This nutshell is based on a recently published paper:
Serum estradiol and progesterone profiles during estrus, pseudopregnancy, and active gestation in Steller sea lions. Renae L. Sattler and Lori Polasek. ZooBiology 2017.
Can endocrinology help explain Steller sea lion population dynamics?
You are probably familiar with human pregnancy tests, the little stick that detects specific hormones in urine—and that if said hormone is at a high enough concentration display a bright PLUS. But, how do we assess pregnancy and hormonal changes in wild animals, say a large marine mammal like a Steller sea lion?
Why Steller sea lions?
Steller sea lions (Eumetopias jubatus) range from northern Hokkaiddo, Japan through the Kuril Islands of Russia, Aleutian Islands of Alaska, and south along the Pacific coast to California.
The population inhabiting U.S. waters is separated at 144˚West longitude (Cape Suckling, AK) into two stocks; the Eastern and Western distinct population segment. Beginning in the 1970’s, Steller sea lion numbers declined >80% and the species was listed as threatened under the Endangered Species Act by 1990. Competition with commercial fisheries for food, increased predation by killer whales, disease, environmental contaminants, and anthropogenic effects (boat strikes, illegal harvest, offshore oil and gas development) were all hypothesized as potential drivers of the population decline. While it is likely several of these factors contributed to the population decline, low fecundity and juvenile recruitment may be responsible for the failure of Steller sea lion to recover to pre-decline numbers (Holmes et al. 2007; Trites and Donnelly 2003). In fact, a harvest of Steller sea lions in the 1970’s (Pitcher and Calkins 1981) and 80’s (Pitcher et al 1998) revealed that the proportion of pregnant females declined by 33% and 42%, respectively from early (October-November) to late gestation (April-May)!
So we wanted to know what is driving these reproductive failures. Was it a normal part of their reproductive strategy? How often do they occur?
Before we can answer those questions, we first have to know the basics of the SSL reproductive cycle. In humans, once an egg is fertilized and implants into the uterine wall, it undergoes 9 months of gestation before birth. SSLs have a 8 month gestation…but they give birth at the same time every year and breed very shortly after. So what is going on for the other 4 months?
In general, adult females arrive at rookeries to pup and breed from mid-May to mid-July. If copulation is successful and an egg is fertilized, the blastocyst enters into a state of suspended development, referred to as embryonic diapause. Embryonic diapause lasts approximately four months and then the blastocyst implants into the uterine wall between late September and October. Following implantation, normal growth and development resume for an eight month gestation. This timeline allows annual synchronicity or times a females return to a rookery to pup and breed each year in May-June. Convenient right? Now, while pregnant females are in diapause, non-pregnant females undergo pseudopregnancy, a physiological state in which the corpus luteum (a temporary endocrine structure created from the ruptured follicle) releases progesterone approximately as long as embryonic diapause. Therefore, from copulation to the time of implantation, pregnant and pseudopregnant females appear hormonally indistinguishable.
Ok… Back to reproductive failures.
Pitcher & Calkins (1981) and Pitcher et al. (1998) identified that the reabsorption of implanted embryos and abortions were occurring during the active gestation period. But a clearer understanding of endocrinology during each stage or the reproductive cycle (estrus, implantation, gestation and pseudopregnancy) was needed to ultimately quantify reproductive failures throughout the Steller sea lion reproductive cycle.
Therefore, we sought to characterize an annual reproductive cycle of pregnant and non-pregnant females using two reproductively important hormones; estradiol and progesterone. We collected monthly serum samples from three resident adult females from 2011 – 2015 housed at the Alaska SeaLife Center in Seward, AK. Specifically, our objectives were to i) quantify annual estradiol and progesterone hormones in pregnant and non-pregnant female animals, ii) enumerate changes in estradiol associated with copulation events and iii) determine if hormones levels can be used to identify pregnancy.
What we learned
Estradiol concentrations displayed a different pattern during the breeding season compared to the rest of the annual reproductive cycle. A spike in serum estradiol was observed in all females in most years occurring sometime in May – August (breeding season), reflective of estrus and sexual receptivity. Our values were similar to ranges reported for wild Steller sea lions (Harmon 2001), California sea lions (Greig et al. 2007), and northern fur seals (Browne et al. 2006). The large range and variability in the height of each female’s estrus spike likely indicates that elevated estradiol associated with estrus is of brief duration, likely less than 7 days (the duration between sample collections) and weekly sample collections were too infrequent to capture the apex of each estrus peak. Outside of the breeding season (October through April), estradiol levels showed little variation, were consistent at low levels, and did not differ between pregnant and non-pregnant females.
