Reproductive Biology of the Chopontil, Claudius Angustatus

Eervtiot ciltd Biol(,gr', I995, l(3):181.

Reproductive Biorogy or the Kinosternidae), "n;;;;,,"';;:;;;|)r)i,,,",,,(restudines:in Southern Veracruz, M6xico Oscan A. Flonns-Vrr,r,nr,ar'3lNn Gnoncn R. Zuc2

lMuseo de Zoologia, Facultad de Ciencias, Universidad Nacional Autdnoma Mdxico, A.P.70-399, Mdxico D.F., 04510 Mdxico; zDepartment of Vertebrate Zoology, National Museum of Natural History, Washington, D.C. 20560 USA

Anstnr,cr. - Adult male Claudius angustatus average slightly larger than females and attain sexual maturityatapproximately 98mm CL. Somefemales become sexually matureat89 mm CL,although some individuals 20-25 mm larger are immature. Nesting and gravid females occur from November through February. Clutch size ranges from 1 to 6 (mode 2) ellipsoidal eggs (x- - 17.5 x 30.5 mm, 6.0 g), and total clutch mass ranges firom 5.L27 .2 g(E = 14.4 g). Clutch number and mass are positively correlated with carapace length. Spermiogenesis occurs throughout much of the year, peakingfrom November to January; spermatogenesis appears continuous for the population, although individuals may have discontinuous spermatogenesis with a resting period in the February to May interval. KBv Wonos. - Reptilia; Testudines; Kinosternidae; Claudius angusta.tus; turtle; reproduction; oogenesisl spermatogenesisl sexual maturity; clutch size; nesting season; morphometrics; Mexico

