed significantly among the seven captive gr ups 2 lower mass than predicted, but not in males (Table 2). described in Table 2 (x =20.20, df=6, P<0.01). The The Cl of captive T. marginata at the Centro Carapax, Oosterbeek sample was the least variable; however, this calculated using the mass-length equations of wild T. sample included repeated measurements on the same in­ marginata, did not differ significantly between the sexes dividuals, which would tend to reduce the variability of CONDITION INDEX IN CAPTIVE TORTOISES 119 the data. Nevertheless, the variability of Cl differed sig­ low Cl of the tortoises prompted increased artificial nificantly among the remaining six groups (x2=11.98, food supply to those enclosures in May 2000. Changing df=5, P<0.05). The average variability of the Cl in all plant species composition is a potential problem for all captive tortoises (forcom parison with wild populations) captive Mediterranean tortoises in enclosures of natural was calculated as the weighted (by sample size) mean vegetation. Tortoises consume the available food plants, SD, using the weighted mean variance. The mean SD which are not regenerated quickly enough to provide a was 0.044 (calculated from the weighted mean vari­ sustainable food supply and are replaced by less palat­ ance). able or less edible species. The enclosures may thus continue to have a green and well-vegetated appearance DISCUSSION but contain little natural food. Tortoises in captivity in Italy and in the Netherlands Scarcity of food plants in enclosures also occurred at were found to have Cl values similar to those in the wild SOPTOM, but there was also a problem with respiratory and appeared to be in good health since reproduction disease (Le Garff, 1998; Pieau, 1999). Both was frequent in both centres (R. E. Willemsen, unpub­ herpesviruses and mycoplasmas have been found incap­ lished observations; Eendebak, 1995). Captivity thus tive tortoises at SOPTOM (Fertard, 1997), although the does not necessarily lead to a general tendency in former were mostly associated with T. aeca.gr The Testudo (that would be seen in most captive tortoises) to mean Cl of T. h. hermanni at SOPTOM is equivalent to be either underweight or overweight. Spratt ( 1990) a relative mass of 91 %. A similar finding has been re­ reached a similar conclusion for giant tortoises. Mass­ ported in the desert tortoise Gopherus agassizii: length equations for wild populations may thus be mass-length relationships differed significantly between appropriate for calculating the Cl of captive tortoises. healthy tortoises and those with upper respiratory tract The western subspecies of T. hermanni was slightly disease (caused by My coplasma agassizii), tortoises heavier than T. h. boettgeri at the same length, a differ­ with clinical signs weighing on average 7% less than ence that corresponds to the more domed shape of T h. those without (Jacobson et al., 1993). Ten percent of hermanni (Ernst & Barbour, 1989). Separate mass­ captive T. h. hermanni at SOPTOM had Cl below -0. 1, length equations should therefore be used to calculate equivalent to a relative mass of80%, the recommended M' in the two subspecies. Most T hermanni in captivity threshold for veterinary attention (Hailey, 2000). A re­ are T. h. boettgeri, of which there was previously a large port from the Societe Herpetologique de France has internationaltrade from the Balkans; relatively fewT. h. recommended the separation of T. h. hermanni enclo­ hermanni were exported. sures at SOPTOM fromthose housing T graeca and T. The seasonal pattern of Cl of T. h. boettgeri at marginata (which may be the sources of exotic diseases Oosterbeek, with maximum values in late summer, was in French tortoises), and improved monitoring of health rather different to that in Greece. This pattern supports (Pieau, 1999). Measurement of Cl would be advisable the hypothesis that while differences in Cl among sites as part of this monitoring. in spring are related to activity and thermoregulation, An additional problem at SOPTOM was the