Zoo Biology 34: 178–182 (2015)
BRIEF REPORT
Age and Body Size of Captive Hawksbill Turtles at the Onset of Follicular Development Isao Kawazu,* Masakatsu Kino, Konomi Maeda, and Hideshi Teruya Okinawa Churashima Foundation, 888 Ishikawa, Motobu, Okinawa, Japan The aim of this study was to record the age and body size of 23 captive female hawksbill turtles at the onset of follicular development. The age, straight carapace length (SCL), and body mass (BM) of the turtles were recorded between 2006 and 2014 at follicular development (determined via ultrasonography) these parameters were 17.7 1.7 years (range: 13–20 years), 77.7 3.3 cm (73.3–83.5 cm), and 61.1 8.0 kg (48.2–76.1 kg), respectively. When the year of the onset of follicular development was designated year 0, the increase in SCL in years -7–0 and 0–3 averaged 2.2 cm and 1.0 cm, respectively. Correspondingly, the increase in BM in years -7–0 and 0–3 averaged 5.0 kg and 2.2 kg, respectively. This is the first study to report the age and body size of captive female hawksbill turtles at the onset of follicular development, which indicates the beginning of sexual maturation. The reduction in growth after follicular development suggests that at the onset of sexual maturation, female hawksbills may utilize energy for follicular development rather than growth. Zoo Biol. 34:178–182, © 2014 Wiley Periodicals, Inc. 2015.
Keywords: straight carapace length; body mass; vitellogenesis
INTRODUCTION Hawksbill turtles (Eretmochelys imbricata) are distributed in tropical and subtropical coral reefs worldwide, and are listed as critically endangered on the International Union for Conservation of Nature (IUCN) red list for threatened species [Mortimer and Donnelly, 2008]. Hence, the active implementation of captive breeding programs offers a unique management opportunity for the recovery and conservation of this endangered species [Owens and Blanvillain, 2013]. Knowledge of the age and body size of hawksbill turtles at the onset of sexual maturation is important for the effective implementation of captive breeding programs. In addition, examination of these reproductive parameters could extend our knowledge of the reproductive biology of sea turtles, thus improving the effectiveness of conservation efforts and resource management. Age and body size at the onset of sexual maturation have been determined for captive green turtles (Chelonia mydas) and Kemp’s ridley turtles (Lepidochelys kempi) [Wood and Wood, 1980, 1988; Bjorndal et al., 2013]. However, these parameters have not yet been ascertained for captive hawksbill turtles. Adult female sea turtles have a seasonal vitellogenic cycle, and vitellogenesis (i.e., follicular development) is
© 2014 Wiley Periodicals, Inc.
completed prior to the nesting season [Owens, 1997; Hamann et al., 2003]. Subsequently, after mating, adult females lay several clutches of eggs on sandy beaches [Miller 1997]. During the sub-adult stage, land turtles generally undergo vitellogensis for a few years prior to reaching sexual maturity, which is indicated by ovulation and egg formation [Kuchling 1999; Saka et al., 2014]. A similar tendency is reported in captive green turtles [Bjorndal et al., 2013]. Hence, follicular development is a direct indicator of the onset of sexual maturation (i.e., puberty) in sea turtles, as has been demonstrated by ultrasonographic observation of ovary condition [Rostal et al., 1990; Kawazu et al., 2014]. Data regarding hawksbill body size during sexual maturation can be Conflict of interest: None Correspondence to: Isao Kawazu, Okinawa Churashima Foundation, 888 Ishikawa, Motobu, Okinawa 905-0206, Japan. E-mail: [email protected]
Received 19 June 2014; Revised 30 September 2014; Accepted 12 November 2014
DOI: 10.1002/zoo.21190 Published online 23 December 2014 in Wiley Online Library (wileyonlinelibrary.com).