Claudius angustatus, the chopontil or narrow-bridged made in the years 1982-1984, predominantly purchased musk turtle, occurs in a narrow band of land from south- from fishermen. To supplement the purchased samples and central Veracruz, Mexico, eastward to Belize (Fig. 1). It to make field observations, Flores-Villela and a field asso- Iives principally in areas with seasonally flooded grasslands ciate performed four I-2 km transect censuses in early July and forages in these grasslands during the flooding. After the 1985. Each transect traversed flooded fields in a series of t-loods, it reproduces and presumably estivates or greatly nonoverlapping. widely spaced loops. The transects took reduces its activity. This behavior during the drier months is 45-90 minutes and an attempt was made to capture all speculative, like many other aspects of its biolo._ey. Clauclirl-r seen. Even though Claudilts angltstatus was described over a The composition of the monthly samples is variable; century ago (Cope, 1865), its life history is known only from each sample can include turtles from one, two, or three years. a tew anecdotal notes (e.g., Smith and Smith, I9l9; Flores- The monthly samples for the analysis of size of gonadal Villela, 1980; Iverson and Berry, 1980; Alvarez del Toro, structures and gametogenic stage consisted of females/ 1982). Few biologist have observed this species in the wild, males as follows: Jan Ill; Feb 813; Mar ll7; Apr and May 0/ and until recently,no more than 50 specimens were available 0; Jun 2916; Jul 33110; Aug 210; Sep l3ll0; Oct 012; Nov 38/ in scientific collections (Smith and Smith, 1979). Thus, 6; Dec I9l0; Total 144145. The sample for determining Claudiu.s was believed to be a rare turtle. However, it was oviducal clutch size contained 58 females. Specimens are not ! Biologists simply did not know where to find it. deposited in collections of the Estacion de Biologfa Tropical Fishermen, presumably for centuries, have harvested C. "Los Tuxtlas" (UNAMLT), Instituto de Biologfa (IBH), and angustatus and other freshwater turtles in coastal Veracruz the Museo de Zoologia, Facultad de Ciencias (MZFC), and adjacent lowlands to the south. This local fishery al- Universidad Nacional Aut6noma de Mdxico. lowed us to gather monthly samples of Claudius and other Data on spermatogenesis derives from examination of species of turtles from this area. The following study offers histological sections (8 pm; Harris's haematoxylin and a summary of the data gathered on the reproductive biology eosin, Berg's nuclear stain) from the middle of the left testis of C. angustatl,ts,, the smallest extant staurotypine turtle and of each adult male. Each testis was classified using the one of the smallest living kinosternids. Mayhew and Wright (1970) spermatogenic cycle stage- schedule. Seminiferous tubule diameter was recorded to the MATERIALS AND METHODS nearest micron on six tubules for each individual. Measure- ments (to 0. 1 mm) and examination of all gross female and Female and male Claudius angustatus were collected male reproductive structures were performed on recently by local fishermen by hand from flooded grasslands along a preserved specimens with vernier calipers and with the tributary of the Papaloapan River, near Lerdo de Tejada, naked eye or under a dissecting microscope. Testes and Veracruz (Fig . 2). Claudius angustatus is harvested from oviducal eggs were weighed to the nearest 0.001 g and 0. 1 g, June through March but mainly during the wet season (June respectively. One to four size classes of ovarian follicles can to October). Our monthly samples derive from collections occur in a female; we recorded only the diameters of the 'T--@artmentofZooIogy,BrighamYouttg(Jttiversity, largest follicles and the total number of all follicles in the left Provo, Utah 84602 USA ovary. Statistical analyses were performed using Systat4.I. SD = I 10. I t I I .22 mm CL) than the smallest mature female. Three of these nonreproductive turtles ( I 15.2,126.0, 139.0 mm CL; all from September samples) had nonvitellogenic follicles (< 2.0 mm diameter) and no evi- dence of corpora lutea. Oogenesis. Females with maturing follicles (> 10 mm diam.) occurred- in all monthly samples (Table 1). Females with corpora lutea were present in the January- March, Jllne, November, and December samples, and those with oviducal eggs in the November-February samples. Three females caught and palpated in September 1982 were recorded as gravid; unfortunately, they were not retained for later dissection and confirmation of the presence of oviducal eggs. Samples were not available for April-May and Octo- ber, so the gametic condition is unknown for these months. All adult females in the November (n - 38) and Decem- ber (n = 19) samples were gravid. The January sample Figure L. Distribution of Claudius angustatus and the location included a single gravid female, and only one female from (diamond) of the study site in Veracrnz,M6xico. Distribution after Iverson (1992). the February sample (n = 8) had oviducal eggs. Corpora lutea occurred in all November, December, RESULTS and January females. Most (7 of 8) February females also had corpora lutea; these seven females also had one or more General Observations large (> l4 mm diam.) follicles. The single March female and 16 of 29 June females had corpora lutea. Corpora lutea Claudius angustatus is active only when the river floods were not present in females from the July, August, and the adjacent grassy marshes. Flooding normally occurs from September samples. June through October. As the marshes dry, turtles reproduce Clutch Size Chopontils commonly had two or three and then disappear. Presumably they burrow in the mud and hard-shelled eggs per clutch (Table 2). One, four, five, and remain inactive until the area floods again. six egg clutches were less common. The number of large Sexual Dffirences. Males were more abundant than corpora lutea in each female matched the number of oviducal females in four field censuses- (28:l 1, males:females). Our eggs. Of the 47 females with corpora lutea, only 14 individu- reproductive samples were biased, however, toward fe- als showed symmetrical or equal production of eggs on the males, because we preferentially purchased females from left and right sides. In l8 females, one ovary produced the fishermen or in local markets. entire clutch (14 eggs), the left ovary in eight females and Adult females and males differed in several morpho- the right ovary in ten females. In the remaining 15 females, logical features, especially in overall body size and tail each ovary produced eggs but production was asymmetrical, more eggs more than the right in length. Males (x = 1 18.3 + 14.5 mm CL, n - | 18) averaged the left producing one or larger than females (t = 109.1 + I 1.0 mm CL, n - 132). This two cases and the converse in l2 cases. Transuterine migra- difference was evident in the size-frequency distribution of tion of ova was common, e.g., the number of corpora lutea the two sexes (Fig. 3). The majority of the females (697o) were less than I 15 mm carapace length (CL); in contrast, the majority of males (557o) were larger (> 115 mm CL). The largest female was l4l mm CL; three males exceeded this size and the largest was I4l mm CL.

Females

Sexual Maturity. - The attainment of sexual maturity was recogn ized by the presence of one or more of the following states: 1) presence of oviducal eggs (- gravid);2) enlarged and maturing vitellogenic follicles (>10.0 mm diameter); 3) presence of corpora lutea. The smallest female with oviducal eggs was 94.0 mm CL. The smallest female with enlarged follicles was 88.9 mm CL and with corpora lutea 99.0 mm CL. A number of females (n - 41 ; all from June-september samples) did not meet the criteria for maturity, yet they were larger (range, 92.6-139.0 mm CL, x and Figure 2. An adult Claudius cutgLrstcttus. Photo by' R.S'. Barbour. Fronps-Vtt-r-Er-A AND Zuc Claudius Reproductive Biology 183 -

