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

INTRODUCTION

Parental care is the main component of the reproductive cost in birds and female mammals, and offspring survival is expected to be more strongly influenced by parent foraging efficiency than breeding periodicity or clutch/litter size (Clutton-Brock 1991Clutton-Brock T. 1991. The evolution of parental care. Princeton University Press, Princeton 368 pp. https://doi.org/10.1515/9780691206981 , Davies et al. 2012Davies N.B., Krebs J.R., West S.A. 2012. An introduction to behavioural ecology. Wiley-Blackwell Oxford. 520 pp). For mammalian females, lactation is the most energetically demanding activity during the breeding cycle, even more than gestation (Gales et al. 1996Gales 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. https://doi.org/10.1071/ZO9960651 , Higgins and Gass 1993Higgins 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. https://doi.org/10.1139/z93-290 ). As a consequence, the foraging efficiency of females is expected to have a major impact on pup growth and survival at weaning (Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 , Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 ). In land-breeding marine mammals such as otariids (eared seals), lactating females behave as central place-foragers, alternating feeding trips to sea with suckling bouts on land during the long lactation, which can be upwards of a year for some species (Schulz and Bowen 2004Schulz 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. https://doi.org/10.1111/j.1748-7692.2004.tb01142.x ). Generally, otariids inhabit continental margins with high primary productivity, likely to satisfy the energy requirements during key foraging periods with high energy demand (Gentry 2009Gentry 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. https://doi.org/10.1016/B978-0-12-373553-9.00083-3 , Webber 2014Webber 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).

The growth rate of otariid pups depends largely on three major maternal care components: the balance between the length of the foraging trips and that of the suckling haul-outs (i.e. the maternal attendance pattern), the amount of milk delivered to the pup, and the quality of the milk delivered (Gentry et al. 1986Gentry 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. https://doi.org/10.1515/9781400854691 , Georges et al. 2001Georges 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. https://doi.org/10.1086/322164 , Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 ). Females can modify their behaviour in different ways to promote the growth rate of their pups according to food availability; consequently, pup growth rate should reflect the foraging tactic adopted by the mother (Gentry et al. 1986Gentry 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. https://doi.org/10.1515/9781400854691 ). The length of foraging trips depends on the distance to foraging grounds, as well as on prey availability, individual foraging efficiency and pup age, the latter considered as a factor that affects the pup fasting ability (Boyd et al. 1994Boyd 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. https://doi.org/10.2307/5235 , Costa 2008Costa 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. https://doi.org/10.1002/aqc.917 , McHuron et al. 2016McHuron 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. https://doi.org/10.1007/s00442-016-3732-0 ). In general, females spend proportionally more time ashore nursing their pups when foraging trip duration is shorter (Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 , Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 , McHuron et al. 2016McHuron 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. https://doi.org/10.1007/s00442-016-3732-0 ), which has been reported to result in faster pup growth rates (Gentry and Kooyman 1986Gentry R.L., Kooyman G.L. 1986. Fur seals: maternal strategies on land and at sea. Princeton University Press, New Jersey, 312 pp. https://doi.org/10.1515/9781400854691 , Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 , Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 ). However, females involved in long foraging trips targeting richer foraging grounds may balance a lower attendance frequency by increasing milk fat content or total milk delivery (Arnould and Boyd 1995Arnould J.P.Y., Boyd I.L. 1995. Temporal patterns of milk production in Antarctic fur seal (Arctocephalus gazella). J. Zool. 237: 1-12. https://doi.org/10.1111/j.1469-7998.1995.tb02741.x , Arnould and Hindell 1999Arnould 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. https://doi.org/10.1086/316702 ), which may explain the positive correlation between the length of foraging trips and the pup absolute mass gain reported in some studies (Guinet et al. 1999Guinet 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. https://doi.org/10.1007/s002650050605 ).

