Hatching success, delay of emergence and ... - Wiley Online Library

J. Zool., Lond. (1997) 243, 543-553

Hatching success, delay of emergence and hatchling biometry of the spur-thighed tortoise, Testudo graeca, in south-western Spain CARMEN DIAZ-PANIAGUA, CLAUDIA KELLER A N D ANAC. ANDREU Estacidn Bioldgica de Doiiana, Apdo. 1056, 41080 Sevilla, Spain

(Accepted 28 February 1997) (With 3 figures in the text) Hatching success, egg incubation, emergence and hatchling characteristics were assessed for 44 naturally incubating nests of Testudo graeca in south-westem Spain. Nest predation rate was 4.5% and overall hatching success was 82.4%. Incubation periods ranged from 78 to 114 days, and hatchlings delayed emergence from the nest from one to 23 days. Emergences occurred from mid August to late September, and were not correlated with nesting dates, but earlier laid nests had longer incubation times, which was probably owing to lower temperatures experienced by clutches laid at the beginning of the nesting season. Variance of hatchling body size and mass was high and was mainly influenced by the gravid female. Mean straight carapace length was 34.14mm, and mean body mass 10.8g. Hatchlings from clutches laid last in the nesting season had significantly better physical condition. Hatchling mass was positively correlated with egg mass, and both variables were positively correlated with emergence date. Both better physical condition and relatively late emergence may confer advantages to hatchlings in the face of unfavourable environmental conditions in autumn.

Introduction The development and survival of chelonian eggs, as well as hatchling characteristics, are influenced both by incubation conditions and by maternal genetic and non-genetic contributions to the eggs (e.g. Packard & Packard, 1988; Brooks et al., 1991; Janzen, 1993 a , h; Bobyn & Brooks, 1994; Rowe, 1995). Most studies on chelonian egg incubation have been carried out under laboratory conditions, where the possibility of controlling for one or more variables allows separate consideration of the effects of one or more of the various factors affecting incubation (reviewed in Packard & Packard, 1988). Only a few studies, however, have dealt with the range of variation in incubation parameters of naturally incubated eggs and its influence on embryos and hatchlings (Pieau, 1982; Packard et al., 1987; Cagle et al., 1993). Incubation time and emergences are supposed to be adjusted to environmental conditions through long-term optimization of traits like the timing of egg-laying and nest-site choice, and, in some cases, by the capability of hatchlings to delay emergence from the nest (Gibbons & Nelson, 1978; Congdon & Gibbons, 1985; Jackson, 1994; Costanzo et al., 1995), in order to maximize hatchling survival rates. Nests in the field are otherwise subject to hazards such as predation and trampling, which may influence significantly the annual recruitment rate into the population (e.g. MacFarland, Villa & Tor0 1974a; Hirth, 1980; Landers, Gamer & McRae, 1980; Thompson, 1983; Congdon et al., 1983; Swingland & Stubbs, 1985; Germano, 1994). The present study has been carried out on a population of Testudo graeca from south-westem Spain, in which females lay one to four annual clutches, with an average clutch size of three to four semispherical, rigid-shelled eggs, laid from April to June (Diaz-Paniagua, Keller & Andreu, 1996). Our aims were to assess: (1) hatching success and causes of egg mortality; (2) incubation time and delay 543 0 1997 The Zoological Society of London

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from hatching to emergence in field developing nests, as well as their relation with nesting date and variation among clutches; and (3) variation among hatchling size and body condition, and the influence of incubation time and clutch on hatchling characteristics.