I o p= 20 .= E E lr o L o .o 10 E z5

70 80 90 100 110 120 130 140 150 Carapace Length Glaeses (mm)

Figure 3. Size distribution of subadult and adult Claudius angustcttus from the Veracruz study site. The sample (n = 250) encompasses specimens in 1982-1984. Class size is arbitrarily set at 10 mm CL. Females are depicted Uy sbtlO bars, malei by open bars. in the right ovary equaled the number of eggs in the right Gravid females occurred in the November-January oviduct in only 27Vo (n = 15) of the females. samples of all years, and this period presumably represents Claudizs eggs are ellipsoidal. Their maximum lengths the major nesting season in southern Veracruz. \.aried from 26.4-33.8 mm (x=30.5 + I.52, n= 130), and the maximum widths varied from 16.2-19.7 mm (x = 17.5 + Males 0.70). Individual egg mass ranged from 4.3-l .9 g (x = 6.0 + 0.70). There was a moderate and direct correlation of body Sexual Maturirl'. - Sexual maturity in males is demon- size and clutch size (Fig. 4; eggnumber to CL, r = 0. 62, P < strated by presence of spermatozoa in the seminiferous 0.001; total clutch mass to CL, r = 0.65, P < 0.001, n - 54). tubules or the ducts of the epididymis. The smallest male The average egg weight of eggs in a clutch had no associa- meeting these conditions and also the smallest male exam- tion with body size (r -0.I7, P - 0.221, n = 54). ined histologically was 98.5 mm CL. A few larger males (6 Nesting Some natural nests (n = 7) were found of 43) had no spermatozoa and showed stage 2 or 3 sper- during field work in July, although no actual nesting legg- matogenesis; these larger males lacking sperm derived laying behavior was observed. Six of the nests had 3 eggs from the months (March, June) of reduced spermatogenesis. and one had 4 eggs. Females lay their eggs on or within Spermatogenesis. - Active spermiogenesis occurred ve-qetation (living or detritus) without digging a nest-pit in in some individuals from all monthly samples, except Octo- the soil. ber. The histology of the two October males was difficult to decipher; stroma was absent between the seminiferous tubules, and cells within the tubules were fragmented. These Table 1, Monthly frequency of occuffence of six oogenic stages in tissue samples probably macerated prior to preservation. adult (> 89 mm CL) female (n Claudius - 144). An individual is Three March males showed stage 2 spermatogenesis with counted only once for the largest or oldest gametic stage. No samples exist for April, May, and October. primary spermatocytes as the most advanced sex cells; these males were the smallest (106, 107, 113 mm CL) in our \ lonth n Follicle Classes Oviducal samples. The other March males (II2, 118,119, II9 mm (diameters, mm) Eggs <1.0 r.0-4.9 5.0-9.9 10.0- 14.9 > 15.0 CL) showed a stage 6 condition with spermatids and spermatozoa bordering the lumina of the seminiferous tubules. Jan I I Presumably the former group consisted of immature indi- Feb 8 34 1 \ Iar I I viduals because their tubule diameters were smaller (- = Apr 0 126.2vs. 193.0 pm, t -3.06, P <0.05) than those males with \ Ia1 0 spermatozoa. Jun 29 2 4 t3 l0 Jul 33 12561 Testicular diameters and masses and seminiferous tu- -{ug 2 ll bule diameters showed a cyclic pattern (Fig. 5). The general Sep I 13 213 pattern of spermatogenesis matched that Oct 0 of testicular size \trr' 38 38 with nearly continuous germ cell production, except for a Dec t9 t9 brief resting period in Februar], then gradually intensifying Number 3 1995 184 cHeloNrnN GoNSERVATT'N AND BroLoGv, volume l, -