The South American sea lion (Otaria flavescens) inhabits the coasts of South America, and its 3500 km range in the southwestern Atlantic spans from warm temperate Uruguay to sub-Antarctic Tierra del Fuego (Cappozzo and Perrin 2009Cappozzo 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. https://doi.org/10.1016/B978-0-12-373553-9.00244-3 ). Previous research has revealed that the growth and survival of South American sea lion pups are influenced by colony size (Campagna et al. 1992Campagna C., Bisioli C., Quintana F., et al. 1992. Group breeding in sea lions: pups survive better in colonies. Anim. Behav. 43: 541-548. https://doi.org/10.1016/S0003-3472(05)81014-0 , Drago et al. 2011Drago M., Cardona L., García N., et al. 2011. Influence of colony size on pup fitness and survival in South American sea lions. Mar. Mamm. Sci. 27: 167-181. https://doi.org/10.1111/j.1748-7692.2010.00402.x ), but little is known about the influence of female foraging behaviour on these parameters. Certainly, foraging trips became longer in Peru during intense El Niño events (Soto et al. 2004Soto 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. https://doi.org/10.1017/S0952836904005965 , 2006Soto 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. https://doi.org/10.3354/meps312277 ), and some components of diving behaviour influence the rate of energy expenditure in other otariid females (Arnould et al. 1996Arnould 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. https://doi.org/10.1111/j.1469-7998.1996.tb05477.x , Costa and Gales 2000Costa 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), but little is known about the effect of individual variability in foraging behaviour on pup growth rate (McHuron et al. 2016McHuron 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. https://doi.org/10.1007/s00442-016-3732-0 ). In this paper we assessed female body mass and quantified two variables of the maternal attendance pattern (duration of the foraging trips and haul-outs) and three variables of diving behaviour (dive time, bottom time and dives per h) to determine their effect on milk energy density and pup growth rate in the western South Atlantic, hypothesizing that longer and more frequent female foraging trips reduce the duration and frequency of lactation bouts and the growth of pups.

MATERIALS AND METHODS

Study area and sample collection

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Sampling was performed during the 2009 and 2015 breeding season (January-February) at Isla de Lobos (Uruguay) and Isla Arce (Argentina), respectively (Fig. 1). Both islands are located ~9 km from the mainland, in two areas differing greatly in marine primary productivity (Acha et al. 2008Acha 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. https://doi.org/10.1016/j.csr.2007.01.031 , Miloslavich et al. 2011Miloslavich P., Klein E., Díaz J.M., et al. 2011. Marine biodiversity in the Atlantic and Pacific coasts of South America: knowledge and gaps. PLoS One 6: e14631. https://doi.org/10.1371/journal.pone.0014631 , Rivas et al. 2006Rivas 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. https://doi.org/10.1016/j.csr.2006.01.013 ), which is higher around Isla de Lobos than around Isla Arce (Fig. 1). Isla de Lobos, with an area of 0.41 km², supports about 1200 sea lions (Franco-Trecu 2015Franco-Trecu V. 2015. Tácticas comportamentales de forrajeo y apareamiento y dinámica poblacional de dos especies de otáridos simpátricas con tendencias poblacionales contrastantes. Ph.D. thesis, Universidad de la República, Montevideo, 237 pp) and Isla Arce, with an area of 0.45 km², supports about 900 (Crespo EA unpublished data). However, samples were collected from two reproductive areas containing a total of 180 and 150 individuals of both sexes and all development stages (pup, young, subadult and adult) for Isla de Lobos and Isla Arce, respectively.

Fig. 1.  Location of South American sea lion breeding colonies studied in Uruguay (Isla de Lobos) and Argentina (Isla Arce) and the annual average values of chlorophyll-a concentration in the 2009 (left panel) and 2015 (right panel) sampling years (NASA 2018NASA. 2018. Moderate-resolution imaging spectroradiometer (MODIS) aqua chlorophyll data; 2018 reprocessing. NASA OB.DAAC, Greenbelt, MD, USA).

On both islands, lactating sea lion females and their pups were captured during the second and third week of January, when females resumed feeding after parturition. We used hoop nets to randomly capture 10 lactating females in Uruguay and 12 in Argentina, along with their 13 (±2) day-old suckling pups (Uruguay, 4 males and 6 females; Argentina, 4 males and 8 females). The age of pups (Table 1) was known because many pups were captured and bleach-marked at birth for another study. Pups were placed in a jute bag and weighed using a 50 kg (±0.1 kg) capacity digital scale, sexed, tagged and then released on the colony. All the females captured in Uruguay were sedated using isoflurane gas mixed with oxygen (0.5-2.5%) administered by a portable-field vaporizer (see Riet-Sapriza et al. 2013Riet-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. https://doi.org/10.1016/j.dsr2.2012.09.005 ), whereas all the females captured in Argentina were placed into a cage and sedated using a combination of midazolam 5% (a benzodiazepine with sedative or tranquilizing action) and dexmedetomidine (a non-narcotic sedative, α2-agonist) administered by intramuscular injection with a dosage of 0.15 to 0.5 mg kg^-1 and 0.003 to 0.005 mg kg^-1, respectively (Drago et al. 2015Drago 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. https://doi.org/10.1002/rcm.7249 , Katz et al. 2018Katz 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. https://doi.org/10.1111/mms.12524 ).

