The Asian Turtle Consortium

Mauremys japonica : Japanese Pond Turtle

Photo by Russ Gurley

Quadruple nesting of a temperate Asian pond turtle (Batagurinae)

David S. Lee and William Mulligan
The Tortoise Reserve, Inc
1879 White Lake Drive, Box 7092
White Lake, North Carolina 28337
< torresinc@aol.com >

Marine turtles are known to produce multiple clutches of eggs per season, loggerheads , Caretta caretta , for example, may nest up to seven times in one summer (Lenarz et al., 1981). Single season double clutching is known for a number of tortoises and freshwater turtles of various families and genera, but single annual clutches appear to be the norm. This is particularly true of temperate North American species, where multiple clutching is known for but a few species. In North American pond turtles (Emididae) double clutching is known in a variety of genera; i.e., some races of box turtles, Terrapine carolina Jackson 1991), while triple clutching is reported for other races of box turtles (Dodd 1997), spotted turtles, Clemmys guttata (Litzgus and Mousseau 2003), and painted turtles, Chrysemys picta and sliders, Trachemys scripta, can produce up to five ! clutches per season (Moll 1973, Jackson 1988). Here we report o n the quadruple clutching of a species of Asian pond turtle. The significance of this is unclear. The general pattern in North American pond turtles is that southern populations produce smaller clutches but deposit eggs more frequently than populations of the same species occurring further north. On a species level northern populations are restricted by shorter summers and typically produce large single clutches. In addition, turtles and tortoises at higher latitudes tend to be larger on both population and species levels, allowing females to maximize clutch size (Tinkle 1961, Wilbur and Morin 1988, Willemsen and Hailey 1999). However there are numerous variations to these trends (see discussions by Dodd 2001 and Litzgus and Mousseau 2003). Compared to North American species, the life histories of most Asian turtles are generally not well documented, and for the many species of Batagures that have not been bred regularly in captivity reproductive information is typica! lly limited.

In the summer of 2005 a single pair of Japanese pond turtles, Mauremys japonica , laid four clutches of eggs. All were fertile. These turtles are maintained in North Carolina in enclosed out door pools. They live in these pools throughout the year hibernating from late October through mid March. During warm spells in the winter they are often seen swimming below the surface, but they do not feed. In 2004 five hatchlings were found in their pen in mid August. The land area of the pen had been flooded for several days by heavy rains resulting from hurricane Charlie. If other clutches were present they did not hatch. In 2005 we added an elevated sand area for nesting and decided to incubate the eggs inside in commercial incubators. Eggs from various clutches of 6 species of temperate and subtropical Asian turtles were all ! incubated at 27 C.

Our single female produced four clutches of eggs in 2005. The total number of eggs was 25, 18 of which hatched. Dates of laying are unknown and dates presented indicate when clutches were found. Clutch 1; 28 June three eggs recovered all of which later died as nearly full term embryos. As several other species shared the same ponds and as the eggs may not have been identified properly young were removed from the eggs and all proved to be M. japonica . Clutch 2: seven of nine eggs hatched on 22 August. Clutch 3; eggs recovered 6 August and five of the seven eggs hatched between 29 and 30 September. Clutch 4: six eggs recovered on 22 August all hatched between 15 and 17 October.

This is one of a few species of Asian pond turtles where published information regarding reproductive biology has been available for a number of decades. Fukada (1965) reported 2-3 clutches are laid annually between mid May and late June. Two to three clutches of five to eight eggs are produced each year, with the number of eggs decreasing with each clutch. Fukada found ten to fifteen days is the normal period between subsequent clutches. The incubation period is reported to be about 70 days. While the quadruple clutching seems exceptional, and may be an aberrant artifact of captivity, studies of a number of North American turtles suggest that this behavior may be the norm for some Asian species as well. However, the potential annual reproductive output of our single adult female is in the same range as the Japanese pond turtles reported by Fukada (1965) that produced three clutches of five to eight eggs. The biological advantage is perhaps the age and size differences betwe! en young from different clutches. Hatchlings from the last clutch had carapace lengths ranging from 30.7 to 32.6 (x=31.6) mm and 5.6-6.1 (5.93) grams, (n=6) while turtles measured on the day clutch four hatched (October 16) from clutch 2 were already 46.6- 49 (x=47.8) mm in length and weighed 15.6-19.3 (17.34) grams (n=7)-- nearly a three fold increase in mass. Fukada (1965) reported hatchlings to be 25 mm in carapace length.