Material and methods The study was carried out at the Biological Reserve of Doiiana, a protected area located in south-westem Spain between the Atlantic coast and the mouth of the Guadalquivir river. The climate is dry and hot in summer and mild in winter. Annual rainfall is an average of 580 mm and concentrates in autumn and winter. Testudu graecu mainly inhabit sandy areas covered by mediten-anean heath. Further details on the tortoise habitat are found in DiazPaniagua, Keller & Andreu (1995). Nests were located from May to June following the method described by Keller (1993). Seven nests were located in 1990, 23 in 1991, and 14 in 1994. Straight carapace length and body mass of females after egg-laying were recorded for each nesting female. Clutch size and egg mass averaged, respectively, 3.5 eggs and 14.2 g, over the 3 years, and did not vary significantly among years (clutch size: F(3,40)= 1.84, P = 0.1562; mean egg mass/ clutch: F(3,3h)= I .27, P = 0.2993) (Table I). Clutch sizelegg size relationships in this population are described elsewhere (Diaz-Paniagua et al., 1996). Stubbs & Swingland (1985) reported egg predation to occur mainly in days close to oviposition. Therefore, in 1990 and 1991, nests were left exposed until mid-August, and until mid-July in 1994. For the remaining time, until emergence, nests were protected under wire-mesh cages. Nests were opened in July, and eggs measured and numbered as described in Dim-Paniagua et al. (1996). From August onwards, nests were visited daily in order to record hatchling emergence. In 1990 and 1991, nests were inspected only visually, so that emergence could be reliably detected only when pieces of egg-shell were dragged out along with the hatchling. In 1994, a grid of thread and wooden sticks was placed over the nest, enabling the detection of hatchling emergence through a disorder in the grid arrangement. In seven of the 14 nests, a section of the nest wall was replaced by a glass plate, so that eggs could be observed inside the nest. The hole on the outer side of the glass plate was filled with a plastic bag containing sand, which could easily be removed for nest inspection. In this way, hatching and delay of emergence could be recorded. Owing to the reduced hatching success observed in these 7 nests, they were not considered in analyses of hatching success (see Results). The date of hatching is considered here as the day when first signs of pipping of the egg shell were observed, while the date of emergence is defined as the day on which the hatchlings leave the nest. Incubation time refers to the period from egg-laying to hatching and time to emergence is considered as the period from egg-laying to emergence, and the difference between both periods is defined as the delay of emergence. All hatchlings were weighed to the nearest 0.1 g and measured (straight carapace and plastron length) to the nearest 0.5 mm. Physical condition of hatchlings was analysed as the residuals of the regression of log body mass on log carapace length. The dates of nesting, hatching and emergence were considered as the number of days from 1 st January for statistical analyses. Since eggs within clutches cannot be considered as statistically independent observations, data for eggs and hatchlings were treated as mean values per clutch. The relationship between variables was investigated through parametric correlational analysis, after assessing normality of variable and residual distributions. Owing to reduced sample sizes, Spearman rank correlation was employed for analyses involving incubation time and the duration of the emergence delay. Results were considered non-significant at P > 0.05. Given the small within clutch sample size (maximum four hatchlings), variability among clutches was analysed through Kruskal-Wallis tests. Only clutches with data for 3 or 4 hatchlings were used in the analyses. The influence of nesting date on hatchling phenotype was tested through parametric ANOVA on 5 groups of clutches grouped according to nesting date (1: < 11 May; 2: 11-19 May; 3: 20 May-1 June; 4: 2-13 June; 5: 713 June), and variables averaged per clutch. When designs involved covariables, the variables were rank transformed across clutches and then submitted to parametric ANCOVA, using PROC GLM (SAS Inst., 1989).

HATCHING AND EMERGENCE OF TESTUDO GRAECA

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TABLE I Fate of nests and eggs of Testudo graeca in Dofiana in each study year. Data from 1994 were divided into unmodified nests ( 1 9 9 4 ~and ) nests modijied for hatching control (1994m) (see Material and methods). Numbers in parenthesis indicate percentages in relation to total number r$eggs/nests. Clutch size and egg mass are indicated as means ? S.D.

