Extraordinary diversity of the pinniped lactation triad: lactation and growth strategies of seals, sea lions, fur seals, and walruses

Abstract

Marine mammals produce a high fat (>25%‐60%), energy rich milk that facilitates rapid growth of offspring. Maternal provisioning in pinnipeds, varies from 4 days (hooded seal) to 24 months (Pacific walrus). Marine mammals evolved different lactation strategies, including extended periods of fasting in the mother and the offspring influenced by environment yet tightly associated with phylogeny. A mutation in alpha-lactalbumin gene is present in otariids (sea lions and fur seals) that prevents lactose production and is thought to allow for maintenance of lactation even with long (up to 23 days) inter-suckling interval by preventing mammary involution. Growth strategies of pinnipeds are partially influenced by milk composition (high percentage of fat) and rate of energy delivery (total calories provided); however, offspring physiology (metabolic hormones) and behavior (increased activity) also impact the rate and composition of mass gain which strongly predict offspring survival. Mammalian reproductive success is highly influenced by early postnatal survival due to the high mortality in the neonatal and post-weaning (transition to independent foraging) periods. Lactation is an essential and critical life history event with significant implications for offspring survival and hence female reproductive success (Lee, 1996). Lactation is influenced by intrinsic and extrinsic factors from dam and offspring; however, recent research has begun to consider milk as the third component of the lactation triad encouraging additional research of milk as an integrated biological system (Christian et al., 2021). Marine mammals have exceptional diversity in nursing strategy thought to have evolved to maximize offspring success for unique environments (Schulz and Bowen, 2004). These maternal lactation strategies are closely tied to off-spring growth strategies. This review will examine the extreme and diverse lactation and growth strategies of pinnipeds including true seals, sea lions, fur seals, and walrus. This review, while not exhaustive, provides an overview of unique adaptations of the pinniped lactation triad with select species examples. Marine mammals have developed unique lactation strategies that facilitate energy transfer in a fully aquatic or semiaquatic environment. Marine mammals are distributed among four Orders of mammals: Mysticeti (baleen whales), Odontoceti (toothed whales, dolphins, and porpoise), Sirenia (manatee and dugong), and Carnivora [polar bears (Ursidae), sea otters (Mustlidae), walrus (Odobenidae), true seals (Phocidae), sea lions and fur seals (Otariidae)]. These species have an exceptional diversity of lactation strategies that vary by maternal energy acquisition and delivery [capital (fasting) vs. income (foraging) investment strategy], duration of lactation, and composition of milk that result in differential relative and absolute growth rates of pups as well as composition of body mass gain. Given the unique logistical challenges of studying lactation in a large, fully aquatic organism, this review will focus primarily on semiaquatic pinnipeds where more detailed studies of lactation physiology and pup growth have been completed. Pinnipeds, including walrus, seals, sea lions, and fur seals, are considered semiaquatic because they are tied to the land or ice for key life history events such as lactation, breeding, and molting; however, aquatic foraging is required for energy acquisition and repletion. Length of lactation in pinnipeds varies from the shortest lactation of any mammal, 4 days in arctic hooded seals (Cystophora cristata), to 18 months in the temperate to subtropical Australian sea lion (Neophoca cinerea), and 2‐3 years in the subarctic walrus (Odobenus rosmarus) (Fay, 1982) although no consistent relationship has been observed between latitude and milk composition (Schulz and Bowen, 2004). Comparison of lactation among diverse species is challenging given differences in duration. While most mammals are still providing colostrum in the first 3‐5 days, hooded seals have delivered 10 L of high fat milk per day (Oftedal et al., 1993). Terrestrial mammals have two primary lactation strategies that can be termed “cash” or “carry”. Species like small rodents utilize a cash strategy where young are left in a nest for short periods while females forage for food, and females return to the nest to provide nutrients to the offspring. In the carry strategy, offspring is always in close proximity to the female and are nursed on demand. This carry strategy is utilized by primates, including humans and hoofstock. Three distinct lactation strategies are observed in marine mammals: aquatic lactation, capital-fasting, and income-foraging strategies. The