Onset of Vitellogenesis of Hawksbills 179
obtained from wild nesting females; however, this method can produce unclear results, owing to difficulties determining whether the females are parous and obtaining age data for wild turtles. In contrast, a study performed in captivity would allow monitoring of growth and follicular development from hatchlings to adult turtles, thereby providing unambiguous data for age and body size at the onset of follicular development. Here, we selected 23 female hawksbill turtles that hatched in captivity, and recorded their age and body size at the onset of follicular development, which was determined via ultrasonographic observation of ovary condition. METHODS Twenty-three female hawksbill turtles were kept in captivity at the Ocean Expo Park, Motobu-cho, Okinawa Prefecture, Japan. Eight of these hatched from eggs laid at Zamami Island (26°140 N, 127°180 E) in 1993, and 15 hatched in captivity in 1994 [Teruya et al., 1997]. During the early juvenile stage (straight carapace length (SCL) 30 cm were kept in cylindrical tanks that were 750 mm in depth and either 1050 mm or 1500 mm in diameter. The water temperature of the tanks ranged from 20–30°C across a 12-month period. This range is similar to that experienced by hawksbills under natural conditions (sea surface temperature) around Okinawa Island (26°300 N, 127°000 E). The turtles were fed at approximately 24-h intervals, with a diet that included fish, shrimp, and squid in quantities equivalent to 0.5–2% of their body mass (BM).
We observed the left and right ovaries of all turtles yearly by ultrasonography using a 5-MHz probe (Mini-dock P04341–04; Sonosite Inc., USA) during January–May from 2006 to 2014. The turtles were placed in dorsal recumbency, and the probes were positioned in the inguinal region of the right and left rear flippers at a water depth of 200 mm, as described previously [Kawazu et al., 2014]. The onset of sexual maturity was judged based on the follicular development observed by ultrasonography, and the age at the onset of sexual maturation was recorded. Concomitantly, SCL and BM were recorded for all turtles each year. Spearman’s rank correlation coefficient was calculated for age versus SCL and BM at the onset of sexual maturation for all turtles. RESULTS Ultrasonographic observations between 2006 and 2014 indicated that all of the female hawksbill turtles developed follicles between 2007 and 2013. The age, SCL, and BM at the onset of follicular development were 17.7 1.7 years (mean SD; range: 13–20 years), 77.7 3.3 cm (73.3–83.5 cm), and 61.1 8 kg (48.2–76.1 kg), respectively. For all turtles, there were significant positive correlations between age and SCL at the onset of follicular development (Fig. 1; Spearman’s rank correlation coefficient ¼ 0.45, n ¼ 23, P < 0.05) and between age and BM (Fig. 1; Spearman’s rank correlation coefficient ¼ 0.63, n ¼ 23, P < 0.05). When the year of the onset of follicular development was designated year 0, the increase in SCL in years -7–0 and 0–3 years averaged 2.2 cm and 1.0 cm, respectively (Fig. 2).
Fig. 1. Relationship of age to straight carapace length and body mass at the onset of follicular development in 23 female hawksbill turtles (Eretmochelys imbricata). The regression lines of straight carapace length and body mass are shown, according to the equations Y ¼ 8.72X þ 62.33 (Spearman’s rank correlation coefficient ¼ 0.45, n ¼ 23, P < 0.05) and Y ¼ 2.95X þ 8.79 (Spearman’s rank correlation coefficient ¼ 0.63, n ¼ 23, P < 0.05), respectively.
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180 Kawazu et al.
Fig. 2. Change in straight carapace length and body mass before and after follicular development for 23 female hawksbill turtles (Eretmochelys imbricata). Year 0 indicates the year of sexual maturation. The bars indicate standard deviation. The number of data points included for each year, from left to right, are 8, 9, 12, 19, 20, 17, 21, 23, 13, 13, and 6.
