Minimally invasive physiological correlates of social behaviour in belugas (Delphinapterus leucas) under human care

  • Justin T. Richard Department of Fisheries, Animal and Veterinary Sciences, University of Rhode Island, Kingston, RI, USA; and Mystic Aquarium, Mystic, CT, USA
  • Rachael Levine Department of Fisheries, Animal and Veterinary Sciences, University of Rhode Island, Kingston, RI, USA; and Mystic Aquarium, Mystic, CT, USA
  • Tracy A. Romano Mystic Aquarium, Mystic, CT, USA
  • Becky L. Sartini Department of Fisheries, Animal and Veterinary Sciences, University of Rhode Island, Kingston, RI, USA
Keywords: reproduction, cetacean, mating strategies, blow, steroid hormones, aquarium

Abstract

Simultaneous observations of reproductive physiology and behaviour were conducted on a group of two male and two female belugas under professionally managed care for one year to explore potential mating strategies. Weekly blow sampling for progesterone in females was used to define the breeding season by detecting three oestrous cycles in one female. Twice weekly blow sampling for testosterone and twice monthly testes measurements via ultrasonography were used to detect reproductive seasonality in both males. Female–male association frequency varied longitudinally, with 70% of all interactions occurring during the 16-week breeding season. Male–male associations did not vary seasonally. Male display behaviours towards the female occurred 14.8 times more frequently during the breeding season (0.164 ± 0.188 behaviours/min) than outside of the breeding season (0.011 ± 0.042 behaviours/min). The cycling female responded variably to male display behaviours by altering swim speed or body orientation towards the male. Although this small sample size limits broad conclusions, the frequent display behaviours, low copulation rate and lack of serious male–male aggression are consistent with predictions for pre-copulatory female mate choice developed from the current knowledge of beluga reproductive physiology. These observations, which are not feasible for wild belugas, provide important management considerations because reduced opportunities for mate choice could limit the reproductive rate, especially in small populations.

Downloads

Download data is not yet available.

References


Bartsh S.S., Johnston S.D. & Siniff D.B. 1992. Territorial behavior and breeding frequency of male Weddell seals (Leptonychotes weddelli) in relation to age, size, and concentrations of serum testosterone and cortisol. Canadian Journal of Zoology 70, 680–692, doi: 10.1139/z92-102.


Brodie P.F. 1971. A reconsideration of aspects of growth, reproduction and behavior of the white whale (Delphinapterus leucas) with reference to the Cumberland Sound, Baffin Island population. Journal Fisheries Research Board of Canada 28, 1309–1318, doi: 10.1139/f71-198.


Brodie P.F. 1989. The white whale Delphinapterus leucas (Pallas, 1776). In S.H. Ridgway & S.R. Harrison (eds.): Handbook of marine mammals. Vol. 4: river dolphins and the larger toothed whales. Pp. 119–144. New York: Academic Press.


Burgess E.A., Lanyon J.M. & Keeley T. 2012. Testosterone and tusks: maturation and seasonal reproductive patterns of live, free-ranging male dugongs (Dugong dugon) in a subtropical population. Reproduction 143, 683–697, doi: 10.1530/REP-11-0434.


Burns J.J. & Seaman G.A. 1988. Investigations of Belukha whales in coastal waters of western and Northern Alaska. II. Biology and ecology. Final report. Outer Continental Shelf Environmental Assessment Program. Fairbanks, AK: Alaska Department of Fish & Game.


Cairns S.J. & Schwager S.J. 1987. A comparison of association indices. Animal Behaviour 35, 1454–1469, doi: 10.1016/S0003-3472(87)80018-0.


Candolin U. 2019. Mate choice in a changing world. Biological Reviews 94, 1246–1260, doi: 10.1111/brv.12501.


Castellote M., Thayre B., Mahoney M., Mondragon J., Lammers M.O. & Small R.J. 2019. Anthropogenic noise and the endangered Cook Inlet beluga whale, Delphinapterus leucas: acoustic considerations for management. Marine Fisheries Review 80(3), 63–88, doi: 10.7755/MFR.80.3.3.


