Ultrasonographic Assessment of the Reproductive Cycle of the Indo-Pacific Humpback Dolphin, Sousa chinensis
Aspects of the general biology of many species of Delphinidae have been studied over the past century, however, despite concerns about conservation and sustainability, detailed studies of reproductive physiology have been lacking. Several species of dolphins have been maintained in captivity for a similar length of time, affording more easily accessible subjects for research, but only recently have scientists begun to investigate reproductive performance and parameters in any detail.
Now, more is known about the reproductive cycle in the female of a few species. Killer whales (Orca orcinus) appear to ovulate regularly throughout the year.19,25 Small cetacean species, such as the dusky dolphin (Lagenorhyncus obscurus)24 and the harbour porpoise, (Phocoena phocoena)14,18 appear to have a clearly limited, seasonal pattern of reproduction. However, medium sized dolphin species, such as the bottlenose dolphin (Tursiops spp.) and the Indo-Pacific hump-backed dolphin (Sousa chinensis) do not seem to have such an easily definable pattern, with reproduction often being described as 'diffusely seasonal'. Data from both wild and captive populations show that births may occur at any time of year.3,7,8,23,26
The maintenance of bottlenose dolphins (Tursiops truncatus and aduncus) in captivity has enabled closer study of the reproductive anatomy4,5,6,10,16,17 and physiology 12,13,20,21,22,27 of this species. The anatomy of the uterus and ovaries is reported and is similar in all cetaceans studied. Serum progesterone data were also similar and indicated an irregular pattern of ovarian cycling in Tursiops, which was difficult to predict.20,27 Data showed that estrus varied markedly between and within individuals. Generally, P levels of < 1.0 ng/ml were determined to indicate anestrus. Elevated levels (3.0-34.0 ng/ml) indicated ovulation and the luteal phase of the cycle, but did not provide useful information about follicular development and the time of ovulation. P levels of 1-3 ng/ml were classified as indeterminate.11,13,20,21,22,27 Studies of serum total estrogen (Et) levels in T. truncatus showed no variation between anestrus and estrus.12,13,20,21,27 Yoshioka et al. (1986) reported serum estradiol (E2) levels of < 70 pg/ml during anestrus and 125-200 pg/ml during estrus. Although contributing useful information about reproductive physiology, investigations of serum steroid hormone levels did not allow direct assessment of ovarian activity in live animals.
More recently, ultrasonography has allowed observation of real time morphologic changes in the ovaries of T. aduncus and correlation of ovarian cycle phase with serum P and E2.1,2 P levels were < 0.2-0.9 ng/ml during anestrus and < 0.2-18.5 ng/ml during estrus. E2 levels were 8.4-106.3 pg/ml during anestrus and 11.2-379.2 pg/ml during estrus. These levels are similar to those reported for T. truncatus. This was the first time real time ovarian events were correlated with serum hormone data in dolphins.
Some aspects of the reproductive biology of the Indo-Pacific humpback dolphin have been studied in the wild in South Africa3,7,9 and Hong Kong.7,15 However, it is difficult to collect sufficient data about reproductive physiology from wild animals and still little detailed information is known about reproduction in S. chinensis. These studies reported similar results, in that births were observed throughout the year, although more newborn calves were seen in spring/summer.3,7 Gestation length has been estimated at about 11 months and females are believed to attain sexual maturity at 9-11 years of age.3,7
Underwater World Singapore (UWS) opened their Dolphin Lagoon in 1999 and is one of two facilities known to maintain the Indo-Pacific humpback dolphin in sufficient numbers for breeding. The group consists of two adult males and three adult females. Underwater World Singapore is committed to controlled breeding and sustainable management of their population, as well as the collection of sound scientific data from the species.
This project to study the ovarian cycle using ultrasonography began in 2002; the aim was to assess and monitor reproductive status and patterns in the females. The specific objectives of the study were to establish the normal sonographic appearance of the ovaries in Indo-Pacific humpback dolphin, determine whether sonography could identify and monitor folliculogenesis, correlate real time ovarian changes with serum hormone levels, and determine any seasonal influence on reproductive status.
