Relationship between the female attendance pattern and pup growth rate in the South American sea lion (Carnivora)




Otaria flavescens, Otaria byronia, pup growth rate, lactating female, milk composition, diving, foraging trip


Changes in the duration and frequency of foraging trips by female otariids may result in changes in the duration and frequency of lactation bouts and hence influence pup growth rate, unless females modify milk energy density and/or the total amount of milk delivered depending on the trip duration. To test this hypothesis on South American sea lions, we measured two attendance pattern components (foraging trip and haul-out duration) and three diving behaviour components of nursing females (dive time, bottom time and number of dives per h) at two different rookeries in Uruguay and Argentina, the composition and energy density of their milk, and the growth rate of their pups. Female foraging trip and haul-out durations depended on pup sex and weight, whereas milk energy density depended on female body mass and foraging trip durations. By contrast, the three dive variables were independent of female body mass or pup sex. Pup growth was also independent of the foraging trip and haul-out duration, with pup sex as the only significant variable. This suggests that individual differences in female foraging behaviour play a minor role in determining pup growth rates during the first three weeks after birth.


Download data is not yet available.


Acha E.M., Mianzan H., Guerrero R., et al. 2008. An overview of physical and ecological processes in the Rio de la Plata Estuary. Cont. Shelf Res. 28: 1579-1588.

Arnould J.P.Y., Boyd I.L. 1995. Temporal patterns of milk production in Antarctic fur seal (Arctocephalus gazella). J. Zool. 237: 1-12.

Arnould J.P.Y., Hindell M.A. 1999. The composition of Australian fur seal (Arctocephalus pusillus doriferus) milk throughout lactation. Physiol. Biochem. Zool. 72: 605-612. PMid:10521328

Arnould J.P.Y., Boyd I.L., Speakman J.R. 1996. The relationship between foraging behaviour and energy expenditure in Antarctic fur seals. J. Zool. 239: 769-782.

Barbano D.M., Clark J.L., Chapman E.D., et al. 1990. Kjeldahl method for determination of total nitrogen content of milk: Collaborative study. J. Assoc. Off. Anal. Chem. 73: 849-859.

Blake R. 1983. Energetics of leaping in dolphins and other aquatic animals. J. Mar. Biol. Assoc. UK 63: 61-70.

Bligh E.G., Dyer W.J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917. PMid:13671378

Bolker B.M. 2008. Ecological models and data in R. Princeton University Press, Princeton, 408 pp.

Boyd I.L., Arnould J.P.Y., Barton T., et al. 1994. Foraging behaviour of Antarctic fur seals during periods of contrasting prey abundance. J. Anim. Ecol. 63: 703-713.

Campagna C., Bisioli C., Quintana F., et al. 1992. Group breeding in sea lions: pups survive better in colonies. Anim. Behav. 43: 541-548.

Campagna C., Werner R., Karesh W., et al. 2001. Movements and locations at sea of South American sea lions (Otaria flavescens). J. Zool. 257: 205-220.

Cappozzo H.L., Perrin W.P. 2009. South American sea lion (Otaria flavescens). In: Perrin W.F., Würsing B., Thewissen J.G.M. (eds), Encyclopedia of Marine Mammals (2nd ed.). Academic Press, pp. 1076-1079.

Cappozzo H.L., Campagna C., Monserrat J. 1991. Sexual dimorphism in newborn Southern sea lions. Mar. Mamm. Sci. 7: 385-394.

Cassini M.H., Fernández-Juricic E. 2003. Costs and benefits of joining South American sea lion breeding groups: testing the assumptions of a model of female breeding dispersion. Can. J. Zool. 81: 1154-1160.

Clutton-Brock T. 1991. The evolution of parental care. Princeton University Press, Princeton 368 pp.

Costa D.P. 2008. A conceptual model of the variation in parental attendance in response to environmental fluctuation: Foraging energetics of lactating sea lions and fur seals. Aquatic Conserv.: Mar. Freshw. Ecosyst. 17: S44-S52.