Table 1.  Female body size, milk energy density, pup age, sex and body size, pup specific growth rate (SGR) and descriptors of the foraging and haul-out behaviour of lactating South American sea lion females from breeding colonies in Uruguay (Isla de Lobos) and Argentina (Isla Arce). Superscripts denote females that are heavier than average.

Colony	Female ID	Female weight (kg)	Energy density (kj g-1 wet mass)	Pup age (d)	Pup sex	Pup weight (kg)		Pup SGR (%/d)	Total no. dives recorded	No. dives per h	Dive depth (m)		Dive duration (min)		Bottom time (min)		Foraging trip number	Foraging trip duration (d)	Haul-out duration (d)
						1st capture	2nd capture				Mean±sd	Max	Mean±sd	Max	Mean±sd	Max		Mean±sd	Mean±sd
Argentina	59	86.0	13.8	14	♀	11.9	14.9	0.9	3220	7.2	72±33	111	2.6±1.2	5.3	2.1±1.1	5.2	5	2.7±0.1	1.3±1.3
	64	91.6	11.5	13	♀	12.9	16.4	0.9	3127	6.9	68±33	114	1.8±0.8	3.9	1.0±0.7	3.5	4	2.8±0.3	2.6±2.6
	70	103.4	16.4	11	♀	11.3	14.9	1.1	4040	8.0	60±36	113	1.8±0.9	4.6	1.1±0.7	4.1	5	2.5±0.4	2.1±2.1
	74	98.3	13.7	12	♂	14.6	15.9	0.4	5715	10.2	47±40	113	1.7±1.3	7.0	1.3±1.0	6.8	6	2.6±0.3	1.5±1.5
	76	72.3	12.2	9	♂	12.1	13.3	0.4	4576	9.3	53±34	114	1.6±1.0	4.7	1.0±0.8	4.4	7	1.9±0.7	1.2±1.2
	78	118.31	15.8	12	♀	14.4	18.4	1.0	3270	8.0	62±35	114	2.0±1.1	5.7	1.3±0.9	5.5	5	2.0±0.6	1.7±1.7
	80	111.3	13.2	14	♀	11.9	13.8	0.6	3326	6.6	66±36	116	2.5±1.2	6.0	1.8±1.1	5.3	6	2.1±0.7	1.6±1.6
Mean total		97.3±15.6	13.8±1.8	12±2		12.7±1.3	15.4±1.7	0.8±0.3	25464	8.0 ± 1.3	59±37	116	2.0±1.2	7	1.3 ± 1.0	7	5	2.3±0.6	1.7±0.6
Uruguay	H2	115.61	12.8	14	♀	12.2	16.6	1.9	8807	21.5	23±7	50	1.7±0.5	4.8	0.9±0.4	3.0	10	1.6±0.8	1.5±0.5
	H3	160.21	12.8	15	♀	15.4	20.9	1.9	6332	14.4	17±6	35	2.1±0.8	5.0	1.2±0.7	3.8	11	1.7±0.5	1.2±0.2
	H4	101.8	18.8	17	♀	14.4	16.2	1.7	7824	18.8	18±6	35	1.7±0.6	4.2	1.1±0.5	3.5	26	0.7±0.5	0.7±0.5
	H5	97.6	11.8	12	♀	12.0			7605	16.1	23±8	57	2.1±0.7	4.6	1.3±0.6	4.0	11	1.7±0.8	1.2±0.7
	H6	120.21	15.0	11	♂	15.2	21.3	2.2	9009	19.7	23±8	78	1.7±0.6	4.4	0.8±0.5	3.8	20	0.9±0.7	0.9±0.3
	H7	128.21	18.5	14	♂	18.2	22.5	1.3	10001	16.1	19±6	36	2.1±0.8	5.4	1.2±0.7	4.0	11	2.4±0.8	1.6±0.8
	H10	152.21	17.4	16	♀	15.5			1269	13.9	29±11	55	2.5±0.8	4.8	1.3±0.7	3.5	2	1.9±0.8	2.6
Mean total		125.1±23.7	15.3±2.9	14±2		14.7±2.1	19.5±2.9	1.8±0.3	7264	17.2±2.8	21±8	57	1.9±0.7	5	1.1±0.6	4	13	1.3±0.9	1.1±0.7

