Editorial Type: Articles
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Online Publication Date: 01 Dec 2015

Reproduction of Captive Asian Giant Softshell Turtles, Pelochelys cantorii

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Article Category: Research Article
Page Range: 143 – 147
DOI: 10.2744/CCB-1139.1
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Abstract

The Asian giant softshell turtle, Pelochelys cantorii, is endangered and has been designated as a first-grade protected animal in China. This article reports the results of a study on the reproductive biology of Asian giant softshell turtles. Two individuals, a male and a female from the Suijiang River in Guangning County, Guangdong Province, were introduced into captivity 8 yrs ago. The 2 turtles have engaged in mating activity since April 2014, and the female laid a total of 66 eggs in 2014 (25 eggs on 15 June, 22 eggs on 30 June, and 19 eggs on 14 July). The egg laying took an average of 50.6 min. Egg shape was spherical, and mean (± SD) egg mass was 13.27 ± 0.97 g, with mean diameter 2.90 ± 0.12 cm. The viability rate was 46% and the hatching rate 33%, and only 10 neonates successfully hatched. Hatchling body weight averaged 10.0 ± 0.56 g, carapace length averaged 42.25 ± 3.69 mm, carapace width averaged 40.25 ± 1.58 mm, and carapace height averaged 12.54 ± 0.91 mm. The juvenile turtles differed from the adults in body color. The juvenile plastron is white; carapace, head, neck, and limbs have some small irregular black and pale yellow spots.

The Asian giant softshell turtle, Pelochelys cantorii (Trionychidae), is widespread, occurring in China, India, Bangladesh, Myanmar, Laos, Cambodia, Thailand, Vietnam, Indonesia, Malaysia, and the Philippines (Das 2008). In China, it is distributed mainly in Jiangsu, Zhejiang, Fujian, Guangdong, Guangxi, and Yunnan provinces (Chinese Animal Fauna Editorial Committee Chinese Academy of Sciences 1998), where it is threatened by overcollection for food and habitat destruction resulting from urbanization and water pollution (Lau and Shi 2000). The species has suffered gradual reduction in its range, its total population has decreased, and it is classified as critically endangered (Huang et al. 1990; Zhao 1998). In 1989, the Asian giant softshell turtle was listed as a first-grade protected animal in China and put on par with the giant panda, Ailuropoda melanoleuca, and the Yangtze River dolphin, Lipotes vexillifer; it is known as the “panda in the water” (Gu et al. 2000).

It is extremely important to conduct conservation research on Asian giant softshell turtles in China and elsewhere, but published research reports on this species are scarce. Gu et al. (2000) and Huang et al. (2003) described the natural distribution and natural reproductive ecology of the turtle in the Oujiang River in Zhejiang Province; Ruan et al. (2001) investigated the present situation of the turtle in Youxi River, Fujian Province; and Chen et al. (2013) analyzed the complete mtDNA sequence of Asian giant softshell turtle from Oujiang River. Thus far, there have been no studies on the reproduction of the turtle in captivity. The Suijiang River, a tributary of the Beijiang River in the Pearl River basin, is an Asian giant softshell turtle habitat in China. Two live individuals caught by fishermen were rescued from the Suijiang River by the Guangning Station of the Guangdong Province Fisheries Policy Administration in 2006 and reared in the pond in the Guangning County Biodiversity Conservation and Cultivation Facility in Zhaoqing, Guangdong Province. The 2 turtles have engaged in mating activity since April 2014, and a study on reproduction was carried out. The data reported herein will benefit efforts to conserve the Asian giant softshell turtle in China and elsewhere within its geographic range.