Centelleghe C., Carraro L., Gonzalvo J., Rosso M., Esposti E., Gili C., Bonato M., Pedrotti D., Cardazzo B., Povinelli M. & Mazzariol S. 2020. The use of unmanned aerial vehicles (UAVs) to sample the blow microbiome of small cetaceans. PLoS One 15, e0235537, doi: 10.1371/journal.pone.0235537.


Citta J.J., O’Corry‐Crowe G., Quakenbush L.T., Bryan A.L., Ferrer T., Olson M.J., Hobbs R.C. & Potgieter B. 2018. Assessing the abundance of Bristol Bay belugas with genetic mark–recapture methods. Marine Mammal Science 34, 666–686, doi: 10.1111/mms.12472.


Clutton-Brock T. & McAuliffe K. 2009. Female mate choice in mammals. The Quarterly Review of Biology 84, 3–27, doi: 10.1086/596461.


Connor R.C., Smolker R. & Bejder L. 2006. Synchrony, social behaviour and alliance affiliation in Indian Ocean bottlenose dolphins, Tursiops aduncus. Animal Behaviour 72, 1371–1378, doi: 10.1016/j.anbehav.2006.03.014.


Dines J.P., Mesnick S.L., Ralls K., May-Collado L., Agnarsson I. & Dean M.D. 2015. A trade-off between precopulatory and postcopulatory trait investment in male cetaceans. Evolution 69, 1560–1572, doi: 10.1111/evo.12676.


DiPaola S., Akai C. & Kraus B. 2007. Experiencing belugas: action selection for an interactive aquarium exhibit. Adaptive Behavior 15, 99–113, doi: 10.1177/1059712306076251.


Glabicky N., DuBrava A. & Noonan M. 2010. Social–sexual behavior seasonality in captive beluga whales (Delphinapterus leucas). Polar Biology 33, 1145–1147, doi: 10.1007/s00300-010-0790-3.


Hänninen L. & Pastell M. 2009. CowLog: open-source software for coding behaviors from digital video. Behavior Research Methods 41, 472–476, doi: 10.3758/BRM.41.2.472.


Harwood L.A., Kingsley M.C.S. & Smith T.G. 2014. An emerging pattern of declining growth rates in belugas of the Beaufort Sea: 1989–2008. Arctic 67, 483–492, doi: 10.14430/arctic4423.


Heide-Jørgensen M.P., Laidre K.L., Borchers D., Marques T.A., Stern H. & Simon M. 2010. The effect of sea-ice loss on beluga whales (Delphinapterus leucas) in west Greenland. Polar Research 29, 198–208, doi: 10.1111/j.1751-8369.2009.00142.x.


Higdon J.W. & Ferguson S.H. 2009. Loss of Arctic sea ice causing punctuated change in sightings of killer whales (Orcinus orca) over the past century. Ecological Applications 19, 1365–1375, doi: 10.1890/07-1941.1.


Hill H.M., Alvarez C.J., Dietrich S. & Lacy K. 2016. Preliminary findings in Beluga (Delphinapterus leucas) tactile interactions. Aquatic Mammals 42, 277–291, doi: 10.1578/AM.42.3.2016.277.


Hill H.M., de Oliveira Silva-Gruber D.G. & Noonan M. 2018. Sex-specific social affiliation in captive beluga whales (Delphinapterus leucas). Aquatic Mammals 44, 250–255, doi: 10.1578/AM.44.3.2018.250.


Hill H.M., Dietrich S., Yeater D., McKinnon M., Miller M., Aibel S. & Dove A. 2015. Developing a catalog of socio-sexual behaviors of beluga whales (Delphinapterus leucas) in the care of humans. Animal Behaviour and Cognition 2, 105–123, doi: 10.12966/abc.05.01.2015.


Hobbs R.C., Wade P.R. & Shelden K.E.W. 2015. Viability of a small, geographically-isolated population of beluga whales, Delphinapterus leucas: effects of hunting, predation, and mortality events in Cook Inlet, Alaska. Marine Fisheries Review 77, 59–88, doi: 10.7755/MFR.77.2.4.