Once sedated, each female was weighed with a 300 kg (±0.1 kg) capacity digital scale, measured and fitted with a time-depth recorder (TDR Sensus Ultra by ReefNet Inc., Mississauga, ON, Canada, for the females from Argentina; Mk9 by Wildlife Computers Inc., Redmond, WA, USA, for the females from Uruguay) attached to a neoprene patch that was glued to the fur on the upper back using quick-set epoxy. Sensus Ultra and Mk9 TDRs provide comparable diving records (Jeglinski et al. 2012Jeglinski 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. https://doi.org/10.3354/meps09649 , Robinson et al. 2009Robinson P.W., Villegas-Amtmann S., Costa D.P. 2009. Field validation of an inexpensive time-depth recorder. Mar. Mamm. Sci. 25: 199-205. https://doi.org/10.1111/j.1748-7692.2008.00227.x ) and both types were programmed to sample depth and time every 5 s. The depth resolution and accuracy was 0.5±0.05 m for the Mk9 TDRs and 0.1±0.03 m for the Sensus Ultra TDRs (Jeglinski et al. 2012Jeglinski 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. https://doi.org/10.3354/meps09649 , Riet-Sapriza et al. 2013Riet-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. https://doi.org/10.1016/j.dsr2.2012.09.005 , Robinson et al. 2009Robinson P.W., Villegas-Amtmann S., Costa D.P. 2009. Field validation of an inexpensive time-depth recorder. Mar. Mamm. Sci. 25: 199-205. https://doi.org/10.1111/j.1748-7692.2008.00227.x ).

From each female, we collected ~5 mL of milk from one or more teats to determine its proximate chemical composition and energy density. Although milk energy density has been documented to change within a single attendance cycle depending on how long the female has been ashore (Georges et al. 2001Georges 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. https://doi.org/10.1086/322164 ), we were not able to control for that source of variability. Milk samples were collected by suction using a vacuum pump (20 mL plastic syringe) positioned over the teat or by manual manipulation of the teat surrounding area. Milk collection was facilitated by an intramuscular injection of oxytocin (60 IU/animal) (Oftedal et al. 1988Oftedal 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. https://doi.org/10.1139/z88-047 , Werner et al. 1996Werner 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. https://doi.org/10.1111/j.1748-7692.1996.tb00583.x ), whose effect on milk composition has been deemed negligible (Oftedal et al. 1987Oftedal 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. https://doi.org/10.1007/978-1-4757-9909-5_6 , 1988Oftedal 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. https://doi.org/10.1139/z88-047 ). All milk samples were stored in liquid nitrogen and later in a freezer at -20°C until chemical analysis.

In the second and third week of February, i.e. about 21 (±5) days after first sampling, the pups were opportunistically recaptured (7 from Uruguay and 10 from Argentina) and weighed again to calculate their specific growth rate (SGR). Furthermore, in the same period, we recaptured 7 females from Uruguay and 7 from Argentina to recover the TDRs. In this case, the sedative drug (midazolam 5% and dexmedetomidine) was administered to sea lion females using a dart (3 mL) shot by means of a CO₂ Dan-Inject Rifle (Børkop, Denmark). After sedation, females were restrained with a hoop net to allow the removal of the instruments by cutting through the neoprene mounting patch, leaving behind the epoxy mount that would fall off during moulting. The same procedure was followed in the two colonies.

Growth

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The SGR of pups, expressed as the relative body weight gained or lost per day (%/d), was calculated according to the following equation:

 [1]

where W _t0 is the initial body weight (kg) of the pup, W _t+d is the final body weight (kg) after d days, and d is the number of days between measurements. We choose the SGR because of the big differences in the body mass of males and females at birth (Cappozzo et al. 1991Cappozzo H.L., Campagna C., Monserrat J. 1991. Sexual dimorphism in newborn Southern sea lions. Mar. Mamm. Sci. 7: 385-394. https://doi.org/10.1111/j.1748-7692.1991.tb00113.x , Drago et al. 2011Drago M., Cardona L., García N., et al. 2011. Influence of colony size on pup fitness and survival in South American sea lions. Mar. Mamm. Sci. 27: 167-181. https://doi.org/10.1111/j.1748-7692.2010.00402.x , Franco-Trecu et al. 2015Franco-Trecu V., Drago M., Baladán 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. https://doi.org/10.1111/mms.12197 ).