absence differences in summer and autumn are related to food of permanent water points in enclosures. Wild T. h. availability (Willemsen & Hailey, 2002). The peak of hermanni in France travel large distances to find free Cl was thus late at Oosterbeek, continuing a trend ob­ water when little succulent plant food is available in served from southernto northern Greece. The peak did summer (Longepierre, 2001). Water availability could not correspond to the hottest time of year; temperatures affect the Cl directly through the degree of body hydra­ in the Netherlands are maximal in July and August, and tion, and indirectly through better ability to digest food decline in September (Anonymous, 1996; data for when water is available. Extensive studies on American Winterswijk in the eastern Netherlands). High Cl in au­ Gopherus tortoises show the importance of the interac­ tumn at Oosterbeek was therefore not due to activity/ tion between food quality, water availability, and thermoregulation, but probably to food availability. energetics (Medica, Bury & Luckenbach, 1980; Turner, Mediterranean habitats are characterised by dry sum­ Medica & Lyons, 1984; Nagy & Medica, 1986; Henen, mers with low food availability in autumn, and low 1997; Nagy, Herren & Vyas, 1998; Wallis, Herren & tortoise activity (Hailey & Willemsen, 2000), whereas Nagy, 1999). Drinking allows these tortoises to main­ food and water were always available in captivity. The tain a positive energy balance when feeding on dry results at Oosterbeek show that declining Cl in autumn plants in summer. This effect of water on digestibility is not constant (for example in preparation for hiberna­ may have contributed to the low Cl at SOPTOM (where tion) , but depends on the environment. most measurements were made in late summer, and wa­ Three groups of tortoises had mean Cl significantly ter was absent), and to the high Cl in late summer at lower than 0, i.e. body mass on average lower than pre­ Oosterbeek (where water was always readily available) dicted: T. marginata and fe male T. graeca at the Centro compared to wild T h. boettgeri. Carapax, and T h. hermanni at SOPTOM. The enclo­ The variability of Cl in captive tortoises (overall sures of T. graeca and T. marginata at the Centro SD=0.044) was between that of wild T. hermanni Carapax were found to have a lack of growing food (SD=0.038) and T. graeca (SD=0.039) and that of wild plants and encroachment of non-edible vegetation. The T. marginata (SD=0.046) (Willemsen & Hailey, 2002). 120 R. E. WILLEMSEN ET AL.

There was thus no greatly increased variability of Cl in Boussekey, M. ( 1988). Recherche experimentale captive populations, even in those groups which had low d'etablissement d'une hierarchie au sein d'un groupe mean Cl (T.marginata, female T. graeca, and T. h. captif de cistudes d 'Europe Emys orbicularis (Repti 1 ia, hermanni at SOPTOM). This suggests that captive Chelonii). Bulletin de la Societe Herpetologique de Mediterranean tortoises do not suffer from aggressive France 46, 1-9. interactions or interferenceco mpetition for food,which Bury, R. B. & Wolfheim, J. H. (1973). Aggression in free­ might tend to increase the variability of Cl between living pond turtles (Clemmys marmorata). BioScience dominant and subordinate individuals. Such aggressive 23, 659-662. interactions have often been observed in omnivorous Bury, R. B., Wolfheim, J. H. & Luckenbach, R. A. (1979). chelonians in captivity (Lardie, 1964; Boice, 1970; Agonistic behavior in free-living painted turtles Froese & Burghardt, 1974; Boussekey, 1988) and in the (Chrysemys picta bellii). Biology of Behavior 4, 227- wild (Bury & Wolfheim, 1973; Bury, Wolfheim & 239. Luckenbach, 1979; Lovich, 1988). Captive tortoises ap­ Devaux, B. ( 1990). Reintroduction de tortues d'Hermann pear to be less aggressive (Evans & Quaranta, 1949, (Testudo hermanni hermanni) dans le massif des 1951; Guyot & Lescure, 1994), perhaps because the Maures. Revue Ecologie (Terre et Vie) Supplement 5, food of herbivores is less subject to competition in the 