Breaking the fast: first report of dives and ingestion events in molting southern elephant seals.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
08 Jan 2024
Historique:
received: 12 04 2023
accepted: 18 12 2023
medline: 9 1 2024
pubmed: 9 1 2024
entrez: 8 1 2024
Statut: epublish

Résumé

Southern elephant seals (SES) experience a 'catastrophic molt', a costly event characterized by the renewal of both hair and epidermis that requires high peripheral vascular circulation. Molting animals are therefore constrained by high metabolic heat loss and are thought to fast and remain on land. To examine the ability of individuals to balance the energetic constraints of molting on land we investigate the stomach temperature and movement patterns of molting female SES. We find that 79% of females swam and 61% ingested water or prey items, despite the cost of cold-water exposure while molting. This behavior was related to periods of warm and low wind conditions, and females that dived and ingested more often, lost less body mass. We conclude that the paradigm of fasting during the molt in this species, and the fitness consequences of this behavior should be reconsidered, especially in the context of a changing climate.

Identifiants

pubmed: 38191678
doi: 10.1038/s42003-023-05720-2
pii: 10.1038/s42003-023-05720-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

64

Informations de copyright

© 2024. The Author(s).

Références

Schmidt-Nielsen, K. How Animals Work (Cambridge University Press, 1972).
Bourlière, F. & Schmidt-Nielsen, K. Animal Physiology-Adaptation and Environment. London, Cambridge University Press, 1975. Rev. Écol. 29, 490–491 (1975).
Ling, J. K. Pelage and molting in wild mammals with special reference to aquatic forms. Q. Rev. Biol. 45, 16–54 (1970).
pubmed: 5446769 doi: 10.1086/406361
Beltran, R. S., Burns, J. M. & Breed, G. A. Convergence of biannual moulting strategies across birds and mammals. Proc. R. Soc. B Biol. Sci. 285, 20180318 (2018).
doi: 10.1098/rspb.2018.0318
Zimova, M. et al. Function and underlying mechanisms of seasonal colour moulting in mammals and birds: what keeps them changing in a warming world? Biol. Rev. 93, 1478–1498 (2018).
pubmed: 29504224 doi: 10.1111/brv.12405
Kjellén, N. Moult in relation to migration in birds-a review. Ornis Svec. 4, 1–24 (1994).
doi: 10.34080/os.v4.23028
Hellebuyck, T., Pasmans, F., Haesebrouck, F. & Martel, A. Dermatological diseases in lizards. Vet. J. 193, 38–45 (2012).
pubmed: 22417690 doi: 10.1016/j.tvjl.2012.02.001
Wheler, C. Skin diseases of exotic pets. Can. Vet. J. 48, 432 (2007).
pmcid: 1831508
Newton, I. Moult and plumage. Ringing Migr. 24, 220–226 (2009).
Ruppert, E. E., Fox, R. S. & Barnes, R. D. Invertebrate Zoology: A Functional Evolutionary Approach (Thomson-Brooks/Cole, 2004).
Valdez, D. J. & Benitez-Vieyra, S. M. Annual molt period and seasonal color variation in the Eared Dove´s crown. PLoS ONE 18, e0280819 (2023).
pubmed: 36827341 pmcid: 9955656 doi: 10.1371/journal.pone.0280819
Maurel, D., Coutant, C., Boissin-Agasse, L. & Boissin, J. Seasonal moulting patterns in three fur bearing mammals: the European badger (Meles meles L.), the red fox (Vulpes vulpes L.), and the mink (Mustela vison). A morphological and histological study. Can. J. Zool. 64, 1757–1764 (1986).
doi: 10.1139/z86-265
Zuberogoitia, I., Zabala-Albizua, J. & Martínez, J. Moult in birds of prey: a review of current knowledge and future challenges for research. Ardeola 65, 183–213 (2018).
Ashwell-Erickson, S., Fay, F. H., Elsner, R. & Wartzok, D. Metabolic and hormonal correlates of molting and regeneration of pelage in Alaskan harbor and spotted seals (Phoca vitulina and Phoca largha). Can. J. Zool. 64, 1086–1094 (1986).