in Table 2. Clutch size frequency as determined by the number of tured, so there is no apparent bias in capture. Differences oviducal eggs and corpoia lutea in Claudius. Corpora lutea were behavior and activity levels between females and males not recordEd from ali females from which oviducal eggs were could cause differential capture rates. It is also possible that measured. males outnumber females in the adult population sampled. Oviducal Eggs Corpora Lutea Eggs ctnd Nesting The nesting season rn Claudius November to February, apparently Number Number Number angustatus occurs from Number judg- per of per of with most nesting in November and early December, eggs Clutch Females Clutch Females ing from the rapid decrease in the presence of oviducal (Table 1). In 1982, we found three females with eggs in late 6 I 8 1 September (as determined by palpation). This early oogo- 2 27 2 20 nial maturation might have been stimulated by an unusual 3 r9 3 13 dry period (3 weeks in August) during the normally wet 4 4 4 3 Season. However, these specimens were not dissected or X- 5 2 5 2 presence of oviducal eggs. The 6 I rayed to confirm the actual major nesting activity occurs in December and early Janu- I +SD= ar1r, as the major flooding of the streamside grasslands ends, + 2.4 + r.l2 2.5 0.090 although rain showers continue. The duration of natural incubation remains unknown' at different temperatures through May and June. Spermiogenesis and spermatogen- although laboratory incubation days (t 194 days, n Vogt esis occuffed at a high level from June through Janu ary . yielded a range of 95-229 - -70; and Flores-Villela, 1992; unpubl. data). Hausmann (1968) (at28'C) for DISCUSSION reported an incubation period of about 150 days eggs from captive animals. These two sets of observations comparable to that The discovery of unburied clutches of eggs hidden in suggest a long natural incubation period, kinosternids, e.g., 115-258 days and among living and dead vegetation shows that the nesting reported for other tropical or 122-293 days fot StauroQpus behavior of Claudius angustatus lacks a preparatory digging for Kinosternon scorpioides 6). The preceding taxa and phase and the resulting nest/egg cavity, similar to some other triporcatus (Ewert, 1985: Table embryonic diapause kinosternid tuftles and a few other tropical turtles, such as other tropical kinosternids have an its long incubation period, Rhinoclemrnys (Ernst and Barbour, 1989; Moll and Moll, (Ewert, 1985), and considering 1990). Claudirzs probablY does also. sizes of 2-8 eggs. Our field censuses reveal that males outnumber fe- Hausmann (1968) reported clutch parameters of Claudius males, 2.5:1. In contrast, egg clutches incubated in the Table 3 shows that the reproductive sized kinosternids. laboratory yield a nearly 1:1 sex ratio (Vogt and Flores- match those of other comparable females appear to attain Villela , 1992). Although this difference may be due to the Sexual Maturitt,. Some and some males at 98 mm CL; census technique, most C. angustatus observed were cap- sexual maturity at 89 mm CL

? -9 20 oB a4 o o tt d o u (U UJ ^o o ooo b %"o o og E= L 3' o o +t ooo gg o .o 2 %o % E o p 10 o@ 2z Gv o F

90 100 110 120 130 90 100 110 120 130 carapace Length (mm) carapace Length (mm)

(y) length (x),y.= + 0'08x' Figure 4. Relationship ofclutch size to body size. The regression equations: numbe-r of-eggs to^calapjrce -5'59 54)' ;:0.62',- p a 0.o-oi, i= 58; total clutch mais (y) to caraiace lengtli lx;, y = -32.49 + 0.44x, r = 0'65, P < 0'001' n = 2so 1.o @ o Ao 3. v o,8 o =,n o { G' 200 E ET = o.6 E .9 o fa o I F qt o.4 -J o 150 oJ (D t+ o o Lr ! o o.2 Er^ v3 o.o 100 6 I 10 12 Months

Figure 5. Spermatogenic activity reflected by the change in mean testicular mass (lefi axis, solid squares) and mean seminif'erous tubule .r,iir.r.r {right axisiopen triangies) during an annual c"ycle. Months. beginning with January. are designated numerically.

these females were senes- ;1t'r\\ e ve r, not all individuals of this size and larger were vitellogenic follicles; possibly, :larLrre or at least reproductive. Female Clouclirus lacking cent. Reproductive senescence is difficult to prove, and :l;rtlrre follicles ranged from 93-139 mm CL. Whether these temporary gonadal involution can result from starvation, .ndir iduals were truly immature or their corpora lutea had injury, or similar circumstances where energy resollrces .ii.appeared (or were missed by the observer) and vitello- must be redirected away from reproduction. Presumably at S.ne sis had not yet begun is uncertain. All qllestionably males mature :n'rn'rature females derived from summer (June-September) sample does not extend below that carapace len.-eth. i;lmples. Although it is unlikely that all individuals rnature Some lar-eer males (to ll4 mm CL) are immature, sug- ;t the same srze,a range of 20-30 mm (i.e., maturity attained gestin..e at least a l5 ntm CL ran-se over which maturity ret\\een 90-115 mm CL) is larger than expected based on occurs in males. trther studies (e.g., 10-15 mm CL range in Sternotherus Gcunetogenesis Cornbinin-Q these data with the pres- ,tlortftus; Mitchell, 1985). Three explanations are possible ence of early and mid-vitellogenic follicles in July-Septem- ft.rr roilreproductive females > I 14 mm CL. 1) Females with ber females suggests the followin-e reproductive scenario. rrtlill but vitellogenic follicles are mature and the corpora Follicular development begins in May and June, but growth Iutea had regressed or were still present but small and is slow throughout the summer and early fall. Maturation escaped observation. 2) Some females do not reprodLlce and ovulation occur in late October and continue through e\ er\.year and remain in oogenic quiescence. 3) Adult-sized early February, but in November most adult females are ie nrales with only previtellogenic follicles may be reproduc- gravid. Many females will ovulate and deposit a second tivelv senescent. Two of the larger females (126, 139 mm clutch in December-February. During March, April, and CL r had only previtellogenic follicles and were from the May, the ovaries rest and follicular growth is slow. The September sample when all other adult females had large colpora lutea are slowly resorbed and disappear by Augttst.