29 1 -297. wild. Aggressive interactions were not observed in cap­ Eendebak, B. T. ( 1995). Incubation period and sex ratio of tivity during this study. Hermann's tortoise, Testudo hermanni boettgeri. In conclusion, housing European tortoises in dense Chelonian Conservation and Biology 1, 227-23 1. groups had no detrimental effect on their body mass Ernst, C. H. & Barbour, R. W. ( 1989). Tu rtles of the world. condition. Stocking densities ten times greater than the Washington, D.C.: Smithsonian Institution Press. highest population densities in the wild are possible, Evans, L. T. & Quaranta, J. V. ( 1949). Patterns of provided that food and water supplies are adequate and cooperative behavior in a herd of 14 giant tortoises at precautions are taken against disease. Further informa­ the Bronx Zoo. Anatomical Record 105, 506. tion is needed, however, on the effects of other regimes Evans, L. T. & Quaranta, J. V. ( 1951 ). A study of the on the Cl and its seasonal variation. Data from non-spe­ social behavior of a captive herd of giant tortoises. cialist facilities with fewer tortoises, and from tortoises Zoologica, New Yo rk 36, 171-181. kept in indoor cages or outdoors in northern Europe Fertard, B. ( 1997). Study of tortoise pathology at the without access to glasshouses, would be particularly in­ Village des To rtues. Report to the Scientific Council teresting. and Board of Directors (In French). Gonfaron: SOPTOM. ACKNOWLEDGEMENTS Froese, A. D. & Burghardt, G. M. (1974). Food competition in captive juvenile snapping turtles We thank Donato Ballasina forfacilities at the Centro Chelydra serpentina. Animal Behaviour 22, 735-740. Carapax, the Communita Montana de Colline Guyot, G. & Clobert, J. ( 1997). Conservation measures for Metallifere, and Corinne Maag for her hospitality and a population of Hermann's tortoise Testudo hermanni protection of tortoises in Italy; Bert Eendebak for data in southern France bisected by a major highway. on captive tortoises at Oosterbeek, Jacques Thiebaud Biological Conservation 79, 251-256. for help in the field at Centre Var, particularly for the Guyot, G. & Lescure, J. ( 1994). Etude preliminaire du measurements on tortoises, and Clive Cummins and an comportement alimentaire en enclos semi-nature! chez anonymous referee for useful comments. We also wish la tortue d 'Hermann (Testudo hermanni hermanni to thank the SIVOM of Centre Var and the collective of Gmelin, 1789). Bulletin de la Societe Herpetologique Cannet des Maures. This study was supported, in part, de France 69, 19-32. by the grant DGAD/SRAE No. 96 103 from the Hailey, A. (2000). Assessing body mass condition in the tortoise Ministere de l'Amenagement du Territoire et de Testudo hermanni. Herpetological Journal10 , 57-61. 'Environnement. I Hailey, A. & Willemsen, R. E. (2000). Population density and adult sex ratio of the tortoise Testudo hermanni in REFERENCES Greece: evidence for intrinsic population regulation . Anonymous. ( 1996). Tables of temperature, relative Journal of Zoology, London 251, 325-338. humidity, precipitation and sunshine fo r the world. Henen, B. T. ( 1997). Seasonal and annual energy budget of Part Ill Europe and the Azores. London: female desert tortoises (Gopherus agassizii). Ecology Meteorological Office. 78, 283-296. Boice, R. ( 1970). Competitive feeding behaviours in IUCN (2000). 2000 IUCN red list of threatened animals. captive Te rrapene c. carolina. Animal Behaviour 18, Gland: IUCN. 703-7 10. Jackson, 0. F. ( 1978). A method of assessing the health of Bour, R. (1986). L'identite des tortues terrestres European and North African tortoises. British europeennes: specimens-types et localites-types. Ve terinary Zoological Society 1978, 25-26. Revue Francais d'Aquariologie et Herpetologie 13, Jackson, 0. F. ( 1980). Weight and measurement data on 111-122. tortoises (Testudo graeca and Testudo hermanni) and CONDITION INDEX IN CAPTIVE TORTOISES 121

