Breath-hold capacities and circadian dive rhythmicity shape optimal foraging strategies in a polar marine mammal, the Weddell seal (Leptonychotes weddellii).
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
29 Oct 2024
29 Oct 2024
Historique:
received:
08
02
2024
accepted:
07
10
2024
medline:
30
10
2024
pubmed:
30
10
2024
entrez:
30
10
2024
Statut:
epublish
Résumé
Air-breathing vertebrates must balance their response to diel shifts in prey accessibility with physiological thresholds and the need to surface after each dive. Weddell seal (Leptonychotes weddellii) dive behaviors were tracked across the year under rapidly-changing light regimes in the Ross Sea, Antarctica ( ~ 75-77°S). This provides a 'natural experiment' with free-living seals experiencing 24-hrs of light (Polar Day), light/dark cycling, and continuous darkness (Polar Night). The Weddell seal's temporal niche switches from nocturnal diving in the summer to diurnality for the remainder of the year. Rhythmicity in dive efforts (depth, duration, post-dive surface recuperation, bottom time, and exceeding physiologic thresholds) is stronger and more closely circadian during times of the year with light/dark cycling compared with Polar Day or Night. With light/dark cycling, animals also make the most extreme dives (those that far exceed the calculated aerobic dive limit, cADL) significantly earlier than solar noon. Offsetting the longest dives that require longer surface recuperation times from mid-day allows animals to maximize total dive time under high-light conditions conducive for visual hunting. We identify an optimal foraging strategy to exploit a diel preyscape in a highly-seasonal environment, while balancing tradeoffs imposed by physiological thresholds in a diving mammal.
Identifiants
pubmed: 39472475
doi: 10.1038/s42003-024-07029-0
pii: 10.1038/s42003-024-07029-0
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1394Subventions
Organisme : National Science Foundation (NSF)
ID : ANT-1853377
Organisme : National Science Foundation (NSF)
ID : ANT-0838937
Organisme : National Science Foundation (NSF)
ID : ANT-0838892
Informations de copyright
© 2024. The Author(s).
Références
Heithaus, M. R. & Frid, A. Optimal diving under the risk of predation. J. Theor. Biol. 223, 79–92 (2003).
pubmed: 12782118
doi: 10.1016/S0022-5193(03)00073-0
Stephens, D. W. & Krebs, J. R. Foraging Theory, Vol. 1 (Princeton Univ. Press, 1986).
Williams, C. T., Barnes, B. M. & Buck, C. L. Persistence, entrainment, and function of circadian rhythms in polar vertebrates. Physiology 30, 86–96 (2015).
pubmed: 25729054
doi: 10.1152/physiol.00045.2014
Boulos, Z., Macchi, M. & Terman, M. Twilight transitions promote circadian entrainment to lengthening light-dark cycles. Am. J. Physiol. Regul. Integr. Comp. Physiol. 271, R813–R818 (1996).
doi: 10.1152/ajpregu.1996.271.3.R813
Karplus, M. Bird activity in the continuous daylight of arctic summer. Ecology 33, 129–134 (1952).
doi: 10.2307/1931264
Swade, R. H. & Pittendrigh, C. S. Circadian locomotor rhythms of rodents in the Arctic. Am. Nat. 101, 431–466 (1967).
doi: 10.1086/282510
van Oort, B. E. H. et al. Circadian organization in reindeer. Nature 438, 1095–1096 (2005).
pubmed: 16371996
doi: 10.1038/4381095a
Wojczulanis-Jakubas, K., Wąż, P. & Jakubas, D. Little auks under the midnight sun: diel activity rhythm of a small diving seabird during the Arctic summer. Polar Res. https://doi.org/10.33265/polar.v39.3309 (2020).
