Variation in blubber cortisol levels in a recovering humpback whale population inhabiting a rapidly changing environment
Wikelski, M. & Cooke, S. J. Conservation physiology. Trends Ecol. Evol. 21, 38–46 (2006).Article
PubMed
Google Scholar
Cattet, M. et al. Understanding grizzly bear health in the context of changing landscapes. Foothills Model Forest Grizzly Bear Research Program Annual Report, 80–86 (2005).Reeder, D. M. & Kramer, K. M. Stress in free-ranging mammals: Integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235. https://doi.org/10.1644/bhe-003.1 (2005).Article
Google Scholar
Dunlop, R. A., Braithwaite, J., Mortensen, L. O. & Harris, C. M. Assessing population-level effects of anthropogenic disturbance on a marine mammal population. Front. Mar. Sci. 8, 230 (2021).Article
Google Scholar
Atkinson, S., Crocker, D., Houser, D. & Mashburn, K. Stress physiology in marine mammals: How well do they fit the terrestrial model?. J. Comp. Physiol. B. 185, 463–486. https://doi.org/10.1007/s00360-015-0901-0 (2015).Article
CAS
PubMed
Google Scholar
Romero, L. M. & Beattie, U. K. Common myths of glucocorticoid function in ecology and conservation. J. Exp. Zool. Part A: Ecol. Integr. Physiol. 337, 7–14. https://doi.org/10.1002/jez.2459 (2022).Article
CAS
Google Scholar
Champagne, C. D. et al. Blubber cortisol qualitatively reflects circulating cortisol concentrations in bottlenose dolphins. Mar. Mamm. Sci. 33, 134–153 (2017).Article
CAS
Google Scholar
Champagne, C. D. et al. Comprehensive endocrine response to acute stress in the bottlenose dolphin from serum, blubber, and feces. Gen. Comp. Endocrinol. 266, 178 (2018).Article
CAS
PubMed
Google Scholar
Teerlink, S., Horstmann, L. & Witteveen, B. Humpback whale (Megaptera novaeangliae) blubber steroid hormone concentration to evaluate chronic stress response from whale-watching vessels. Aquat. Mamm. 44, 411 (2018).Article
Google Scholar
Mingramm, F. M., Keeley, T., Whitworth, D. J. & Dunlop, R. A. Blubber cortisol levels in humpback whales (Megaptera novaeangliae): A measure of physiological stress without effects from sampling. Gen. Comp. Endocrinol. 291, 113436 (2020).Article
CAS
PubMed
Google Scholar
Saco, Y. et al. Evaluation of serum cortisol, metabolic parameters, acute phase proteins and faecal corticosterone as indicators of stress in cows. Vet. J. 177, 439–441 (2008).Article
CAS
PubMed
Google Scholar
Rolland, R. M. et al. Evidence that ship noise increases stress in right whales. Proc. R. Soc. B: Biol. Sci. 279, 2363–2368. https://doi.org/10.1098/rspb.2011.2429 (2012).Article
Google Scholar
Rocha, R., Clapham, P. J. & Ivashchenko, Y. V. Emptying the oceans: A summary of industrial whaling catches in the 20th century. Mar. Fish. Rev 76, 37–48 (2014).Article
Google Scholar
Comission, I. W. Report of the scientific committee. Journal of Cetacean Research and Management SC/68C (2021).Ducklow, H. W. et al. West Antarctic Peninsula: An ice-dependent coastal marine ecosystem in transition. Oceanography 26, 190–203 (2013).Article
Google Scholar
Laws, R. Seals and whales of the Southern Ocean 81–96 (Philosophical Transactions of the Royal Society of London. Series B, 1977).