aquatic lactation strategy utilized by walrus, sirenians, and dolphins is the most similar to the terrestrial “carry” strategy where the offspring remain in close proximity to the cow with nursing on demand that is initiated by the offspring. This provisioning strategy often lasts for multiple years and affords the opportunity for significant maternal investment for lactation and social learning (Noren et al., 2014; Mann, 2019; Sepúlveda and Harcourt, 2021). Walruses are the only pinniped species that exhibit this strategy; nursing on demand for more than 2 years (Schulz and Bowen, 2004). Walruses are shallow, benthic foragers; thus, limited diving and foraging abilities of young walrus pups likely do not limit female acquisition of prey facilitating this aquatic lactation strategy (Fay, 1982; Noren et al., 2014). Most true seals (phocids) and all baleen whales (mysticetes) exhibit a capital-fasting lactation strategy (Figure 1) where all energy capital to be provided to offspring is acquired before parturition at distant foraging grounds (Schulz and Bowen, 2004; Irvine et al., 2017). During energy demanding lactation, females do not eat to replenish energy provisioned to offspring. Other than bears, mysticetes and phocids are the only other mammalian species where lactation and forging are temporally and spatially separated (Oftedal, 1993). Females fast for weeks (phocids) to months (mysticetes). Large maternal body size relative to offspring is key to this strategy, and females must have predictable, high quality foraging grounds to acquire enough energy before parturition to successfully transfer all needed energy, primarily as fat, to their offspring (Oftedal, 1993; Irvine et al., 2017). Graphical representation of the Capital-Fasting Maternal Investment Strategy utilized by Phocids (true seal) in four different species. Species common name above image with genus species in italic within image. At birth, pups are nursed persistently (yellow) from 4 to 24 days, while the dam is fasting. Pups are abruptly weaned followed by a 2‐6 week post-weaning fast (red) where dams are no longer attending pups and pups are not consuming other food resources. Duration of fast is dependent on species and acquired pup energy reserves stored as blubber (subcutaneous adipose). Small bodied harbor seals (bottom panel) do not have the energy reserves for a strict post-weaning fast and instead weaning pups gradually (orange) with supplementation of small forage fish and extended maternal care where foraging behavior is learned. Harbor seal strategy is more similar to the otariid (sea lion and fur seal) Investment-Foraging Strategy. True independent foraging (blue) includes only fish consumption. Variation in provisioning strategy results in differential growth rates from 6% to 10% of birth weight gained per day during nursing (Schulz and Bowen, 2004). The capital-fasting strategy appears to have evolved twice under two distinct conditions (Skibiel et al., 2013). The first condition is the extreme separation of whale foraging and calving grounds. For example, mysticetes forage in cool high productivity waters while calving occurs in warm nutrient poor waters (Irvine et al., 2017). The second evolution occurred in phocids where a brief and highly synchronous lactation period is advantageous due to dependance on ephemeral and relatively unpredictable seasonal ice that supports resting, breeding, parturition, and nursing (Schulz and Bowen, 2004; Skibiel et al., 2013). The relatively unstable nature of the seasonal ice cover likely contributed to the evolution of precocial offspring with rapid growth rates in conjunction with precipitous transfer of energy via nutrient dense milk from dam to offspring (Schulz and Bowen, 2004). Years with poor ice conditions (thin, late onset, or early retreat) are associated with poor pup production in phocids dependent on ice for parturition and lactation (Laidre et al., 2008). Sea lions, fur seals (otariids), and some phocids exhibit an income-foraging lactation strategy (Figure 2; Schulz and Bowen, 2004). Females arrive at rookeries (sites of parturition and nursing) with energy reserves sufficient to nurse pups consistently for a few days up to 2 weeks. Following this discrete nursing period females begin to alternate between foraging at sea while pups are fasting on rookeries, and the dam fasting on land while providing nutrition to the pup (Figure 2). This fasting-foraging cycle continues for months to years dependent on species and population (Hastings et al., 2021), and foraging trip duration increases as the pup ages (Higgins and Gass, 1993; Arnould and Boyd, 1995). The Steller sea lion (Eumetopias jubatus) Income-Foraging lactation strategy diagramed above provides an example of the typical otariid pattern although significant species differences exist in duration of lactation and