Huffeldt, N. P. & Merkel, F. R. Sex-specific, inverted rhythms of breeding-site attendance in an Arctic seabird. Biol. Lett. 12, 20160289 (2016).
pubmed: 27651530
pmcid: 5046920
doi: 10.1098/rsbl.2016.0289
Gomes, A., Pereira, J. & Bugoni, L. Age-specific diving and foraging behavior of the Great Grebe (Podicephorus major). Waterbirds 32, 149–156 (2009).
doi: 10.1675/063.032.0118
Arnold, W. et al. Circadian rhythmicity persists through the Polar night and midnight sun in Svalbard reindeer. Sci. Rep. 8, 1–12 (2018).
doi: 10.1038/s41598-018-32778-4
Cullen, J. M. The diurnal rhythm of birds in the Arctic summer. Ibis 96, 31–46 (1954).
doi: 10.1111/j.1474-919X.1954.tb04109.x
Folk, G. E., Thrift, D. L., Zimmerman, M. B. & Reimann, P. C. Mammalian activity – rest rhythms in Arctic continuous daylight. Biol. Rhythm Res. 37, 455–469 (2006).
doi: 10.1080/09291010600738551
Ware, J. V. et al. The clock keeps ticking: circadian rhythms of free-ranging polar bears. J. Biol. Rhythms 35, 180–194 (2020).
pubmed: 31975640
doi: 10.1177/0748730419900877
Brierley, A. S. Diel vertical migration. Curr. Biol. 24, R1074–R1076 (2014).
pubmed: 25458213
doi: 10.1016/j.cub.2014.08.054
Benoit, D., Simard, Y., Gagné, J., Geoffroy, M. & Fortier, L. From polar night to midnight sun: photoperiod, seal predation, and the diel vertical migrations of polar cod (Boreogadus saida) under landfast ice in the Arctic Ocean. Polar Biol. 33, 1505–1520 (2010).
doi: 10.1007/s00300-010-0840-x
Bollens, S. M., Rollwagen-Bollens, G., Quenette, J. A. & Bochdansky, A. B. Cascading migrations and implications for vertical fluxes in pelagic ecosystems. J. Plankton Res. 33, 349–355 (2010).
doi: 10.1093/plankt/fbq152
Houston, A. I. Energetic constraints and foraging efficiency. Behav. Ecol. 6, 393–396 (1995).
doi: 10.1093/beheco/6.4.393
Houston, A. I. & Carbone, C. The optimal allocation of time during the diving cycle. Behav. Ecol. 3, 255–265 (1992).
doi: 10.1093/beheco/3.3.255
Kooyman, G. L. Weddell Seal: Consummate Diver (Cambridge Univ. Press, 1981).
Kooyman, G. L. Diverse Divers: Physiology and Behavior (Springer-Verlag, 1989).
Burns, J. M., Lestyk, K. C., Folkow, L. P., Hammill, M. O. & Blix, A. S. Size and distribution of oxygen stores in harp and hooded seals from birth to maturity. J. Comp. Physiol. B 177, 687–700 (2007).
pubmed: 17576570
doi: 10.1007/s00360-007-0167-2
Kooyman, G. L., Castellini, M. A., Davis, R. W. & Maue, R. A. Aerobic diving limits of immature Weddell seals. J. Comp. Physiol. 151, 171–174 (1983).
doi: 10.1007/BF00689915
Kooyman, G. L., Wahrenbrock, E. A., Castellini, M. A., Davis, R. W. & Sinnett, E. E. Aerobic and anaerobic metabolism during voluntary diving in Weddell seals: evidence of preferred pathways from blood chemistry and behavior. J. Comp. Physiol. 138, 335–346 (1980).
doi: 10.1007/BF00691568
Thompson, D. & Fedak, M. A. How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim. Behav. 61, 287–296 (2001).
doi: 10.1006/anbe.2000.1539
Stephenson, R. Physiological control of diving behaviour in the Weddell seal Leptonychotes weddelli: a model based on cardiorespiratory control theory. J. Exp. Biol. 208, 1971–1991 (2005).
pubmed: 15879077
doi: 10.1242/jeb.01583
Burns, J. M. et al. Winter habitat use and foraging behavior of crabeater seals along the Western Antarctic Peninsula. Deep Sea Res. Part II Topical Stud. Oceanogr. 51, 2279–2303 (2004).
