Reproductive Ecology of the Ploughshare Tortoise (Geochelone yniphora) Miguel Pedrono; Lora L. Smith; Augustin Sarovy; Robert Bourou; Hafany Tiandray Journal of Herpetology, Vol. 35, No. 1. (Mar., 2001), pp. 151-156. Stable URL: http://links.jstor.org/sici?sici=0022-1511%28200103%2935%3A1%3C151%3AREOTPT%3E2.0.CO%3B2-4 Journal of Herpetology is currently published by Society for the Study of Amphibians and Reptiles.
Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/about/terms.html. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/journals/ssar.html. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission.
The JSTOR Archive is a trusted digital repository providing for long-term preservation and access to leading academic journals and scholarly literature from around the world. The Archive is supported by libraries, scholarly societies, publishers, and foundations. It is an initiative of JSTOR, a not-for-profit organization with a mission to help the scholarly community take advantage of advances in technology. For more information regarding JSTOR, please contact
[email protected].
http://www.jstor.org Tue Feb 19 07:27:06 2008
SHORTER COMMUNICATIONS gunncntnqo undergo direct development. Terrestrial deposition of large, unpigmented eggs in sites without available aquatic nesting sites has also been reported for Oreophrynelln quelchii, a direct developing species from the tepius of the Guayanan Highlands (McDirmid and Gorzula, 1989). Apparent hatchling individuals have been encountered in the field, but larvae or aquatic eggs have never been found. Osorilophryile typically occur in places where aquatic breeding sites are uncommon or absent, and adults are unable to swim according to Ruiz-Carranza and Hernandez-Camaad~o(1976) and laboratory observation with 0 . guacnn~ayo.Therefore, we suggest that 0 . guncnmmio is a direct developer. Adult female 0.guncanzqo are more likely to be encountered in exposed areas (on larger leaves or on the ground) than other sex or age classes. In addition to hatchlings encountered during summer months, two size classes of females were typically present in populations sampled: large, colorful adults and smaller, drab subadults, which are indistinguishable from adult males. Lindquist and Hetherington (1998) described an ontogenetic shift in color pattern in the toad Atelopus zeteki. Recent metamorphs and subadults are cryptically patterned with dorsal coloration matching background color and occupy less exposed microhabitats than adults. Adults are brightly colored with immaculate yellow or patterned dorsums. We hypothesize that juvenile coloration and behavior may be correlated with a lack of skin toxicity sufficient for deterring predators. Although 0 . guncarnqo appears to be a generalist predator throughout its ontogeny, it is possible that skin toxins accumulate with age (Lindquist and Hetherington, 1998) because likely sources of precursor alkaloids (formicids, and coleoptera) are consumed by all age classes (Table 1). Color dimorphism associated with size in this species may indicate a trade-off between predator-avoidance and antipredator mechanisms (Brodie et al., 1991; Hileman and Brodie, 1994). Aposematic coloration in adult females may serve as an antipredator mechanism whereby they are able to advertise increased skin toxicity associated with age or size to deter predators rather than rely on predator avoidance alone. Ackrzo?~~led~~rrze~~ts.-We thank L. Coloma and J. M. Guayasamin for their assistance in data collection. Assistance with data analysis was provided by R. Brown, D. Gluesenkamp, and W. Hodges. Helpful comments on early drafts of this manuscript were provided by R. Brown and D. Cannatella. The manuscript was greatly improved by the comments of M. Given, A. Mathis, and an anonymous reviewer.
151
phylogenetic relationships among frogs of the genus Atelopus (Anura: Bufonidae). Unpubl. Ph.D. diss., Univ. of Kansas, Lawrence. GLUESENKAMP, A. G. 1995. A new species of Osorilophryize (Anura: Bufonidae) from Volcan Sumaco, Ecuador with notes on other members of the genus. Herpetologica 51:268-279. GRAYBEAL, A. 1995. Phylogenetic relationships of bufonid frogs based on molecular and morphological characters. Unpubl. Ph.D. diss., Univ. of California, Berkeley. J R. 1994. Survival HILEMAN, K. S., AND E. D. BRODIE strategies of the salamander Desrnogrzathus ochrophac,us: interactions of predator-avoidance and antipredator mechanisms. Anim. Behav. 47:1-6. HOOGMOED, M. S. 1987. New Osornophryne (Amphibia: Anura: Bufonidae) from the Atlantic versant of the Andes in Ecuador. Zool. Mededel. 61:209-242. LIXDQUIS~, E. D., AND T. E. HET~IERINGTON. 1998. Tadpoles and juveniles of the Panamanian golden frog, Atelopus zeteki (Bufonidae), with information on development and patterning. Herpetologica 54: 370-376. MARTIN, W. F. 1972. Evolution of vocalization in the genus Blrfo. In W. F. Blair (ed.), Evolution in the Genus Bufo, pp. 279-309. Univ. of Texas Press, Austin. MCDIARMID, R. W., AND S. GORZCTLA. 1989. Aspects of the reproductive ecology and behavior of the tepui toads, genus Oreophrynelln (Anura, Bufonidae). Copeia 1989:445451. RUI~-CARRANZA, P. M., AND 1. I. HERNANDEZ-CAMAgenero nuevo de anfibios CHO.1976. Osori~ophryi~e, bufbnidos de Colombia y Ecuador. Caldasia 11:93148. Accepted: 7 May 2000.
