Some Evidence of Seasonality in Reproductive Parameters of Male Indo-Pacific Bottlenose Dolphins (Tursiops aduncus)
IAAAM 2006
Queeny W.H. Yuen1; Fiona M. Brook1; Michael T.C. Ying1; Reimi E. Kinoshita2
1Department of Optometry and Radiology, The Hong Kong Polytechnic University, Kowloon, Hong Kong SAR, China; 2Department of Zoological Operations and Education, Ocean Park Corporation, Aberdeen, Hong Kong SAR, China

Abstract

Seasonality in male cetacean reproduction remains a subject about which there are few systemic investigations and a lack of consensus. Seasonality refers to the timing of reproductive events which occur in a cyclic manner and are geared towards optimizing seasonal changes in environmental conditions to benefit the survival of a species.1 Seasonal patterns in reproductive activities differ among species and populations, because of differences in lifestyle and ecology.1

Reproductive seasonality in females may be explained by the interaction between factors such as availability of environmental resources, energetic costs and survivability of offspring. However, male seasonality is more difficult to explain, as there is no evidence to support sperm production per se is energetically expensive.1 Male seasonality is usually associated with changes in testicular size and fluctuations in testosterone production. In the past, testes size in bottlenose dolphins was studied in carcasses, thus seasonality was postulated on a cross-sectional basis.2,3 Few longitudinal studies have been carried out. Most investigated seasonality based only on evaluation of testosterone levels.4,5,6 Schroeder and Keller7 monitored sperm density as well as testosterone levels, and Brook8 further added testes size measured by ultrasonography. The number of subjects in these studies are small.

Seasonality is integral to the understanding of male dolphin reproductive physiology, which is essential to develop advanced reproductive technologies (ART) for this species.9 Knowledge gained may be particularly useful in deciding the best timing for semen collection, and possibly when cryopreservation of a sample is best.

The results presented here are part of a longitudinal study that has been on going for more than 3 years. The aim of the overall study is to find out when the onset of spermatogenesis occurs and monitor changes in testes size and testosterone levels during sexual maturation. There are 5 subjects in this study (Table 1). The dimensions of the testes are measured weekly using B-mode ultrasonography. Semen samples are collected under trained behaviour, immediately after ultrasonography. Semen samples are collected successively until no more semen is present in spite of effort, or micturition occurs. Each ejaculate is assessed for quality parameters, including density, count, motility, viability, pH and volume. Blood samples for serum testosterone level evaluation are taken monthly, on the same day as ultrasound examination and semen collection. The mean measurement of each month for each parameter is used to determine seasonal changes.

Table 1. Subjects.

Subject ID

Origin

Present age
(Feb 2006)

Maturity status

Age at sexual
maturity**

M1

Wild born

>22yr (est.)

Sexually mature

7-8yr (est.)

M2

Captive born

*11yr

Sexually mature

7yr 4mo

M3

Captive born

10yr 6mo

Sexually mature

7yr 3mo

M4

Captive born

7yr 5mo

Sexually mature

6yr 7mo

M5

Captive born

6yr 8mo

Sexually mature

6yr 8mo

* Died May 2005
**Sexual maturity is defined in this study as the onset of spermatogenesis

The testes volume of three older males, (Figures 1-3) decreased during the winter months, ie December-February. Peak testes volume is found during the summer months of May-July. Peak testes volumes in M2 and M3 continue to increase year by year, indicating that although sexually mature, their testes have not yet reached full size and presumably full reproductive capacity. M4 began to produce spermatozoa in April 2005, and his testes already indicate a pattern of seasonal change, with peak volumes reached in July 2005 (Figure 4). There is no cyclic pattern in the testes size of the youngest male (M5). The onset of spermatogenesis for this subject occurred very recently (February 2006).

An annual pattern in sperm density is not as readily seen. M1 has exhibited lower sperm densities in January and February (Figure 4), however, the highest sperm densities vary throughout the year in this subject and no definitive seasonality of sperm production is seen. Further monitoring is required to determine if there is any pattern in sperm density of the remaining subjects, as the onset of spermatogenesis in these males is comparatively recent.

Click on the image to see a larger view

Figure 1.
 

Figure 1. M1 mean monthly testes volume.

Figure 2.
 

Figure 2. M2 mean monthly testes volume.

Figure 3.
 

Figure 3. M3 mean monthly testes volume.

Figure 4.
 