Høier R. & Heide-Jørgensen M.P. 1994. Steroid hormones and prolactin in white whales (Delphinapterus leucas) from west Greenland. Bioscience 39, 227–238.


Iossa G., Soulsbury C.D., Baker P.J. & Harris S. 2008. Sperm competition and the evolution of testes size in terrestrial mammalian carnivores. Functional Ecology 22, 655–662, doi: 10.1111/j.1365-2435.2008.01409.x.


Katsumata E., Furuta C., Katsumata H., Watanabe G. & Taya K. 2006. Basal body temperature method for detecting ovarian cycle in the captive beluga (Delphinapterus leucas). Journal of Reproduction and Development 52, 59–63, doi: 10.1262/jrd.17066.


Kaufman A.B. & Rosenthal R. 2009. Can you believe my eyes? The importance of interobserver reliability statistics in observations of animal behaviour. Animal Behaviour 78, 1487–1491, doi: 10.1016/j.anbehav.2009.09.014.


Kelley T.C., Stewart R.E.A., Yurkowski D.J., Ryan A. & Ferguson S.H. 2014. Mating ecology of beluga (Delphinapterus leucas) and narwhal (Monodon monoceros) as estimated by reproductive tract metrics. Marine Mammal Science 31, 479–500, doi: 10.1111/mms.12165.


Kleinenberg S.E., Yablokov A.V., Bel’kovich B.M. & Tarasevich M.N. 1969. Beluga (Delphinapterus leucas): investigation of the species. Jerusalem: Israel Program for Scientific Translations.


Lacey E.A., Wieczorek J.R. & Tucker P.K. 1997. Male mating behaviour and patterns of sperm precedence in Arctic ground squirrels. Animal Behaviour 53, 767–779, doi: 10.1006/anbe.1996.0342.


Lilley M.K., Ham J.R. & Hill H.M. 2020. The development of socio-sexual behaviour in belugas (Delphinapterus leucas) under human care. Behavioural Processes 171, 104025, doi: 10.1016/j.beproc.2019.104025.


Loseto L.L., Richard P., Stern G.A., Orr J. & Ferguson S.H. 2006. Segregation of Beaufort Sea beluga whales during the open-water season. Canadian Journal of Zoology 84, 1743–1751, doi: 10.1139/z06-160.


Mann J. 2006. Establishing trust: socio-sexual behavior and the development of male–male bonds among Indian Ocean bottlenose dolphins. In V. Sommer & P.L. Vasey (eds.): Homosexual behavior in animals: an evolutionary perspective. Pp. 107–130. New York: Cambridge University Press.


Martin P. & Bateson P. 2007. Measuring behavior: an introductory guide. 3rd edn. Cambridge: Cambridge University Press.


Michaud R. 2005. Sociality and ecology of the odontocetes. In K.E. Ruckstuhl & P. Neuhaus (eds.): Sexual segregation in vertebrates: ecology of the two sexes. Pp. 303–326. New York: Cambridge University Press.


Milner J.M., Nilsen E.B. & Andreassen H.P. 2007. Demographic side effects of selective hunting in ungulates and carnivores. Conservation Biology 21, 36–47, doi: 10.1111/j.1523-1739.2006.00591.x.


Mitoyen C., Quigley C. & Fusani L. 2019. Evolution and function of multimodal courtship displays. Ethology 125, 503–515, doi: 10.1111/eth.12882.


Møller A.P. & Legendre S. 2001. Allee effect, sexual selection and demographic stochasticity. Oikos 92, 27–34, doi: 10.1034/j.1600-0706.2001.920104.x.


Muraco H. & Kuczaj S.A. 2015. Conceptive estrus behavior in three bottlenose dolphins (Tursiops truncatus). Animal Behavior and Cognition 2, 30–48, doi: 10.12966/abc.02.03.2015.


