Metabolic compensation during high energy output in fasting, lactating grey seals (Halichoerus grypus): metabolic ceilings revisited

Lactation is the most energetically expensive period for female mammals and is associated with some of the highest sustained metabolic rates (SusMR) in vertebrates (reported as total energy throughput). Females typically deal with this energy demand by increasing food intake and the structure of the alimentary tract may act as the central constraint to ceilings on SusMR at about seven times resting or standard metabolic rate (SMR). However, demands of lactation may also be met by using a form of metabolic compensation such as reducing locomotor activities or entering torpor. In some phocid seals, cetaceans and bears, females fast throughout lactation and thus cannot offset the high energetic costs of lactation through increased food intake. We demonstrate that fasting grey seal females sustain, for several weeks, one of the highest total daily energy expenditures (DEE; 7.4 x SMR) reported in mammals, while progressively reducing maintenance metabolic expenditures during lactation through means not explained by reduction in lean body mass or behavioural changes. Simultaneously, the energy-exported in milk is progressively increased, associated with increased lipoprotein lipase activity in the mammary gland, resulting in greater offspring growth. Our results suggest that females use compensatory mechanisms to help meet the extraordinary energetic costs of lactation. Additionally, although the concepts of SusMR and ceilings on total DEE may be somewhat different in fasting lactating species, our data on phocid seals demonstrate that metabolic ceilings on milk energy output, in general, are not constrained by the same kind of peripheral limitations as are other energy-consuming tissues. In phocid seals, the high ceilings on DEE during lactation, coupled with metabolic compensation, are undoubtedly important factors enabling shortened lactation.     

The dynamics of parent-offspring relationships in mammals

Evolutionary theories about parent-offspring relationships have predicted that young will aggressively demand food and care from their parents at the time of weaning - when the parents should, in their own interests, reserve their efforts for future offspring. Detailed studies of the behavioural development of mammals have given only limited support for these expectations. Often the mother is more amenable to the needs of her offspring than evolutionary theory predicts, and often offspring are sensitive to the state of their mother, tuning the pattern of their own development accordingly. Such aggression as is seen between mother and offspring tends to occur at stages other than weaning. The mismatch between theory and evidence may arise because a mother needs to monitor her offspring's state as well as her own and respond appropriately in order to maximize her own reproductive success. Similarly, an offspring needs to monitor its mother and prepare for the world in which it will grow up, in order to maximize its chances of surviving to breed.     

Ambient temperature affects postnatal litter size reduction in golden hamsters

Background

To better understand how different ambient temperatures during lactation affect survival of young, we studied patterns of losses of pups in golden hamsters (Mesocricetus auratus) at different ambient temperatures in the laboratory, mimicking temperature conditions in natural habitats. Golden hamsters produce large litters of more than 10 young but are also known to wean fewer pups at the end of lactation than they give birth to. We wanted to know whether temperature affects litter size reductions and whether the underlying causes of pup loss were related to maternal food (gross energy) intake and reproductive performance, such as litter growth. For that, we exposed lactating females to three different ambient temperatures and investigated associations with losses of offspring between birth and weaning.

Results

Overall, around one third of pups per litter disappeared, obviously consumed by the mother. Such litter size reductions were greatest at 30 °C, in particular during the intermediate postnatal period around peak lactation. Furthermore, litter size reductions were generally higher in larger litters. Maternal gross energy intake was highest at 5 °C suggesting that mothers were not limited by milk production and might have been able to raise a higher number of pups until weaning. This was further supported by the fact that the daily increases in litter mass as well as in the individual pup body masses, a proxy of mother’s lactational performance, were lower at higher ambient temperatures.

Conclusions

We suggest that ambient temperatures around the thermoneutral zone and beyond are preventing golden hamster females from producing milk at sufficient rates. Around two thirds of the pups per litter disappeared at high temperature conditions, and their early growth rates were significantly lower than at lower ambient temperatures. It is possible that these losses are due to an intrinsic physiological limitation (imposed by heat dissipation) compromising maternal energy intake and milk production.

     

Milk composition of free-living yellow-pine chipmunks (Tamias amoenus): temporal variation during lactation

Milk is the sole food source of mammals during early postnatal development, and its composition may be modified to meet changing nutritional and energetic demands from birth to weaning. These demands are especially acute in small mammals that breed in highly seasonal environments. We investigated the temporal course of milk composition during lactation in free-living yellow-pine chipmunks, Tamias amoenus, a small altricial omnivorous rodent that produces a single annual litter immediately after emerging from hibernation. Over the course of lactation the total energy concentration of milk increased more than two-fold, to approximately 13 kJ ml(-1). The main component of the milk was lipids, which increased from 10 to 30% of total milk content by wet mass. Proteins increased from approximately 5 to 10%, whereas carbohydrates remained low, at 4-5%. The progressive augmentation of milk energy content during lactation contributes to the increased demands of rapid growth in this altricial species.     