doi: 10.1139/z86-163
Walcott, S. M., Kirkham, A. L. & Burns, J. M. Thermoregulatory costs in molting Antarctic Weddell seals: impacts of physiological and environmental conditions. Conserv. Physiol. 8, coaa022 (2020).
pubmed: 32274067 pmcid: 7125049 doi: 10.1093/conphys/coaa022
Thometz, N. M. et al. Maintaining control: metabolism of molting Arctic seals in water and when hauled out. J. Exp. Biol. 226, jeb244862 (2023).
pubmed: 36576033 doi: 10.1242/jeb.244862
Le Boeuf, B. J., Blackwell, S. B., Morris, P. A. & Thorson, P. H. Sex differences in diving and foraging behaviour of northern elephant seals. Mar. Mamm. Adv. Behav. Popul. Biol. https://doi.org/10.1093/oso/9780198540694.003.0009 (1993).
Kooyman, G., Hunke, E., Ackley, S., Van Dam, R. & Robertson, G. Moult of the emperor penguin: travel, location, and habitat selection. Mar. Ecol. Prog. Ser. 204, 269–277 (2000).
doi: 10.3354/meps204269
Feltz, E. T. & Fay, F. H. Thermal requirements in vitro of epidermal cells from seals. Cryobiology 3, 261–264 (1966).
pubmed: 5970349 doi: 10.1016/S0011-2240(66)80020-2
Kuhn, C. E., Crocker, D. E., Tremblay, Y. & Costa, D. P. Time to eat: measurements of feeding behaviour in a large marine predator, the northern elephant seal Mirounga angustirostris. J. Anim. Ecol. 78, 513–523 (2009).
pubmed: 19040681 doi: 10.1111/j.1365-2656.2008.01509.x
Scholander, P. F., Walters, V., Hock, R. & Irving, L. Body insulation of some arctic and tropical mammals and birds. Biol. Bull. 99, 225–236 (1950).
pubmed: 14791421 doi: 10.2307/1538740
Worthy, Ga. J., Morris, P. A., Costa, D. P. & Le Boeuf, B. J. Moult energetics of the northern elephant seal (Mirounga angustirostris). J. Zool. 227, 257–265 (1992).
doi: 10.1111/j.1469-7998.1992.tb04821.x
Nadel, E. R. Energy exchanges in water. Undersea Biomed. Res. 11, 149–158 (1984).
pubmed: 6485144
Paterson, W. D. et al. Increased metabolic rate of hauled-out harbor seals (Phoca vitulina) during the molt. Physiol. Biochem. Zool. 94, 152–161 (2021).
pubmed: 33710938 doi: 10.1086/713958
Perrin, W. F., Würsig, B. & Thewissen, J. G. M. Encyclopedia of Marine Mammals (Academic Press, 2009).
Read, A. J. An introduction to marine mammal biology and conservation by E. C. M. Parsons Mar. Mammal Sci. 29, 239–240 (2013).
Atkinson, S., Becker, B. L., Johanos, T. C., Pietraszek, J. R. & Kuhn, B. C. S. Reproductive morphology and status of female Hawaiian monk seals (Monachus schauinslandi) fatally injured by adult male seals. Reproduction 100, 225–230 (1994).
doi: 10.1530/jrf.0.1000225
Badosa, E., Pastor, T., Gazo, M. & Aguilar, A. Moult in the Mediterranean monk seal from Cap Blanc, western Sahara. Afr. Zool. 41, 183–192 (2006).
doi: 10.1080/15627020.2006.11407354
Slip, D. J., Gales, N. J. & Burton, H. R. Body-mass loss, utilization of blubber and fat, and energetic requirements of male southern elephant seals, Mirounga leonina, during the molting fast. Aust. J. Zool. 40, 235–243 (1992).
doi: 10.1071/ZO9920235
Beck, C. A., Bowen, W. D. & Iverson, S. J. Sex differences in the seasonal patterns of energy storage and expenditure in a phocid seal. J. Anim. Ecol. 72, 280–291 (2003).
doi: 10.1046/j.1365-2656.2003.00704.x
Boyd, I., Arnbom, T. & Fedak, M. Water flux, body composition, and metabolic rate during molt in female southern elephant seals (Mirounga leonina). Physiol. Zool. 66, 43–60 (1993).
doi: 10.1086/physzool.66.1.30158286
Carlini, A. R., Marquez, M. E. I., Daneri, G. A. & Poljak, S. Mass changes during their annual cycle in females of southern elephant seals at King George Island. Polar Biol. 21, 234–239 (1999).
doi: 10.1007/s003000050358