Google Scholar
Savoca, M. S. et al. Baleen whale prey consumption based on high-resolution foraging measurements. Nature 599, 85–90. https://doi.org/10.1038/s41586-021-03991-5 (2021).Article
ADS
CAS
PubMed
Google Scholar
Pallin, L. J. et al. High pregnancy rates in humpback whales (Megaptera novaeangliae) around the Western Antarctic Peninsula, evidence of a rapidly growing population. R. Soc. Open Sci. https://doi.org/10.1098/rsos.180017 (2018).Article
PubMed
PubMed Central
Google Scholar
Bender, N. A., Crosbie, K. & Lynch, H. J. Patterns of tourism in the Antarctic Peninsula region: A 20-year analysis. Antarct. Sci. 28, 194–203. https://doi.org/10.1017/s0954102016000031 (2016).Article
ADS
Google Scholar
Operators, I. A. o. A. T. (2019).Trumble, S. J. et al. Baleen whale cortisol levels reveal a physiological response to 20th century whaling. Nat. Commun. https://doi.org/10.1038/s41467-018-07044-w (2018).Article
PubMed
PubMed Central
Google Scholar
Cates, K. A. et al. Corticosterone in central north pacific male humpback whales (Megaptera novaeangliae): Pairing sighting histories with endocrine markers to assess stress. Gen. Comp. Endocrinol. 296, 113540 (2020).Article
CAS
PubMed
Google Scholar
Sprogis, K. R., Videsen, S. & Madsen, P. T. Vessel noise levels drive behavioural responses of humpback whales with implications for whale-watching. eLife https://doi.org/10.7554/elife.56760 (2020).Article
PubMed
PubMed Central
Google Scholar
Rolland, R. et al. Fecal glucocorticoids and anthropogenic injury and mortality in North Atlantic right whales Eubalaena glacialis. Endanger. Species Res. 34, 417–429. https://doi.org/10.3354/esr00866 (2017).Article
Google Scholar
Modest, M. et al. First description of migratory behavior of humpback whales from an Antarctic feeding ground to a tropical calving ground. Anim. Biotelem. 9, 1–16 (2021).Article
Google Scholar
Amaral, R. S. Use of alternative matrices to monitor steroid hormones in aquatic mammals: A review. Aquat. Mamm. 36, 162 (2010).Article
Google Scholar
Graham, K. M., Burgess, E. A. & Rolland, R. M. Stress and reproductive events detected in North Atlantic right whale blubber using a simplified hormone extraction protocol. Conserv. Physiol. https://doi.org/10.1093/conphys/coaa133 (2021).Article
PubMed
PubMed Central
Google Scholar
Atkinson, S. et al. Pregnancy rate and biomarker validations from the blubber of eastern North Pacific blue whales. Mar. Mamm. Sci. https://doi.org/10.1111/mms.12616 (2019).Article
Google Scholar
Hunt, K. E., Rolland, R. M., Kraus, S. D. & Wasser, S. K. Analysis of fecal glucocorticoids in the North Atlantic right whale (Eubalaena glacialis). Gen. Comp. Endocrinol. 148, 260–272. https://doi.org/10.1016/j.ygcen.2006.03.012 (2006).Article
CAS
PubMed
Google Scholar
Mashburn, K. L. & Atkinson, S. Evaluation of adrenal function in serum and feces of Steller sea lions (Eumetopias jubatus): Influences of molt, gender, sample storage, and age on glucocorticoid metabolism. Gen. Comp. Endocrinol. 136, 371–381. https://doi.org/10.1016/j.ygcen.2004.01.016 (2004).Article
CAS
PubMed
Google Scholar
Jeanniard Du Dot, T. et al. Changes in glucocorticoids, IGF-I and thyroid hormones as indicators of nutritional stress and subsequent refeeding in Steller sea lions (Eumetopias jubatus). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol 152, 524–534. https://doi.org/10.1016/j.cbpa.2008.12.010 (2009).Article
