Abstract
The polar bear (Ursus maritimus) is threatened by climate changes and also from persistent organic pollutants affecting polar bear endocrinology governing growth and reproduction. To provide further insight into basic polar bear endocrinology, we determined the levels of steroids in multiple tissues and plasma from East Greenland polar bears. Tissue samples from 10 polar bears, 5 males (2 adults, 3 juveniles) and 5 females (all juveniles) were obtained from the Inuit hunt in Scoresby Sound during springtime. Eleven steroids: pregnenolone, 17-hydroxypregnenolone, progesterone, 17-hydroxyprogesterone, dehydroepiandrosterone, androstenedione, testosterone, dihydrotestosterone, estrone, 17α-estradiol and 17β-estradiol were determined in brain, adrenal cortex, testis, testicular vein, plasma, and ovary using GC–MS/MS. In brain tissue, the neuroactive progestagen pregnenolone (11.9 ± 4.4 ng/g ww) and dehydroepiandrosterone (2.26 ± 0.43 ng/g ww) were found in high concentrations. Very high levels of testosterone and androstenedione were observed in testes (>100 ng/g ww) and plasma from testicular vein (testosterone: 108 ± 41 ng/ml; androstenedione: 35.2 ± 11.1 ng/ml). Additionally, a strong correlation was found between the levels of steroids in testes and testicular vein plasma. Progestagens were found in very high levels in ovaries from juvenile females (>100 ng/g ww). Finally, our study indicates that polar bears synthesize androstenedione via the ∆-4 pathway. The present study adds new insight to our knowledge on polar bear endocrinology, which may be used in future studies on polar bear ecology and studies on some of the threats from pollution and climate changes that these animals are facing.
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References
Basu N, Scheuhammer AM, Sonne C, Letcher RJ, Born EW, Dietz R (2009) Is dietary mercury of neurotoxicological concern to wild polar bears (Ursus maritimus)? Environ Toxicol Chem 28:133–140
Buffet NC, Djakoure C, Maitre SC, Bouchard P (1998) Regulation of the human menstrual cycle. Front Neuroendocrinol 19:151–186
Cattet MRL, Caulkett NA, Obbard ME, Stenhouse GB (2002) A body-condition index for ursids. Can J Zool 80:1156–1161
Conley AJ, Bird IM (1997) The role of cytochrome p450 17 alpha-hydroxylase and 3 beta-hydroxysteroid dehydrogenase in the integration of gonadal and adrenal steroidogenesis via the delta 5 and delta 4 pathways of steroidogenesis in mammals. Biol Reprod 56:789–799
Conley AJ, Corbin CJ, Thomas JL, Gee NA, Lasley BL, Moeller BC, Stanley SD, Berger T (2012) Costs and consequences of cellular compartmentalization and substrate competition among human enzymes involved in androgen and estrogen synthesis. Biol Reprod 86:1–8
Do Rego JL, Seong JY, Burel D, Leprince J, Luu-The V, Tsutsui K et al (2009) Neurosteroid biosynthesis: enzymatic pathways and neuroendocrine regulation by neurotransmitters and neuropeptides. Front Neuroendocrinol 30:259–301
Dietz R, Rigét FF, Sonne C, Born EW, Bechshøft T, McKinney MA, Letcher RJ (2013a) Part 1: three decades (1984–2010) of legacy contaminant trends in East Greenland polar bears (Ursus maritimus). Environ Int 59:485–493. doi:10.1016/j.envint.2012.09.004
Dietz R, Rigét FF, Sonne C, Born EW, Bechshøft T, McKinney MA, Drimmei R, Muir DCG, Letcher RJ (2013b) Part 2: three decades (1984–2010) of flame retardant trends in East Greenland polar bears (Ursus maritimus). Environ Int 59:494–500. doi:10.1016/j.envint.2012.09.008
Dietz R, Gustavson K, Sonne C, Desforges J-P, Rigét FF, Pavlova V, McKinney MA, Letcher RJ (2015) Physiologically-based pharmacokinetic modelling of immune, reproductive and carcinogenic effects from contaminant exposure in polar bears (Ursus maritimus) across the Arctic. Environ Res 140:45–55
Fail P, Sloan C, Johnson J, Brown V (2005) Steroidogenesis screening assays and endocrine disruptors. U.S. Environmental Protection Agency Endocrine Disruptor Screening Program. EPA Contract Number 68-W-01-023 Work Assignments 2-6 and 5-5, Task 3. http://www.epa.gov/endo/pubs/edmvs/steroidogenesis_drp_final_3_29_05.pdf
Ganong WF (2005) Review of medical physiology, 22nd edn, Appleton and Lange, California