doi: 10.1016/j.dsr2.2004.07.021
Bennett, K. A., McConnell, B. J. & Fedak, M. A. Diurnal and seasonal variations in the duration and depth of the longest dives in southern elephant seals (Mirounga leonina): possible physiological and behavioural constraints. J. Exp. Biol. 204, 649–662 (2001).
pubmed: 11171347
doi: 10.1242/jeb.204.4.649
Shero, M. R., Goetz, K. T., Costa, D. P. & Burns, J. M. Temporal changes in Weddell seal dive behavior over winter: are females increasing foraging effort to support gestation? Ecol. Evol. 8, 11857–11874 (2018).
pubmed: 30598782
pmcid: 6303723
doi: 10.1002/ece3.4643
Goetz, K. T. et al. Seasonal habitat preference and foraging behaviour of post-moult Weddell seals in the western Ross Sea. R. Soc. Open Sci. 10, 220500 (2023).
pubmed: 36704255
pmcid: 9874274
doi: 10.1098/rsos.220500
Hindell, M. A., Slip, D. J., Burton, H. R. & Bryden, M. M. Physiological implications of continuous, prolonged, and deep dives of the southern elephant seal (Mirounga leonina). Can. J. Zool. 70, 370–379 (1992).
doi: 10.1139/z92-055
Shero, M. R. & Burns, J. M. in Ethology and Behavioral Ecology of Phocids (eds Daniel P. Costa & Elizabeth A. McHuron) 481–515 (Springer Int. Pub., 2022).
Heerah, K. et al. Ecology of Weddell seals during winter: Influence of environmental parameters on their foraging behaviour. Deep Sea Res. Part II Top. Stud. Oceanogr. 88-89, 23–33 (2013).
doi: 10.1016/j.dsr2.2012.08.025
Williams, T. M. The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J. Exp. Biol. 207, 973–982 (2004).
pubmed: 14766956
doi: 10.1242/jeb.00822
Boehme, L. et al. Bimodal winter haul-out patterns of adult Weddell seals (Leptonychotes weddellii) in the Southern Weddell Sea. PLoS ONE 11, e0155817 (2016).
pubmed: 27196097
pmcid: 4873014
doi: 10.1371/journal.pone.0155817
Kronfeld-Schor, N. & Dayan, T. Partitioning of time as an ecological resource. Annu. Rev. Ecol. Evol. Syst. 34, 153–181 (2003).
doi: 10.1146/annurev.ecolsys.34.011802.132435
Sánchez-vázquez, F. J., Azzaydi, M., Martínez, F. J., Zamora, S. & Madrid, J. A. Annual rhythms of demand-feeding activity in sea bass: evidence of a seasonal phase inversion of the diel feeding pattern. Chronobiol. Int. 15, 607–622 (1998).
pubmed: 9844749
doi: 10.3109/07420529808993197
Cisewski, B., Strass, V. H., Rhein, M. & Krägefsky, S. Seasonal variation of diel vertical migration of zooplankton from ADCP backscatter time series data in the Lazarev Sea, Antarctica. Deep Sea Res. Part I Oceanogr. Res. Pap. 57, 78–94 (2010).
doi: 10.1016/j.dsr.2009.10.005
Picco, P., Schiano, M. E., Pensieri, S. & Bozzano, R. Time-frequency analysis of migrating zooplankton in the Terra Nova Bay polynya (Ross Sea, Antarctica). J. Mar. Syst. 166, 172–183 (2017).
doi: 10.1016/j.jmarsys.2016.07.010
Fuiman, L., Davis, R. & Williams, T. Behavior of midwater fishes under the Antarctic ice: observations by a predator. Mar. Biol. 140, 815–822 (2002).
doi: 10.1007/s00227-001-0752-y
Smith, M. S. R. Studies on the Weddell seal (Leptonychotes weddelli lesson) in McMurdo Sound Antarctica. PhD in Zoology thesis, University of Canterbury (1966).