Liwanag, H. E. M., Berta, A., Costa, D. P., Abney, M. & Williams, T. M. Morphological and thermal properties of mammalian insulation: the evolution of fur for aquatic living. Biol. J. Linn. Soc. 106, 926–939 (2012).
doi: 10.1111/j.1095-8312.2012.01900.x
Testut, L., Woppelmann, G., Simon, B. & Téchiné, P. The sea level at Port-aux-Français, Kerguelen Island, from 1949 to the present. Ocean Dyn. 56, 464–472 (2006).
doi: 10.1007/s10236-005-0056-8
Chaise, L. L. et al. Local weather and body condition influence habitat use and movements on land of molting female southern elephant seals (Mirounga leonina). Ecol. Evol. 8, 6081–6090 (2018).
pubmed: 29988430 pmcid: 6024128 doi: 10.1002/ece3.4049
Chaise, L. L. et al. Environmental and physiological determinants of huddling behavior of molting female southern elephant seals (Mirounga leonina). Physiol. Behav. 199, 182–190 (2019).
pubmed: 30385351 doi: 10.1016/j.physbeh.2018.10.016
Guinet, C., Roux, J. P., Bonnet, M. & Mison, V. Effect of body size, body mass, and body condition on reproduction of female South African fur seals (Arctocephalus pusillus) in Namibia. Can. J. Zool. 76, 1418–1424 (1998).
doi: 10.1139/z98-082
Crocker, D., Williams, J., Costa, D. & Le Boeuf, B. Maternal traits and reproductive effort in northern elephant seals. Ecology 82, 3541–3555 (2001).
doi: 10.1890/0012-9658(2001)082[3541:MTAREI]2.0.CO;2
Sato, K., Tsuchiya, Y., Kudoh, S. & Naito, Y. Meteorological factors affecting the number of Weddell seals hauling-out on the ice during the molting season at Syowa Station, East Antarctica. Polar Biosci. 16, (2003).
Wilson, R., Cooper, J. & Plotz, Joachim, J. Can we determine when marine endotherms feed? A case study of seabirds. J. Exp. Biol. 167, 267–275 (1992).
Charrassin, J.-B. et al. Feeding behaviour of free-ranging penguins determined by oesophageal temperature. Proc. Biol. Sci. 268, 151–157 (2001).
pubmed: 11209884 pmcid: 1088584 doi: 10.1098/rspb.2000.1343
Pütz, K. et al. Foraging strategy of king penguins (aptenodytes Patagonicus) during summer at the Crozet Islands. Ecology 79, 1905–1921 (1998).
doi: 10.1890/0012-9658(1998)079[1905:FSOKPA]2.0.CO;2
Catry, P., Phillips, R. A., Phalan, B., Silk, J. R. D. & Croxall, J. P. Foraging strategies of grey-headed albatrosses Thalassarche chrysostoma: integration of movements, activity and feeding events. Mar. Ecol. Prog. Ser. 280, 261–273 (2004).
doi: 10.3354/meps280261
Kuhn, C. E. & Costa, D. P. Identifying and quantifying prey consumption using stomach temperature change in pinnipeds. J. Exp. Biol. 209, 4524–4532 (2006).
pubmed: 17079722 doi: 10.1242/jeb.02530
Carlini, A. R. et al. Lactation costs in southern elephant seals at King George Island, South Shetland Islands. Polar Biol. 27, 266–276 (2004).
doi: 10.1007/s00300-003-0584-y
Enstipp, M. R., Grémillet, D. & Jones, D. R. The effects of depth, temperature and food ingestion on the foraging energetics of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). J. Exp. Biol. 209, 845–859 (2006).
pubmed: 16481574 doi: 10.1242/jeb.02064
Adams, N. J. & Brown, C. R. in Penguin Biology (eds Davis, L. J. & Darby, J. T.) 297–315 (Elsevier, 1990).
Guillemette, M., Pelletier, D., Grandbois, J.-M. & Butler, P. J. Flightlessness and the energetic cost of wing molt in a large sea duck. Ecology 88, 2936–2945 (2007).
pubmed: 18051662 doi: 10.1890/06-1751.1
Ankney, C. D. Does the wing molt cause nutritional stress in lesser snow geese? Auk 96, 68–72 (1979).
Stout, B. E. & Cooke, F. Timing and location of wing molt in horned, red-necked and Western Grebes in North America. Waterbirds 26, 88–93 (2003).
doi: 10.1675/1524-4695(2003)026[0088:TALOWM]2.0.CO;2