Costa D.P., Gales N.J. 2000. Foraging energetics and diving behavior of lactating New Zealand sea lions, Phocarctos hookeri. J. Exp. Biol. 203: 3655-3665.

Davies N.B., Krebs J.R., West S.A. 2012. An introduction to behavioural ecology. Wiley-Blackwell Oxford. 520 pp. Delignette-Muller M.L., Dutang C. 2015. Fitdistrplus: an R package for fitting distributions. J. Stat. Softw. 64: 1-34.

Dormann C.F., Elith J., Bacher S., et al. 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36: 27-46.

Drago M., Crespo E.A., Aguilar A., et al. 2009. Historic diet change of the South American sea lion in Patagonia as revealed by isotopic analysis. Mar. Ecol. Prog. Ser. 384: 273- 286.

Drago M., Cardona L., Aguilar A., et al. 2010a. Diet of lactating South American sea lions, as inferred from stable isotopes, influences pup growth. Mar. Mamm. Sci. 26: 309-323.

Drago M., Cardona L., Crespo E.A., et al. 2010b. Change in the foraging strategy of female South American sea lions (Carnivora: Pinnipedia) after parturition. Sci. Mar. 74: 589-598.

Drago M., Cardona L., Garc.a N., et al. 2011. Influence of colony size on pup fitness and survival in South American sea lions. Mar. Mamm. Sci. 27: 167-181.

Drago M., Franco-Trecu V., Cardona L., et al. 2015. Diet-to-female and female-to-pup isotopic discrimination in South American sea lions. Rapid Commun. Mass Spectrom. 29: 1513-1520. PMid:26212166

Eisert R., Oftedal O.T., Barrell G.K. 2013. Milk composition in the Weddell seal (Leptonychotes weddellii): Evidence for a functional role of milk sugar in pinnipeds. Physiol. Biochem. Zool. 86: 159-175. PMid:23434776

Franco-Trecu V. 2015. T.cticas comportamentales de forrajeo y apareamiento y din.mica poblacional de dos especies de ot.ridos simp.tricas con tendencias poblacionales contrastantes. Ph.D. thesis, Universidad de la Rep.blica, Montevideo, 237 pp.

Franco-Trecu V., Drago M., Riet-Sapriza F.G., et al. 2013. Bias in diet determination: Incorporating traditional methods in Bayesian mixing models. PLoS One 8: e80019. PMid:24224031 PMCid:PMC3818279

Franco-Trecu V., Drago M., Balad.n C., et al. 2015. Postharvesting population dynamics of the South American sea lion (Otaria byronia) in the southwestern Atlantic. Mar. Mamm. Sci. 31: 963-978.

Franco-Trecu V., Szephegyi M.N., Do.o F., et al. 2019. Marine mammal bycatch by the industrial bottom trawl fishery at the R.o de la Plata Estuary and the adjacent Atlantic Ocean. Lat. Am. J. Aquat. Res. 47: 89-101.

Gales N.J., Costa D.P., Kretzmann M. 1996. Proximate composition of Australian sea lion milk throughout the entire supra- annual lactation period. Aust. J. Zool. 44: 651-657.

Gentry R.L. 2009. Eared Seals Otariidae. In: Perrin W.F., Würsing B., Thewissen J.G.M. (eds), Encyclopedia of marine mammals, second edition ed. Academic Press, pp. 339-342.

Gentry R.L., Kooyman G.L. 1986. Fur seals: maternal strategies on land and at sea. Princeton University Press, New Jersey, 312 pp.

Gentry R.L., Costa D.P., Croxall J.P., et al. 1986. Synthesis and conclusion. In: Gentry R.L., Kooyman G.L. (eds), Fur seals: maternal strategies on land and at sea. Princeton University Press, pp. 220-264.

Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308.[0295:MCITSF]2.0.CO;2

Georges J.Y., Groscolas R., Guinet C., et al. 2001. Milking strategy in subantarctic fur seals Arctocephalus tropicalis breeding on Amsterdam Island: evidence from changes in milk composition. Physiol. Biochem. Zool. 74: 548-559. PMid:11436139

Guinet C., Goldsworthy S.D., Robinson S. 1999. Sex differences in mass loss rate and growth efficiency in Antarctic fur seal (Arctocephalus gazella) pups at Macquarie Island. Behav. Ecol. Sociobiol. 46: 157-163.

Higgins L.V., Gass L. 1993. Birth to weaning: parturition, duration of lactation, and attendance cycles of Australian sea lions (Neophoca cinerea). Can. J. Zool. 71: 2047-2055.

Hückst.dt L.A., Tift M.S., Riet-Sapriza F., et al. 2016. Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lion Otaria byronia. J. Exp. Biol. 219: 2320-2330. PMid:27247316

International Dairy Federation. 1987. International Standard IDF 21B:1987 (=ISO 6731:1989). Milk, cream and evaporated milk: determination of total solids content (reference method). International Dairy Federation, Brussels.

Jeanniard du Dot T., Trites A.W., Arnould J.P.Y., et al. 2017. Reproductive success is energetically linked to foraging efficiency in Antarctic fur seals. PLoS ONE 12: e0174001. PMid:28453563 PMCid:PMC5409505

Jeanniard du Dot T., Trites A.W., Arnould J.P.Y., et al. 2018. Trade-offs between foraging efficiency and pup feeding rate of lactating northern fur seals in a declining population. Mar. Ecol. Prog. Ser. 600: 207-222.

Jeglinski J.W.E., Werner C., Robinson P.W., et al. 2012. Age, body mass and environmental variation shape the foraging ontogeny of Galapagos sea lions. Mar. Ecol. Prog. Ser. 453: 279-296.

Katz H., Reisfeld L., Franco-Trecu V. 2018. Chemical immobilization protocols in free-ranging South American fur seal (Arctocephalus australis) and adult female South American sea lion (Otaria byronia). Mar. Mamm. Sci. 35: 327-335.

Kleiber M. 1975. The fire of life. Krieger Publishing Co. Inc., New York.

Koen-Alonso M., Crespo E.A., Pedraza S.N. 2000. Food habits of the South American sea lion, Otaria flavescens, off Patagonia, Argentina. Fish. Bull. 98: 250-263.

Kretzmann M.B., Costa D.P., Higgins L.V., et al. 1991. Milk composition of Australian sea lions, Neophoca cinerea: variability in lipid content. Can. J. Zool. 69: 2556-2561.

Lavigne D.M., Stewart R.E.A., Fletcher F. 1982. Changes in composition and energy content of harp seal milk during lactation. Physiol. Zool. 55: 1-9.

Lunn N.J., Boyd I.L., Croxall J.P. 1994. Reproductive performance of female Antarctic fur seals: The influence of age, breeding experience, environmental variation and individual quality. J. Anim. Ecol. 63: 827-840.

Luque S.P. 2007. Diving behaviour analysis in R. R News 7: 8-14.

McHuron E.A., Robinson P.W., Simmons S.E., et al. 2016. Foraging strategies of a generalist marine predator inhabiting a dynamic environment. Oecologia 182: 995-1005. PMid:27651228

Miloslavich P., Klein E., J.M., et al. 2011. Marine biodiversity in the Atlantic and Pacific coasts of South America: knowledge and gaps. PLoS One 6: e14631. PMid:21304960 PMCid:PMC3031619

NASA. 2018. Moderate-resolution imaging spectroradiometer (MODIS) aqua chlorophyll data; 2018 reprocessing. NASA OB.DAAC, Greenbelt, MD, USA.