Gazdar AF, Oie HK, Shackleton CH, Chen TR, Triche TJ, Myers CE, Chrousos GP, Brennan MF, Stein CA, La Rocca RV (1990) Establishment and characterization of a human adrenocortical carcinoma cell line that expresses multiple pathways of steroid biosynthesis. Cancer Res 50:5488–5496
Government of Greenland (2015) Kvoter for 2015. http://naalakkersuisut.gl/da/Naalakkersuisut/Departementer/Fiskeri-Fangst-og-Landbrug/Fangst-og-jagtafdelingen/Kvoter-og-andre-begraensninger/2015-kvoter
Gustavson L, Ciesielski TM, Bytingsvik J, Styrishave B, Hansen M, Lie E, Aars J, Jenssen BM (2015a) Hydroxylated polychlorinated biphenyls decrease circulating steroids in female polar bears (Ursus maritimus). Environ Res 138:191–201
Gustavson L, Jenssen BM, Bytingsvik J, Styrishave B, Hansen M, Aars J, Eggen GS, Ciesielski TM (2015b) Steroid hormone profile in female polar bears (Ursus maritimus). Polar Biol 38:1183–1194
Haave M, Ropstad E, Derocher AE, Lie E, Dahl E, Wiig Ø, Skaare JU, Jenssen BM (2003) Polychlorinated biphenyls and reproductive hormones in female polar bears at Svalbard. Environ Health Perspect 111:431–436
Hansen M, Jacobsen N, Nielsen FK, Björklund E, Styrishave B, Halling-Sørensen B (2011a) Determination of steroid hormones in blood by GC–MS/MS. Anal Bioanal Chem 400:3409–3417
Hansen M, Krogh K, Halling-Sørensen B, Björklund E (2011b) Determination of ten steroid hormones in animal waste manure and agricultural soil using inverse and integrated clean-up pressurized liquid extraction and gas chromatography-tandem mass spectrometry. Anal Methods 3:1087–1095
Harlow HJ, Beck TDI, Walters LM, Greenhouse SS (1990) Seasonal serum glucose, progesterone and cortisol levels of black bears (Ursus americanus). Can J Zool 68:183–187
Haugestøl GL (2009) Effects of endocrine disrupting chemicals in male polar bears (Ursus maritimus) at Svalbard. Master thesis at the Department of Biology, NTNU, Trondheim
Hojo Y, Higo S, Kawato S, Hatanaka Y, Ooishi Y, Murakami G et al (2011) Hippocampal synthesis of sex steroids and corticosteroids: essential for modulation of synaptic plasticity. Front Endocrinol 2:1–17
Howell-Skalla LA, Chattet MRL, Ramsay MA, Bahr JM (2002) Seasonal changes in testicular size and serum LH, prolactin and testosterone concentrations in male polar bears (Ursus maritimus). Reproduction 123:729–733
ICH Guideline (2005) International conference on harmonisation of technical requirements for registration of pharmaceuticals for human use. Validation of Analytical Procedures: Text and Methodology Q2(R1):1–17
Jenssen BM, Villanger GD, Gabrielsen KM, Bytingsvik J, Bechshoft T, Ciesielski TM, Sonne C, Dietz R (2015) Anthropogenic flank attack on polar bears: interacting consequences of climate warming and pollutant exposure. Front Ecol Evol 3:1–7
Letcher RJ, Bustnes JO, Dietz R, Jenssen BM, Jørgensen EH, Sonne C (2010) Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 408:2995–3043
Lintelmann J, Katayama A, Kurihara N, Shore L, Wenzel A (2003) Endocrine disruptors in the environment (IUPAC technical report). Pure Appl Chem 75:631–681
Lønø O (1970) The polar bear (Ursus maritimus) in the Svalbard area. Nor Polarinst Skr 149:1–117
McKinney MA, Atwood T, Dietz R, Sonne C, Iverson SJ, Peacock E (2014) Validation of adipose lipid content as a body condition index for polar bears. Ecol Evol 4:516–527. doi:10.1002/ece3.956
Molnár PK, Derocher AE, Thiemann GW, Lewis MA (2010) Predicting survival, reproduction and abundance of polar bears under climate change. Biol Conserv 143:1612–1622
Molnár PK, Derocher AE, Klanjscek T, Lewis MA (2011) Predicting climate change impacts on polar bear litter size. Nat Commun 2:186. doi:10.1038/ncomms1183
Nielsen FK, Hansen CH, Fey JA, Hansen M, Jacobsen NW, Halling-Sørensen B, Björklund E, Styrishave B (2012) H295R cells as a model for steroidogenic disruption: a broader perspective using simultaneous chemical analysis of 7 key steroid hormones. Toxicol In Vitro 26:343–350
Oskam IC, Ropstad E, Dahl E, Lie E, Derocher AE, Wiig O, Larsen S, Wiger R, Skaare JU (2003) Organochlorines affect the major androgenic hormone, testosterone, in male polar bears (Ursus maritimus) at Svalbard. J Tox Environ Health A 66:2119–2139
Palmer SS, Nelson RA, Ramsay MA, Stirling I, Bahr JM (1988) Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears. Biol Reprod 38:1044–1050