Our progesterone values were also similar to those reported for wild Steller sea lions (Harmon 2001), California sea lions (Greig et al. 2007) and northern fur seals (Browne et al. 2006) during comparable seasons. For the resident female Steller sea lions, serum progesterone was elevated in all females in all years from June through November. This finding supports the notion that the corpus luteum is producing progesterone in all females regardless of pregnancy status. Following November, progesterone values notably different between pregnant and non-pregnant females.
Progesterone is utilized to identify pregnancy in a variety of taxa. In fact, excreted progesterone is the hormone used in at-home human pregnancy tests. Comparison of progesterone concentrations in two of our study animals when pregnant and non-pregnant showed progesterone to be a promising diagnostic tool during the 3-5 month window (December – February) of the 8-month active gestation following implantation. Ultrasound diagnostics are reliably able to detect a fetal heartbeat during this window as well. However, following February, progesterone concentrations in pregnant females steadily declined as parturition neared, making differentiating pregnant from non-pregnant females not as clear. It is possible that after progesterone decreases, an alternative hormone could continue to differentiate pregnant animals from non-pregnant animals from February to May. If so, the combination of these hormones could aid in quantifying absorption and abortion rates.
Why is this important?
Today, the Eastern Steller sea lion stock has been delisted. While this is a success story invoked by the protection the Endangered Species Act, the Western stock has not experienced the same recovery. Overall, the western stock numbers are stable or rising, but there are strong regional differences and thus the stock has remained listed as endangered (Fritz et al. 2013; Allen & Angliss 2012; Johnson & Fritz 2014). Our study provides foundational data on key reproductive hormones throughout estrus, embryonic diapause/pseudopregnancy and gestation. From this groundwork, future studies can refine methodologies to identify pregnancies and subsequent reproductive failures throughout the entire reproductive cycle and potentially aid in the continued investigation of drivers of the Western stock of Steller sea lions population trends.
Written by: Renae Sattler
Photo credit for Featured Image: Jamie King, Alaska Department of Fish and Game 2007 under NMFS Permit #358-1888.
Allen, B. M., & Angliss, R. P. (2012). Alaska marine mammal stock assessments, 2011. U.S. Dep. Commer., NOAA Tech. Memo. NMFSAFSC-234, p 288.
Browne, P., Conley, A. J., Spraker, T., Ream, R. R., & Lasley, B. L. (2006). Sex steroid concentration and localization of steroidogenic enzyme expression in free-ranging female northern fur seals (Callorhinus ursinus). General and Comparative Endocrinology, 147, 175–183.
Fritz, L., Sweeney, K., Johnson, D., Lynn, M., Gelatt, T., & Gilpatrick, J. (2013). Aerial and ship-based surveys of Steller sea lions (Eumetopias jubatus) conducted in Alaska in June–July 2008 through 2012, and an update on the status and trend of the western distinct population segment in Alaska. NOAA Tech. Memo. NMFS-AFSC-251 9.
Greig, D. J., Mashburn, K. L., Rutishauser, M., Gulland, F. M. D., Williams, T. M., & Atkinson, S. (2007). Seasonal changes in circulating progesterone and estrogen concentrations in the California sea lion (Zalophus californianus). Journal of Mammalogy, 88, 67–72.
Harmon, H. L. (2001). Seasonal reproductive endocrinology and anatomy of Steller sea lions (Eumetopias jubatus). M. Sc. Thesis, University of Alaska Fairbank. Available online at: http://www.alaskasealife.org/New/Contribute/pdf/Harmon_thesis_2001.pdf
Holmes, E. E., Fritz, L. W., York, A. E., & Sweeney, K. (2007). Age-structured modeling reveals long-term declines in the natality of western Steller sea lions. Ecological Applications, 17(8), 2214–2232.
Johnson, D. J., & Fritz, L. (2014). AgTrend: A Bayesian approach for estimating trends of aggregated abundance. Methods in Ecology and Evolution, 5, 1110–1115.
Pitcher, K. W., & Calkins, D. G. (1981). Reproductive biology of Steller sea lions in the Gulf of Alaska. Journal of Mammalogy, 62, 599–605.
Pitcher, K. W., Calkins, D. G., & Pendleton, G. W. (1998). Reproductive performance of Steller sea lions: An energetics-based reproductive strategy? Canadian Journal of Zoology, 76, 2075–2083.
Sattler R, Polasek L. Serum estradiol and progesterone profiles during estrus, pseudopregnancy, and active gestation in Steller sea lions. Zoo Biology. 2017; 36:323–331. https://doi.org/10.1002/zoo.21381
Trites, A. W., & Donnelly, C. P. (2003). The decline of Steller sea lions (Eumetopias jubatus) in Alaska: A review of the nutritional stress hypothesis. Mammal Review, 33(1), 3–28.
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