Oftedal O.T., Boness D.J., Tedman R.A. 1987. The behavior, physiology, and anatomy of lactation in the pinnipedia. In: Genoways H.H. (ed), Current Mammalogy. Plenum Publishing Corporation, pp. 175-245.

Oftedal O.T., Boness D.J., Bowen W.D. 1988. The composition of hooded seal (Cystophora cristata) milk: an adaptation for postnatal fattening. Can. J. Zool. 66: 318-322.

Oftedal O.T., Eisert R., Barrell G.K. 2014. Comparison of analytical and predictive methods for water, protein, fat, sugar, and gross energy in marine mammal milk. J. Dairy Sci. 97: 4713-4732. PMid:24931527

R Core Team. 2018. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.

Reid K., Forcada J. 2005. Causes of offspring mortality in the Antarctic fur seal, Arctocephalus gazella: the interaction of density dependence and ecosystem variability. Can. J. Zool. 83: 604-609.

Riedman M., Ortiz C.L. 1979. Changes in milk composition during lactation in the northern elephant seal. Physiol. Zool. 52: 240-249.

Riet-Sapriza F.G., Costa D.P., Franco-Trecu V., et al. 2013. Foraging behavior of lactating South American sea lions, Otaria flavescens and spatial-resource overlap with the Uruguayan fisheries. Deep Sea Res. II 88-89: 106-119.

Rivas A.L., Dogliotti A.I., Gagliardini D.A. 2006. Seasonal variability in satellite-measured surface chlorophyll in the patagonian shelf. Cont. Shelf Res. 26: 703−720.

Robinson P.W., Villegas-Amtmann S., Costa D.P. 2009. Field validation of an inexpensive time-depth recorder. Mar. Mamm. Sci. 25: 199-205.

Rodriguez D.H., Dassis M., de Leon A.P., et al. 2013. Foraging strategies of Southern sea lion females in the La Plata River Estuary (Argentina-Uruguay). Deep Sea Res. II 88-89: 120-130.

Schielzeth H. 2010. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 1: 103-113.

Schulz T.M., Bowen W.D. 2004. Pinniped lactation strategies: evaluation of data on maternal and offspring life history traits. Mar. Mamm. Sci. 20: 86-114.

Soto K.H., Trites A.W., Arias-Schreiber M. 2004. The effects of prey availability on pup mortality and the timing of birth of South American sea lions (Otaria flavescens) in Peru. J. Zool. 264: 419-428.

Soto K.H., Trites A.W., Arias-Schreiber M. 2006. Changes in diet and maternal attendance of South American sea lions indicate changes in the marine environment and prey abundance. Mar. Ecol. Prog. Ser. 312: 277-290.

Tremblay Y., Cherel Y. 2003. Geographic variation in the foraging behaviour, diet and chick growth of rockhopper penguins. Mar. Ecol. Prog. Ser. 251: 279-297.

Trillmich F., Limberger D. 1985. Drastic effects of El Ni.o on Galapagos ecuador pinnipeds. Oecologia 67: 19-22. PMid:28309839

Webber M.A. 2014. Family Otariidae (Eared seals). In: Wilson D.E., Mittermeier R.A. (eds), Handbook of the mammals of the world. Lynx Ediciones, pp. 34-101.

Werner R., Figueroa-Carranza A., Ortiz C.L. 1996. Composition and energy content of milk from southern sea lions (Otaria flavescens). Mar. Mamm. Sci. 12: 313-317.

Williams T. 2001. Intermittent swimming by mammals: a strategy for increasing energetic efficiency during diving. Am. Zool. 41: 166-176.



How to Cite

Drago M, Cardona L, Franco-Trecu V, Riet-Sapriza FG, Crespo EA, García N, Inchausti P. Relationship between the female attendance pattern and pup growth rate in the South American sea lion (Carnivora). Sci. mar. [Internet]. 2021Jun.11 [cited 2024Apr.15];85(2):81-90. Available from:




Funding data

Most read articles by the same author(s)