joririinl o Herprtology, Vol. 35, No. 1 , pp. 151-156, 2001 Copyngit 2001 Soaety for the Studv of Amphibians and Reptiles
Reproductive Ecology of the Ploughshare Tortoise (Geochelone yniphora)
MIGUELPEDRONO,Lnjlorntoire d'Ecologie, U M R 7625, U n i x r s i t i Pierre et Mnrie Curie, 7 qrtni St Berrznrd, 75252 Pnris, France; E-nznil: rnpedrorzo@sin~jussieu.fr;and Durre11 Wildlife Conserzintion Trust, Les Augres Mnnor, TrinBRODIE JR.,E. D., D. R. FORMANOWICZ, A N D E. D. BROity, Jersey JE3 5Bc Chnilnel Islnnds, British Isles DIE 111. 1991. Predator avoidance and antipredator mechanisms: distinct pathways to survival. Ethol. LORAL. SMITH,'Depnrtmeilt of W i l d l ~ f eEcology and CoilEcol. Evol. 3:73-77. serintiorz, Unizlersity of Floridn, Gninesville, Florida 32611 CANNA-I-ELLA, D. C. 1986. A new species of OsorrzoU S A ; nrzd Durrell Wildlife Coi~serzintzonTrust, Les AlrgrPs phr!/ne (Anura: Bufonidae) from the Andes of Ec- Mnnor, Trirzity, Jersey IE3 5BE Chnr~nelIslnnds, British uador. Copeia 1986:618422. Isles COCROFT, R. R., A N D M. J. RYAN.1995. Patterns of SARO\'Y,ROBERTROUROU,AND HAFANY advertisement call evolution in toads and chorus AU~;USTIN Durrell W i l d / @ Consermtioil Trust, B.P 8511, TIANDRAY, frogs. Anim. Behav. 49:283-303. COLOMA, L. R. 1997. Morphology, systematics and Ailtarznnarizo 101, Mndngfficnr
SHORTER COMMUNICATIONS lations for a period of five years and the following reproductive parameters were monitored: date of oviposition, nest site selection, clutch size, egg mass, incubation, and hatching success. We also monitored factors that might influence recruitment such as nest predation and egg fertility. These data were considered especially vital because the remaining populations are extremely small (Smith et al., 1999b). Relationships between female body size and productivity also were examined. Studies suggest that, in some chelonians, an increase in individual size results in increased fitness (Froese and Burghardt, 1974; Swingland and Coe, 1979; Wilbur and Morin, 1988; Congdon and Gibbons, 1990; but see Congdon et al., 1999). Therefore, rue felt it was particularly important to determine whether maternal size had an affect on reproductive parameters in the ploughshare tortoise. Assuming covariation between life-history variables and body size for chelonians (Elgar and Heaphy, 1989), we predicted that the reproductive output in the ploughshare tortoise would increase with maternal body size. The ploughshare tortoise occurs in bamboo shrub habitat that contains a mixture of bamboo thickets, shrubs, grasses, and open areas (Juvik et al., 1981; Curl et al., 1985; Smith et al., 1999a). Frequent anthrothe ploughshare pogenic fires are thought to alter the of exam(GeocilelowJ ~ ~ ~in ~ P / ~ ~ Mads~ ~ ) the habitat (Smith et al,, 199ga), Therefore, gascar. ined nest site selection to determine whether anv uarticular component of the habitat (en., " bamboo 'th'ickets, shrubs, grasslands) was of particular ~mportance The ploughshare tortoise (Geochrlor~eyniphorn) is en- to nesting females. demic to a very limited area around Baly Bay in The two ploughshare tortoise populations examnorthwestern Madagascar (Fig. 1) and is considered ined in this study ruere located at Cape Sada and Amthe rarest tortoise in the world (Juvik et al., 1981; batomainty (Fig. 1). Cape Sada is an approximately Hoogmoed, 1985). The restricted distribution and en- 150-ha peninsula located on the east side of Raly Ray dangered status of the ploughshare tortoise are (16'02'S, 4Y20'E). The peninsula contains a mixture thought to be the result of historic commercial ex- of bamboo (Perrlrrtialntios n~ndngascnr~ells~s) and shrubs ploitation and habitat alteration resulting from fre(primarily Grn~i~ialin btn,ii~ii,Bnuhir~inperi~lllci)with quent anthropogenic bush fires (Juvik et al., 1981; Curl open patches of grass and bare rocks. The Ambatoet al., 1985). The few remaining ploughshare tortoise mainty region is approximately 4000 ha in size and is populations are small and isolated from one another located west of Baly Bay (16"03'S, 4Y06'E). This re(Smith et al., 1999b). In 1986, at the request of the gion contains deciduous dry forest, bamboo, dense International Union for the Conservation of Xature, shrubs, and large areas of palm savanna characterized the Durrell Wildlife Conser\ration Trust initiated a reby FLteropogor~ cor~tortusand Biirtznrckin rzobilis. The coLrery program for the ploughshare tortoise (Durrell dominant plants in the bamboo scrub community at et al., 1994). The recovery plan included an in-country captive-breeding program and research on the status Ambatomainty are the same as those at Cape Sada. and ecology of wild populations. The captive-breed- The climate in the region is tropical, with distinct wet ing program has resulted in the production of 255 and dry seasons (Donque, 1972). The wet season exoffspring from a founder stock of 20 adult tortoises tends from November through April, and the highest (L. Durrell, pers. comm.). Research on free-ranging temperatures occur during these months. Little or no ploughshare tortoises focused on the status and dis- rainfall occurs during the six-month dry season (May tribution of the species (Curl et al., 1985; Smith et al., through October), and most rivers and small streams are dry during this period. 