METHODS

Captive Care, Condition, and Management

Observations were made of the 2 captive Asian giant softshell turtles (female  =  20.75 kg; male  =  14.70 kg) from April to September 2014. The pond housing the Asian giant softshell turtles is a rectangular cement structure surrounded by a brick wall 1.2 m high around the pond to prevent escape. The pond area is 1000 m2, and water depth ranges from 1.0 to 1.2 m. The bottom of the pond is covered by a layer of sediment 30 cm thick. The pond water is groundwater maintained at pH 7.0. To regulate water quality, the pond was stocked with 40 Ctenopharyngodon idellus, 20 Hypophthalmichthys molitrix, and 20 Aristichthys nobilis. Pistia stratiotes enclosed with bamboo were included at 2 corners in the pond. Water level was maintained by adding or draining water as needed. Live Cirrhinus molitorella fry and Corbicula fluminea were put in the pond regularly as food for the turtles. A platform (4.5 × 4.5 m, length × width) with a roof was built in the middle of the pond, slightly below the surface of the water level in the pond. A sand pile 50 cm high was placed on the platform as a nesting substrate.

Observations of Reproductive Behavior

Mating and egg-laying behavior were observed and recorded by cameras (ANSPO infrared camera ASP-699A) installed in the pond between April and August. Turtle eggs were collected by 1200 hrs each day after nesting was detected, and nests were observed and measured. Egg mass and diameter were measured using an electronic balance and a Vernier caliper, respectively. The method for artificial incubation of the turtle egg was that of Zhu et al. (2006, 2013). The incubator was a plastic box, size 40 × 60 cm, with vermiculite as the incubation medium. The eggs were arranged in the incubator with 3-cm spacing on a layer of vermiculite 5 cm thick and covered with a second layer of vermiculite 2 cm thick. The incubation temperature was the local natural indoor temperature. According to the Guangning County weather network, in 2014, average maximum and average minimum temperatures, respectively, were 33.33°C and 25.37°C in June, 35.13°C and 25.87°C in July, 33.97°C and 24.97°C in August, and 33.60°C and 23.97°C in September. The moisture content of the vermiculite was maintained between 30% and 40%. Morphological data were collected on hatching. The incubation period and hatching rate were recorded.

Statistics

For egg mass and diameter, comparisons among nests were carried out using 1-way analysis of variance followed by Fisher’s LSD test. The hatching rate was compared among nests using Fisher’s exact test. Mean values are followed by ± SD, and statistical significance was accepted as p < 0.05.

RESULTS

Adult Morphology and Sex Characteristics

Morphometric data for the 2 adult turtles are shown in Table 1. The female had a longer carapace length, higher carapace height, and shorter tail. The female’s carapace is grayish black (Fig. 1A), and her cloacal orifice is dark gray (Fig. 1B). The male’s carapace is light grayish-brown (Fig. 1C), with the basal part of the tail pink and his cloacal orifice white (Fig. 1D).

Figure 1. Sex characteristics of Asian giant softshell turtle: (A) female, (B) female cloacal orifice, (C) male, (D) male cloacal orifice.Figure 1. Sex characteristics of Asian giant softshell turtle: (A) female, (B) female cloacal orifice, (C) male, (D) male cloacal orifice.Figure 1. Sex characteristics of Asian giant softshell turtle: (A) female, (B) female cloacal orifice, (C) male, (D) male cloacal orifice.
Figure 1. Sex characteristics of Asian giant softshell turtle: (A) female, (B) female cloacal orifice, (C) male, (D) male cloacal orifice.

Citation: Chelonian Conservation and Biology 14, 2; 10.2744/CCB-1139.1

Table 1. Morphometric data for captive male and female Asian giant softshell turtles in the Guangning County Biodiversity Conservation and Cultivation Facility in Zhaoqing, Guangdong Province, China.
Table 1.

Breeding Behavior

Between April and June 2014, the 2 turtles were observed repeatedly chasing and mating in the pond, making large waves on the surface of the water. In mid-June, the female was observed several nights climbing the sand pile in search of a nest site. The female laid 25 eggs, 22 eggs, and 19 eggs (mean  =  22.0 eggs) beginning at 2022 hrs (15 June), 2126 hrs (30 June), and 2256 hrs (14 July), respectively.