Neimanis A.S., Read A.J., Foster R.A. & Gaskin D.E. 2000. Seasonal regression in testicular size and histology in harbor porpoises (Phocoena phocoena) from the Bay of Fundy and Gulf of Maine. London Journal of Zoology 250, 221–229, doi: 10.1111/j.1469-7998.2000.tb01072.x.


O’Brien J.K., Steinman K.J., Schmitt T. & Robeck T.R. 2008. Semen collection, characterization and artificial insemination in the beluga (Delphinapterus leucas) using liquid-stored spermatozoa. Reproduction, Fertility and Development 20, 770–783, doi: 10.1071/RD08031.


O’Corry-Crowe G.M., Mahoney A.R., Suydam R., Quakenbush L., Whiting A., Lowry L. & Harwood L. 2016. Genetic profiling links changing sea-ice to shifting beluga whale migration patterns. Biology Letters 12, 20160404, doi: 10.1098/rsbl.2016.0404.


O’Corry-Crowe G.M., Suydam R., Quakenbush L., Smith T.G., Lydersen C., Kovacs K.M., Orr J., Harwood L., Litovka D. & Ferrer T. 2020. Group structure and kinship in beluga whale societies. Scientific Reports 10, 11462, doi: 10.1038/s41598-020-67314-w.


O’Corry-Crowe G.M., Suydam R.S., Rosenberg A., Frost K.J. & Dizon A.E. 1997. Phylogeography, population structure and dispersal patterns of the beluga whale Delphinapterus leucas in the western Nearctic revealed by mitochondrial DNA. Molecular Ecology 6, 955–970, doi: 10.1046/j.1365-294X.1997.00267.x.


Orbach D.N., Kelly D.A., Solano M. & Brennan P.L.R. 2017. Genital interaction during simulated copulation among marine mammals. Proceedings of the Royal Society B 284, article no. 20171265, doi: 10.1098/rspb.2017.1265.


Orbach D.N., Packard J.M., Keener W., Ziltener A. & Würsig B. 2019. Testes size, vaginal complexity, and behavior in toothed whales (odontocetes): arms race or tradeoff model for dusky dolphins (Lagenorhynchus obscurus), harbor porpoises (Phocoena phocoena), and bottlenose dolphins (Tursiops spp.)? Journal of Comparative Psychology 133, article no. 359, doi: 10.1037/com0000162.


Orbach D.N., Packard J.M., Kirchner T. & Würsig B. 2015. Evasive behaviours of female dusky dolphins (Lagenorhynchus obscurus) during exploitative scramble competition. Behaviour 152, 1953–1977, doi: 10.1163/1568539X-00003310.


Puente A.E. & Dewsbury D.A. 1976. Courtship and copulatory behavior of bottlenose dolphins (Tursiops truncatus). Cetology 21, 1–9.


Quader S. 2005. Mate choice and its implications for conservation and management. Current Science 89, 1220–1229.


R Core Team 2020. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.


Richard J.T., Robeck T.R., Osborn S.D., Naples L., McDermott A., LaForge R., Romano T.A. & Sartini B.L. 2017. Testosterone and progesterone concentrations in blow samples are biologically relevant in belugas (Delphinapterus leucas). General and Comparative Endocrinology 246, 183–193, doi: 10.1016/j.ygcen.2016.12.006.


Richard J.T., Schmitt T., Haulena M., Vezzi N., Dunn J.L., Romano T.A. & Sartini B.L. 2017. Seasonal variation in testes size and density detected in belugas (Delphinapterus leucas) using ultrasonography. Journal of Mammalogy 98, 874–884, doi: 10.1093/jmammal/gyx032.


Richard J.T., Schultz K., Goertz C., Hobbs R., Romano T.A. & Sartini B.L. 2017. Assessing the quantity and downstream performance of DNA isolated from beluga (Delphinapterus leucas) blow samples. Aquatic Mammals 43, 398–408, doi: 10.1578/AM.43.4.2017.398.


Robeck T.R., Monfort S.L., Calle P.P., Dunn J.L., Jensen E., Boehm J.R., Young S. & Clark S.T. 2005. Reproduction, growth and development in captive beluga (Delphinapterus leucas). Zoo Biology 24, 29–49, doi: 10.1002/zoo.20037.