Figure 4. M1 mean monthly sperm density.

A seasonal pattern in testosterone levels is most evident in M1 (Figure 5). Lowest levels occurred during December and January while peak levels appear to spread over a longer period, from March to September. In M4, a significant increase in testosterone level also began in March (2005), the onset of spermatogenesis occurred the following month and a high level was subsequently reached in July 2005 (Figure 6). Lower levels were found also in December and January for M4, M2 (Figure 7) and M3 (Figure 8). Testosterone levels in M5 have remained very low throughout the study period, with a recorded maximum of 1.47ng/ml in January 2006, 2 weeks before sperm was first found in his ejaculate.

Click on the image to see a larger view

Figure 5.
 

Figure 5. M1 mean monthly testosterone levels.

Figure 6.
 

Figure 6. M4 mean monthly testosterone levels.

Figure 7.
 

Figure 7. M2 mean monthly testosterone levels.

Figure 8.
 

Figure 8. M3 mean monthly testosterone levels.

The results of this study so far provide some evidence for seasonal changes in testes size, sperm density and testosterone levels in male T. aduncus, with the most obvious pattern seen in the oldest subject. Further investigation is required to confirm the changes in reproductive parameters and to determine relationships between these as the younger subjects continue to develop. The present results also strongly suggest that the process of achieving full sexual maturity takes several years.

Overall, knowledge gained in this study will contribute towards better understanding of the reproductive physiology of male dolphins and may be useful in investigation of dolphins in the wild and population management. Knowledge of sexual maturation is key for controlled breeding management in captivity. Segregation of known sexually mature males from young inexperienced females will prevent undesirable pregnancies which may result in poor calf survivability. Prompt inclusion of young males for natural breeding and / or collection and cryopreservation of semen for artificial insemination will increase genetic security for untimely losses and widen gene pools within and between captive groups.

Acknowledgments

The authors are grateful to Gary Wong, Harriet Chiu and the trainers of Ocean Park's Marine Mammal Department for their invaluable contributions in dolphin training, husbandry and semen collection, and the Clinical Laboratory staff for their support, assistance and the author's training in semen evaluation.

This project is funded by the Research Grants Council of Hong Kong (Grant ref: PolyU5287/01).

References

1.  Boyd IL, C Lockyer, HD Marsh. 1999. Reproduction in marine mammals. In Biology of Marine Mammals. J.E. Reynolds, III, and S.A. Rommel, editors. The Smithsonian Institution. 218-286.

2.  Harrison RJ, RC Boice, RL Brownell, Jr. 1969. Reproduction in wild and captive dolphins. Nature. 222:1143-1147.

3.  Cockcroft VG, GJB Ross. 1990. Age, growth, and reproduction of bottlenose dolphins Tursiops truncatus from the East coast of southern Africa. Fish. Bull. 88:289-302.

4.  Harrison RJ, SH Ridgway. 1971. Gonadal activity in some bottlenose dolphins (Tursiops truncatus). J. Zool. London. 165:355-366.

5.  Kirby VL. 1990. Endocrinology of marine mammals. In CRC Handbook of Marine Mammal Medicine: Health, Disease, and Rehabilitation. L.A. Dierauf, editor. CRC Press Boca Raton, Florida. 303-351

6.  Suzuki M, S Uchida, K Ueda, T Tobayama, E Katsumata, M Yoshioka, K Aida. 2003. Diurnal and annual changes in serum cortisol concentrations in Indo-Pacific bottlenose dolphins Tursiops aduncus and killer whales Orcinus orca. Gen. Comp. Endocrinol. 132:427-433

7.  Schroeder JP, KV Keller. 1989. Seasonality of serum testosterone levels and sperm density in Trusiops truncatus. J. Exp. Zool. 249:316-321.

8.  Brook FM. 1997. The Use of Diagnostic Ultrasound in Assessment of the Reproductive Status of the Bottlenose Dolphin, Tursiops aduncas, in Captivity & Applications in management of a controlled Breeding Programme. In Dept. of Optometry and Radiology. The Hong Kong Polytechnic University, Hong Kong. 339.

9.  Robeck TR, BE Curry, JF McBain, DC Kraemer. 1994. Reproductive biology of the bottlenose dolphin (Tursiops truncatus) and the potential application of advanced reproductive technologies. J. Zoo and Wild. Med. 25:321-336.

Speaker Information
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Queeny W.H. Yuen


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