No. nests

Year

Clutch size

Egg mass

3.1 ? 0.7 3.7 ? 0.9 3.0 t 1.0 3.6 ? 0.8 3.5 ? 0.9

l4.2? 3.0 14.7 -C 1.3 13.6 ? 2.0 13.4 2 2.0 14.2 2 1.8

~.

1990 1991 1994u 1994m TOTAL

7 23 7 7 44

Total no. Nests predated of eggs (%I 22 86 23 25 156

Eggs broken ~.

2 (28.6) 0 0 0 2 (4.5)

2 0 2 2 6

Eggs unhatched

Eggs hatched

(%)

(%)

5 (22.7) 6 (7.0) 2 ( 8.7) 9 (36.0) 22 (14.1)*

9 (40.9) 80 (93.0) 19 (82.6) 14 (56.0) 122 (78.2)*

..

(9.0) (8.7) (8.0) (3.8)

* 9.9% unhatched eggs and 82.4% hatched eggs not considering results from modified nests Results Hatching success

Six eggs, belonging to three nests, were found broken when the nests were opened for egg measurement and represented 3.8% of the 156 eggs monitored during the study period. All broken eggs belonged to clutches of four or five eggs. Only two of the 44 nests were preyed upon, both in 1990. The predators were not identified. One of these nests contained two broken eggs, the smell of which could have attracted the predator. In 1991 and 1994, no signs of predation were observed. A total of 22 eggs did not hatch, 10 of which represented three entire clutches. No correlation was observed between hatching success (expressed as the percentage of hatched eggs in a clutch) and clutch size or mean egg mass/clutch. Two whole clutches and two additional eggs from modified nests in 1994 did not hatch, a much higher proportion than that observed for other groups (Table I). Since we cannot discard that higher egg failure in modified nests was due to increased nest manipulation, it is more reasonable to consider hatching success only in relation to unmodified nests, which thus averaged 82.4% for the whole study period. Hatching and emergence

From one to four emergences were registered for 28 nests (54 hatchlings in total). All emergences occurred during August and September, with 66% registered within the last week of August and the first two weeks of September (Table 11).

T A B L EI1 Sample size, range of nesting and emergence dates and summary statistics of emergences f o r the three study years Year 1990 1991 1994 TOTAL

No. nests

No. hatchlings

4 12 12 28

7 24 23 54

Range of nesting dates

1 May-30 4 May-21 12 May-I3 1 May-21

* Values are means, followed by the range

May Jun. Jun. Jun.

Range of emergence dates

19 Aug-I0 25 Aug-27 17 Aug-20 17 Aug-27

Sept. Sept. Sept. Sept.

Time to emergence (days)* 102.4 (94-113) 112.2 (82-140) 97.5 (84-121) 104.0 (82- 140)

546

140 , (a) 130 :

70 60

8

0

Emergence Hatching

i

h

$

9 -

3

10 5

$

0

Sept. 30

Q

t

0

0 0

a,

c

$

Sept. 15

$ C

a,

Aug. 31

E

W

Aug. 15 20 Apr.

30 Apr.

15 31 May May Nesting date

15 Jun.

FIG.1. Relationship between nesting date and: (a) incubation time and time to emergence; (b) delay of emergence; and (c) emergence date. Each point represents one individual.

Time to emergence averaged 102.4 days in 1990, 112.2 days in 1991 and 97.5 days in 1994 and did not differ significantly among years (F(2,2s)= 2.65, P = 0.088). While nesting dates spanned over a period of 50 days, emergences were more synchronized, occurring within a period of 34 days (Table 11). Earlier clutches had generally longer times to emergence than later ones (date of nesting x time to emergence: r = -0.755, P < 0.0001, N = 20) (Fig. la), therefore emergences did not occur in the same order as nesting dates. For example, out of four cases of two successive clutches of a same female, laid at approximately monthly intervals, only once did hatchlings from the first clutch emerge earlier, and in all cases both clutches emerged at intervals of one to eight days. Nevertheless, all clutches laid in June emerged in September (Fig. lc). Out of 10 clutches for which emergence dates of all hatchlings were recorded, emergences were synchronous in four cases, while in the other six we observed intervals of up to 11 days between the first and last emergence. Analysis of covariance of time to emergence for four females for which 2-3 clutches were available, using nesting date as a covariate, revealed a significant variation in time to emergence