Robeck T.R., Schneyer A.L., McBain J.F., Dalton L.M., Walsh M.T., Czekala N.M. & Kraemer D.C. 1993. Analysis of urinary immunoreactive steroid metabolites and gonadotropins for characterization of the estrous cycle, breeding period, and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biology 12, 173–187, doi: 10.1002/zoo.1430120204.


Robeck T.R., Steinman K.J., Yoshioka M., Jensen E., O’Brien J.K., Katsumata E., Gili C., McBain J.F., Sweeney J. & Monfort S.L. 2005. Estrous cycle characterization and artificial insemination using frozen-thawed spermatozoa in the bottlenose dolphin (Tursiops truncatus). Reproduction 129, 659–674, doi: 10.1530/rep.1.00516.


Schaeff C.M. 2007. Courtship and mating behavior. In D.L. Miller (ed.): Reproductive biology and phylogeny of Cetacea: whales, dolphins, and porpoises. Pp. 349–370. Enfield, NH: Science Publishers.


Schroeder J.P. & Keller K.V. 1989. Seasonality of serum testosterone levels and sperm density in Tursiops truncatus. The Journal of Experimental Zoology 249, 316–321, doi: 10.1002/jez.1402490310.


Scott E.M., Mann J., Watson-Capps J.J., Sargeant B.L. & Connor R.C. 2004. Aggression in bottlenose dolphins: evidence for sexual coercion, male–male competition, and female tolerance through analysis of tooth-rake marks and behaviour. Behaviour 142, 21–44, doi: 10.1163/1568539053627712.


Soulsbury C.D. 2010. Ovulation mode modifies paternity monopolization in mammals. Biology Letters 6, 39–41, doi: 10.1098/rsbl.2009.0703.


Soulsbury C.D. & Iossa G. 2010. The impact of ovulation mode on sperm quantity and quality in mammals. Evolutionary Ecology 24, 879–889, doi: 10.1007/s10682-009-9344-y.


Steinman K.J., O’Brien J.K., Monfort S.L. & Robeck T.R. 2012. Characterization of the estrous cycle in female beluga (Delphinapterus leucas) using urinary endocrine monitoring and transabdominal ultrasound: evidence of facultative induced ovulation. General and Comparative Endocrinology 175, 389–397, doi: 10.1016/j.ygcen.2011.11.008.


Wade P.R., Reeves R.R. & Mesnick S.L. 2012. Social and behavioral factors in cetacean responses to overexploitation: are odontocetes less “resilient” than mysticetes? Journal of Marine Biology 2012(2), article no. 567276, doi: 10.1155/2012/567276.


Wells R.S. 1984. Reproductive behavior and hormonal correlates in Hawaiian spinner dolphins, Stenella longirostris. Reports to the International Whaling Commission Special Issue 6, 465–472.


Werth A.J. & Ford T.J. Jr. 2012. Abdominal fat pads act as control surfaces in lieu of dorsal fins in the beluga (Delphinapterus). Marine Mammal Science 28, 516–527, doi: 10.1111/j.1748-7692.2012.00567.x.


Wingfield J.C., Hegner R.E., Dufty A.M. Jr. & Ball G.F. 1990. The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. The American Naturalist 136, 829–846, doi: 10.1086/285134.


Wu H., Hao Y., Yu X., Xian Y., Zhao Q., Chen D., Kuang X., Kou Z., Feng K., Gong W. & Wang D. 2010. Variation in sexual behaviors in a group of captive male Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis): motivated by physiological changes? Theriorgenology 74, 1467–1475, doi: 10.1016/j.theriogenology.2010.06.018.
Published
2021-07-26
How to Cite
Richard J. T., Levine R., Romano T. A., & Sartini B. L. (2021). Minimally invasive physiological correlates of social behaviour in belugas (<em>Delphinapterus leucas</em&gt;) under human care. Polar Research, 40(S1). https://doi.org/10.33265/polar.v40.5504

Most read articles by the same author(s)