Correspondingly, the increase in BM in years -7–0 and 0–3 years averaged 5.0 kg and 2.2 kg, respectively (Fig. 2). DISCUSSION This study is the first to report the age and body size of captive female hawksbill turtles at the onset of follicular development. Knowledge of these reproductive parameters will be useful for improving captive programs for hawksbill turtles, and may aid conservation and resource management efforts. The age data obtained in the current study revealed that the vitellogenesis of female hawksbill turtles occurs between 13 and 20 years of age. Some captive green turtles show slowed growth at least 2 years prior to sexual maturity [Bjorndal et al., 2013]. In the present study, a similar observation was made in captive hawksbill turtles, which showed a reduction of growth just after the onset of vitellogenesis (Fig. 2). Our results, together with those of captive green turtles [Bjorndal et al., 2013], indicate that the maturation age of captive hawksbills is between 15 and 22 years. The age of wild hawksbills at sexual maturation was evaluated to be 20–40 years [Meylan and Donnelly, 1999], which is higher than that of our captive turtles. This difference in age of maturation between captive and wild animals has also been reported for other sea turtles. For instance, the age at of sexual maturation in captive (nesting turtle) and wild (estimated age based on skeletochronological analysis) green turtles is 8–12 years [Wood and Wood, 1980; Bjorndal et al., 2013] and >30 years [Zug et al., 2002], respectively. Correspondingly, captive and wild Kemp’s Zoo Biology
ridley turtles begin sexual maturation at 5–7 years of age [Wood and Wood, 1988] and 11–19 years of age [Zug et al., 1997], respectively. These differences in age of maturation might be explained by the differences in growth conditions of wild and captive turtles, including quality and distribution of food, as described previously [Hamann et al., 2003]. Although the maturation age of wild hawksbill turtles was evaluated to be 20–40 years [Meylan and Donnelly, 1999], wild hawksbill turtles around Anegada, one of the British Virgin Islands in the Caribbean Sea, were observed to have a maximum growth rate of 20 cm/year (carved carapace length) and these turtles matured within 10 years [Hawkes et al., 2014]. These data are remarkably higher than our growth rate (2.2 cm before the onset of vitellogenesis; Fig. 2) and age at onset of follicular development (minimum age 13 years; Table 1). The high growth rates and young maturation age [Hawkes et al., 2014] were hypothesized to depend on the turtles’ habitat, which had warm temperatures with abundant and diverse forage food. Some wild hawksbill turtles are known to mainly feed on sponge species [Meylan, 1988; Leon and Bjorndal, 2002), whereas our captive turtles were fed fish, shrimp, and squid (quantities:
BRIEF REPORT
Age and Body Size of Captive Hawksbill Turtles at the Onset of Follicular Development Isao Kawazu,* Masakatsu Kino, Konomi Maeda, and Hideshi Teruya Okinawa Churashima Foundation, 888 Ishikawa, Motobu, Okinawa, Japan The aim of this study was to record the age and body size of 23 captive female hawksbill turtles at the onset of follicular development. The age, straight carapace length (SCL), and body mass (BM) of the turtles were recorded between 2006 and 2014 at follicular development (determined via ultrasonography) these parameters were 17.7 1.7 years (range: 13–20 years), 77.7 3.3 cm (73.3–83.5 cm), and 61.1 8.0 kg (48.2–76.1 kg), respectively. When the year of the onset of follicular development was designated year 0, the increase in SCL in years -7–0 and 0–3 averaged 2.2 cm and 1.0 cm, respectively. Correspondingly, the increase in BM in years -7–0 and 0–3 averaged 5.0 kg and 2.2 kg, respectively. This is the first study to report the age and body size of captive female hawksbill turtles at the onset of follicular development, which indicates the beginning of sexual maturation. The reduction in growth after follicular development suggests that at the onset of sexual maturation, female hawksbills may utilize energy for follicular development rather than growth. Zoo Biol. 34:178–182, © 2014 Wiley Periodicals, Inc. 2015.
Keywords: straight carapace length; body mass; vitellogenesis
INTRODUCTION Hawksbill turtles (Eretmochelys imbricata) are distributed in tropical and subtropical coral reefs worldwide, and are listed as critically endangered on the International Union for Conservation of Nature (IUCN) red list for threatened species [Mortimer and Donnelly, 2008]. Hence, the active implementation of captive breeding programs offers a unique management opportunity for the recovery and conservation of this endangered species [Owens and Blanvillain, 2013]. Knowledge of the age and body size of hawksbill turtles at the onset of sexual maturation is important for the effective implementation of captive breeding programs. In addition, examination of these reproductive parameters could extend our knowledge of the reproductive biology of sea turtles, thus improving the effectiveness of conservation efforts and resource management. Age and body size at the onset of sexual maturation have been determined for captive green turtles (Chelonia mydas) and Kemp’s ridley turtles (Lepidochelys kempi) [Wood and Wood, 1980, 1988; Bjorndal et al., 2013]. However, these parameters have not yet been ascertained for captive hawksbill turtles. Adult female sea turtles have a seasonal vitellogenic cycle, and vitellogenesis (i.e., follicular development) is
© 2014 Wiley Periodicals, Inc.