Shero, M. R., Kirkham, A. L., Costa, D. P. & Burns, J. M. Iron mobilization during lactation reduces oxygen stores in a diving mammal. Nat. Commun. 13, 4322 (2022).
pubmed: 35918323
pmcid: 9345918
doi: 10.1038/s41467-022-31863-7
Beltran, R. S. et al. Seasonal resource pulses and the foraging depth of a Southern Ocean top predator. Proc. R. Soc. B Biol. Sci. 288, 20202817 (2021).
doi: 10.1098/rspb.2020.2817
Walcott, S. M., Kirkham, A. L. & Burns, J. M. Thermoregulatory costs in molting Antarctic Weddell seals: impacts of physiological and environmental conditions: themed issue article: conservation of Southern Hemisphere mammals in a changing world. Conserv. Physiol. 8, coaa022 (2020).
pubmed: 32274067
pmcid: 7125049
doi: 10.1093/conphys/coaa022
Lake, S. E., Burton, H. R. & Hindell, M. A. Influence of time of day and month on Weddell seal haul-out patterns at the Vestfold Hills, Antarctica. Polar Biol. 18, 319–324 (1997).
doi: 10.1007/s003000050194
Boyd, I. L. Time and energy constraints in pinniped lactation. Am. Nat. 152, 717–728 (1998).
pubmed: 18811346
doi: 10.1086/286202
Last, KimS., Hobbs, L., Berge, J., Brierley, AndrewS. & Cottier, F. Moonlight drives ocean-scale mass vertical migration of zooplankton during the Arctic Winter. Curr. Biol. 26, 244–251 (2016).
pubmed: 26774785
doi: 10.1016/j.cub.2015.11.038
Bailey, S. M., Udoh, U. S. & Young, M. E. Circadian regulation of metabolism. J. Endocrinol. 222, R75–R96 (2014).
pubmed: 24928941
pmcid: 4109003
doi: 10.1530/JOE-14-0200
Barrell, G. K. & Montgomery, G. W. Absence of circadian patterns of secretion of melatonin or cortisol in Weddell seals under continuous natural daylight. J. Endocrinol. 122, 445–449 (1989).
pubmed: 2769165
doi: 10.1677/joe.0.1220445
Griffiths, D. J., Bryden, M. M. & Kennaway, D. J. A fluctuation in plasma melatonin level in the Weddell seal during constant natural light. J. Pineal Res. 3, 127–134 (1986).
pubmed: 3723326
doi: 10.1111/j.1600-079X.1986.tb00735.x
Huffeldt, N. P. Photic barriers to poleward range-shifts. Trends Ecol. Evol. 35, 652–655 (2020).
pubmed: 32473743
doi: 10.1016/j.tree.2020.04.011
Aschoff, J. Exogenous and endogenous components in circadian rhythms. In Cold Spring Harb. Symp. Quant. Biol. 11–28 (Cold Spring Harbor Laboratory Press, 1960).
Roenneberg, T. & Foster, R. G. Twilight times: light and the circadian system. Photochem. Photobiol. 66, 549–561 (1997).
pubmed: 9383985
doi: 10.1111/j.1751-1097.1997.tb03188.x
Davis, R. W. et al. Hunting behavior of a marine mammal beneath the Antarctic fast ice. Science 283, 993–996 (1999).
pubmed: 9974394
doi: 10.1126/science.283.5404.993
Mass, A. M. & Supin, A. Y. Adaptive features of aquatic mammals’ eye. Anat. Rec. 290, 701–715 (2007).
doi: 10.1002/ar.20529
Smith, W. O. et al. Spatial and temporal variations in variable fluoresence in the Ross Sea (Antarctica): oceanographic correlates and bloom dynamics. Deep Sea Res. Part I Oceanogr. Res. Pap. 79, 141–155 (2013).
doi: 10.1016/j.dsr.2013.05.002
O’Driscoll, R. L., Macaulay, G. J., Gauthier, S., Pinkerton, M. & Hanchet, S. Distribution, abundance and acoustic properties of Antarctic silverfish (Pleuragramma antarcticum) in the Ross Sea. Deep Sea Res. Part II Top. Stud. Oceanogr. 58, 181–195 (2011).
doi: 10.1016/j.dsr2.2010.05.018
Fuiman, L. A., Williams, T. M. & Davis, R. W. Homing tactics of Weddell seals in the Antarctic fast-ice environment. Mar. Biol. 167, 116 (2020).
