Reproductive Success


Pregnancy Diagnosis

Trends in pregnancy rate is a key data stream used to help inform management choices regarding populations of marine mammals. Healthy growing populations predominately have higher pregnancy and overall reproductive success rates; inversely, declining populations typically experience higher reproductive failures as one of the first signs of poor population health. Determining pregnancy rates can help give an indication of population health and track recovery of exploited or threatened populations. Pregnancy rates are found by determining the proportion of females in a population which are pregnant and are therefore likely to contribute to increasing a population. Identifying areas with higher pregnancy rate within a population can also help identify areas that are vulnerable to human-linked threats. The pregnancy state of marine mammals can be diagnosed via several different ways but one of the most accurate and efficient methods for free-ranging cetaceans has found to be measuring progesterone in skin biopsies (Kellar et al. 2014).

Blubber progesterone graph of rank-ordered female humpback whales

Blubber progesterone concentrations of rank-ordered female humpback whales. The vertical gap towards the right side of the plot illustrates the substantial difference between animals classified as pregnant (filled circles) and those classified as nonpregnant (open circles). Clark et al. 2016 Progesterone, the primary hormone of pregnancy, is a steroid hormone which can be/has been quantified from many different tissues. Small (6mm) dart biopsies of the skin are a minimally-invasive and common tool used to study cetaceans because of the potential to gather genetic, contaminant, microbiome, and endocrine information all from a small sample taken without imposing capture-stress on a wild marine mammal. We can analyze the blubber that is collected from these biopsies and, through an extraction process, obtain levels of progesterone. Highly elevated progesterone hormone levels in blubber tissue provides strong evidence that an animal is pregnant (Kellar et al. 2006, Kellar et al. 2013, Trego et al. 2013). Progesterone levels of pregnant animals are found to be, in almost all cases, orders of magnitude larger than those of non-pregnant females (including immature animals and males) across multiple species of cetaceans and pinnipeds. We have shown this method of determining reproductive rates to be accurate and consistent with other methods of determining pregnancy rates while being less invasive.

blubber progesterone concentrations as a function of total body length
Kellar et al. 2006

Our work has allowed for monitoring of populations affected by human-derived disturbances so that we may better understand our impact and the population’s ability to recover. We can do this by assessing pregnancy rates and reproductive success in the affected areas relative to those in similar but unaffected areas. Examples of this work include identifying a major decline in pregnancy success rate in bottlenose dolphins affected by the Deepwater Horizon Oil Spill (Kellar et al. 2017) and showing an inhibitive effect of tuna purse-sein fishery on pregnancy in pantropical spotted dolphins in the eastern tropical Pacific (Kellar et al. 2013). Overall, determining reproductive rates in this way provides an additional tool in our stewardship of protected marine mammal populations. We have also used this approach to highlight areas and times of year that are important for reproduction so that resource users who want to conduct activities in a region can minimize their impact on the most valuable animals (Kellar et al. 2014).

LITERATURE CITED

Clark, C. T., A. H. Fleming, J. Calambokidis, N. M. Kellar, C. D. Allen, K. N. Catelani, M. Robbins, N. E. Beaulieu, D. Steel, and J. T. Harvey. 2016. Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales. Conservation Physiology 4:1-13.

Kellar, N. M., J. Keliher, M. L. Trego, K. N. Catelani, C. Hanns, J. C. C. George, and C. Rosa. 2013. Variation of bowhead whale progesterone concentrations across demographic groups and sample matrices. Endangered Species Research 22:61-72.

Kellar, N. M., T. R. Speakman, C. R. Smith, S. M. Lane, B. C. Balmer, M. L. Trego, K. N. Catelani, M. N. Robbins, C. D. Allen, and R. S. Wells. 2017. Low reproductive success rates of common bottlenose dolphins Tursiops truncatus in the northern Gulf of Mexico following the Deepwater Horizon disaster (2010-2015). Endangered Species Research 33:143-158.