By spreading out the reproductive season over four separate nesting events, the female turtles would place a number distinct size classes of offspring into the system, with the different sizes, or starting dates possibly having survival advantages (response to drought, flooding, food availability, predator search images, and seasonal predators such as migratory herons) greater than those from the other clutches. For temperate species early hatching would allow hatchlings to grow prior to hibernation and late hatchlings to possibly get through their first winter on food reserves from absorbed yolks. More importantly clutches deposited over time would decrease the likelihood that the total reproductive out put of a single individual would be consumed by a nest predator (Obbard and Brooks 1981). Thus, multiple clutching may be more important to long-term existence of populations than total reproductive output.

Increase in clutch size with increasing latitudes has been reported in a number of North American turtles (Congdon and Gibbons 1985, Iverson 1992, Iverson et al., 1993, 1997, Iverson and Smith 1993, and Tinkle, 1961). It seems likely that Asian pond turtles should have similar reproductive strategies where in lower latitudes smaller multiple clutches would have a significant survival advantage. Japan has a long north/south axis with the endemic M. japonica being found on Honshu, Keosha and Shikoko Islands extending from latitude 41 N south to 31 N. It would be interesting to know if females from the northern portion of their range produce larger but fewer clutches. Of equal interest would be the documentation of reproductive output of captive individuals maintained out doors at different latitudes. Is multiple clutchin! g a long-term genetic adaptation, simply an individual's response to climate, or both? In any scenario it is clear that long before academic biologists learned to charge windmills, or that Don Quixote knew about all this egg storage stuff (De Cervantes 1605), turtles living in appropriate climates had already discovered advantages to not venture all their eggs in one basket. We think farmer Brown's daughter rediscovered this ca.1931. (OK, so we are overly pro-turtle.)

The Japanese pond turtles discussed here are part of the Asian Turtle Consortium's long-term effort focused on breeding declining populations of Asian turtles for the future goal of repatriation into their native counties. The Tortoise Reserve is pleased to be able to contribute to this private sector conservation program.

Literature Cited:

De Cervantes, M. 1605. Ingenioso Hidalgo Don Quixote de la Mancha (The History of the various and Wittie Errant Knight Don Quixote de la Mancha). Part I, Book III, Chapter 9.

Congdon, J. D. and J. W. Gibbons. 1985. Egg components and reproductive characteristics of turtles: relationships to body size. Herpetologica. 41: 194-205.

Dodd, C. K, Jr. 1997. Clutch size and frequency in Florida box turtles ( Terrapene carolina bauri ): implications for conservation. Chelonian Conservation Biol. 2: 370-377.

Dodd, C. K. 2001. North American Box Turtles: a natural history. University of Oklahoma Press, Norman. Pp. 231.

Fukada, H. 1965. Breeding habits of some Japanese reptiles (critical review). Bull. Kyoto Gak. Univ. Ser. B 27:65-82.

Jackson, D. R. 1988. Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida: Bulletin Florida State Museum Biol. Sci. 33: 113-158.

Jackson, D. R. 1991. Multiple clutches and nesting behavior in the Gulf Coast box turtle. Florida Field Naturalist 19: 14-16.

Lenarz, M. S., N. B. Frazer, M. S. Ralston, and R. C. Most. 1981. Seven nest records for loggerhead turtle ( Caretta caretta ) in one season. Herp. Review 19:9.

Litzgus, J. D. and T. A. Mousseau. 2003. Multiple clutching in southern spotted turtles, Clemmys guttata . Jour Herpetology 37(1): 17-23.

Moll, E. O. 1973. Latitudinal and intersubspecific variation in reproduction of the painted turtle, Chrysemys picta . Herpetologica. 29: 307-318.

Obbard, M. E. and R. J. Brooks. 1981. Fate of overwintering clutches of the common snapping turtle ( Chelydra serpentina ) in Alonquin Park, Ontario. Canada Field-Naturalists. 95: 305-352.

Tinkle, D. W. 1961. Geographic variation in reproduction, size, sex ratios and maturity of Sternotherus odoratus . Ecology. 42: 68-76.

Wilbur, H. M. and P. J. Morion. 1988. Life history evolution in turtles: in C. Gans and R. B. Huey ( eds. ), Biology of the Reptilia. Vol. 16. Ecology B. Defense and Life History, pp. 387-437. Alan R. Liss, Inc., New York.

Willemsen, R. E. and A. Hailey. 1999. Variation of adult body size of the tortoise Testudo hermanni in Greece: proximate and ultimate causes. Jour. Zoology. 248: 379-396.