doi: 10.1007/s00227-020-03730-w
Castellini, M. A., Davis, R. W. & Kooyman, G. L. Blood chemistry regulation during repetitive diving in Weddell seals. Physiol. Zool. 61, 379–386 (1988).
doi: 10.1086/physzool.61.5.30161259
Costa, D. P. & Favilla, A. B. Field physiology in the aquatic realm: ecological energetics and diving behavior provide context for elucidating patterns and deviations. J. Exp. Biol. 226, jeb245832 (2023).
pubmed: 37843467
doi: 10.1242/jeb.245832
Hassrick, J. L. et al. Condition and mass impact oxygen stores and dive duration in adult females northern elephant seals. J. Exp. Biol. 213, 585–582 (2010).
pubmed: 20118309
doi: 10.1242/jeb.037168
Tyack, P. L., Johnson, M., Soto, N. A., Sturlese, A. & Madsen, P. T. Extreme diving of beaked whales. J. Exp. Biol. 209, 4238–4253 (2006).
pubmed: 17050839
doi: 10.1242/jeb.02505
Burns, J. M. The development of diving behavior in juvenile Weddell seals: pushing physiological limits in order to survive. Can. J. Zool. 77, 737–747 (1999).
doi: 10.1139/z99-022
Kramer, D. L. The behavioral ecology of air breathing by aquatic animals. Can. J. Zool. 66, 89–94 (1988).
doi: 10.1139/z88-012
Fuiman, L. A., Madden, K. M., Williams, T. M. & Davis, R. W. Structure of foraging dives by Weddell seals at an offshore isolated hole in the Antarctic fast ice environment. Deep Sea Res. II 54, 270–289 (2007).
doi: 10.1016/j.dsr2.2006.11.011
Ponganis, P. J. & Stockard, T. K. The Antarctic toothfish: how common a prey for Weddell seals? Antarct. Sci. 19, 441–442 (2007).
doi: 10.1017/S0954102007000715
Lenky, C., Eisert, R., Oftedal, O. T. & Metcalf, V. Proximate composition and energy density of nototheniid and myctophid fish in McMurdo Sound and the Ross Sea, Antarctica. Polar Biol. 35, 717–724 (2012).
doi: 10.1007/s00300-011-1116-9
Schreer, J. F. & Testa, J. W. Classification of Weddell seal diving behavior. Mar. Mamm. Sci. 12, 227–250 (1996).
doi: 10.1111/j.1748-7692.1996.tb00573.x
Shero, M. R., Costa, D. P. & Burns, J. M. Scaling matters: incorporating body composition into Weddell seal seasonal oxygen store comparisons reveals maintenance of aerobic capacities. J. Comp. Physiol. B 185, 811–824 (2015).
pubmed: 26164426
doi: 10.1007/s00360-015-0922-8
Castellini, M. A., Kooyman, G. L. & Ponganis, P. J. Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J. Exp. Biol. 165, 181–194 (1992).
pubmed: 1588250
doi: 10.1242/jeb.165.1.181
Sparling, C. E. & Fedak, M. A. Metabolic rates of captive grey seals during voluntary diving. J. Exp. Biol. 207, 1615–1624 (2004).
pubmed: 15073194
doi: 10.1242/jeb.00952
Shero, M. R., Krotz, R. T., Costa, D. P., Avery, J. P. & Burns, J. M. How do overwinter changes in body condition and hormone profiles influence Weddell seal reproductive success? Funct. Ecol. 29, 1278–1291 (2015).
doi: 10.1111/1365-2435.12434
Beltran, R. S., Kirkham, A. L., Breed, G. A., Testa, J. W. & Burns, J. M. Reproductive success delays moult phenology in a polar mammal. Sci. Rep. 9, 5221 (2019).
pubmed: 30914781
pmcid: 6435649
doi: 10.1038/s41598-019-41635-x
Fedak, M. A., Lovell, P., McConnell, B. J. & Hunter, C. Overcoming the constraints of long range radio telemetry from animals: Getting more useful data from smaller packages. Integr. Comp. Biol. 42, 3–10 (2002).