Hindell, M., Slip, D. & Burton, H. The diving behavior of adult male and female southern elephant seals, Mirounga leonina (Pinnipedia, Phocidae). Aust. J. Zool. 39, 595–619 (1991).
doi: 10.1071/ZO9910595
McConnell, B., Fedak, M., Burton, H. R., Engelhard, G. H. & Reijnders, P. J. H. Movements and foraging areas of naive, recently weaned southern elephant seal pups. J. Anim. Ecol. 71, 65–78 (2002).
doi: 10.1046/j.0021-8790.2001.00576.x
Campagna, C., Fedak, M. & McConnell, B. Post-breeding distribution and diving behavior of adult male southern elephant seals from Patagonia. J. Mammal. 80, 1341–1352 (1999).
doi: 10.2307/1383185
McIntyre, T. et al. A lifetime at depth: vertical distribution of southern elephant seals in the water column. Polar Biol. 33, 1037–1048 (2010).
doi: 10.1007/s00300-010-0782-3
Le Boeuf, B. J. & Laws, R. M. in Elephant Seals (eds Le Boeuf, B. J. & Laws, R. M.) 1–26 (University of California Press, 1994).
Carlini, A. R. et al. Food consumption estimates of southern elephant seal females during their post-breeding aquatic phase at King George Island. Polar Biol. 28, 769–775 (2005).
doi: 10.1007/s00300-005-0004-6
Baird, R. W., Hanson, M. B. & Dill, L. M. Factors influencing the diving behaviour of fish-eating killer whales: sex differences and diel and interannual variation in diving rates. Can. J. Zool. 83, 257–267 (2005).
doi: 10.1139/z05-007
Horsburgh, J. M., Morrice, M., Lea, M. & Hindell, M. A. Determining feeding events and prey encounter rates in a southern elephant seal: a method using swim speed and stomach temperature. Mar. Mammal. Sci. 24, 207–217 (2008).
doi: 10.1111/j.1748-7692.2007.00156.x
Chaise, L. L. et al. Implantation of subcutaneous heart rate data loggers in southern elephant seals (Mirounga leonina). Polar Biol. 40, 2307–2312 (2017).
doi: 10.1007/s00300-017-2144-x
Kingma, B., Frijns, A. & van Marken Lichtenbelt, W. The thermoneutral zone: implications for metabolic studies. Front. Biosci. (Elite Ed.) 4, 1975–1985 (2012).
pubmed: 22202013 doi: 10.2741/e518
Hansen, P. J. Effects of heat stress on mammalian reproduction. Philos. Trans. R. Soc. B Biol. Sci. 364, 3341–3350 (2009).
doi: 10.1098/rstb.2009.0131
Alsharif, I. Comprehensive exploration of the molecular response, clinical signs, and histological aspects of heat stress in animals. J. Therm. Biol. 110, 103346 (2022).
pubmed: 36462855 doi: 10.1016/j.jtherbio.2022.103346
Ortiz, C. L., Costa, D. & Le Boeuf, B. J. Water and energy flux in elephant seal pups fasting under natural conditions. Physiol. Zool. https://doi.org/10.1086/physzool.51.2.30157864 (1978).
Costa, D. P., Boeuf, B. J. L., Huntley, A. C. & Ortiz, C. L. The energetics of lactation in the Northern elephant seal, Mirounga angustirostris. J. Zool. 209, 21–33 (1986).
doi: 10.1111/j.1469-7998.1986.tb03563.x
Codde, S. A., Allen, S. G., Houser, D. S. & Crocker, D. E. Effects of environmental variables on surface temperature of breeding adult female northern elephant seals, Mirounga angustirostris, and pups. J. Therm. Biol. 61, 98–105 (2016).
pubmed: 27712667 doi: 10.1016/j.jtherbio.2016.09.001
Campagna, C. & Le Boeuf, B. J. Thermoregulatory behaviour of southern sea lions and its effect on mating strategies. Behaviour 107, 72–90 (1988).
doi: 10.1163/156853988X00205
Twiss, S. et al. Behavioral evidence of thermal stress from overheating in UK breeding gray seals. Mar. Mammal. Sci. 18, 455–468 (2002).
doi: 10.1111/j.1748-7692.2002.tb01048.x
Mauck, B., Bilgmann, K., Jones, D. D., Eysel, U. & Dehnhardt, G. Thermal windows on the trunk of hauled-out seals: hot spots for thermoregulatory evaporation? J. Exp. Biol. 206, 1727–1738 (2003).
pubmed: 12682104 doi: 10.1242/jeb.00348