RESULTS

We collected data from 14 females ranging in body mass from 72.3 to 160.2 kg (Table 1). At first capture, male pups ranged from 12.1 to 18.2 kg and female pups from 11.3 to 15.5 kg. The number of dives per h ranged from 6.6 to 21.5 (Table 1). The average duration of the female foraging trips ranged from 0.7±0.5 to 2.8±0.3 days, and the average of haul-out lasted from 0.7±0.5 to 2.6±2.6 days (Table 1). The average dive time ranged from 1.7±0.6 to 2.6±1.2 minutes and the average bottom time ranged from 0.8±0.5 to 2.1±1.1 minutes. The average duration of the female foraging trips was explained by a model including only pup mass and sex and their interaction (Table 2). It should be noted that the selected model explained 71% of the deviance, although most of the deviance (51%) was explained by the random effect of colony. The pup mass*sex interaction term in the selected model was significant because the weight of female pups had a negligible influence on the average duration of females’ foraging trips, whereas females with heavier male pups were involved in longer foraging trips (Fig. 2).

As above, the best model for explaining average haul-out duration included only pup mass and sex and their interaction (Table 2). The statistically significant interaction term resulted from the opposite relationship between haul-out duration and pup mass for female and male pups (Fig. 2). As above, the random colony effect explained a large part of the total deviance explained by the model (21.6% out of 47%). Dive descriptors (dive time, bottom time and dives per h) were not affected significantly by female body mass or pup sex. The random colony effect did not increase the total deviance explained by dive descriptor models.

The average milk contents, on a wet weigh basis, was 54.8% water, 28.7% lipids, 14.2% proteins, 2.1% ash and 0.3% carbohydrates (Fig. 3). The resulting average energy density was 14.7 kj g^-1, and the model selected to explain the variability of milk energy density across females included female mass, the average duration of foraging trips and their interaction (Table 3). The female mass*trip duration interaction term was significant because larger females produced milk with a higher energy density after long trips, whereas the opposite was true for smaller females (Fig. 4). It should be noted that a single specimen involved in very short foraging trips, but producing high energy milk had a disproportionate impact on the pattern of females with a body mass below the average.

Finally, the only statistically significant model for pup SGR contained only pup sex and showed that the SGR was significantly higher for female pups (Male: mean=1.098 day^-1, Female: mean=1.253 day^-1; p=0.011), with no statistically significant effect of milk energy density, pup mass or the average duration of foraging trips and haul-outs. Again, the random effect of colony substantially increased the deviance explained by the model (33% out of 62%).

DISCUSSION

The results reported here revealed no significant effect of the female attendance pattern on pup growth rate, but a strong effect of pup sex and pup mass on female foraging behaviour. This is because females with male pups were involved in longer foraging trips and longer haul-outs than females with female pups. Furthermore, longer foraging trips resulted in the production of more energetic milk, but only for heavier females. Distribution of heavier females was uneven between colonies, as only one female from Argentina but five from Uruguay were heavier than average. However, pup growth rate was independent of milk energy density or haul-out duration, with male pups growing more slowly than female pups. The overall evidence suggests that, during the first three weeks of the lactation period, female South American sea lions balance the duration of the foraging trips and haul-outs according to the demands of their pups, which probably depend on pup body mass and sex. As a result, pup growth rate is independent of the attendance pattern and the energy density of milk. However, caution is needed, and all the results should be considered as an approximation because of the small sample size.

Longer foraging trips may be due to at least three different reasons: a lower foraging efficiency (Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 ), exploitation of closer patches with low food density (Soto et al. 2006Soto 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. https://doi.org/10.3354/meps312277 ) or targeting more distant foraging grounds with high food density (Jeanniard du Dot et al. 2018Jeanniard 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. https://doi.org/10.3354/meps12638 , McHuron et al. 2016McHuron 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. https://doi.org/10.1007/s00442-016-3732-0 ). Foraging trip durations have been negatively correlated with pup growth rate in the two former scenarios (Gentry and Kooyman 1986Gentry R.L., Kooyman G.L. 1986. Fur seals: maternal strategies on land and at sea. Princeton University Press, New Jersey, 312 pp. https://doi.org/10.1515/9781400854691 , Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 , Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 ), but positively correlated in the third scenario (Arnould and Hindell 1999Arnould 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. https://doi.org/10.1086/316702 , Jeanniard du Dot et al. 2018Jeanniard 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. https://doi.org/10.3354/meps12638 , McHuron et al. 2016McHuron 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. https://doi.org/10.1007/s00442-016-3732-0 ). Nevertheless, access to distant foraging grounds is profitable only for females with high energy reserves, which may explain why in this study longer foraging trips resulted in milk with a higher energy density only for females that are heavier than average. However, we did not satellite track the foraging trips in Isla Arce (Argentina) and hence cannot verify whether females involved in longer foraging trips actually used the highly productive front over the shelf break (Fig. 1).