Nest construction and clutch deposition required an average of 50.6 ± 1.9 min. The process was divided into 4 stages: stage I was nest site selection, stage II was excavation of the egg chamber, stage III was laying and covering the eggs, and stage IV was leaving the nest and entering the water. In stage I, the female climbed up the sand pile and selected a nest site. Once the nest position was selected, the female started digging. Selecting a nest site took an average of 7.3 ± 2.8 min. In stage II, the female excavated the nest using her hind limbs. Nest depth was approximately 20 cm. Nest excavation required an average of 10.3 ± 3.1 min. In stage III, the female deposited eggs. The eggs were deposited in 3 to 4 layers in the nest, and nest dimensions were ~ 12 cm in width and ~ 14 cm in length. After laying, the turtle covered the nest using her hind limbs. Laying the eggs and covering them took an average of 15.5 ± 0.9 min. In stage IV, the female moved from the nest, walked around on the sand pile, and re-entered the water. This process took an average of 17.5 ± 3.0 min.

Egg Laying and Hatching

The female deposited 3 clutches during the breeding season, with an interclutch interval of approximately 15 d. The eggs were spherical with rigid shells. The results of egg laying and hatching are shown in Table 2. Egg size varied among clutches, and the second nest’s average egg mass and diameter were both significantly greater than those of the first and third nests (p < 0.05). The second nest eggs had higher deformity rates and lower rates of viability. Eggs were 13.27 ± 0.97 g in weight and 2.90 ± 0.12 cm in diameter.

Table 2. Results of egg laying and hatching of Asian giant softshell turtle in 2014. Hatching rate  =  eggs hatched/eggs exhibiting viability.
Table 2.

Each fertilized egg had a white spot on the shell. The viability rate of the first and third clutches was significantly higher than that of the second clutch (p < 0.05). None of the eggs of the second nest successfully hatched. The incubation period of the third clutch was shorter than that of the first clutch; average incubation period was 66.17 d. The hatching rates of the 3 nests’ eggs did not differ significantly (p < 0.05). Over the entire season, 10 eggs hatched successfully (33.3%).

Hatchling Morphological Characteristics

Hatchlings are similar to adults in their morphology (Fig. 2). For hatchlings, body mass averaged 10.0 ± 0.56 g, carapace length averaged 42.25 ± 3.69 mm, carapace width averaged 40.25 ± 1.58 mm, and carapace depth averaged 12.54 ± 0.91 mm. The hatchling plastron is white; carapace, head, neck, and limbs have some small irregular black and pale yellow spots, which are obviously different from adults, and the margin of the carapace is white. The rim of the hatchling eye has 6 evenly spaced black spots.

Figure 2. Hatchling Asian giant softshell turtle (4 d after hatching).Figure 2. Hatchling Asian giant softshell turtle (4 d after hatching).Figure 2. Hatchling Asian giant softshell turtle (4 d after hatching).
Figure 2. Hatchling Asian giant softshell turtle (4 d after hatching).

Citation: Chelonian Conservation and Biology 14, 2; 10.2744/CCB-1139.1

DISCUSSION

Sex Characteristics

In softshell turtles, adults exhibit sexual dimorphism, especially in the tail. The male tail is thick and long, and the cloacal orifice is located relatively far from the body, as in Trionyx sinensis, Cyclanorbis senegalensis, Palea steindachneri, and Apalone ferox (Ernst and Barbour 1989). However, given our small sample size, statements regarding potential sexual size dimorphism in this species are premature.

Breeding Behavior

Similar to other aquatic turtles, Asian giant softshell turtles stay in the water most of the time. In the breeding season, the egg-laying process of the turtle is similar to that of P. steindachneri (Yang et al. 1998) and Mauremys mutica (Zhao et al. 2008). The Asian giant softshell turtle’s egg-laying process was briefer than that of M. mutica, which took 6 stages; the process took a total time that was less than in P. steindachneri and M. mutica, which took 60 and 116 min, respectively. As in other turtles, parental care apparently does not occur in the Asian giant softshell turtle.

