The relationship of maternal characteristics and circulating progesterone concentrations with reproductive outcome in the bottlenose dolphin (Tursiops truncatus) after artificial insemination, with and without ovulation induction, and natural breeding

Abstract

Bottlenose dolphins (Tursiops truncatus) undergoing natural breeding and artificial insemination (AI) were examined to characterize serum progesterone concentrations and determine relationships among age, parity, and reproductive outcome. Progesterone profiles of five cycle types (n = 119 total cycles from 54 animals) were characterized as follows: (i) conception and production of a live term calf (conceptive-term, n = 73); (ii) conception and abortion after Day 60 (conceptive-abortion, n = 12); (iii) unknown conception status with prolonged, elevated progesterone and absence of a fetus (conceptive-unknown, n = 14); (iv) conception failure with normal luteal phase progesterone concentrations (non-conceptive, n = 14, AI cycles only); and (v) conception failure with progesterone insufficiency occuring after spontaneous ovulation or owing to premature ovulation induction using GnRH (non-conceptive-PI, n = 6, AI cycles only). By Day 21 post-insemination (PI), progesterone concentrations were similar (P > 0.05) among conceptive-term, conceptive-abortion and conceptive-unknown, and higher (P < 0.05) for conceptive-term than non-conceptive and non-conceptive-PI cycles. Progesterone concentrations of known conceptive cycles peaked by Week 7 PI (P < 0.05) and remained elevated for the remainder of pregnancy (Weeks 8 up to 54, ≥5 days pre-partum). During midpregnancy (Days 121–240), conceptive-term cycles had higher (P > 0.05) progesterone concentrations than conceptive-abortion and unknown conception status cycles. Parity was not associated with reproductive outcome based on cycle type (P > 0.05). Age of females in conceptive-unknown (26.5 ± 10.1 yrs) and conceptive-abortion (22.1 ± 9.4 yrs) groups was higher (P < 0.05) than in conceptive-term (15.7 ± 7.2 yrs). The conceptive-unknown cycle type possibly represents undetected early embryonic loss occurring before Day 60 PI. Length of gestation using known conception dates was 376.1 ± 11.0 days and the range of this parameter (355–395 days) has implications for peri-parturient management procedures for the species.

Introduction

Initial studies on the reproductive endocrinology of the female bottlenose dolphin (Tursiops truncatus) examined concentrations of steroids, including progesterone, in a small number of ovariectomized, non-pregnant and pregnant females [1]. Circulating progesterone concentrations diagnostic of pregnancy in the bottlenose dolphin were later characterized as values exceeding 3 ng/mL that were maintained at this concentration for more than 6 to 8 wk [2]. Monthly progesterone profiles have since been described in the parturient bottlenose dolphin after serial sampling of captive animals, but several discrepancies exist. For example, a biphasic pattern of serum progesterone during pregnancy was reported by Cornell, et al. [3], but not by Kirby [4]. Further, although a similar biphasic progesterone profile was reported by Schroeder and Keller [5], the timing of the progesterone decline before the second increase differed from that described by Cornell, et al. [3].

Progesterone profiles published to date comprise only the last ∼11 mo of gestation, as known conception dates based on ovulation timing were not available [3], [4], [5]. Consequently, there remains a dearth of information on progesterone profiles in early pregnancy (Weeks 1–8) for this species. In other mammalian species, the first 4 to 8 wk of pregnancy represent the period where embryonic loss is most likely to occur (ruminants [6], [7], horses [8], humans [9]). Because pregnancy confirmation by transabdominal ultrasonographic detection of a dolphin conceptus is most reliably performed after Day 50 of gestation using known conception dates (TR Robeck, unpublished), knowledge of normal progesterone profiles in early pregnancy would be useful to determine if they differ from those of cycles with known conception failure or presumptive embryonic loss.

Available evidence indicates that the primary source of progesterone during pregnancy in the bottlenose dolphin is the CL [10]. In agreement with the well documented role of progesterone as a mammalian pregnancy support hormone [11], [12], sustained periods of abnormally low concentrations of progesterone in bottlenose dolphin pregnancies result in abnormal fetal development [10]. Whereas the normal hormone milieu in the parturient dolphin is yet to be thoroughly characterized, documentation of progesterone concentrations throughout normal pregnancy would assist with the clinical management of pregnancy abnormalities, such as progesterone insufficiency. Monitoring pregnancies with known conception dates through the advent of artificial insemination (AI) will also allow determination of the true gestation length range for this species, which has implications for peri-parturient management practices.

The overall goal of this research was to characterize circulating progesterone profiles during pregnancy, using known conceptions dates, to provide baseline data for gestational health assessments for the species. Specific objectives were to examine females undergoing natural breeding and AI (with and without ovulation induction in the latter) to: (i) characterize weekly progesterone concentrations during conceptive and non-conceptive cycles; (ii) examine the relationship of progesterone concentration during early pregnancy with reproductive success; (iii) examine the relationship of maternal age and parity at conception with progesterone concentrations and reproductive success; (iv) characterize the gestation length for the species using known conception dates; and (v) examine seasonal effects on conception timing in naturally mated females.