1999b) and a study of home range and microhabitat Ele\ren adult female tortoises (eight at Cape Sada use (Smith et al., 1999a). To date, obser\rations on the and three at Ambatomainty) were fitted with radireproductive ecology of the species have been limited to captive populations (McKeown et al., 1982; Reid, otracking de~zices.The sex of adult tortoises was de1995). Our study represents the first analysis of termined based on differences in shell morphology (L. ploughshare tortoise reproduction in wild popula- Smith and M. Pedrono, unpubl. data). At the time of first capture, straight-line carapace length (CL) was tions. Field data were collected from two tortoise popu- recorded to the nearest 1.0 mm and body mass was taken to the nearest 50 g. Transmitters were mounted on the posterior costal scutes so that they would not ' Present Address: U.S. Geological S w q , Florida Ca- impede mating. During the reproductive period, from ribbean Saence Center, 7920 hW 71st Street, Gaines~ille, 15 January to 30 May, females were radio-tracked three to four times per day to monitor nesting activity. Florida 32653 USA; E-mail:
[email protected]\7.
SHORTER COMMUNICATIONS .
,~
TAHLC I . Egg and clutch parameters for ploughshare tortoises (Geociwlone yniphora) from Cape Sada and Ambatomainty, Madagascar. * Clutch frequency was measured only in the 1998 nesting season.
I
1
'"
f
r j -
,, i
'
.(,
j
I
Parameter
1
5 4
I
,,, 3
-
>
C-rr,
L'
Egg mass (g) 122 Clutch size 71 Clutch mass 38 Clutch frequency* 11
Mean -+ SE
36.2 3.2 115.2 2.45
t 6.6 t 0.9
-+ 30.4 2 0.9
Range
20.0-54.0 1-6 41.0-157.0 1 4
Clutch Sire (kg$,,
Frc,. 2. Clutch size distribution for 71 ploughshare tortoise (Geochelone ynlphoua) nests at Cape Sada and Ambatomainty, Madagascar. The mean clutch inter~zalwas calculated early in the study; this value was then used to predict subsequent nesting dates once the first nesting event had occurred. When a female was obser\red nesting, eggs were removed from the nest and counted; care was taken not to turn or roll eggs during handling. In 1997 and 1998, eggs were weighed to the nearest 0.5 g and egg diameter was measured to the nearest 0.1 mm. Nests were marked and left undisturbed until late in the dry season (October), when wire cages were placed over the nests to confine emerging hatchlings. Cages were partially shaded to protect hatchlings from the sun and nests were checked daily for emerging hatchlings. We defined "incubation" as the time between egg deposition and hatchling emergence from the nest; lve did not determine whether the hatchlings emerged immediately upon hatching or exhibited delayed emergence. Individual hatchlings were uniquely marked with enamel paint on the marginal scutes. Straight-line carapace length (CL) of each hatchling was recorded to the nearest 0.1 mm and body mass was measured to the nearest 0.5 g. M s t s were excavated on December 30 to determine whether or not any remaining eggs rvere viable. Eggs that had not hatched were removed from the nest and examined to determine whether an embryo was present. Reproductive data for the two populations were pooled to increase the power of statistical analyses. Although we recognized that environmental differences between the sites could have an effect on reproductive parameters, the two populations are in rela-
ti\rely close proximity (24 km apart) and the habitats appeared similar. Statistical analyses were run using SAS software (SAS Institute, Inc., 1994). We used ttests for comparison of means, and the Pearson correlation coefficient r to assess relationships between body measurements and reproducti\~e variables. Clutch mass was logarithmically transformed to normalize its distribution for t-test analyses. The significance level for statistical tests was a = 0.05. We recorded nesting activity in iemale ploughshare tortoises from 19 January and 29 May (all years pooled). Most nest sites were located in open areas within grasslands (40.5% of the nests recorded, hr = 71), bamboo stands (21%1),and savanna (4.5%); no nests were discovered in dense bamboo or deciduous dry forest. Interestingly the remaining 34'2, of nest sites were in openings in bamboo thickets that rvere created by small brush fires. The three nests located in savanna habitat were deposited by the same female, who traveled nearly 1 km from her normal activity range in dense bamboo to nest. Four nests were deposited in areas within bamboo stands that had been disturbed by African bush pigs (Potamochoerus larzat1rs).