Embryonic Development and Hatching

The results indicated that Asian giant softshell turtles can lay eggs 3 times in a year at 15-d intervals. Multiple egg-laying episodes are also found in other turtles. The average clutch size was 22 eggs in this study, smaller than the clutches of sizes reported by Gu et al. (2000), Huang et al. (2003), and Ernst and Barbour (1989). There may be a positive relationship between maternal body size and clutch size in Asian giant softshell turtles, as in some other freshwater turtles (Congdon and Gibbons 1983; Iverson 1997), but information on this species is scarce.

The nest was also shallower, and fewer layers of eggs were laid than in the previous reports, perhaps due to the small body size of the female (Macip-Ríos et al. 2009). The viability rate was only 10% in the wild (Huang et al. 2003) but was 46% in this study. These data suggest that the viability rate in captivity is far higher than it is in the wild, but the difference could also relate to differences in egg-handling protocols.

The egg of the Asian giant softshell turtle is round and rigid, similar to but larger than the egg of T. sinensis (Zhu et al. 2013). Mean egg diameter in our study was somewhat less than the egg diameter of 3.0 cm reported by Huang et al. (2003), but the mean egg mass in our study was much less than the egg mass of 18.32 g recorded by Huang et al. (2003). The egg diameters are similar, but a large weight difference is apparent.

In this study, the incubation period of the third clutch of eggs was shorter than that of the first clutch, probably due to an increase in incubation temperature. The third clutch of eggs was incubated in July and August, when the temperature was relatively high, resulting in a relatively brief incubation period.

The hatchlings of the Asian giant softshell turtle have a body shape similar to that of the adults, but the body color is obviously different. Juvenile A. ferox, Aspideretes gangeticus, Nilssonia formosa, T. sinensis, and P. steindachneri are also different from adults in body color (Ernst and Barbour 1989). This pattern seems to be characteristic of softshell turtles.

ACKNOWLEDGMENTS

We thank all of the people who helped care for the 2 captive Asian giant softshell turtles over the past 8 yrs. The research was conducted with permission of the Guangning Station, Guangdong Province Fisheries Policy Administration, and financial support was provided by the Ministry of Agriculture Financial Project (#2130135/2/1) and the Administration of Ocean and Fisheries of Guangdong Province, China.