CAS
Google Scholar
Foley, C. A. H., Papageorge, S. & Wasser, S. K. Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conserv. Biol. 15, 1134–1142. https://doi.org/10.1046/j.1523-1739.2001.0150041134.x (2001).Article
Google Scholar
Challis, J. R., Matthews, S. G., Gibb, W. & Lye, S. J. Endocrine and paracrine regulation of birth at term and preterm. Endocr. Rev. 21, 514–550 (2000).CAS
Google Scholar
Robeck, T. R., Steinman, K. J. & O’Brien, J. K. Characterization and longitudinal monitoring of serum androgens and glucocorticoids during normal pregnancy in the killer whale (Orcinus orca). Gen. Comp. Endocrinol. 247, 116–129 (2017).Article
CAS
PubMed
Google Scholar
Rolland, R. M., Hunt, K. E., Kraus, S. D. & Wasser, S. K. Assessing reproductive status of right whales (Eubalaena glacialis) using fecal hormone metabolites. Gen. Comp. Endocrinol. 142, 308–317 (2005).Article
CAS
PubMed
Google Scholar
Burgess, E. A., Hunt, K. E., Kraus, S. D. & Rolland, R. M. Adrenal responses of large whales: Integrating fecal aldosterone as a complementary biomarker to glucocorticoids. Gen. Comp. Endocrinol. 252, 103–110. https://doi.org/10.1016/j.ygcen.2017.07.026 (2017).Article
CAS
PubMed
Google Scholar
Ducklow, H. W. et al. Marine pelagic ecosystems: The west Antarctic Peninsula. Philos. Trans. R. Soc. London B: Biol. Sci. 362, 67–94 (2007).Article
PubMed
Google Scholar
Rogers, A. et al. Antarctic futures: An assessment of climate-driven changes in ecosystem structure, function, and service provisioning in the Southern Ocean. Ann. Rev. Mar. Sci. 12, 87–120 (2020).Article
CAS
PubMed
Google Scholar
Hillbrand, F. & Elsaesser, F. Concentrations of progesterone in the backfat of pigs during the oestrous cycle and after ovariectomy. J. Reprod. Fertil. 69, 73–80 (1983).Article
CAS
PubMed
Google Scholar
Funasaka, N. et al. Seasonal difference of diurnal variations in serum melatonin, cortisol, testosterone, and rectal temperature in Indo-Pacific bottlenose dolphins (Tursiops aduncus). Aquat. Mamm. 37, 433 (2011).Article
Google Scholar
Oki, C. & Atkinson, S. Diurnal patterns of cortisol and thyroid hormones in the Harbor seal (Phoca vitulina) during summer and winter seasons. Gen. Comp. Endocrinol. 136, 289–297. https://doi.org/10.1016/j.ygcen.2004.01.007 (2004).Article
CAS
PubMed
Google Scholar
Lavigne, D., Innes, S., Worthy, G. & Edwards, E. F. Lower critical temperatures of blue whales, Balaenoptera musculus. J. Theor. Biol. 144, 249–257 (1990).Article
ADS
Google Scholar
Nichols, R. C. et al. Intra-seasonal variation in feeding rates and diel foraging behaviour in a seasonally fasting mammal, the humpback whale. R. Soc. Open Sci. https://doi.org/10.1098/rsos.211674 (2022).Article
PubMed
PubMed Central
Google Scholar
Bierlich, K. C. Incorporating Photogrammetric Uncertainty in UAS-based Morphometric Measurements of Baleen Whales, (2021).Kellar, N. M. et al. Blubber cortisol: A potential tool for assessing stress response in free-ranging dolphins without effects due to sampling. PLoS ONE 10, e0115257 (2015).Article
PubMed
PubMed Central
Google Scholar
Bejder, L. & Samuels, A. Evaluating the effects of nature-based tourism on cetaceans. Mar. Mamm. Fish. Tour. Manag. Issues 1, 229–256 (2003).