Table 3. Some reproductive parameters in selected species of warm-temperate to tropical kinosternid turtles (see Iversc-rn et al ., 1991, for i.it;..r on other kinosternid species and populations).

Size at Sexual Egg-Laying Clutch Size Number of Maturity (mm CL) Season (range/mode) Clutches/yr Tlron f emale male Location Source

C:,-iudius rlll€ ItStA|US 89 98 Nov-Feb t-6t2 l -2 Veracruz Present study A', rlrr sterttott uluntosae r00 Jul-Aug 3-5 l4 | -?2 Sonora Iverson, 1989 Iteryerai r 16 2-4t- multiple Tamaulipas Carr and Mast, 1988 Itirtipes 91 May-Sep t-6 I 3 multiple Chihuahua Iverson et al., I 99 I ie uc o stontunt 102 ll8 Continuous t-2 ll multiple Panama Moll and Moll, 1990 5..,'r: otlterus ,',tloretus 66 May-Jul t-5 I 3 2-4 Alabama McPherson and Marion. 198 I The preceding scenario predicts two egg clutches for siendo de noviembre a enero la 6poca de mayor intensidad: many females. Double clutches are certainly possible in la espermiogen6sis parece ser continua en la poblaciSn Claudias because most (> 90Vo) females in November and estudiada, aunque algunos individuos pueden presentar este December have mature follicles (> 15 mm diam.) and fen6meno de forma discontinua con un periodo de desc anzo corpora lutea and/or oviducal eggs. These follicles are near entre febrero y mayo. ovulation size. Unfortunately, the absence of March-May samples does not allow us to determine the presence or LITERATURE CITED absence of mature or atretic follicles immediately following the nesting period. Multiple clutching occurs in some kinosternids, e.g., Alabama Sternothe ruts odoralus with 2-4 Ar-vnnEZDELToRo, MrcuEr- . 1982.Los Reptiles de Chiapas. Tercera Tuxtla Guti6rrez, Chiapas: clutches (McPherson and Marion, 1983), but not all, e.9., EdiciSn, corregida y aumentada. Publicaciones del Instituto de Historia Natural ,248 pp. Iowa Kinosternonflavescens (Iverson, 1991) (also see Table 3). CnRR, JoHN L., AND MRst, Roonntc B. 1988. Natural history Spermatogenesis is apparently continuous at the popu- observations of Kinosternon herrerai (Testudines: lation level, since one or more individuals in each monthly Kinosternidae). Trianea l:87-97 . sample (except in the small and peculiar October sample) Core, Eownno D. 1865. Third contribution to the herpetology of displayed spermatogenesis and spermiogenesis. Individuals tropical America. Proc. Acad. Nat. Sci. Philad. 17:185-198. (adult-sized) show early stages of spermatogenesis in March EnNSr, Cnnl H., AND BRnnouR, RocEn W. 1989. Turtles of the and June. Perhaps males use a variety of spermatogenic World. Washington, D.C.: Smithsonian Institution Press, 313 pp. behaviors during this post-nesting period: some continuing EweRr, MtcHnEl A. 1985. Embryology of turtles. In: Gans, C., full spermatogenesis at a reduced rate; others producing B illett, F., and Maderson, P.F.A. (Eds. ). Biology ofthe Reptilia. Vol. 14, Development A. New York: John Wiley and Sons, pp. l5-261 . primary spermatocytes that delay further meiotic matura- FlonEs-Vrllpln, OscRR A. 1 980. Reptiles de importancia economica. tion; and still others experiencing a full gametic resting Thesis, Faculdad de Ciencias, UNAM, M6xico. phase. Our samples for this critical period are lacking or too HRusvRwN, PErEn. 1968. Claudius angustcttus. Int. Turtle Tort. small to provide an answer. Soc. I. 2(3):14-15. IvEnsoN, JoHN B. 1989. Natural history of the Alamos mud turtle,