transition to independent foraging. Top bar indicates female pattern of foraging at sea (light yellow) and fasting on land (red) while provisioning her pup. Bottom bar provides pup pattern of nursing (dark yellow) and fasting (light red) on land while the female is foraging at sea. Pups are nursed consistently for 2 weeks (range from 4 to 14 days) immediately post-partum. After which, pups and females begin an alternate foraging-fasting cycle where pups fast on shore while females forage at sea. Most Steller sea lion pups wean at 12 months of age; however, the transition to independent foraging (blue) is not discrete and pups may continue to nurse well into the juvenile phase at 2 or 3 years of age (Hastings et al., 2021). A unique physiological adaptation has occurred in otariids to maintain milk production despite prolonged periods, three weeks or more (>21 days), of foraging at sea with interspersed production of large quantities of energy dense milk on land. In most mammals, mammary gland involution begins quickly following delayed milk removal (Li et al., 1997) and increased hydrostatic pressure cause by milk accumulation downregulates gene expression of milk proteins (Lefèvre et al., 2010). However, in otariids the gene that codes for alpha-lactalbumin, important for lactose synthesis, is knocked down (Reich and Arnould, 2007; Sharp et al., 2008). This is hypothesized to contribute to the of milk and also to the of involution despite days to weeks of no milk removal while the dam is foraging at sea. In to mammary is required to maintain lactation in phocids et al., While is quickly involution occurs due to increased hydrostatic lactation by foraging as short as days in harbor seal dams small body results in a of milk fat and in involution et al., The species of pinniped exhibit exceptional diversity in of environment and to be important in the evolution of lactation strategy and duration unique to (Skibiel et al., et al., In phocids species of true seal) utilize the capital-fasting strategy (Figure 1) and nurse pups for days to with a few including seals temperate harbor seals, and seals In otariids species of fur seal and sea lion the income-foraging strategy where lactation lasts months to years (Figure 2; Schulz and Bowen, 2004). Duration of lactation has significant impact on maternal energy investment with short lactation energy as fat, and with longer lactation periods, females more energy as well as and 2017). provided by Schulz and to energy transfer relative to maternal body phocids 3 transfer with the of hooded seals The relative energy transfer is by composition of milk and duration of 4 Schulz and Bowen, provide energy relative to maternal mass however, given this investment continues for months to years the energy investment is with studies the of lactation in pinnipeds, for the female a significant et al., Most phocids for from 4 days in the hooded seal (Figure the shortest lactation duration of any (Oftedal et al., up to 4 months in the seal et al., The capital-fasting strategy of maternal maintenance energy to for the increased energy required for lactation, and to maintenance results in early of lactation et al., seal (Cystophora pups 10 of milk with and for 4 days of their birth mass day (Oftedal et al., 1993; et al., energy of hooded seal milk is (Oftedal et al., 1993). energy is per day to a gain in body This energy be similar to a Growth consuming fat, per day for 4 days although the fat percentage still be than hooded seal transfer relative to maternal body mass to of lactation with bodied to transfer a of energy in a period of et al., and 2017). species or mass to have to transfer to offspring et al., and 2017). of factors has been to energy transfer to pups lactation duration in phocids and otariids or increased maternal foraging trip duration in otariids et al., et al., 2021). the nursing the pup. While otariids and phocids have highly lactation otariids have longer lactation with seals duration is 4 months while most sea lions nurse for Australian sea lions that nurse for months (Schulz and Bowen, 2004). Steller sea lions (Eumetopias jubatus) exhibit the typical lactation strategy (Figure where females fast while pups nurse during the 2 week (range from 4 to 14 days) period and et al., females to have a longer period before the to the pup to fast the cow et al., within the species and foraging duration varies by et al., While most Steller sea lion pups wean before parturition of a is not to a or nursing (Hastings et al., 2021). While is of all in pinnipeds most species birth to pup per has been in walrus, seals, seals, and fur seals et al., and of females nursing more than pup is due to termed or by the female or initiated by a pup and Harcourt, 2021). While true weaning is occurs among otariids and phocids with to the although due to from the female and pup and Harcourt, 2021). of