Ryg, M., Lydersen, C., Markussen, N. H., Smith, T. G. & Øritsland, N. A. Estimating the blubber content of phocid seals. Can. J. Fish. Aquat. Sci. 47, 1223–1227 (1990).
doi: 10.1139/f90-142
Slip, D., Burton, H. & Gales, N. Determining blubber mass in the southern elephant seal, Mirounga leonina, by ultrasonic and isotopic techniques. Aust. J. Zool. 40, 143 (1992).
doi: 10.1071/ZO9920143
Mellish, J., Nienaber, J., Polasek, L. & Horning, M. Beneath the surface: profiling blubber depth in pinnipeds with infrared imaging. J. Therm. Biol. 38, 10–13 (2013).
pubmed: 24229798 doi: 10.1016/j.jtherbio.2012.09.003
de Kock, L., Oosthuizen, W. C., Beltran, R. S., Bester, M. N. & de Bruyn, P. J. N. Determinants of moult haulout phenology and duration in southern elephant seals. Sci. Rep. 11, 13331 (2021).
pubmed: 34172785 pmcid: 8233432 doi: 10.1038/s41598-021-92635-9
Wilson, R. P. et al. Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J. Exp. Biol. 198, 1115–1135 (1995).
pubmed: 9318941 doi: 10.1242/jeb.198.5.1115
Rembauville, M. et al. Plankton assemblage estimated with BGC-Argo floats in the Southern Ocean: implications for seasonal successions and particle export. J. Geophys. Res. (Oceans) 122, 8278–8292 (2017).
doi: 10.1002/2017JC013067
Lubcker, N. et al. Low trophic level diet of juvenile southern elephant seals Mirounga leonina from Marion Island: a stable isotope investigation using vibrissal regrowths. Mar. Ecol. Prog. Ser. 577, 237–250 (2017).
doi: 10.3354/meps12240
Orgeret, F., Cox, S. L., Weimerskirch, H. & Guinet, C. Body condition influences ontogeny of foraging behavior in juvenile southern elephant seals. Ecol. Evol. 9, 223–236 (2019).
pubmed: 30680109 doi: 10.1002/ece3.4717
Walters, A. et al. Spatially explicit estimates of prey consumption reveal a new krill predator in the Southern Ocean. PLoS ONE 9, e86452 (2014).
pubmed: 24516515 pmcid: 3905967 doi: 10.1371/journal.pone.0086452
Lawson, G. L. et al. Development of an animal-borne “sonar tag” for quantifying prey availability: test deployments on northern elephant seals. Anim. Biotelemetry 3, 22 (2015).
doi: 10.1186/s40317-015-0054-7
Goulet, P., Guinet, C., Swift, R., Madsen, P. T. & Johnson, M. A miniature biomimetic sonar and movement tag to study the biotic environment and predator-prey interactions in aquatic animals. Deep Sea Res. Part I Oceanogr. Res. Pap. 148, 1–11 (2019).
doi: 10.1016/j.dsr.2019.04.007
Adachi, T. et al. Forced into an ecological corner: round-the-clock deep foraging on small prey by elephant seals. Sci. Adv. 7, eabg3628 (2021).
pubmed: 33980496 pmcid: 8115928 doi: 10.1126/sciadv.abg3628
Gille, S. T. Warming of the Southern Ocean since the 1950s. Science 295, 1275–1277 (2002).
pubmed: 11847337 doi: 10.1126/science.1065863
McMahon, C. R., Burton, H., McLean, S., Slip, D. & Bester, M. Field immobilisation of southern elephant seals with intravenous tiletamine and zolazepam. Vet. Rec. 146, 251–254 (2000).
pubmed: 10737295 doi: 10.1136/vr.146.9.251
Sauvé, C. C., Van de Walle, J., Hammill, M. O., Arnould, J. P. Y. & Beauplet, G. Stomach temperature records reveal nursing behaviour and transition to solid food consumption in an unweaned mammal, the harbour seal pup (Phoca vitulina). PLoS ONE 9, e90329 (2014).
pubmed: 24587327 pmcid: 3936010 doi: 10.1371/journal.pone.0090329
Payne, E. H., Gebregziabher, M., Hardin, J. W., Ramakrishnan, V. & Egede, L. E. An empirical approach to determine a threshold for assessing overdispersion in Poisson and negative binomial models for count data. Commun. Stat. Simul. Comput. 47, 1722–1738 (2018).
pubmed: 30555205 pmcid: 6290908 doi: 10.1080/03610918.2017.1323223
Charlanne, L. M. Rcode_Breaking_the_fast. zenodo https://doi.org/10.5281/zenodo.10400487 (2023).