All females produced at least one clutch per year and the production of multiple clutches per season was common. The mean clutch size was 3.2 -+ 0.9 eggs (A' = 71, range = 1-6 eggs; Fig. 2 ) and clutch frequency was 2.45 + 0.9 (N = 11, range = 1 4 ) . Egg and clutch parameters are presented in Table 1. Both clutch frequency and mean clutch mass were significantly correlated with maternal body mass (Table 2). When the largest female was removed from the sample, a significant positive relationship between mean egg mass and female body mass was found ( r = 0.84, df = 8, P < 0.01). Although this large female pro-
TABLE2. Pearson correlation coefficients for reproductive variables in ploughshare tortoises (Geocheloneyniphora) from Cape Sada and Ambatomainty, Madagascar. "P < 0.02. t The largest female was removed from the sample. Comparison
Mean Mean Mean Mean Mean Mean Mean Mean
clutch frequency vs. maternal body mass*
egg mass vs. clutch size
clutch mass vs. female body mass*
clutch size \,s. female body mass
clutch size vs. maternal CL
hatchling body mass vs. mean egg mass*
hatchling body mass vs. maternal body mass*+
hatchling CL vs. maternal CL
154
SHORTER COMMUNICATIONS
FIG. 3. Length of incubation in relation to month of oviposition for 33 ploughshare tortoise (Gcochelonc ytliphorn) nests at Cape Sada and Ambatomainty, Madagascar.
duced small eggs, she produced the largest clutch (six eggs) observed in this study. These results suggest that, up to a certain egg size, there is a positive relationship between maternal body mass and egg mass. Thereafter, an increase in maternal body mass results in an increase in clutch size (see Smith and Fretwell, 1974; Rowe, 1995). As in other large tortoises (Elgar and Heaphy, 1989), ploughshare tortoise eggs were nearly spherical. We suspected that reproductive output in ploughshare tortoises might vary by date of oviposition because of the seasonal variation in quality and availability of food. However, no effect of the deposition date on clutch mass or clutch size was detected. First clutches were not significantly larger than last clutches (t = 0.43, df = 20, P > 0.05), and clutch size did not differ significantly between the start and end of the nesting season (t = -0.73, df = 20, P > 0.05). The mean incubation period across all five nesting seasons was 237 i 23 days (N = 33, range = 197-281 days). Hatchlings emerged at the onset of the rainy season during daylight hours. Length of incubation varied with the deposition date (Fig. 3), with eggs deposited early in the season having the longest incubation period. Hatchlings within a nest generally emerged on the same day or, rarely, over a two-day period. The mean body mass of hatchlings was 24.1 i- 5.4 g (N = 69, range = 11.0-35.0 g), and the mean CL was 44.7 + 3.3 mm (N = 69, range = 35.3-50.2 mm). Because nests were left in situ, we were not able to compare the mass of individual eggs and hatchlings directly. Therefore, we compared mean hatchling body mass to the mean egg mass of each clutch. Mean hatchling body mass was significantly correlated with mean egg mass (Table 2) and represented roughly 660h of the egg mass. A significant relationship also was observed between mean hatchling body mass and maternal body mass when the largest female was removed from the sample (Table 2). Of the 71 nests monitored between 1993 and 1998, hvo (2.Uoh)were destroyed by African bush pigs (one at Cape Sada and one at Ambatomainty). No other evidence of nest predation was observed. From 1993 to 1998, the hatching rate was 54.6% (N = 163 eggs). Of the 57 eggs checked from 1993 to 1998, 71.9% were fertile (N = 57). The actual fertility rate may have been lugher than reported because it was impossible to detect embryos that
had died during the first development stages. We obsemed significant variation in hatdung success between indi~idualfemales (x' = 30.54, df = 2, P < 0.0001); for example, some females produced clutches with a mean hatdung success of only 14.3% as compared to 82.8?,1in others. Hatdung success was not affected by initial egg mass (r = 0.39, df = 6, P > 0.05). Using the estimates of the mean clutch size, clutch frequency, and mean hatching rate determined in this study, on average, a reproductive female ploughshare tortoise produces 4.3 hatchlings per year. Maternal body mass was positively correlated with clutch mass, either through an increase in egg mass or increased clutch size. This pattern has commonly been observed in other chelonians (Landers et al., 1980; Congdon and Gibbons, 1983; Hailey and Loumbourdis, 1988; Elgar and Heaphy, 1989; Iverson, 1992). However, a trade-off between clutch size and egg size was not evident (e.g., large clutches with smaller eggs; small clutches with larger eggs). In this study, it seemed that very large females produced larger clutches and that hatchling mass was positively correlated with egg mass as has been reported in other chelonians (Packard et al., 1980; Morris et al., 1983). Thus, larger females produced hatchlings of greater body mass. Howe~zer,mean hatchling mass was more closely correlated with mean egg mass, than with female body size (see Rowe, 1995),suggesting that other factors such as incubation temperature and humidity in the nest chamber may also influence hatchling size. Female ploughshare tortoises nested in all years ot the study and produced multiple clutches per season. Possible