pubmed: 21708689
doi: 10.1093/icb/42.1.3
Castellini, M. A. & Kooyman, G. L. Length, girth and mass relationships in Weddell seals (Leptonychotes weddellii). Mar. Mamm. Sci. 6, 75–77 (1990).
doi: 10.1111/j.1748-7692.1990.tb00227.x
Foldager, N. & Blomqvist, C. G. Repeated plasma volume determination with the Evans blue dye dilution technique: the method and the computer program. Comput. Biol. Med. 21, 35–41 (1991).
pubmed: 2044359
doi: 10.1016/0010-4825(91)90033-6
El-Sayed, H., Goodall, S. R. & Hainsworth, F. R. Re-evaluation of Evans blue dye dilution method of plasma volume measurement. Clin. Lab. Haem. 17, 189–194 (1995).
Reynafarje, B. Simplified method for the determination of myoglobin. J. Lab. Clin. Med. 61, 138–145 (1963).
pubmed: 13981912
Prewitt, J. S., Freistroffer, D. V., Schreer, J. F., Hammill, M. O. & Burns, J. M. Postnatal development of muscle biochemistry in nursing harbor seal (Phoca vitulina) pups: limitations to diving behavior? J. Comp. Physiol. B 180, 757–766 (2010).
pubmed: 20140678
doi: 10.1007/s00360-010-0448-z
Davis, R. W. & Kanatous, S. B. Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J. Exp. Biol. 202, 1091–1113 (1999).
pubmed: 10101108
doi: 10.1242/jeb.202.9.1091
Shero, M. R., Pearson, L. E., Costa, D. P. & Burns, J. M. Improving the precision of our ecosystem calipers: a modified morphometric technique for estimating marine mammal mass and body composition. PLoS ONE 9, e91233 (2014).
pubmed: 24614685
pmcid: 3948782
doi: 10.1371/journal.pone.0091233
Williams, T. M., Fuiman, L. A., Horning, M. & Davis, R. W. The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J. Exp. Biol. 207, 973–982 (2004).
pubmed: 14766956
doi: 10.1242/jeb.00822
Kleiber, M. The Fire of Life: An Introduction to Animal Energetics. (R. E. Krieger Pub. Co., 1975).
Schreer, J. F., Kovacs, K. M. & O’Hara Hines, R. J. Comparative diving pattern of pinnipeds and seabirds. Ecol. Monogr. 71, 137–162 (2001).
doi: 10.1890/0012-9615(2001)071[0137:CDPOPA]2.0.CO;2
Thieurmel, B. & Elmarhraoui, A. Package ‘suncalc’: Compute sun position, sunlight phases, moon position and lunar phase. R package v. 0.5.1 (2022).
Ruf, T. The Lomb-Scargle periodogram in biological rhythm research: analysis of incomplete and unequally spaced time-series. Biol. Rhythm Res. 30, 178–201 (1999).
doi: 10.1076/brhm.30.2.178.1422
Sokolove, P. G. & Bushell, W. N. The chi square periodogram: Its utility for analysis of circadian rhythms. J. Theor. Biol. 72, 131–160 (1978).
pubmed: 566361
doi: 10.1016/0022-5193(78)90022-X
VanderPlas, J. T. Understanding the Lomb–Scargle Periodogram. Astrophys. J. Suppl. Ser. 236, 16 (2018).
doi: 10.3847/1538-4365/aab766
Baluev, R. V. Assessing the statistical significance of periodogram peaks. Mon. Not. R. Astron. Soc. 385, 1279–1285 (2008).
doi: 10.1111/j.1365-2966.2008.12689.x
Costa, D. P. Weddell seals as a utonomous sensors of the winter oceanography of the Ross Sea. U.S. Antarct. Program (USAP) Data Center https://doi.org/10.15784/600025 (2014).
Shero, M. Weddell seal dive behavior and rhythmicity from 2010-2012 in the Ross Sea. U.S. Antarctic Program (USAP) Data Center https://doi.org/10.15784/601835 (2024).