completed prior to the nesting season [Owens, 1997; Hamann et al., 2003]. Subsequently, after mating, adult females lay several clutches of eggs on sandy beaches [Miller 1997]. During the sub-adult stage, land turtles generally undergo vitellogensis for a few years prior to reaching sexual maturity, which is indicated by ovulation and egg formation [Kuchling 1999; Saka et al., 2014]. A similar tendency is reported in captive green turtles [Bjorndal et al., 2013]. Hence, follicular development is a direct indicator of the onset of sexual maturation (i.e., puberty) in sea turtles, as has been demonstrated by ultrasonographic observation of ovary condition [Rostal et al., 1990; Kawazu et al., 2014]. Data regarding hawksbill body size during sexual maturation can be Conflict of interest: None Correspondence to: Isao Kawazu, Okinawa Churashima Foundation, 888 Ishikawa, Motobu, Okinawa 905-0206, Japan. E-mail: [email protected]
Received 19 June 2014; Revised 30 September 2014; Accepted 12 November 2014
DOI: 10.1002/zoo.21190 Published online 23 December 2014 in Wiley Online Library (wileyonlinelibrary.com).
Onset of Vitellogenesis of Hawksbills 179
obtained from wild nesting females; however, this method can produce unclear results, owing to difficulties determining whether the females are parous and obtaining age data for wild turtles. In contrast, a study performed in captivity would allow monitoring of growth and follicular development from hatchlings to adult turtles, thereby providing unambiguous data for age and body size at the onset of follicular development. Here, we selected 23 female hawksbill turtles that hatched in captivity, and recorded their age and body size at the onset of follicular development, which was determined via ultrasonographic observation of ovary condition. METHODS Twenty-three female hawksbill turtles were kept in captivity at the Ocean Expo Park, Motobu-cho, Okinawa Prefecture, Japan. Eight of these hatched from eggs laid at Zamami Island (26°140 N, 127°180 E) in 1993, and 15 hatched in captivity in 1994 [Teruya et al., 1997]. During the early juvenile stage (straight carapace length (SCL) 30 cm were kept in cylindrical tanks that were 750 mm in depth and either 1050 mm or 1500 mm in diameter. The water temperature of the tanks ranged from 20–30°C across a 12-month period. This range is similar to that experienced by hawksbills under natural conditions (sea surface temperature) around Okinawa Island (26°300 N, 127°000 E). The turtles were fed at approximately 24-h intervals, with a diet that included fish, shrimp, and squid in quantities equivalent to 0.5–2% of their body mass (BM).
We observed the left and right ovaries of all turtles yearly by ultrasonography using a 5-MHz probe (Mini-dock P04341–04; Sonosite Inc., USA) during January–May from 2006 to 2014. The turtles were placed in dorsal recumbency, and the probes were positioned in the inguinal region of the right and left rear flippers at a water depth of 200 mm, as described previously [Kawazu et al., 2014]. The onset of sexual maturity was judged based on the follicular development observed by ultrasonography, and the age at the onset of sexual maturation was recorded. Concomitantly, SCL and BM were recorded for all turtles each year. Spearman’s rank correlation coefficient was calculated for age versus SCL and BM at the onset of sexual maturation for all turtles. RESULTS Ultrasonographic observations between 2006 and 2014 indicated that all of the female hawksbill turtles developed follicles between 2007 and 2013. The age, SCL, and BM at the onset of follicular development were 17.7 1.7 years (mean SD; range: 13–20 years), 77.7 3.3 cm (73.3–83.5 cm), and 61.1 8 kg (48.2–76.1 kg), respectively. For all turtles, there were significant positive correlations between age and SCL at the onset of follicular development (Fig. 1; Spearman’s rank correlation coefficient ¼ 0.45, n ¼ 23, P < 0.05) and between age and BM (Fig. 1; Spearman’s rank correlation coefficient ¼ 0.63, n ¼ 23, P < 0.05). When the year of the onset of follicular development was designated year 0, the increase in SCL in years -7–0 and 0–3 years averaged 2.2 cm and 1.0 cm, respectively (Fig. 2).