explanations for the evolution of the multiclutch reproductive pattern in ploughshare tortoises include a decrease in risk of nest predation (Auffenberg and Iverson, 1979); an increase in hatching success with staggered nesting dates (Reid et al, 1989); and an increase in fecundity within the morphological constraints on clutch and egg size (Moll, 1979; Hailey and Loumbourdis, 1988; Wilbur and Morin, 1988). It is not known whether nest predator(s) exert selective pressure on ploughshare tortoise populations. The only nest predator confirmed in this study was the African bush pig, which is not native to Madagascar (Oliver and Brisbin, 1993). It seems unlikely that the production of multiple clutches protects oifspring from the unpredictable timing of seasonal rainfall, because hatchlings at nearly all nests emerged at the onset of seasonal rains, regardless of the date of deposition. It is possible that, as has been suggested for other chelonians, ploughshare tortoises produce multiple clutches to offset morphological constraints on egg and clutch size. It also seems possible that the selective advantage of multiple clutches is expressed through increased hatchling survival rather than embryo survival; that is, multiple clutches of larger eggs may allow for the production of larger hatchlings that may h a w increased survivorship. However, recent work by Congdon et al. (1999) with common snaphas chalping turtle hatchlings (Ciu.l!/drn ~c~p~iifiliil) lenged the concept that "bigger is better" in chelonian offspring. A demographic study of ploughshare tortoise populations will be necessary to determinc whether large hatchlings have a selective advantage over small hatchlings. Despite extremely low population densities in re-
SHORTER COMMUNICATIONS
maining ploughshare tortoise populations (Smith et al., 1999b; M. Pedrono and A. Sarovy unpubl. data), successful reproduction is occurring in the wild. The egg fertility rate (71.9%) and hatching success (54.6%) observed in this study were similar to those reported for other tortoises (e.g., Swingland and Coe, 1978, for Dipsochelys elephantinn; Fowler de Neira and Roe, 1984, for Geochelone niyra). Furthermore, nest predation was quite low (2.8%) in comparison to that of other Testudines; 7 to 33% for Esiudo iz. hernlanizi (Guyot, 1996), 10-20% for Testudo k. boetigeri (Hailey and Loumbourdis, 1990), and 89% for Gopherus polypl~mus(Landers et al., 1980). Taken together, these factors suggest tbat populations might increase in size in the future, provided harvest and frequent, intense fires are excluded. Intense brush fires are known to kill ploughshare tortoises (L. Durrell, pers. comm.); however, the role of natural fire in the maintenance of ploughshare tortoise habitat should be explored. Our results suggest that low intensity fires may actually create suitable nesting habitat for the ploughshare tortoise. Future investigations should address the habitat requirements of ploughshare tortoises. The geographic distribution of the species coincides with that of the deciduous bamboo (Perrierhambos rnadagascariensis; Curl et al., 1985). However, in this study, we documented nesting in savanna habitat (4.5% of sample); this represents the first record of ploughshare tortoises venturing into this habitat. In addition, we encountered two other individuals, an adult male and subadult female in true savanna suggesting that the ecological spectrum of this tortoise may be broader than was previously thought. Possible geographic variation in reproductive characteristics between populations also should be explored. It also will be important to determine whether the ploughshare tortoise has environmental sex-determination (ESD; Ewert and Nelson, 1991) and/or sperm storage in females (Palmer et al., 1998). Determining whether this species has ESD is of particular importance because the release of captive-bred juveniles is being considered as a possible conservation tool for this species (Pedrono and Sarovy 2000), and at least one population has a femalebiased sex ratio (Smith et al., 1999b). Finally, it would be interesting to investigate the method by which males locate females, despite very low adult densities. We suspect that olfaction may play an important role in sexual partners meeting in the wild. In captivity, when adults of the two sexes are kept separate and out of sight of one another, males have been observed attempting to cross fences to get access to females (M. Razandrimamilafiniarivo, pers. comm.). Knowledge of all aspects of reproduction will be crucial in choosing the best conservation, restoration, and monitoring strategies (Tinkle et al., 1981; Dodd, 1997), as well as in the development of a population viability model for the species. AcknoziLdgments.-We are grateful to the Durrell Wildlife Conservation Trust for their financial and logistic support and particularly L. Durrell, director of the ploughshare tortoise recovery program, for the opportunity to study this species in nature. The Trust staff in Madagascar are gratefully acknowledged. The manuscript was improved by the constructive comments of M. Robert and A. Feistner. Our study could not have been accomplished without the logistical as-
sistance and friendship of the people of Ambarindranahary Antsahamena, Antsira, and Soalala. Finally, we thank the Malagasy Government for authorization to live and work in Madagascar.