Auteurs

Laura M Charlanne (LM)

Université de Strasbourg, CNRS, IPHC UMR 7178, F-67000, Strasbourg, France. laura.charlanne@iphc.cnrs.fr.

Laureline Chaise (L)

Hex·Data, 847 Route de Frans, 69400, Villefranche-sur-Saône, France.

Damien Sornette (D)

Hex·Data, 847 Route de Frans, 69400, Villefranche-sur-Saône, France.

Erwan Piot (E)

CNRS UMR5536, Université de Bordeaux, 33076, Bordeaux, France.
UMR 7179, CNRS/MNHN, Laboratoire MECADEV, 1 avenue du petit château, 91400, Brunoy, France.

Dominic J McCafferty (DJ)

Scottish Centre for Ecology and the Natural Environment, School of Biodiversity, One Health and Veterinary Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

André Ancel (A)

Université de Strasbourg, CNRS, IPHC UMR 7178, F-67000, Strasbourg, France.

Caroline Gilbert (C)

UMR 7179, CNRS/MNHN, Laboratoire MECADEV, 1 avenue du petit château, 91400, Brunoy, France.
Ecole Nationale Vétérinaire d'Alfort, 7 avenue du Général de Gaulle, 94704, Maisons-Alfort, France.

Classifications MeSH