This study reveals that sexual segregation of behaviour can be exhibited as early as nutritional independence in capital breeders. Female pups from both regions spent more time diving per day than males. CIS females made shorter distance trips than males, diving in shallower water and achieving a higher proportion of the dive duration in the bottom phase. The same level of sexual segregation in depth, proportion bottom time and trip duration was not observed in NS pups, suggesting that sex differences in the ontogeny of foraging behaviour may be mediated by extrinsic factors. In both regions, pup behaviour changed rapidly: dive duration, depth, bottom time and benthic diving increased over the first 40 days after leaving the colony. These findings are important in the context of both foraging ecology and conservation management, as we outline below.

Grey seal adults exhibit substantial sexual size dimorphism23, which is thought to drive differences in feeding areas32. Grey seal pups are not size-dimorphic24, but seal pups and juveniles may experience differences in energy requirements before overt size and body composition differences emerge43. Kelso et al.43 found that male northern elephant seal (M. angustirostris) pups had higher rates of energy expenditure than females during the post-weaning fast, but were more effective at sparing protein reserves. These differences are likely related to the development of sex-specific metabolic strategies required for successful breeding43. Differences in metabolic demand during the ontogeny of foraging behaviour could therefore drive sex-specific feeding strategies and habitat requirements. Our findings support this possibility; we found that females from both regions spent longer performing behaviours consistent with foraging across two different temporal scales (individual dives and 24 h period). At the individual dive scale, time in the bottom phase is indicative of time at potential foraging depth, with the descent and ascent phases of the dive representing the transit to and from any potential prey patch10. Despite the lack of sex difference in total dive duration, females spent longer in the bottom phase than males relative to total dive duration. At the 24 h scale, females spent on average 2 h more diving than males in both regions. We also found a moderate sex difference in the proportion of dives that reached the seabed, with females performing more benthic dives than males. Females may therefore have increased chance of prey capture during individual dives, which could represent an energetic advantage10,44, and contribute to higher survival probability of female pups29. However, we cannot exclude the possibility that females spend more time diving because they are searching and are unsuccessful. Using direct observations of prey capture (i.e. stomach temperature telemetry, accelerometers or video cameras) to ground-truth putative foraging as identified from location and dive data would help to evaluate foraging success45, and draw links between differences in ontogeny of foraging behaviour and survival probability.

Sex differences in bottom time, proportion of benthic dives, and time spent diving per day may be related to differences in the type and quality of prey items consumed by male and female pups. For example, if females target lower energy prey items, they will need to spend longer foraging than males for the same energetic gain. Grey seals adults are benthic foragers with a broad diet that varies between the sexes46,47. Beck et al.47 used quantitative fatty acid analysis to investigate niche breadth in grey seals in the northwest Atlantic. They found that the diet composition of YOY animals was significantly broader than that of adults, but found no sex differences for young animals. However, grey seal diet varies regionally and seasonally46,47, and therefore extrinsic factors unique to certain locations may shape sex differences in diet for young animals. No specific information currently exists on the diet of recently-weaned grey seal pups in the UK once they have left the colony due to the logistical constraints of collecting tissue and/or faecal samples specifically from this age-class. However, a recent study of stable isotope ratios obtained from the teeth of older juvenile grey seals in the North Sea suggests that they feed on a wide variety of low trophic level, benthic prey close to shore48. The sharp increase in proportion of benthic dives over the first 40 days, and the subsequent reduction in trip distance, may therefore be indicative of pups learning to exploit benthic prey, and finding foraging grounds closer to shore where they can effectively reach the bottom. Additional dive analysis also suggests that shallow waters <20 m deep may represent important foraging habitat for grey seal pups (see Supplementary Results: Effects of bathymetric depth on benthic diving).

Water depth is an important regulating factor in foraging behaviour and habitat preference in older grey seals49,50. Breed et al.35 reported that adult and YOY females in the northwest Atlantic population forage in shallower water than males. Our data from CIS pups, showing that females dived in significantly shallower water than males, support these findings and suggest that water depth may play a key role in the development of habitat (and possibly diet) segregation among the sexes in some regions. We also found a moderate sex difference in trip distance for CIS pups, with males travelling further than females. Given that there was no sex difference in trip duration, this may mean that CIS males travel further offshore to forage compared to females, accessing deeper water, and potentially spending longer travelling per unit time spent foraging than females. CIS females performed a greater proportion of benthic dives in shallow water (<20 m) than males (see Supplementary Results: Effects of bathymetric depth on benthic diving). The fact that CIS pups dived in shallower water than NS pups likely means that they were able to achieve greater dive bottom time and proportion of benthic dives as they spent less time in the ascent and descent phases of the dive. Sex differences in trip distance and water depth of dive locations were not strongly evident for NS pups. As with other metrics, sex differences may be mediated by extrinsic factors that vary among regions, such as prey distribution, physical oceanography, and the diversity of available habitats. In general, the North Sea is a more homogeneous ecosystem, with less variation in bathymetry and habitat types than the Celtic and Irish Seas51, which may reduce sexual niche separation in NS pups.

Intra and inter-specific competition may impact trip distance and duration in central place foragers. Juvenile grey seals in the northwest Atlantic travel further and for longer on foraging trips than adults, likely as a result of competitive exclusion from the best foraging grounds closer to shore52. Age-related segregation has also been reported for other phocid species53. We found that NS pups travelled further offshore and performed longer trips than CIS individuals. Population density of grey seal adults is much higher on the east coast of Scotland compared to the Celtic and Irish Seas39,54. Moreover, Russell et al.36 showed that adult males in the North Sea reduce their time spent travelling to foraging locations in winter, whilst juveniles show an increase. Given that NS pups leave the colony during the winter months, and we see the longest trips performed during this time, competitive exclusion by conspecifics may be a feature of movement patterns specifically during the winter, forcing pups to make longer trips further offshore. In addition, harbour seals are present in coastal regions of the North Sea, but not in the Celtic and Irish Seas54. Inter-specific competition may also contribute to NS pups travelling further offshore than CIS pups.

Our results show that NS pups can make trips of over two months in duration, travelling greater distances than commonly observed in adult foraging trips and hauling out less frequently34. We also found that pups significantly reduced their trip duration and distance in the third month (Fig. 2). A similar temporal dynamic has been observed in other phocids, with young seals reducing trip duration after an initial increase41, and may be indicative of an increase in foraging efficiency, or a change in foraging strategy as pups age. Moreover, the higher initial trip duration and distance may represent an exploration phase in the development of NS pups. Votier et al.55 found that immature northern gannets (Morus bassanus) develop knowledge of foraging grounds during early-life exploratory trips. This may also be the case for grey seal pups, as, like gannets, they receive no parental guidance in the location of foraging resources. Furthermore, we found that some pups returned to forage repeatedly in areas that they had previously discovered during their initial exploratory trip (Fig. 2). Exploration may therefore be an important behaviour in determining future foraging success8.

CIS pups also performed exploratory trips, although their duration and distance was lower than those performed by NS pups. Individuals from NS colonies are not as geographically constrained as CIS pups by the proximity of land and shelf edge and therefore have more marine space to explore. Upon leaving the colony, CIS pups are more likely to encounter coastline, and therefore suitable haul-out locations, than pups in the North Sea. Alternatively, the offshore phase could be driven by environmental variables not measured in this study. For example, surface currents may direct pups further from land in the North Sea. The reduction in trip distance after 60 days for NS pups may therefore be related to a seasonal change in physical oceanography, or an increase in their ability to resist surface currents as muscle strength improves. Grey seals are known to rest at sea36, and this study provides further evidence that they do not need to return to shore to rest, even when very young.

Our results show that pup movements can change rapidly throughout the initial months at sea. Therefore, accurately quantifying foraging effort from these data may require extension of current analytical techniques, such as state-space models (SSMs)45, to account for temporal changes in movement patterns. Moreover, as a priority for future work, analysis of pup foraging habitat preference may allow us to infer potential prey species based on habitat features such as substrate type, and further assess the implications of early-life sexual segregation in movement patterns for foraging ecology.

In addition to ontogenetic changes in muscular and cardio-vascular systems, oxygen storage capacity and metabolic rate, and the development of knowledge of profitable foraging areas, there are likely to be seasonal changes in foraging habitat and prey distribution which may further explain differences in pup behaviour over time. Given that pups leave the colony on different dates in both regions (see Supplementary Note: Colony departure dates), local conditions may dictate some of the patterns observed here. Bennett et al.56 have shown that maximum dive depth of adult southern elephant seals may be regulated by seasonally-mediated factors, however, due to a paucity of tracking data from post-breeding adult grey seals in the UK, seasonal changes in at-sea behaviour are unclear. It was therefore not possible to disentangle ontogeny from seasonal effects on pup behaviour. Furthermore, some of the variance in early-life behavioural ontogeny may be explained by the fact that post-weaning fast duration varies among individuals24, and age at the point of departure from the colony is not equal for all pups. Natal and weaning dates were not known for all pups in this study, and time since departing colony was therefore used as a measure of at-sea experience. Future research should aim to achieve simultaneous tagging of adults, juveniles and pups, coupled with colony-based monitoring, which will allow us to further tease apart intrinsic and extrinsic drivers of variation in grey seal foraging behaviour and investigate the potential for competitive exclusion36.

Investigating the factors that affect the ontogeny of early-life behaviours is key to understanding how populations may respond to natural and anthropogenic threats. Bennett et al.22 suggested that grey seal pups have an average of 36 days in which to find food after leaving the colony before their protein reserves are critically depleted and starvation occurs. Our results show that profound changes in pup behaviour happen during the first 40 days after departure from the colony, indicating this initial period at sea is likely of particular importance for development of effective foraging strategies. Consequently, pups may be most vulnerable to disturbance from a number of growing anthropogenic activities, such as increased vessel traffic57, intensive fishing practices58 and offshore construction59 during this period, with substantial consequences for survival. Given the importance of early-life survival for maintaining stable populations31, and the rapid development of key behaviours during this period, conservation managers should make special considerations for pups during their initial months at sea to effectively mitigate these threats and avoid population-level impacts. With continuing development of biologging technology and analytical techniques, further work is urgently needed to fully explore and describe the ontogeny of fundamental behaviours in naïve marine predators and identify critical habitat for young animals during their most vulnerable life stage.