their relationship to health. Jo urnal of Small Animal · Pieau, C. (1999). Affaire S.O.P.T.O.M . .... suite et fi n. Practice 21, 409-4 16. Bulletin de la Societe Herpetologique de France, Jackson, 0. F. ( 1985). The clinical examination of reptiles. Supplement 90, 14-17. In Reptiles: breeding, behaviour and veterinary Sokal, R. R. & Rohlf, F. J. ( 198 I). Biometry. Second aspects, 91-97. Townson, S. & Lawrence, K. (Eds). edition. San Francisco: W. H. Freeman. London: British Herpetological Society. Spratt, D. M. (1990). 'Jackson's ratio' and the Aldabra Jacobson, E. R., Weinstein, M., Berry, K., Hardenbrook, giant tortoise (Geochelone gigantea). Veterinary B., Tomlinson, C. & Freitas, D. (1993). Problems with Record 127, 262-263. using weight versus carapace length relationships to Stubbs, D., Hailey, A., Pulford, E. & Tyler, W. (1984). assess tortoise health. Veterinary Record 132, 222- Population ecology of European tortoises: review of 223. field techniques. Amphibia-Reptilia 5, 57-68. Lambert, M. R. K. ( 198 I). Temperature, activity and field Stubbs, D., Swingland, I. R., Hailey, A. & Pulford, E. sighting in the Mediterranean spur-thighed or common (I985). The ecology of the Mediterranean tortoise garden tortoise Testudo graeca. Biological Testudo hermanni in northern Greece. The effects of a Conservation 21, 39-54. catastrophe on population structure and density. Lambert, M. R. K. (1983). Some factors influencing the Biological Conservation 31, 125-152. Moroccan distribution of the western Mediterranean Turner, F. B., Medica, P. A. & Lyons, C. L. (1984). spur-thighed tortoise, Testudo graeca graeca L., and Reproduction and survival of the desert tortoise those precluding its survival in NW Europe. (Scaptochelys agassizii) in lvanpah Valley, California. Zoological Journal of the Linnean Society 79, 149- Copeia 1984, 811-820. 179. Wallis, l. R., Henen, B. T. & Nagy, K. A. ( 1999). Egg size Lardie, R. L. ( 1964). Pugnacious behavior in the soft-shell and annual egg production by fe male desert tortoises turtle Trionyx sp inife r pallidus and implications of ( Gopherus agassizii): importance of food abundance, territoriality. Herpeto/ogica 20, 281-284. body size, and date of egg shelling. Jo urnal of Le Garff, B. (1998). Vie de la Societe, VIII. Questions Herpetology 33, 394-408. diverses: affaire SOPTOM. Bulletin de la Societe Willemsen, R. E. & Hailey, A. (1989). Status and Herpetologique de France 85-86, 68-69. conservation of tortoises in Greece. Herpetological Longepierre, S. (2001 ). Ecophysiologie de Testudo Journal I, 315-330. hermanni hermanni Gmelin, 1789: evaluation des Willemsen, R. E. & Hailey, A. (1999). Variation of adult contraintes environnementales et alimentaires en body size of the tortoise Testudo hermanni in Greece: mi lieu nature! dans le sud de la France. These de proximate and ultimate causes. Journal of Zoology, doctorat. Universite Claude Bernard Lyon I- Ecole London 248, 3 79-396. Normale Superieure de Paris. Willemsen, R. E. & Hailey, A. (2002). Body mass Longepierre, S. & Grenot, C. ( 1997). Distribution de la condition in Greek tortoises: regional and interspecific tortue d 'Hermann (Testudo hermanni hermanni). variation. Herpetological Journal 12, 105-1 14. Compte-Rendu de l 'etude ecologique de 10 secteurs dans la Plaine des Ma ures. Le Luc: SIVOM du Centre Var. Longepierre, S., Hailey, A. & Grenot, C. (2001). Home range area in the tortoise Testudo hermanni in relation to habitat complexity: implications for conservation of biodiversity. Biodiversity and Conservation 10, 113 1- 1140. Lovich, J. ( 1988). Aggressive basking behavior in eastern painted turtles (Chrysemys picta picta). Herpeto/ogica 44, 197-202. Medica, P. A., Bury, R. B. & Luckenbach, R. (1980). Drinking and construction of water catchments by the desert tortoise, Gopherus agassizii, in the Mojave desert. Herpetologica 36, 301-304. Nagy, K. A., Hen en, B. T. & Vyas, D. B. ( 1998). Nutritional quality of native and introduced food plants of wild desert tortoises. Journal of Herpetology 32, 260-267. Nagy, K. A. & Medica, P A. ( 1986). Physiological ecology of desert tortoises in southern Nevada. Herpeto/ogica 42, 73-92. Accepted: I 0. 6. 02