This project was aimed to collect data about the ovarian cycle of the Indo-Pacific humpback dolphin (Sousa chinensis) using sonographic examination of the ovaries and serum hormone level assessment. The ovaries of two non-pregnant females were assessed at least once weekly and one pregnant female was assessed when possible. A total of 15 normal ovarian cycles, one episode of follicular atresia and one episode of a luteinized cystic follicle were detected using ultrasonography and serum progesterone levels. Two more cycles were detected on serum progesterone levels but not on ultrasonography. The mean ovarian cycle, mean follicular phase, mean follicle diameter measured just before ovulation, mean luteal phase and average diameter of the corpus luteum were determined. Data showed an irregular pattern of ovarian cycling, varying between and within subjects. Serum progesterone and estradiol levels were measured 1-3 times per month in two females and intermittently in one other female. Recorded progesterone and estradiol levels during the follicular phase, luteal phase, and anestrus are reported. Progesterone levels during pregnancy are also included.
This project would not have been possible without the efforts of the team of marine mammal trainers and veterinary technicians at UWS, as well as the support of the managers and owners. Progesterone assays were performed by the O & G Research Laboratory, The National University of Singapore. This project is funded by the Research Grants Council of Hong Kong [Grant ref: PolyU5287/01].
1. Brook FM. 1997. The use of diagnostic ultrasound in assessment of the reproductive status of the bottlenose dolphin, Tursiops truncatus aduncas, in captivity & applications in management of a controlled breeding programme. Ph.D. Dissertation. The Hong Kong Polytechnic University, Hong Kong.
2. Brook F. 2000. Sonographic testicular and ovarian assessment in the bottlenose dolphin, Tursiops truncatus aduncus. In: Duffield D. A. and T. R. Robeck (eds.). Report from the Bottlenose Dolphin Breeding Workshop. American Zoological Association Marine Mammal Taxon Advisory Group, Silver Spring, Maryland. Pp. 207-222.
3. Cockcroft VG. 1989. Biology of Indopacific humpback dolphins (Sousa plumbea) off Natal, South Africa. In: Abstracts of the Eighth Biennial Conference on the Biology of Marine Mammals. Pp. 13.
4. Harrison RJ. 1969. Reproduction and reproductive organs. In: Andersen H. T. (ed.). The Biology of Marine Mammals. Academic Press, New York. Pp. 253-348.
5. Harrison RJ, DA McBrearty. 1977. Ovarian appearances in captive delphinids (Tursiops and Lagenorhynchus). Aquatic Mammals 5, Pp. 57-66.
6. Harrison RJ, RL Brownell, RC Boice. 1972. Reproduction and gonadal appearances in some odontocetes. In: Harrison R. J. (ed.). Functional Anatomy of Marine Mammals. Academic Press, New York. Pp. 361-429.
7. Jefferson T. 2000. Population biology of the Indo-Pacific humpback dolphin in Hong Kong waters. Wildlife Monographs. 144, Pp. 65.
8. Joseph B, D Duffield, T Robeck. 2000. Summary data on reproduction of bottlenose dolphins in controlled environments. In: Duffield D. A. and T. R. Robeck (eds.). Report from the Bottlenose Dolphin Breeding Workshop. American Zoological Association Marine Mammal Taxon Advisory Group, Silver Spring, Maryland. Pp. 42-55.
9. Karczmarski L. 1996. Ecological studies of humpback dolphins Sousa chinensis in the Algoa Bay region, eastern Cape, South Africa. Ph.D. dissertation, University of Port Elizabeth, South Africa.
10. Kasuya T, H Marsh. 1984. Life history and reproductive biology of the short-finned pilot whale, Globicephala macrorhynchus, off the Pacific coast of Japan. In: Perrin W. F., R. L. Brownell and D. P. DeMaster (eds.). Reproduction in Whales, Dolphins and Porpoises. Report of the International Whaling Commission, Special Issue 6, Cambridge, Cambridge. Pp. 259-310.
11. Kirby VL. 1984. Hormonal evidence of spontaneous ovulation in captive dolphins (Tursiops truncatus and Delphinus delphis). In: Perrin W. F., R. L. Brownell and D. P. DeMaster (eds.). Reproduction in Whales, Dolphins and Porpoises. Report of the International Whaling Commission, Special Issue 6, Cambridge, Cambridge. Pp. 479-484.
12. Kirby VL. 1990. Endocrinology of marine mammals. In: Dierauf, L. A.(ed.). CRC Handbook of Marine Mammal Medicine: Health, Disease and Rehabilitation. CRC Press, Boca Raton, Florida. . Pp. 303-351.