547

HATCHING AND EMERGENCE OF TESTUDO GRAECA

TABLE 111 Body size (straight carapace length) and body mass of hatchling Testudo graeca in Dofianu. Statistics are presented as averaged mean values per nest and means f o r the total number of individuals (in purenthesis). ANCOVA statisrics of interclutch variability with time to emergence as covariable are given for each variable

Body mass (8)

Mean 2 S.D. Range N Clutch Time to emergence

10.77 2 2.01 8.10- 15.6 26 F(8.24) = 378.69, F(1,24)= 25.41,

(10.67 ? 2.17) (7.0-16.25) (79) P = 0.0001 P = 0.3386

Body size (mm) 3 4 . 1 4 i 1.92 30.33-38.59 26 Fo,,,, = 4.14, F, 1,24) = 3.80,

(34.11 i 2 . 5 3 ) (28.7-39.9) (78) P = 0.0032 P = 0.0632

among females (F(female) = 38.00, P < 0.0001). Nesting date, however, was also shown in this case to have a stronger influence on time to emergence (F(temerg) = 497.29, P < 0.0001). The model accounted for 98.6% of the variance observed in time to emergence. Hatching and delay of emergence were recorded for five clutches and 14 eggs. Hatching was detected between 20 August and 7 September, incubation averaging 94.9 days ( 2 13.4, range 78-1 14). When averaged per clutch, mean incubation time was 95.47 days (t 13.1). Incubation time differed significantly among clutches (Kruskal-Wallis H = 11.33, P = 0.023 1, d.5 = 4) and also varied within clutches, with intervals of zero to six days between first and last hatching. As expected, clutches laid earlier in the nesting season had longer incubation times than later ones, although the correlation was not significant (nor with any other variable), probably due to the small sample size (Fig. la). Hatchlings remained inside the nest on average for 9.13 days (t6.06, range 1-23) before emerging. Within clutches, differences between shortest and longest delays of emergence varied between one and eight days. Like incubation time, delay of emergence was not significantly correlated with nesting date, nor with any other variable (Fig. Ib).

Hatchlings Hatchlings showed a considerable size variability (Table 111),averaging 34.1 mm straight carapace length and 10.8 g body mass. Analysis of variance using time to emergence as a covariate, revealed a significant interclutch effect on hatchling size and mass, while time to emergence had no effect on hatchling phenotype (Table 111). The same results were obtained for physical condition of hatchlings (F,1,,h(8,24) = 3.87, P = 0.0047; F,,,,,(1,24) = 1.09, P=O.3075). Individuals emerging later were significantly heavier and larger (body size x emergence date: r = 0.390, P = 0.048; body mass x emergence date: r=0.640, P=O.O04, N=26) (Fig. 2a). Physical condition of hatchlings was not significantly correlated with date of, nor time to, emergence. ANOVA on clutches grouped according to nesting date revealed significant differences for hatchling physical condition (F(4,21) = 4.60, P = 0.0079), which was mainly due to the better physical condition of hatchlings from latest nests (Tukey a posteriori test) (Fig. 3). Nesting date had no influence on body size and mass. Hatchling size, mass and physical condition were not significantly related to maternal body size, mass and physical condition, nor clutch size, but hatchling size and mass were significantly correlated with egg mass (r(size) = 0.672, P = 0.0002; r(mass) = 0.668, P = 0.0003, N = 24) (Fig. 2b). Egg size and mass were not related to nesting date, nor time to emergence, but egg mass was positively and significantly correlated with date of emergence (r = 0.560, P = 0.0044, N = 24).