A longer foraging time resulting from aiming at highly productive but distant foraging grounds results in less frequent haul-outs, which must be compensated with increased milk energy density or total milk delivery. Here we assessed the quality of the milk delivered and the maternal attendance pattern, but not the total amount of milk delivered to the pup. Furthermore, milk energy density can decrease by ~5% throughout a single attendance cycle, depending on how long the female has been ashore and the pups’ age (Georges et al. 2001Georges 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. https://doi.org/10.1086/322164 ). Unfortunately, we collected milk samples opportunistically and hence were unable to control for the stage of the attendance cycle. Nevertheless, female foraging efficiency does not seem to be relevant during the first three weeks of nursing, because no relationship was found in the studied populations between pup growth rate and the attendance pattern. Female foraging efficiency may become more relevant as pups grow and females need to supply them with more milk (Georges and Guinet 2000Georges J.Y., Guinet C. 2000. Maternal care in the subantarctic fur seals on Amsterdam Island. Ecology 81: 295-308. https://doi.org/10.1890/0012-9658(2000)081[0295:MCITSF]2.0.CO;2 , Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 ).

Unlike trip durations, the number of dives per h, average diving time and average bottom time were independent from all explanatory variables considered. South American sea lions seldom dive longer than their aerobic dive limit and hence dive duration is strongly determined by their total oxygen stores (Hückstädt et al. 2016Hückstädt 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. https://doi.org/10.1242/jeb.138677 ). There is no information on the oxygen stores of South American sea lions from northern Patagonia, but the oxygen stores of South American sea lions from Uruguay and the Falkland Islands are fairly similar despite differences in body mass (Hückstädt et al. 2016Hückstädt 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. https://doi.org/10.1242/jeb.138677 ). Thus, the absence of any effect of female body size on average dive time and average bottom time reported in this study is no surprise.

It should be noted that colony had a strong random effect on some of the response variables analysed here. Although the study design confounded colony and year, it is worth exploring the potential causes of that effect. The growth and survival rates of otariid pups is largely dependent on both environmental conditions (Reid and Forcada 2005Reid 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. https://doi.org/10.1139/z05-045 , Soto et al. 2004Soto 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. https://doi.org/10.1017/S0952836904005965 , Trillmich and Limberger 1985Trillmich F., Limberger D. 1985. Drastic effects of El Niño on Galapagos ecuador pinnipeds. Oecologia 67: 19-22. https://doi.org/10.1007/BF00378445 ) and stress caused by social interactions, with colony size as a major determinant of the strength of social interactions in the South American sea lion (Cassini and Fernández-Juricic 2003Cassini 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. https://doi.org/10.1139/z03-098 , Drago et al. 2011Drago M., Cardona L., García N., et al. 2011. Influence of colony size on pup fitness and survival in South American sea lions. Mar. Mamm. Sci. 27: 167-181. https://doi.org/10.1111/j.1748-7692.2010.00402.x ). The study was conducted in two reproductive areas containing a total of 180 (Isla de Lobos) and 150 individuals (Isla Arce) of both sexes and all development stages, but population density was higher in Isla de Lobos (2926 sea lions km^-2) than in Isla Arce (2000 sea lions km^-2) when the whole rookeries are considered. Pup SGR was expected to be lower at the more densely populated site (Isla de Lobos) if social stress was the causal factor for the strong colony/year effect observed in the present study, as reported in previous studies (Drago et al. 2011Drago M., Cardona L., García N., et al. 2011. Influence of colony size on pup fitness and survival in South American sea lions. Mar. Mamm. Sci. 27: 167-181. https://doi.org/10.1111/j.1748-7692.2010.00402.x ). However, the opposite was true, and pups from Isla de Lobos grew faster than those from Isla Arce. This suggests, but does not prove, that differences in environmental conditions determining differences in food availability for females may explain the strong colony/year effect observed in the present study.