AUFFENBERG, W., AND J. B. IVERSON.1979. Demography of terrestrial turtles. Iiz M. Harless and H. Morlock (eds.), Turtles: Perspectives and Research, pp. 541-569. John Wiley and Sons, New York. CONGDON,J. D., AND J. W. GIBBONS.1983. Relationships of reproductive characteristics to body size in Pseudenlys scripta. Herpetologica 39:147-151. . 1990. The evolution of turtle life histories. In J. W. Gibbons (ed.), Life History and Ecology of the Slider Turtle, pp. 45-54. Smithsonian Institution Press, Washington, DC. CONGDON, J. D., R. D. NAGLE,A. E. DUNHAM,C. W. BECK,0 . M. KINNEY,AND S. R. YEOMANS.1999. The relationship of body size to survivorship of hatchling snapping turtles (Cl~lydraserpentinn): an evaluation of the "bigger is better" hypothesis. Oecologia 121:224-235. CURL,D. A,, I. C. SCOONES, M. K. GUY,A N D G. RAKOTOARISOA. 1985. The Madagascan tortoise Geoclvlone yiziphora: current status and distribution. Biol. Conserv. 34:35-54. DODDJR., C. K. 1997. Clutch size and frequency in Florida box turtles (Terrqole carolina hmri): implications for consenlation. Chel. Consen?.Biol. 2:37&377. DONQUE,G. 1972. The climatology of Madagascar. liz R. Battistini and G. Richard-Vindard (eds.), Biogeography and Ecology in Madagascar, pp. 87144. Dr. W. Junk B. V., The Hague, The Netherlands. D. REID, AND J. DURRELL, L., R. RAKOTONINDRINA, DURBIN. 1994. The recovery of the angonoka (Geochelone ynip11ora)-an integrated approach to species conservation. In P. J. S. Olney, G. M. Mace, and A. T. C. Feistner (eds.), Creative Conservation: Interactive Management of Wild and Captive Animals. pp. 384-393. Chapman and Hall, London. ELGAR,M. A., AND L. J. HEAPHY.1989. Covariation between clutch size, egg weight and egg shape: comparative evidence for chelonians. J. Zool., Lond. 219:137-152. EWERT,M. A., AND C. E. NELSON.1991. Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1991:5049. FOWLER DE NEIRA,L. E., AND J. H. ROE. 1984. Emergence success of tortoise nests and the effect of feral burros on nest success on Volcan Alcado, Galapagos. Copeia 1984:702-707. FROESE,A. D., AND G. M. BURGF~ARDT. 1974. Food competition in captive juvenile snapping turtles, Ckelydrn serpentinn. Anim. Behav. 22:735-750. GUYOT,G. 1996. Biologie de la conservation chez la tortue d'Hermann Franqaise. Unpubl. Ph.D. diss., Univ. Pierre et Marie Curie, Paris. 1988. Eggs size HAILEY, A,, AND N. S. LOUMBOURDIS. and shape, clutch dynamics, and reproductive effort in European tortoises. Can. J. Zool. 66:15271536. . 1990. Population ecology and conservation of tortoises: demographic aspects of reproduction in Testudo hermanni. Herpetol. J. 1:425434.