13. Kirby VL, SH Ridgway. 1984. Hormonal evidence of spontaneous ovulation in captive dolphins (Tursiops truncatus and Delphinus delphis). In: Perrin, W. F., R. L. Brownell and D. P. DeMaster (eds.). Reproduction in Whales, Dolphins and Porpoises. Report of the International Whaling Commission, Special Issue 6, Cambridge, Cambridge. Pp. 459-464.
14. Neimanis AS, AJ Read, RA Foster, DE Gaskin. 2000. Seasonal regression in testicular size and histology in harbour porpoises (Phocoena phocoena) from the Bay of Fundy and the Gulf of Maine. Journal Zoology London 50, Pp. 221-229.
15. Parsons ECM. 1997. Hong Kong's cetaceans: The biology, ecology and behaviour of Sousa chinensis and Neophocaena phocaenoides. Ph.D Dissertation, University of Hong Kong, Hong Kong.
16. Perrin WF, SB Reilly. 1984. Reproductive parameters of dolphins and small whales of the family Delphinidae. In: Perrin, W. F., R. L. Brownell and D. P. DeMaster (eds.). Reproduction in Whales, Dolphins and Porpoises. Report of the International Whaling Commission, Special Issue 6, Cambridge, UK. Pp. 97-125.
17. Perrin WF, JM Coe, JR Zweifel. 1976. Growth and reproduction of the spotted porpoise, Stenella attenuata, in the offshore eastern tropical Pacific. Fisheries Bulletin U.S. 74, Pp. 229-269.
18. Read AJ, AA Hohn. 1995. Life in the fast lane: the life history of harbor porpoises from the Gulf of Maine. Marine Mammal Science 11, Pp. 423-440.
19. Robeck TR, AL Schneyer, JF McBain, LM Dalton, MT Walsh, NM Czekala, DC Kraemer. 1993. Analysis of urinary immunoreactive steroid metabolites and gonadotropins for characterization of the estrous cycle, breeding period and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biology 12, Pp. 173-187.
20. Sawyer-Steffan JE, VL Kirby. 1980. A study of serum steroid hormone levels in captive female bottlenose dolphins, their correlation with reproductive status, and their application to ovulation induction in captivity. Rep. No. PB80-177199, US Marine Mammal Commission, NTIS, Springfield, Virginia.
21. Sawyer-Steffan JE, VL Kirby, WC Gilmartin. 1983. Progesterone and estrogens in the pregnant and non-pregnant dolphin, Tursiops truncatus, and the effects of induced ovulation. Biology Reproduction 28, Pp. 897-901.
22. Schroeder JP. 1990. Breeding bottlenose dolphins in captivity. In: Leatherwood S. and R. R. Reeves (eds.). The Bottlenose Dolphin. Academic Press Inc., San Diego, California. Pp. 435-446.
23. Urian KW, DA Duffield, AJ Read, RS Wells, ED Shell. 1996. Seasonality of reproduction in bottlenose dolphins, Tursiops truncatus. Journal Mammalogy 77, Pp. 394-403.
24. Van Waerebeek K, AJ Read. 1994. Reproduction of dusky dolphins, Lagenorhyncus obscurus, from coastal Peru. Journal Mammalogy 75, Pp. 1054-1062.
25. Walker LA, L Cornell, KD Dahl, NM Czekala, CM Dargen, BE Joseph, AJW Hsueh, BL Lasley. 1988. Urinary concentrations of ovarian steroid hormone metabolites and bioactive follicle-stimulating hormone in killer whales (Orcinus orcus) during ovarian cycles and pregnancy. Biology Reproduction 39, Pp.1013-1020.
26. Wells R. 2000. Reproduction in wild bottlenose dolphins: Overview of patterns observed during a long-term study. In: Duffield, D.A. and T. R. Robeck (eds.). Report from the Bottlenose Dolphin Breeding Workshop. American Zoological Association Marine Mammal Taxon Advisory Group, Silver Spring, Maryland. Pp. 57-74.
27. Yoshioka M, E Mohri, T Tobayama, K Aida, I Hanyu. 1986). Annual changes in serum reproductive hormone levels in captive female bottlenose dolphins. Bulletin Japanese Society Fisheries 11, Pp. 1939-1946.