Payne AH, Hales DB (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocrinol Rev 25:947–970
Pedersen KE, Basu N, Letcher R, Greaves AK, Sonne C, Dietz R, Styrishave B (2015) Brain region-specific perfluoroalkylated sulfonate (PFSA) and carboxylic acid (PFCA) accumulation and neurochemical biomarker responses in East Greenland polar bears (Ursus maritimus). Environ Res 138:22–31
Ramsay MA, Stirling I (1986) On the mating system of polar bears. Can J Zool 64:2142–2151
Ramsay MA, Stirling I (1988) Reproductive biology and ecology of female polar bears (Ursus maritimus). J Zool Lond 214:601–634
Rode KD, Regehr EV, Douglas DC, Durner G, Derocher AE, Thiemann GW, Budge SM (2014) Variation in the response of an Arctic top predator experiencing habitat loss: feeding and reproductive ecology of two polar bear populations. Glob Change Biol 20:76–88
Ropstad E, Oskram IC, Lyche JL, Larsen HJ, Lie E, Haave M, Dahl E, Wiger R, Skaare JU (2006) Endocrine disruption induced by organochlorines (OCs): field studies and experimental models. J Tox Environ Health A 69:53–76
Schliebe S, Rode KD, Gleason JS, Wilder J, Proffitt K, Evans TJ, Miller S (2008) Effects of sea ice extent and food availability on spatial and temporal distribution of polar bears during the fall open-water period in the Beaufort sea. Polar Biol 31:999–1010
Sonne C (2010) Health effects from long-range transported contaminants in arctic top predators: an integrated review based on studies of polar bears and relevant model species. Environ Int 36:461–491
Sonne C, Leifsson PS, Dietz R, Born EW, Letcher RJ, Hyldstrup L et al (2006) Xenoendocrine pollutants may reduce size of sexual organs in East Greenland polar bears (Ursus maritimus). Environ Sci Technol 40:5668–5674
Sonne C, Gustavson K, Rigét FF, Dietz R, Birkved M, Letcher RJ, Muir DCG, Bossi R, Vorkamp K, Born EW, Petersen G (2009) Reproductive performance in East Greenland polar bears (Ursus maritimus) may be affected by organohalogen contaminants as shown by critical body residue modelling and risk quotients estimation. Chemosphere 77:1558–1568
Sonne C, Letcher RJ, Bechshøft TØ, Rigét FF, Muir DCG, Leifsson PS, Born EW, Hyldstrup L, Basu N, Kirkegaard M, Dietz R (2012) Two decades of biomonitoring polar bear health in Greenland: a review. Acta Vet Scan 54:S15
Sonne C, Dietz R, Letcher RJ, Pedersen KM, Rigét FF, Styrishave B (2014) Steroid hormones in blood plasma from Greenland sledge dogs (Canis familiaris) dietary exposed to organohalogen polluted minke whale (Balaenoptera acuterostrata) blubber. Toxicol Environ Chem 96:273–286
Spinnel E, Fick J, Andersson PL, Haglund P (2008) Streamlined combustion gas measurements for improved national dioxin inventories. Environ Sci Technol 42:9255–9261
Theimann GW, Iverson SJ, Stirling I (2008) Polar bear diets and Arctic marine food webs: insights from fatty acid analysis. Ecol Monogr 78:591–613
Tsubota T, Howell-Skalla L, Boone WR, Garshelis DL, Bahr M (1998) Serum progesterone, oestradiol, luteinizing hormone and prolactin profiles in the female black bear (Ursus americanus). Anim Reprod Sci 53:107–118
Tsutsui K, Ukena K, Takase M, Kohchi C, Lea RW (1999) Neurosteroid biosynthesis in vertebrate brains. Comp Biochem Physiol C 124:121–129
Tsutsui K, Ukena K, Usui M, Sakamoto H (2000) Novel brain function: biosynthesis and actions of neurosteroids in neurons. Neurosci Res 36:261–273
Widmaier EP, Raff H, Strang KT (2006) Vander’s human physiology: the mechanisms of body function. McGraw-Hill Higher Education, New York
Acknowledgments
Samples were collected in collaboration with local Inuit subsistence hunters and funded by a number of projects under the Danish Cooperation for Environment in the Arctic (DANCEA) programme including the ARCTIC, PELATES and the CORE programmes. We would also like to thank Phia Hansen for graphic layout and the AURORAE Field Crew for assistance during field work.
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Styrishave, B., Pedersen, K.E., Clarke, O. et al. Steroid hormones in multiple tissues of East Greenland polar bears (Ursus maritimus). Polar Biol 40, 37–49 (2017). https://doi.org/10.1007/s00300-016-1922-1
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DOI: https://doi.org/10.1007/s00300-016-1922-1