Marine primary productivity is a major determinant of otariid pup growth and survival worldwide (Lunn et al. 1994Lunn 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. https://doi.org/10.2307/5260 , Reid and Forcada 2005Reid 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. https://doi.org/10.1139/z05-045 , Soto et al. 2004Soto 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. https://doi.org/10.1017/S0952836904005965 ), and populations of the same species inhabiting areas of contrasting primary productivity are expected to differ in pup production. Females breeding at Isla de Lobos (Uruguay) prey on large demersal fishes (Franco-Trecu et al. 2013Franco-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. https://doi.org/10.1371/journal.pone.0080019 ) on the continental shelf within a few kilometres of the rookery (Franco-Trecu et al. 2019Franco-Trecu V., Szephegyi M.N., Doño F., et al. 2019. Marine mammal bycatch by the industrial bottom trawl fishery at the Río de la Plata Estuary and the adjacent Atlantic Ocean. Lat. Am. J. Aquat. Res. 47: 89-101. https://doi.org/10.3856/vol47-issue1-fulltext-10 , Riet-Sapriza et al. 2013Riet-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. https://doi.org/10.1016/j.dsr2.2012.09.005 , Rodriguez et al. 2013Rodriguez 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. https://doi.org/10.1016/j.dsr2.2012.07.012 ). These foraging grounds are adjacent to the highly productive plume of Río de la Plata (Acha et al. 2008Acha 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. https://doi.org/10.1016/j.csr.2007.01.031 , Fig. 1). Horizontal tracking data are lacking for females from Isla Arce (Argentina), but the females from other rookeries in northern Patagonia less than 300 km north of Isla Arce have similar at-sea and haul-out times and forage both nearshore and offshore (Campagna et al. 2001Campagna 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. https://doi.org/10.1017/S0952836901001285 ) to capture a mixture of demersal and pelagic prey (Drago et al. 2009Drago 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. https://doi.org/10.3354/meps08017 , 2010bDrago 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. https://doi.org/10.3989/scimar.2010.74n3589 , Koen-Alonso et al. 2000Koen-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). However, the pups of females relying more heavily on pelagic offshore fishes grow faster (Drago et al. 2010aDrago 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. https://doi.org/10.1111/j.1748-7692.2009.00321.x ), although accessing the frontal system over the continental shelf may require longer foraging trips.

Primary productivity off Patagonia is highly variable, with several frontal areas of enhanced productivity (Rivas et al. 2006Rivas 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. https://doi.org/10.1016/j.csr.2006.01.013 ), but overall the habitat is more heterogeneous and less productive than Río de la Plata (Fig. 1). The average duration of female foraging trips and haul-outs at Isla Lobos (Uruguay) in 2009 appeared shorter than those observed at Isla Arce (Argentina) in 2015, which in turn were similar to those observed previously in other rookeries from northern Patagonia (Campagna et al. 2001Campagna 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. https://doi.org/10.1017/S0952836901001285 ). Furthermore, females from Isla Arce (Argentina) in 2015 spent ashore only 66% of the time spent by females at Isla de Lobos (Uruguay) in 2009 during the three weeks covered by the study period. In parallel, pups at Isla Arce (Argentina) in 2015 grew more slowly than those at Isla de Lobos (Uruguay) in 2009 (Table 1). This suggests that the longer foraging trips observed in Argentina (Campagna et al. 2001, this study) and the slower growth rate of pups could be the consequence of a lower prey availability and a higher cost of capture (Jeanniard du Dot et al. 2017Jeanniard 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. https://doi.org/10.1371/journal.pone.0174001 , 2018Jeanniard 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. https://doi.org/10.3354/meps12638 , Soto et al. 2006Soto 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. https://doi.org/10.3354/meps312277 ) in Argentina than in Uruguay. However, simultaneous sampling in Uruguay and Argentina over several years and location data are required to confirm this hypothesis.

The results reported here revealed that pup sex and mass are the major determinant of female foraging and haul-out behaviour, which is likely related to the higher body mass of male pups. Furthermore, individual differences in the duration of foraging trips and haul-out are of little significance for explaining the growth rate of pups. Temporal or regional differences in prey availability are probably more relevant, although further research is necessary to account for temporal and geographic variability in food availability.