LITERATURE CITED

  • Chen, X.,
    Zhou, Z.,
    Peng, X.,
    Huang, X.,
    and
    Chen, Z.
    2013. Complete mitochondrial genome of the endangered Asian giant softshell turtle Pelochelys cantorii (Testudinata: Trionychidae). Mitochondrial DNA24:111113.
  • Chinese Animal Fauna Editorial Committee Chinese Academy of Sciences. 1998. Chinese Animal Fauna: Reptilia. Volume 1. General Testudines Crocodylia.
    Beijing
    :
    Science Press
    , pp. 5861.
  • Congdon, J.D.
    and
    Gibbons, J.W.
    1983. Relationships of reproductive characteristics to body size in Pseudemys scripta. Herpetologica39:147151.
  • Das, I.
    2008. Pelochelys cantorii Gray 1864—Asian giant softshell turtle. In:
    Rhodin, A.G.J.,
    Pritchard, P.C.H.,
    van Dijk, P.P.,
    Saumure, R.A.,
    Buhlmann, K.A.,
    and
    Iverson, J.B.
    (Eds.).Conservation Biology of Freshwater Turtles and Tortoises: A Compilation Project of the IUCN/SSC Tortoise and Freshwater Turtle Specialist Group.
    Chelonian Research Monographs
    5:011.1011.6.
  • Ernst, C.H.
    and
    Barbour, R.W.
    1989. Turtles of the World.
    Washington, DC
    :
    Smithsonian Institution Press
    , pp. 98111.
  • Gu, H.,
    Ma, X.,
    Ge, Y.,
    and
    Hong, L.
    2000. Studies on the distribution and reproduction of Pelochelys cantorii Gray, 1864 in the Oujiang River, Zhejiang Province. Sichuan Journal of Zoology19:151153. (In Chinese with English abstract.)
  • Huang, M.H.,
    Cai, C.,
    Jin, Y.,
    Gu, H.,
    Zhang, S.,
    Guo, H.,
    and
    Wei, J.
    1990. Fauna of Zhejiang. Amphibia Reptilia.
    Hangzhou
    :
    Zhejiang Science and Technology Publishing House
    , 306 pp.
  • Huang, W.H.,
    Zhou, S.Y.,
    Wang, K.W.,
    and
    Lian, X.M.
    2003. An investigation of naturally reproductive ecology of Pelochelys bibroni. Journal of Anhui University Natural Science Edition27:103107. (In Chinese with English abstract.)
  • Iverson, J.B.
    1997. Local and geographic variation in the reproductive biology of the snapping turtle (Chelydra serpentina). Herpetologica53:96117.
  • Lau, M.
    and
    Shi, H.
    2000. Conservation and trade of terrestrial and freshwater turtles and tortoises in the People’s Republic of China. In:
    van Dijk, P.P.,
    Stuart, B.L.,
    and
    Rhodin, A.G.J.
    (Eds.). Asian Turtle Trade: Proceedings of a Workshop on Conversation and Trade of Freshwater Turtles and Tortoises in Asia. Chelonian Research Monographs2:3038.
  • Macip-Ríos, R.,
    Cisneros, M.D.L.A.,
    Aguilar-Miguel, X.S.,
    and
    Casas-Andreu, G.
    2009. Population ecology and reproduction of the Mexican mud turtle (Kinosternon integrum) in Tonatico, Estado de México. Western North American Naturalist69:501510.
  • Ruan, D.M.,
    Su, X.H.,
    Chen, X.Z.,
    Zhou, M.Q.,
    Lian, K.P.,
    and
    Wu, J.Z.
    2001. Investigation of present situation of large soft-shelled turtle (Pelochelys bibroni) at Youxi River in Fujian Province. Chinese Journal of Zoology36(
    6
    ):4245. (In Chinese with English abstract.)
  • Yang, J.C.,
    Zhou, Y.F.,
    Rao, J.H.,
    and
    Wu, X.P.
    1998. The biologic studies on Palea steindachneri. Zoological Research19:497499. (In Chinese.)
  • Zhao, E.M.
    1998. China Red Data Book of Endangered Animals. Amphibia and Reptilia.
    Beijing
    :
    Science Press
    , pp. 162164.
  • Zhao, W.H.,
    Wei, C.Q.,
    Guo, J.H.,
    Zhu, X.P.,
    and
    Chen, Y.L.
    2008. Observation on the egg-laying behavior of Mauremys mutica. Chinese Journal of Zoology43(
    4
    ):9296. (In Chinese with English abstract.)
  • Zhu, A.L.,
    Shi, Y.,
    Zhu, X.P.,
    Wei, C.Q.,
    Li, W.,
    and
    Duan, A.L.
    2013. Effects of different temperature on embryonic development, hatchling traits and hatchling moving of Trionyx sinensis. Genomics and Applied Biology32:303307. (In Chinese with English abstract.)
  • Zhu, X.P.,
    Wei, C.Q.,
    Zhao, W.H.,
    Du, H.J.,
    Chen, Y.L.,
    and
    Gui, J.F.
    2006. Effects of incubation temperatures on embryonic development in the Asian yellow pond turtle. Aquaculture259:243248.
Copyright: © 2015 Chelonian Research Foundation 2015
Figure 1.
Figure 1.

Sex characteristics of Asian giant softshell turtle: (A) female, (B) female cloacal orifice, (C) male, (D) male cloacal orifice.


Figure 2.
Figure 2.

Hatchling Asian giant softshell turtle (4 d after hatching).


Contributor Notes

The first two authors contributed equally to this work

Corresponding author

Handling Editor: Peter V. Lindeman

Received: 10 Dec 2014
Accepted: 05 Apr 2015
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