	Mauremys japonica : Japanese Pond Turtle Photo by Russ Gurley Quadruple nesting of a temperate Asian pond turtle (Batagurinae) David S. Lee and William Mulligan The Tortoise Reserve, Inc 1879 White Lake Drive, Box 7092 White Lake, North Carolina 28337 < torresinc@aol.com > Marine turtles are known to produce multiple clutches of eggs per season, loggerheads , Caretta caretta , for example, may nest up to seven times in one summer (Lenarz et al., 1981). Single season double clutching is known for a number of tortoises and freshwater turtles of various families and genera, but single annual clutches appear to be the norm. This is particularly true of temperate North American species, where multiple clutching is known for but a few species. In North American pond turtles (Emididae) double clutching is known in a variety of genera; i.e., some races of box turtles, Terrapine carolina Jackson 1991), while triple clutching is reported for other races of box turtles (Dodd 1997), spotted turtles, Clemmys guttata (Litzgus and Mousseau 2003), and painted turtles, Chrysemys picta and sliders, Trachemys scripta, can produce up to five ! clutches per season (Moll 1973, Jackson 1988). Here we report o n the quadruple clutching of a species of Asian pond turtle. The significance of this is unclear. The general pattern in North American pond turtles is that southern populations produce smaller clutches but deposit eggs more frequently than populations of the same species occurring further north. On a species level northern populations are restricted by shorter summers and typically produce large single clutches. In addition, turtles and tortoises at higher latitudes tend to be larger on both population and species levels, allowing females to maximize clutch size (Tinkle 1961, Wilbur and Morin 1988, Willemsen and Hailey 1999). However there are numerous variations to these trends (see discussions by Dodd 2001 and Litzgus and Mousseau 2003). Compared to North American species, the life histories of most Asian turtles are generally not well documented, and for the many species of Batagures that have not been bred regularly in captivity reproductive information is typica! lly limited. In the summer of 2005 a single pair of Japanese pond turtles, Mauremys japonica , laid four clutches of eggs. All were fertile. These turtles are maintained in North Carolina in enclosed out door pools. They live in these pools throughout the year hibernating from late October through mid March. During warm spells in the winter they are often seen swimming below the surface, but they do not feed. In 2004 five hatchlings were found in their pen in mid August. The land area of the pen had been flooded for several days by heavy rains resulting from hurricane Charlie. If other clutches were present they did not hatch. In 2005 we added an elevated sand area for nesting and decided to incubate the eggs inside in commercial incubators. Eggs from various clutches of 6 species of temperate and subtropical Asian turtles were all ! incubated at 27 C. Our single female produced four clutches of eggs in 2005. The total number of eggs was 25, 18 of which hatched. Dates of laying are unknown and dates presented indicate when clutches were found. Clutch 1; 28 June three eggs recovered all of which later died as nearly full term embryos. As several other species shared the same ponds and as the eggs may not have been identified properly young were removed from the eggs and all proved to be M. japonica . Clutch 2: seven of nine eggs hatched on 22 August. Clutch 3; eggs recovered 6 August and five of the seven eggs hatched between 29 and 30 September. Clutch 4: six eggs recovered on 22 August all hatched between 15 and 17 October. This is one of a few species of Asian pond turtles where published information regarding reproductive biology has been available for a number of decades. Fukada (1965) reported 2-3 clutches are laid annually between mid May and late June. Two to three clutches of five to eight eggs are produced each year, with the number of eggs decreasing with each clutch. Fukada found ten to fifteen days is the normal period between subsequent clutches. The incubation period is reported to be about 70 days. While the quadruple clutching seems exceptional, and may be an aberrant artifact of captivity, studies of a number of North American turtles suggest that this behavior may be the norm for some Asian species as well. However, the potential annual reproductive output of our single adult female is in the same range as the Japanese pond turtles reported by Fukada (1965) that produced three clutches of five to eight eggs. The biological advantage is perhaps the age and size differences betwe! en young from different clutches. Hatchlings from the last clutch had carapace lengths ranging from 30.7 to 32.6 (x=31.6) mm and 5.6-6.1 (5.93) grams, (n=6) while turtles measured on the day clutch four hatched (October 16) from clutch 