C. DIAZ-PANIAGUA, C. KELLER AND A . C. ANDREU

548

60

-

Body length (mm)

~~~

1 Aug.

15 Aug.

31 Aug.

15 Sept.

I

-"

30 Sept.

Emergence date

1

B v

14

OO

0

1 8

10

12

14

16

18

20

Egg mass (9) FIG.2. Relationship between eggs and hatchlings: (a) emergence date x hatchling size and mass; and (b) egg mass x hatchling mass. Each point represents one individual.

Discussion Hatching success

Egg mortality in this study was caused by shell-breakage, presumably during egg-laying, development failures and nest predation, although none of these factors had an important impact on hatching success. Shell-breakage was registered only in nests of four or five eggs, which represent no more than 50% of the total number of clutches laid in Dofiana in 1994 (Diaz-Paniagua et aE., 1996), whereas 10% of eggs failed to hatch (if modified nests are not considered), which is somewhat lower than the frequencies of unhatched eggs reported for other terrestrial species (MacFarland, Villa & Toro, 1974b; Swingland & Coe, 1978; Landers, Gamer & McRae, 1980; Fowler de Neira & Roe, 1984; Burke et al., 1996). Egg failure might have been associated with infertility (MacFarland et al., 1974b; Swingland & Coe, 1978; Turner et al., 1986), or with embryo mortality due to genetic causes or inadequate

HATCHING AND EMERGENCE OF TESTUDO G R A E C A

549

0.12

0.08 C

0 .-

6

0.04

f:

0

0

-0

0 m

0

-0.04

-0.08

+ 13 Jun.

Nesting date FIG.3 . Variation of average body condition per clutch with nesting date. The central point represents the mean, the box -C 1 S.E.,the vertical bar ? 1 S.D. Numbers over each box indicate sample size (no. of clutches per group). Clutches laid after 13 June differ significantly in hatchling body condition from earlier clutches.

incubation conditions (e.g. Ewert, 1979; Pieau, 1982; Turner et ul., 1986; Packard et ul., 1987; Lindeman, 1991; Packard, Packard & Benigan, 1991; Eendebak, 1995). The nest predation rate of 4.5% registered during this study may be regarded as exceptionally low, if compared with the available data for other species, and especially considering that no nest predation occurred during two of the study years. Although predation rates of tortoise nests are generally lower than those registered for freshwater turtles (Iverson, 1991), nest losses over 50% due to predation have been reported for several tortoise species (Geochelone elephantopus, MacFarland, Villa & Toro, 1 9 7 4 ~Testudo ; hermanni, Swingland & Stubbs, 1985; Gopherus polyphenzus, Landers et al., 1980; Marshall, 1987 (in Germano, 1994); Gopherus agassizii, Turner et al., 1987 (in Germano, 1994)). In the closely related species Testudo hermanni, nest predation was found to be a major cause of the population decline of this species in France, where nest destruction rates were as high as 95% (Stubbs & Swingland, 1985; Swingland & Stubbs, 1985), and in at least 50% of cases the identified predator was the badger (Meles meles), a species which also occurs in our study area in Doiiana. Nesting areas in France are limited, so that tortoise nests occur in high densities on a few specific sites (Swingland & Stubbs, 1985); Geochelone nests are conspicuous and urine-soaked (MacFarland et al., 1 9 7 4 ~ ; Swingland & Coe, 1978), and those of Gopherus are frequently dug at the female’s burrow entrance, all of which facilitates nest-finding by predators. In Doiiana, nesting areas are not limited and the small and very well camouflaged nests are scattered over extensive areas of tortoise habitat (Diaz-Paniagua et al., 1996), which is likely to reduce predation. The same may have been the cause of the absence of nest predation observed for Testudo hermunni in Greece (Swingland & Stubbs, 1985). Hatching and emergence The incubation periods registered for field-developing nests in this study are generally in accordance

550

c. DIAZ-PANIAGUA, c. KELLER A N D A . c. ANDREU