Fig. 1. Relationship of age to straight carapace length and body mass at the onset of follicular development in 23 female hawksbill turtles (Eretmochelys imbricata). The regression lines of straight carapace length and body mass are shown, according to the equations Y ¼ 8.72X þ 62.33 (Spearman’s rank correlation coefficient ¼ 0.45, n ¼ 23, P < 0.05) and Y ¼ 2.95X þ 8.79 (Spearman’s rank correlation coefficient ¼ 0.63, n ¼ 23, P < 0.05), respectively.
Zoo Biology
180 Kawazu et al.
Fig. 2. Change in straight carapace length and body mass before and after follicular development for 23 female hawksbill turtles (Eretmochelys imbricata). Year 0 indicates the year of sexual maturation. The bars indicate standard deviation. The number of data points included for each year, from left to right, are 8, 9, 12, 19, 20, 17, 21, 23, 13, 13, and 6.
Correspondingly, the increase in BM in years -7–0 and 0–3 years averaged 5.0 kg and 2.2 kg, respectively (Fig. 2). DISCUSSION This study is the first to report the age and body size of captive female hawksbill turtles at the onset of follicular development. Knowledge of these reproductive parameters will be useful for improving captive programs for hawksbill turtles, and may aid conservation and resource management efforts. The age data obtained in the current study revealed that the vitellogenesis of female hawksbill turtles occurs between 13 and 20 years of age. Some captive green turtles show slowed growth at least 2 years prior to sexual maturity [Bjorndal et al., 2013]. In the present study, a similar observation was made in captive hawksbill turtles, which showed a reduction of growth just after the onset of vitellogenesis (Fig. 2). Our results, together with those of captive green turtles [Bjorndal et al., 2013], indicate that the maturation age of captive hawksbills is between 15 and 22 years. The age of wild hawksbills at sexual maturation was evaluated to be 20–40 years [Meylan and Donnelly, 1999], which is higher than that of our captive turtles. This difference in age of maturation between captive and wild animals has also been reported for other sea turtles. For instance, the age at of sexual maturation in captive (nesting turtle) and wild (estimated age based on skeletochronological analysis) green turtles is 8–12 years [Wood and Wood, 1980; Bjorndal et al., 2013] and >30 years [Zug et al., 2002], respectively. Correspondingly, captive and wild Kemp’s Zoo Biology
ridley turtles begin sexual maturation at 5–7 years of age [Wood and Wood, 1988] and 11–19 years of age [Zug et al., 1997], respectively. These differences in age of maturation might be explained by the differences in growth conditions of wild and captive turtles, including quality and distribution of food, as described previously [Hamann et al., 2003]. Although the maturation age of wild hawksbill turtles was evaluated to be 20–40 years [Meylan and Donnelly, 1999], wild hawksbill turtles around Anegada, one of the British Virgin Islands in the Caribbean Sea, were observed to have a maximum growth rate of 20 cm/year (carved carapace length) and these turtles matured within 10 years [Hawkes et al., 2014]. These data are remarkably higher than our growth rate (2.2 cm before the onset of vitellogenesis; Fig. 2) and age at onset of follicular development (minimum age 13 years; Table 1). The high growth rates and young maturation age [Hawkes et al., 2014] were hypothesized to depend on the turtles’ habitat, which had warm temperatures with abundant and diverse forage food. Some wild hawksbill turtles are known to mainly feed on sponge species [Meylan, 1988; Leon and Bjorndal, 2002), whereas our captive turtles were fed fish, shrimp, and squid (quantities:
