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 1991, Davies et al. 2012). For mammalian females, lactation is the most energetically demanding activity during the breeding cycle, even more than gestation (Gales et al. 1996, Higgins and Gass 1993). 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 2000, Jeanniard du Dot et al. 2017). 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 2004). Generally, otariids inhabit continental margins with high primary productivity, likely to satisfy the energy requirements during key foraging periods with high energy demand (Gentry 2009, Webber 2014).

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. 1986, Georges et al. 2001, Georges and Guinet 2000). 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. 1986). 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. 1994, Costa 2008, McHuron et al. 2016). In general, females spend proportionally more time ashore nursing their pups when foraging trip duration is shorter (Georges and Guinet 2000, Jeanniard du Dot et al. 2017, McHuron et al. 2016), which has been reported to result in faster pup growth rates (Gentry and Kooyman 1986, Georges and Guinet 2000, Jeanniard du Dot et al. 2017). 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 1995, Arnould and Hindell 1999), 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. 1999).

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 2009). Previous research has revealed that the growth and survival of South American sea lion pups are influenced by colony size (Campagna et al. 1992, Drago et al. 2011), 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. 2004, 2006), and some components of diving behaviour influence the rate of energy expenditure in other otariid females (Arnould et al. 1996, Costa and Gales 2000), but little is known about the effect of individual variability in foraging behaviour on pup growth rate (McHuron et al. 2016). 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.

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%).

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. 2017), exploitation of closer patches with low food density (Soto et al. 2006) or targeting more distant foraging grounds with high food density (Jeanniard du Dot et al. 2018, McHuron et al. 2016). Foraging trip durations have been negatively correlated with pup growth rate in the two former scenarios (Gentry and Kooyman 1986, Georges and Guinet 2000, Jeanniard du Dot et al. 2017), but positively correlated in the third scenario (Arnould and Hindell 1999, Jeanniard du Dot et al. 2018, McHuron et al. 2016). 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. 2001). 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 2000, Jeanniard du Dot et al. 2017).

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. 2016). 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. 2016). 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 2005, Soto et al. 2004, Trillmich and Limberger 1985) 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 2003, Drago et al. 2011). 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. 2011). 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. 1994, Reid and Forcada 2005, Soto et al. 2004), 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. 2013) on the continental shelf within a few kilometres of the rookery (Franco-Trecu et al. 2019, Riet-Sapriza et al. 2013, Rodriguez et al. 2013). These foraging grounds are adjacent to the highly productive plume of Río de la Plata (Acha et al. 2008, 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. 2001) to capture a mixture of demersal and pelagic prey (Drago et al. 2009, 2010b, Koen-Alonso et al. 2000). However, the pups of females relying more heavily on pelagic offshore fishes grow faster (Drago et al. 2010a), 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. 2006), 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. 2001). 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. 2017, 2018, Soto et al. 2006) 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.