with those registered for Testudo graeca under laboratory conditions (Pieau, 1972; Blasco, Crespillo & SLnchez, 1986/87), and for field incubating nests of Testudo kleinmanni (Geffen & Mendelssohn, 1991). The timing of incubation was mainly influenced by nesting dates, in that eggs from early clutches had the longest incubation periods and times to emergence. The same was also observed for Geochelone elephantopus (MacFarland et al., 19746) and Geochelone gigantea (Swingland & Coe, 1978). Since temperature is the variable most affecting incubation of rigid-shelled turtle eggs (Packard et al., 1981; Packard, Packard & Boardman, 1982; Janzen, 1993a), the observed variation is very likely to reside in the different thermal environments experienced by clutches laid at different moments of the two-month nesting season. Higher incubation temperatures normally result in shorter incubation times in reptiles (e.g. Gutzke et al., 1987; Packard & Packard, 1988; Congdon & Gibbons, 1990; Brooks et al., 1991; Van Damme et al., 1992; Cagle et al., 1993), and in Doiiana mean temperatures in May are considerably lower than in June (19-yr monthly means of 17 "C and 20.6 "C, respectively; data from a meteorological station at the study site). Thus, mean temperatures experienced by a clutch during the initial phases of incubation increase from May to June, resulting in progressively shorter incubation periods and the more synchronized pattern of emergence observed during the three study years. The delay of emergence in Testudo graeca hatchlings is likely to be mediated by the absorption of external yolk sacs, which the new-borns still carry upon hatching, as has been observed in Gopherus polyphemus (Linley & Mushinsky, 1994) and Geochelone gigantea (Swingland & Coe, 1978). One T. graeca hatchling removed from the nest after hatching also carried a yolk sac weighing 11% of its body weight. The delays observed in this study were somewhat shorter than those registered for Geochelone gigantea (Swingland & Coe, 1978). Residual yolk provides hatchlings with energy for maintenance after completion of the embryo development (Packard & Packard, 1988). Since the amount of yolk remains is dependent on maternal investment in the egg and incubation conditions (Congdon, 1989), the observed variation in the duration of delays among, as well as within clutches, may be owing, at least in part, to variations in the amount of residual yolk at the disposal of each individual. In none of the three study years was any hatchling observed to stay in the nest past September. Although spring emergence is generally restricted to species or populations of species inhabiting high latitudes (Gibbons & Nelson, 1978; Congdon & Gibbons, 1985), there is evidence to support the idea that this strategy may also evolve in turtle populations from areas where winters are more amenable (Cagle, 1950; Jackson, 1994), but where drought conditions may favour spring emergence (Jackson, 1994). Prolonged drought periods are not infrequent in south-western Spain-two of the study years (1990 and 1994) were characterized by extremely scarce rainfall-and environmental conditions in autumn are strongly dependent on the amount of rainfall, which has a very irregular distribution, but rarely starts to fall before the end of September. Thus hatchlings emerged before the usual time of rainfall onset in all three study years, apparently before receiving any cue to the quality of the external environment regarding feeding resources. The same behaviour of hatchlings was observed for Geochebne gigantea on Aldabra (Swingland & Coe, 1978). Otherwise, overwintering in the nest was also observed to occur in consequence of the inability of hatchlings to break through the hardened nest roof in autumn, whereas hatchlings from nests incubated in sand emerged more frequently in autumn (DePari, 1996). Thus, hatchlings of tortoise species nesting in sandy soil, as in the present case, are not likely to depend on the effect of soil softening by rainfall during the emergence process. So far no evidence of prolonged emergence delay has been produced from field studies of any tortoise (MacFarland et al., 1 9 7 4 ~Swingland ; & Coe, 1978; Fowler de Neira & Roe, 1984; Turner et al., 1986;

HATCHING AND EMERGENCE OF TESTUDO GRAECA