on the female and her pup are observed with extended duration of lactation et al., 2021). prey quality and impact female foraging trip duration for otariids the income provisioning For example, in the female Steller sea lions foraging on quality prey such as have longer foraging trip duration with females consuming primarily a energy dense prey and et al., likely the and of prey while to high energy prey facilitates a more rapid of energy reserves needed to continue the pup et al., in prey or quality female body fat and percentage of energy during lactation et al., These are also in poor offspring growth and body condition with mass and fat reserves at In years with warm such as events in the results in and quality of increased foraging trip duration for females and delayed weaning for pups et al., 2021). In Steller sea lions two maternal factors contribute to survival in years (Hastings et al., 2021). due to a period 2 pups the fast with body fat relative to more typical years with two weeks of maternal investment to the first fast and maternal foraging trip are longer in longer periods of fasting for the pup and et al., 2021). in the significant in pup production is associated with sea in otariid species et al., of increased impact fur seal likely due to of prey et al., on the lactation triad have been observed in multiple otariid species including in milk nursing increased foraging at extended duration of nursing including of pup in of of (Higgins and Gass, 1993; et al., and et al., 2021). has the to reproductive success in species dependent on ice for and lactation and within more temperate and species due to the of sufficient energy for lactation, pup survival et al., et al., all mammals, including and mammals, is a of milk composition and energy than factors such as latitude and of prey (Lefèvre et al., Skibiel et al., 2013). In within of closely pinniped species factors are important for lactation which composition of milk and rate of energy transfer et al., milk from colostrum to milk within 24 in seals et al., and immediately following birth in hooded seals (Oftedal et al., The composition of pinniped milk (Figure provides an energy high milk to their offspring et al., of pinniped milk from to with cow and milk that et al., In fat of pinniped milk from to with the milk fat in cow or milk is also rich in with an of from to with to in humans and species (Schulz and Bowen, 2004; et al., composition of select pinniped relative to humans and of lactation provided in income-foraging strategy otariids two of sea seal Australian sea lion (Neophoca and fur seal the of Steller sea lions (Eumetopias jubatus) and fur seals similar the of Three phocids seal seal hooded seal (Cystophora with the capital-fasting lactation strategy the extreme high fat, energy dense milk composition of unique in pinniped milk from to are from et et and et lactation with colostrum with fat and percentage of milk is increased in milk to lactation (Oftedal et al., The is hooded seals that lactation with similar to lactation In otariids the in fat percentage is more In some lactation may months on the typical duration of lactation and 2021). in no relationship has been between percentage milk fat female or on shore before milk however, longer foraging trip duration results in milk fat composition and Boyd, et al., 2021). The increased energy of milk for the additional energy pups due to extended fasting duration such that pup growth rate or rate of milk energy delivery is by the females are from the pup and Boyd, et al., 2021). composition is also unique in marine mammals with large quantities of long and that their marine et al., 2004). milk in phocids and are primarily of with and et al., et al., 2014; et al., 2017). The of pinniped milk are different from and milk and while milk from is of and et al., are highly in pinniped milk species et al., et al., 2014; et al., 2017). and are to be critical for et al., and are highly in pinniped milk with milk et al., 2014; et al., 2021). However, is the of in of pinnipeds et al., 2021). that is from dam blubber and into milk et al., et al., 2014). this is also during the fast of seal pups in pinniped growth and (Noren et al., 2013). In most mammals, has an important as an energy for composition of mass and et al., In to other mammalian in pinniped species lactose is in milk et al., 1993; et al., 2021). of in pinnipeds is important often to results of than are present (Oftedal et al., 2014). or likely facilitate the and accumulation in pinniped A mutation in the alpha-lactalbumin is present in otariid species including sea lion fur seals fur seals, and walrus that prevents lactose production and is thought to allow maintenance of lactation with long (up to 23 days) inter-suckling interval by preventing involution (Reich and Arnould, 2007; Sharp et al., 2008). While lactose is in most pinniped has other of that likely have nutrition in pinniped milk in and are a highly of research in lactation et al., et al., however, limited research is for are not limited and (Christian et al., 2021). to contribute to the such as and are in milk immediately birth et al., et al., 2021). 