Kellar, N. M., M. L. Trego, S. J. Chivers, and F. I. Archer. 2013. Pregnancy patterns of pantropical spotted dolphins (Stenella attenuata) in the eastern tropical Pacific determined from hormonal analysis of blubber biopsies and correlations with the purse-seine tuna fishery. Marine Biology 160:3113-3124.

Kellar, N. M., M. L. Trego, S. J. Chivers, F. I. Archer, and W. L. Perryman. 2014. From progesterone in biopsies to estimates of pregnancy rates: Large scale reproductive patterns of two sympatric species of common dolphin, Delphinus spp. off California, USA and Baja, Mexico. Bulletin, Southern California Academy of Sciences 113:58-80.

Kellar, N. M., M. L. Trego, C. I. Marks, and A. E. Dizon. 2006. Determining pregnancy from blubber in three species of delphinids. Marine Mammal Science 22:1-16.

Pallin, L. J., C. S. Baker, D. Steel, N. M. Kellar, J. Robbins, D. W. Johnston, D. P. Nowacek, A. J. Read, and A. S. Friedlaender. 2018. High pregnancy rates in humpback whales (Megaptera novaeangliae) around the Western Antarctic Peninsula, evidence of a rapidly growing population. Royal Society open science 5:180017.

Trego, M. L., N. M. Kellar, and K. Danil. 2013. Validation of blubber progesterone concentrations for pregnancy determination in three dolphin species and a porpoise. Plos One 8.

Blubber Testosterone in Bottlenose Dolphins

The ability to determine sexual maturity status in male cetaceans can improve understanding of age structure and help assess the overall health of wild populations. Just as the concentration of the progesterone hormone can help diagnosis whether or not a female animal is pregnant, the concentration of testosterone can help inform whether or not a male is sexually mature (Kellar et al. 2009). Moreover, because skin samples (which often include blubber) are the most commonly obtained biological samples taken from live cetaceans, the ability to quantify testosterone from this tissue would be particularly helpful. Fortunately, during annual live-capture health assessments of Sarasota Bay bottlenose dolphins, blood and blubber are routinely collected and evaluated for their composition and additional blubber is collected via minimally invasive dart biopsy during other field operations. In previous studies, testosterone levels have been measured in either blood or blubber samples but no study has compared the results from both matrices simultaneously. As such, we attempted to assess the maturity status of known male bottlenose dolphins using blubber obtained with dart biopsies and examine how the associated testosterone concentrations compared with measured in the blood.


Figure: The relationship of blubber testosterone to serum testosterone in male bottlenose dolphins in Sarasota Bay, Florida (Sherman and Kellar 2019).

Here we present the serum and blubber testosterone data from 60 combined samples, representing 30 sampling events and 24 individual male bottlenose dolphins. These findings show a strong correlation between blubber and serum testosterone concentrations and the amount present in either matrix appears to be a robust indicator of maturity status. These findings represent an information advancement in a tool to help evaluate the age structure of wild dolphin populations outside of Sarasota Bay. Additionally, recent research has provided evidence that testosterone production is impaired in dolphins with higher persistent organic contaminant loads; as such, the biochemical methods we are developing here may help in the monitoring of pollutant impacts on biological functions of other wild cetacean populations (Trego et al. 2018).



References:

Kellar, Nicholas M., Marisa L. Trego, Corina I. Marks, Susan J. Chivers, Kerri Danil, and Frederick I. Archer. "Blubber testosterone: A potential marker of male reproductive status in short‐beaked common dolphins." Marine Mammal Science 25, no. 3 (2009): 507-522.

Sherman, K., & Kellar, N. (2019, January). Blubber testosterone in bottlenose dolphins. Nicks and Notches, 17. January 2019 The previous link is a link to Non-Federal government web site. Click to review NOAA Fisheries disclaimer

Trego, Marisa L., Eunha Hoh, Nicholas M. Kellar, Sara Meszaros, Michelle N. Robbins, Nathan G. Dodder, Andrew Whitehead, and Rebecca L. Lewison. "Comprehensive screening links halogenated organic compounds with testosterone levels in male Delphinus delphis from the Southern California bight." Environmental Science & Technology 52, no. 5 (2018): 3101-3109.
Last modified: 4/25/2019