2 were already 46.6- 49 (x=47.8) mm in length and weighed 15.6-19.3 (17.34) grams (n=7)-- nearly a three fold increase in mass. Fukada (1965) reported hatchlings to be 25 mm in carapace length. By spreading out the reproductive season over four separate nesting events, the female turtles would place a number distinct size classes of offspring into the system, with the different sizes, or starting dates possibly having survival advantages (response to drought, flooding, food availability, predator search images, and seasonal predators such as migratory herons) greater than those from the other clutches. For temperate species early hatching would allow hatchlings to grow prior to hibernation and late hatchlings to possibly get through their first winter on food reserves from absorbed yolks. More importantly clutches deposited over time would decrease the likelihood that the total reproductive out put of a single individual would be consumed by a nest predator (Obbard and Brooks 1981). Thus, multiple clutching may be more important to long-term existence of populations than total reproductive output. Increase in clutch size with increasing latitudes has been reported in a number of North American turtles (Congdon and Gibbons 1985, Iverson 1992, Iverson et al., 1993, 1997, Iverson and Smith 1993, and Tinkle, 1961). It seems likely that Asian pond turtles should have similar reproductive strategies where in lower latitudes smaller multiple clutches would have a significant survival advantage. Japan has a long north/south axis with the endemic M. japonica being found on Honshu, Keosha and Shikoko Islands extending from latitude 41 N south to 31 N. It would be interesting to know if females from the northern portion of their range produce larger but fewer clutches. Of equal interest would be the documentation of reproductive output of captive individuals maintained out doors at different latitudes. Is multiple clutchin! g a long-term genetic adaptation, simply an individual's response to climate, or both? In any scenario it is clear that long before academic biologists learned to charge windmills, or that Don Quixote knew about all this egg storage stuff (De Cervantes 1605), turtles living in appropriate climates had already discovered advantages to not venture all their eggs in one basket. We think farmer Brown's daughter rediscovered this ca.1931. (OK, so we are overly pro-turtle.) The Japanese pond turtles discussed here are part of the Asian Turtle Consortium's long-term effort focused on breeding declining populations of Asian turtles for the future goal of repatriation into their native counties. The Tortoise Reserve is pleased to be able to contribute to this private sector conservation program. Literature Cited: De Cervantes, M. 1605. Ingenioso Hidalgo Don Quixote de la Mancha (The History of the various and Wittie Errant Knight Don Quixote de la Mancha). Part I, Book III, Chapter 9. Congdon, J. D. and J. W. Gibbons. 1985. Egg components and reproductive characteristics of turtles: relationships to body size. Herpetologica. 41: 194-205. Dodd, C. K, Jr. 1997. Clutch size and frequency in Florida box turtles ( Terrapene carolina bauri ): implications for conservation. Chelonian Conservation Biol. 2: 370-377. Dodd, C. K. 2001. North American Box Turtles: a natural history. University of Oklahoma Press, Norman. Pp. 231. Fukada, H. 1965. Breeding habits of some Japanese reptiles (critical review). Bull. Kyoto Gak. Univ. Ser. B 27:65-82. Jackson, D. R. 1988. Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida: Bulletin Florida State Museum Biol. Sci. 33: 113-158. Jackson, D. R. 1991. Multiple clutches and nesting behavior in the Gulf Coast box turtle. Florida Field Naturalist 19: 14-16. Lenarz, M. S., N. B. Frazer, M. S. Ralston, and R. C. Most. 1981. Seven nest records for loggerhead turtle ( Caretta caretta ) in one season. Herp. Review 19:9. Litzgus, J. D. and T. A. Mousseau. 2003. Multiple clutching in southern spotted turtles, Clemmys guttata . Jour Herpetology 37(1): 17-23. Moll, E. O. 1973. Latitudinal and intersubspecific variation in reproduction of the painted turtle, Chrysemys picta . Herpetologica. 29: 307-318. Obbard, M. E. and R. J. Brooks. 1981. Fate of overwintering clutches of the common snapping turtle ( Chelydra serpentina ) in Alonquin Park, Ontario. Canada Field-Naturalists. 95: 305-352. Tinkle, D. W. 1961. Geographic variation in reproduction, size, sex ratios and maturity of Sternotherus odoratus . Ecology. 42: 68-76. Wilbur, H. M. and P. J. Morion. 1988. Life history evolution in turtles: in C. Gans and R. B. Huey ( eds. ), Biology of the Reptilia. Vol. 16. Ecology B. Defense and Life History, pp. 387-437. Alan R. Liss, Inc., New York. Willemsen, R. E. and A. Hailey. 1999. Variation of adult body size of the tortoise Testudo hermanni in Greece: proximate and ultimate causes. Jour. Zoology. 248: 379-396.
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