55 1

Geffen & Mendelssohn, 1991; Butler et al., 1995), although most species inhabit typically dry and unpredictable environments regarding rainfall. This seems to indicate that the selective pressure towards an increase in the relative amount of yolk reserves has apparently not been as strong in tortoise as in freshwater turtle species subject to adverse post-emergent scenarios.

Hatchlings Hatchling size was significantly clutch-dependent and positively correlated with egg size. In studies that considered clutch effects separately from those of incubation conditions, interclutch differences were stronger than those implied by differences in incubation conditions (Brooks et al., 1991), including data from field incubated nests (Packard, Miller & Packard, 1993; Cagle et al., 1993), and were mainly expressed in the effect of' egg size (Roosenberg & Kelley, 1996). Although the few available studies regarding egg incubation in turtle species with rigid-shelled eggs indicate that higher incubation temperatures produce larger hatchlings (Janzen, 1993~; Remor de Souza & Vogt, 1994),in the present study hatchling size was apparently not influenced by incubation conditions, since we detected no significant correlation of nesting date and incubation time with hatchling size. Hatchlings from clutches with average larger egg size emerged later, regardless of nesting date, time to emergence, incubation time and duration of emergence delay. Since emerging relatively later in Doiiana probably favours hatchling fitness, by avoiding summer peak temperatures (which occur throughout August and start to decline during September), larger egg sizes may confer an adaptive advantage to hatchlings, apart from that which may be produced by larger hatchling size per se (e.g. Swingland & Coe, 1979; Janzen, 1993b). The better physical condition of latest clutch hatchlings suggests that incubation conditions of clutches subject to the highest mean incubation temperatures produce relatively larger amounts of residual yolk in relation to hatchling size, since metabolic efficiency in the conversion of energy reserves into tissues is lower under high incubation temperature (Packard & Packard, 1988). Hatchlings with better physical condition, and presumably disposing of larger amounts of energy reserves, are likely to have higher probabilities of surviving to the following spring in dry years, when pasture is scarce, and of low quality during autumn, thus favouring clutches laid during the second half of June. We thank M. C. Quintero, Gemma Gomez Aranda, Ingeborg de Boois and the summer students in Doiiana, for their collaboration in field work. Previous versions of this manuscript benefited from comments of J. Juste and an anonymous reviewer. This work was partially funded by DGICYT (PB88-0009 and PB94-0008) and JUNTA DE ANDALUCIA (Grupo 4088). CK was supported by a grant from ICVAECI in 1990 and 1991 and by grant no. 204322/89-8 from CNPq (Brazil) in 1994. REFERENCES Blasco, M., Crespillo, E. & Sanchez, J . M. (1986/87). The growth dynamics of Testudo graeca L. (Reptilia: Testudinidae) and other data on its populations in the Iberian Peninsula. Isr. J. Zool. 34: 139-147. Bobyn, M. L. & Brooks, R. J. (1994). Interclutch and interpopulation variation in the effects of incubation conditions on sex, survival and growth of hatchling turtles (Chelydra serpenrina) J. Znol. (Lond.) 233: 233-257. Brooks, R. J., Bobyn, M. L., Galbraith, D. A,, Layfield, J. A. & Nancekivell, E. G. (1991). Maternal and environmental influences on growth and survival of embryonic and hatchling snapping turtles (Chelydra serpentina). Can. J. Zool. 69: 2667-2676. Burke, R. L., Ewert, M. A,, McLemore, J. B. &Jackson, D. R. (1996). Temperature-dependent sex detemination and hatching success in the gopher tortoise (Gopherus polyphemus). Chel. Cons. B i d . 2: 86-88. Butler. J. A,, Bowman, R. D., Hull, T. D. & Sowell, S. (1995). Movements and home range of hatchling and yearling gopher tortoises, Gopherus polyphemus. Chel. Cons. Biol. 1: 173-180.

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