Acknowledgments Kino st e mon alamosce (Kinosternidae). Southw. Nat. 34(1):1 34- I 42. IvEnsoN, JoHN B. 1 991 . Life history and demography of the yellow We thank the following individuals for their assistance mud turtle, K i no s t e rnon fl av e s c e ns. Herpetologic a 47 (4) :37 3 -39 5 . with this study. Camilo and Agustin (fishermen of the IvEnsoN, JoHN B. 1992. A Revised Checklist with Distribution Maps of the Turtles of the World. Richmond, Indiana: Privately printed. Zubreta village near Lerdo de Tejada city), Miriam Benabib, Ivenson, JoHN B., BnnTHELMESS, ERrrn L., SMITH, GEopnnEv R., AND Claudia Carnevale, Adrian Morales, Mardocheo Palma, and nE RrveRR, CRTHERTNE E. 1991. Growth and reproduction in the Richard Vogt assisted in gathering specimens and data in the mud turtle Kinosternon hirtipes in Chihuahua, M6xico. J. field and laboratory. R. Vogt suggested, encouraged, and Herpet. 25(l):64-72. regularly offered advice during the tield stage of this study. IvEnsoN, JoHN B., AND Benny, JnuEs F. 1980. Claudius Cope J.C. Mitchell and C.H. Ernst provided valuable suggestions namow-bridged musk turtle. Clsudicts angustatus Cope narrow- for improving the manuscript. bridged musk turtle. Cat. Amer. Amphib. Rept. 236.1-236.2. OFV had a scholarship from Programa de Superaci6n MnyHEw, WrLnun W., AND WntcHr, SHIRLEy J. 1970. Seasonal changes testicular histology three species the hzard del Personal Acaddmico, UNAM at the Instituto de Biologia. in of of genus Uma. J. Morphol. 130: 163- 186. During the final phase of this work OFV received support McPHEnsoN, RocEn J., RNp MnntoN, KEN R. 1 98 I . The reproductive from the Direcci6n General de Asuntos del Personal biology of female Sternotherus odoratus in an Alabama popula- Acad6mico grant no. IN-201789 to J. Llorente and OFV. tion. J. Herpetol. l5(4):389-396. This support was greatly appreciated. MrrcHeLL, JosEpH C. 1985. Female reproductive cycle and life history attributes in a Virginia population of stinkpot turtles, RssuivrBx Sternotherus odoratus. Copeia I985 (0:9a1-949. MoLL, DoN, AND MoLL, Epwnno O. 1990. The slider turtle in the Los machos adultos de Claudius angustatus alcanzan la Neotropics: Adaptation of a temperate species to a tropical In: Gibbons, J.W. (Ed.). Life History and Ecology madurez sexual aproximadamente a 98 mm de longitud del environment. of the Slider Turtle. Washington, D.C.: Smithsonian Institution carapacho y son ligeramente de mayor talla que las hembras. Press, pp. 152- 161 . Algunas hembras alcanzanla madurez sexual a los 89 mm de Srr,rrtr, Hosnnr M., RxD SvtttH, Rozgt-t-n B. 1979. Synopsis of the longitud del carapacho, aunque algunas entre 20 y 25 mm Herpetofauna of Mexico. Vol. VI. Guide to Mexican Turtles m6s grandes son inmaduras tod avia. Las hembras gr6vidas Bibliographic Addendum III. North Bennington, Vermont: John y la anidaci6n ocurren de noviembre a febrero. La puesta de Johnson,1044 pp. huevos varia de I a 6 huevos elipsoidales (x = 17 .5 x 30.5 Vocr, Rrcnnnn C., Rr.ro FlonEs-Vrt-r-EI-e, OscRR A. 1992. Effects of ffiffi, 6.0 g) con una masa total de la puesta de 5 .2-27 .2 g 6 incubation temperature on sex determination in a community of = 14.4 g). nt nfmero de huevos y la masa de la puesta est6 neotropical freshwater turtles in southern Mexico. Herpetologica correlacionada positivamente con la longitud del carapacho. 48(3 ):265-27 0. La espermiogdnesis se presenta la mayor parte del aflo, Accepted: l5 Oct 1994