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In of in milk are associated with mass gain at body mass at 3 and years of age et al., research is for in seal however, are in milk with milk of in pups is associated with growth rate and accumulation et al., of in seal milk and in pups that is increased during life history events that independent of et al., While increases in to to during periods of the pattern is is observed in pinniped during growth following and in periods associated with seasonal et al., of and other in pinniped milk of While terrestrial mammals birth to relatively offspring of maternal mass at marine mammals birth precocial young that are relative to maternal mass and 2017). This relative growth rate significant maternal energy investment during as well as and essential for and however, this investment results in a more developed offspring with significant immediately birth and 2017). growth during the nursing period is a significant of first survival in otariids et al., et al., and phocids et al., et al., In in pup and facilitate the rapid and transfer of milk to pup blubber et al., et al., et al., percentage milk fat is not associated with absolute growth rate or relative to birth mass (Schulz and Bowen, 2004). growth rate relative to pup birth mass is to rate of energy transfer seals that maximize energy transfer rates have period of lactation and 2017). In differential growth are observed between and female pups to maternal provisioning milk energy duration of and food In females fat milk that is not limited by maternal or food while fat milk and provisioning may be limited the cow has energy reserves and et al., 2021). in other pinniped species have no differences in provisioning between and some that are hypothesized to to pup not et al., et al., in other mammals have results with a energy and provided to however, this varies by milk energy, or (Lee, et al., research milk energy including energy and milk to be to differences in milk and differences in maternal provisioning differences in such as growth and that impact differential nutrient and growth rate of and females has been well in terrestrial however, limited studies have been in pinnipeds (Lee, 2008). In to differences in maternal of and of pups may also in the and of nutrients to impact differential growth rate between growth rate can vary from of birth in hooded seals, to 2 of birth in and with such as harbor seals, only of birth Schulz and Bowen, 2004). In phocids the capital-fasting lactation strategy, pup growth growth is primarily accumulation as termed In income-foraging otariids growth rate is of birth termed growth strategy (Schulz and Bowen, 2004). species differences in growth strategies are In two closely fur seals, fur seals have growth and physiological and behavior that result in early of foraging and weaning age with fur seals et al., large in growth rate and appears to be a where offspring birth weight before weaning of milk independent of food et al., This has been observed not only for pinnipeds also mammalian (Lee, 1996). This that growth the of lactation and of has in with of ice for reproductive success and population et al., However, and even marine species are also by et al., this review and of and of warm events on the pinniped lactation triad of events food quality and maternal forging success and energy reserves to in phocids and otariids et al., Maternal body condition the energy to offspring growth and and hence survival et al., et al., et al., The impact of on the pinniped lactation triad is well with to maternal provisioning strategy, energy to pup growth and survival all population well The pinniped lactation triad a unique opportunity to exceptional diversity in lactation strategies including lactation milk composition including and other provisioning and pup lactation including high fat, energy dense delivered to precocial offspring in precipitous offspring may of research for in and is a research at the and at the of lactation and growth from a a in and is also a and Lactation has been studying pinniped physiology for more than years and has in pinniped research in and research is by the of is a of at the of the at the of in from and and in the of at research is on growth physiology and in species with an on maternal to of the of and is a and the of from to as of from to an in and the in the three that provided and of the that the of this Sea and seal with from of and and under and and to of and hooded seals with from under with by the of and and

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