Google Scholar
New, L. F. et al. The modelling and assessment of whale-watching impacts. Ocean Coast. Manag. 115, 10–16 (2015).Article
Google Scholar
Avila, I. C., Correa, L. M. & Parsons, E. Whale-watching activity in Bahía Málaga, on the Pacific coast of Colombia, and its effect on humpback whale (Megaptera novaeangliae) behavior. Tour. Mar. Environ. 11, 19–32 (2015).Article
Google Scholar
Amrein, A. M., Guzman, H. M., Surrey, K. C., Polidoro, B. & Gerber, L. R. Impacts of whale watching on the behavior of humpback whales (Megaptera novaeangliae) in the Coast of Panama. Front. Mar. Sci. 7, 1105 (2020).Article
Google Scholar
Heenehan, H. et al. Caribbean Sea soundscapes: monitoring humpback whales, biological sounds, geological events, and anthropogenic impacts of vessel noise. Front. Mar. Sci., 347 (2019).Keay, J. M., Singh, J., Gaunt, M. C. & Kaur, T. Fecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: A literature review. J. Zoo Wildl. Med. 37, 234–244 (2006).Article
PubMed
Google Scholar
Harris, K., Gende, S. M., Logsdon, M. G. & Klinger, T. Spatial pattern analysis of cruise ship-humpback whale interactions in and near Glacier Bay National Park, Alaska. Environ. Manag. 49, 44–54. https://doi.org/10.1007/s00267-011-9754-9 (2012).Article
ADS
Google Scholar
Palsbøll, P. J., Larsen, F. & Hansen, E. S. Sampling of skin biopsies from free-raging large cetaceans in west greenland: Development of new biopsy tips and bolt designs. International Whaling Commission Special Issue Series (1991).Weinstein, B. G., Double, M., Gales, N., Johnston, D. W. & Friedlaender, A. S. Identifying overlap between humpback whale foraging grounds and the Antarctic krill fishery. Biol. Cons. 210, 184–191 (2017).Article
Google Scholar
Lambertsen, R. H. A biopsy system for large whales and its use for cytogenetics. J. Mammal. 68, 443–445. https://doi.org/10.2307/1381495 (1987).Article
Google Scholar
Gilson, A., Syvanen, M., Levine, K. & Banks, J. Deer gender determination by polymerase chain reaction. Calif. Fish Game 84, 159–169 (1998).
Google Scholar
Aasen, E. & Medrano, J. F. Amplification of the ZFY and ZFX genes for sex identification in humans, cattle, sheep and goats. Bio/Technology 8, 1279–1281 (1990).CAS
PubMed
Google Scholar
Valsecchi, E. & Amos, W. Microsatellite markers for the study of cetacean populations. Mol. Ecol. 5, 151–156 (1996).Article
CAS
PubMed
Google Scholar
Palsbøll, P., Bérubé, M., Larsen, A. & Jørgensen, H. Primers for the amplification of tri-and tetramer microsatellite loci in baleen whales. Mol. Ecol. 6, 893–895 (1997).Article
PubMed
Google Scholar
Berube, M., Jørgensen, H., McEwing, R. & Palsbøll, P. J. Polymorphic di-nucleotide microsatellite loci isolated from the humpback whale, Megaptera novaeangliae. Mol. Ecol. 9, 2181–2183 (2000).Article
CAS
PubMed
Google Scholar
Waldick, R., Brown, M. & White, B. Characterization and isolation of microsatellite loci from the endangered North Atlantic right whale. Mol. Ecol. 8, 1763–1765 (1999).Article
CAS
PubMed
Google Scholar
Baker, C. S. et al. Strong maternal fidelity and natal philopatry shape genetic structure in North Pacific humpback whales. Mar. Ecol. Progress Ser. 494, 291 (2013).Article
ADS
Google Scholar
Constantine, R. et al. Abundance of humpback whales in Oceania using photo-identification and microsatellite genotyping. Mar. Ecol. Prog. Ser. 453, 249–261 (2012).Article
ADS
Google Scholar
Peakall, R. & Smouse, P. E. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6, 288–295 (2006).Article
Google Scholar
Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).Article
PubMed
Google Scholar
Kellar, N. M., Trego, M. L., Marks, C. I. & Dizon, A. E. Determining pregnancy from blubber in three species of delphinids. Mar. Mamm. Sci. 22, 1–16 (2006).Article
Google Scholar
Pallin, L., Robbins, J., Kellar, N., Bérubé, M. & Friedlaender, A. Validation of a blubber-based endocrine pregnancy test for humpback whales. Conserv. Physiol. https://doi.org/10.1093/conphys/coy031 (2018).Article
PubMed
PubMed Central
Google Scholar
Kellar, N. M. et al. Low reproductive success rates of common bottlenose dolphins Tursiops truncatus in the northern Gulf of Mexico following the Deepwater Horizon disaster (2010–2015). Endanger. Species Res. 33, 143–158 (2017).Article
Google Scholar
R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria, 2021).ArcMap (version 10.8.2) (Redlands, CA: Esri Inc, 2022). More