SHORTER COMMUNICATIONS HOOGMOED, M. S. 1985. Two reptiles among the 12 most threatened animals of the world. Amphib.Reptilia 6:101-115. IVERSON, J. B. 1992, Correlates of reproductive output in turtles (order Testudines). Herpetol. Monogr. 6: 2542. JUVIK, J. O., A. J. ANDRIANARIVO, AND C. B. BI.ANC. 1981. The ecology and status of Geocklone yniphom: a critically endangered tortoise in northwestern Madagascar. Biol. Conserv. 19:297-316. J. L., J. A. GARNER, AND W. A. MCRAE.1980. LANDERS, Reproduction of gopher tortoises (Gopherus polypJletnus) in southwestern Georgia. Herpetologica 36353-361. MCKEOWN, S.,J. 0 . JUVIK, AND D. E. MEIER.1982. Observations on the reproductive biology of land tortoises Geocklolle enlys and Geochelorie yniphora in the Honolulu Zoo. Zoo Biol. 1:223-235. ~\.~oLL, E. 0 . 1979. Reproductive cycles and adaptations. In M. Harless and H. Morlock (eds.),Turtles: Perspectives and Research, pp. 305-331. John b'iley and Sons, New York. T. L. BOARDMAN, G. L, MORRIS, K. A., G. C. PACKARD, 1983. Effect of the P~uKs'rls,AND M. J. PACKARD. hydric environment on growth of embryonic snapping turtles (Chrlydra serpentina).Herpetologica 39: 272-285. OLIVER, b'. L. R., AND I. LEHRBRISBIN.1993. Introduced and feral pigs: problems, policy, and priorities. 111 W. L. R. Oliver (ed.), Pigs, Peccaries and Hippos, Status Survey and Conservation Action Plan, pp. 179-191. International Union for the Conservation of Nature, Gland, Switzerland. M. J. PACKARD, AND T. PACKARD, G. C., T. L. TAIGEN, L. BOARDMAN. 1980. Water relations of pliableshelled eggs of common snapping turtle (Chelydra serpentina). Can. J. Zool. 58:1404-1411. PALMER, K. S., D. C. ROSTAL, J. S. GRUMBLES, AND M. MULVEY.1998. Long-term sperm storage in the desert tortoise (Gopherus agassizii). Copeia 1998: 702-705. PEDRONO, M., AND A. SARO~Y. 2000. Trial release of the world's rarest tortoise Geochelone yniphora in Madagascar. Biol. Conserv. 95:333-342. REID,D. 1995. Observations on hatchling and juvenile captive-bred angonoka Geochelone ynipholp in Madagascar. Dodo, J. Jersey Wildl. Preserv. Trust 31: 112-119. REID,D., L. DURRELL, AND G. RAKOTOBEARISON. 1989. The captive breeding project for the angonoka Gcochebne yniplu7ra in Madagascar. Dodo, J. Jersey b'ildl. Preserv. Trust 26:3438. ROWE,J . W. 1995. Hatchling size in the turtle Chrysemys p~ctnbellii from western Nebraska: relationships to egg and maternal body size. J. Herpetol. 29:73-79. SAS INSTITU'TL. 1994. SAS User's Guide: Statistics. Statistical Analysis Systems Institute (ed.). Cary, North Carolina. 1974. The optimal SMITH,C. C., AND S. D. FRE~vLLL. balance between size and number of offspring. Am. Nat. 108:499-506. SMITH,L. L., R. Bounou, J. MAHATOLY, AND C. SIBO. 1999a. Home range and microhabitat use in the angonoka (Geocllrlone yniphora) in Madagascar. Chel. Conserv Biol. 3:393400.
SVITI-I,L. L., D. REID,R. BOUROU, J. MAHATOL~, AND C. SIRO.1999b. Status and distribution of the angonoka tortoise (Geoc/leloi~eyniphora) of western Madagascar. Biol. Conserv. 91:23-33. SWINGLAND, I. R., AND M. COE. 1978. The natural regulation of giant tortoise populations on Aldabra Atoll: recruitment. Phil. Trans. R. Soc. Lond. B Biol. Sci. 286177-188. TINKLE, D. W., J. D. CONCDON, AND P.C. RCEEN.1981. Nesting frequency and success: implications for the demography of painted turtles. Ecology 62:14261432. WILBUR,H. R., AND P.J. MORIN.1988. Life history evolution in turtles. lit C. Gans and R. Huey (eds.), Biology of the Reptilia, pp. 389439. Alan R. Hiss, New York. Accepted: 31 May 2000.
Ic~iir~loi 11 Hrrputolop, Lbl. 35, ko. 1, pp 15h-160,2001 Copyri&t 2001 so'C;etyfor the Study of Arnphlbians and Reptlles
Ontogeny of Sexual Size Dimorphism
in the Tropical Garden Lizard,
Calotes versicolor (Daud.)
BFL~GY.GFIRI A. SHANBHAG,' AND K, SAIDAPUX, SIUNIVAS Dtyarilt~mtof Zoology, Karllcztnk Unizwsity, Dhritad-580 003, Iiuiul
~JKUXZAS R . hDDER,
Sexual dimorphism may occur in morphology, coloration, and behavior of an organism. Sexual size dimorphism (SSD) also occurs in animals where one sex is larger than the other in some body parameter. SSD in body size has been reported in many species of lizards. Males may attain larger size than females in some cases, whereas females are larger than males in others (Carothers, 1984; Vitt and Cooper, 1985; Anderson and Vitt 1990; Huang, 1996; Watkins, 1996; Shine et al., 1998). It is commonly reported that males have relatively broader heads than females (Schoener, 1975; Carothers, 1984; Vitt and Cooper, 1985; Cooper and Vitt, 1989; Vial and Stewart, 1989; Anderson and Vitt, 1990; Huang, 1996).SSD may appear at any stage during the life history of animals. However, studies on the ontogeny of SSD in lizards are scarce (Carothers, 1984; Hews and Moore, 1995; Hews, 1996; Barbadillo and Bauwens, 1997). Cnlotes zrrsicoior (Agamidae) is a relatively large Iizard (adult SVL 8.5-15.0 cm) commonly distributed throughout India. It breeds from May to October in Dharwad (Shanbhag and Prasad, 1993). The present study was undertaken to investigate whether SSD occurs in C. ivrsicoior of comparable SVL, with respect to the head size (length, w-idth, depth) and the tail (length and thickness) from a single population. If SSD occurs in this species, then at what stage of the life history (at hatching, juvenile stage, during sub-
' Corresponding Author. E-mail: karuniQbgl.vsn1. netin.
http://www.jstor.org
LINKED CITATIONS - Page 1 of 2 -
You have printed the following article: Reproductive Ecology of the Ploughshare Tortoise (Geochelone yniphora) Miguel Pedrono; Lora L. Smith; Augustin Sarovy; Robert Bourou; Hafany Tiandray Journal of Herpetology, Vol. 35, No. 1. (Mar., 2001), pp. 151-156. Stable URL: http://links.jstor.org/sici?sici=0022-1511%28200103%2935%3A1%3C151%3AREOTPT%3E2.0.CO%3B2-4
This article references the following linked citations. If you are trying to access articles from an off-campus location, you may be required to first logon via your library web site to access JSTOR. Please visit your library's website or contact a librarian to learn about options for remote access to JSTOR.
Literature Cited Sex Determination in Turtles: Diverse Patterns and Some Possible Adaptive Values Michael A. Ewert; Craig E. Nelson Copeia, Vol. 1991, No. 1. (Feb. 7, 1991), pp. 50-69. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819910207%293%3A1991%3A1%3C50%3ASDITDP%3E2.0.CO%3B2-N
Emergence Success of Tortoise Nests and the Effect of Feral Burros on Nest Success on Volcan Alcedo, Galapagos Lynn E. Fowler de Neira; John H. Roe Copeia, Vol. 1984, No. 3. (Aug. 1, 1984), pp. 702-707. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819840801%293%3A1984%3A3%3C702%3AESOTNA%3E2.0.CO%3B2-O
Correlates of Reproductive Output in Turtles (Order Testudines) John B. Iverson Herpetological Monographs, Vol. 6. (1992), pp. 25-42. Stable URL: http://links.jstor.org/sici?sici=0733-1347%281992%296%3C25%3ACOROIT%3E2.0.CO%3B2-D
Long-Term Sperm Storage in the Desert Tortoise (Gopherus agassizii) Kevin S. Palmer; David C. Rostal; Janice S. Grumbles; Margaret Mulvey Copeia, Vol. 1998, No. 3. (Aug. 3, 1998), pp. 702-705. Stable URL: http://links.jstor.org/sici?sici=0045-8511%2819980803%293%3A1998%3A3%3C702%3ALSSITD%3E2.0.CO%3B2-5
http://www.jstor.org
LINKED CITATIONS - Page 2 of 2 -
Hatchling Size in the Turtle Chrysemys picta bellii from Western Nebraska: Relationships to Egg and Maternal Body Size John W. Rowe Journal of Herpetology, Vol. 29, No. 1. (Mar., 1995), pp. 73-79. Stable URL: http://links.jstor.org/sici?sici=0022-1511%28199503%2929%3A1%3C73%3AHSITTC%3E2.0.CO%3B2-W
The Optimal Balance between Size and Number of Offspring Christopher C. Smith; Stephen D. Fretwell The American Naturalist, Vol. 108, No. 962. (Jul. - Aug., 1974), pp. 499-506. Stable URL: http://links.jstor.org/sici?sici=0003-0147%28197407%2F08%29108%3A962%3C499%3ATOBBSA%3E2.0.CO%3B2-G
The Natural Regulation of Giant Tortoise Populations on Aldabra Atoll: Recruitment I. R. Swingland; M. J. Coe Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, Vol. 286, No. 1011, The Terrestrial Ecology of Aldabra. (Jul. 3, 1979), pp. 177-188. Stable URL: http://links.jstor.org/sici?sici=0080-4622%2819790703%29286%3A1011%3C177%3ATNROGT%3E2.0.CO%3B2-E
Nesting Frequency and Success: Implications for the Demography of Painted Turtles Donald W. Tinkle; Justin D. Congdon; Philip C. Rosen Ecology, Vol. 62, No. 6. (Dec., 1981), pp. 1426-1432. Stable URL: http://links.jstor.org/sici?sici=0012-9658%28198112%2962%3A6%3C1426%3ANFASIF%3E2.0.CO%3B2-K