Concurrent lactation and pregnancy: pregnant domestic horse mares do not increase mother-offspring conflict during intensive lactation

Lactation is the most energy demanding part of parental care in mammals, so parent-offspring conflict arises over milk provided by the mother. In some species females commonly become pregnant shortly after parturition of previous young. This further intensifies mother-offspring conflict due to concurrent pregnancy and lactation. In equids it has been well established that pregnant females wean their foals earlier than non-pregnant ones. Intensified mother-offspring conflict was presumed to associate with pregnancy also during the period of intensive lactation, i.e., before the weaning process starts. We investigated the effect of pregnancy on suckling behaviour characteristics as indicators of mother-offspring conflict in domestic horses. Contrary to expectation, here we provide evidence of a decreased mother-offspring conflict related to pregnancy in lactating females during first two trimesters of pregnancy. Pregnant mares provided longer suckling bouts and did not reject or terminate suckling of their foals more often than non-pregnant mares. Our results suggest that pregnant mares cope with parallel investment into a nursed foal and a foetus through enhancing nursing behaviour in early stages of pregnancy before the initially low requirements of the foetus increase. They compensate their suckling foal with the perspective of its early weaning due to ongoing pregnancy.     

Kin Recognition and Maternal Care under Restricted Feeding in House Mice (Mus domesticus)

This study tests the hypothesis that female house mice (F1 generation of wild caught Mus domesticus) should preferentially invest in own offspring if confronted with young of different degrees of relatedness. The maternal behaviour of females with litters of 4 own and 4 unrelated alien young (cross-fostered at day 1 of lactation) was analysed during a lactation period of 22 days both under ad libitum and under restricted feeding (food was restricted by 20%). Cross-fostering and restricted feeding had no effect on the amount of time spent nursing until weaning. Under both feeding conditions the females did not differ in their maternal behaviour towards own and alien young: there were no significant differences either in the amount of time spent nursing own versus alien pups or in the time spent licking own versus alien young. Weight gain of own and alien = wild littermates did not differ significantly in mixed litters and was similar both under ad libitum and under restricted feeding. Such indiscriminate behaviour might be adaptive if female house mice prefer to communally nest with a relative and thus improve their inclusive fitness by investing in own and related offspring in a communal nest. Under moderate restricted feeding females could not wean the entire litter but reduced litter size by cannibalizing on average 2.7 pups (75% of the pups were killed when they were 4–8 days old). Females with cross-fostered litters killed as many own as alien young. This suggests that females cannot discriminate between own and unrelated young if cross-fostering takes place at day 1 of lactation. Besides testing kin recognition abilities, the experiments also allow analysis of the weaning strategy of females under food shortage. Under restricted feeding, body weight of the females was significantly lower during middle lactation than under ad libitum feeding. Weaning weight of young in reduced litters under food restriction (9–10 g) did not differ significantly from weaning weight of young in litters of 7–10 young, but was lower than that of young in similar sized litters (litter size 6), under ad libitum feeding. The maternal behaviour of cannibalizing some young under food shortage can be interpreted as a weaning strategy which results in the largest number of offspring that can be raised to a minimal weaning weight of 9–10 g. Such a weaning strategy might represent a favourable trade-off between number and size of young produced.     

The origins of lactation and the evolution of milk: a review with new hypotheses

Lactation is central to mammalian reproduction, and an understanding of the origins of lactation is necessary to comprehend the early evolution of the Class Mammalia. In modern mammals, lactation is a staggeringly complex phenomenon involving morphological, physiological, biochemical, ecological, and behavioural adaptations. Because such a complex web of adaptations could not have arisen de novo, lactation must have begun as a much simpler process. Hypotheses regarding the original adaptive value of proto-lacteal secretions invoke thermoregulatory, antibiotic, behavioural or nutritive functions. In this review, we evaluate each of these hypotheses and attempt to reconstruct the origins of lactation in the light of current concepts of the biology of early mammals and their ancestors, the origin of mammary glands, the evolution of extravitelline nutrient provision, and the physiology and biochemistry of milk synthesis and secretion. Drawing upon empirical evidence and theoretical considerations, we present a gradualistic scenario involving the following steps. First, incubation of eggs was aided by development of a vascularized abdominal incubation patch. Secondly, anti-microbial secretions from cutaneous glands of the incubation patch enhanced survival of eggs or offspring. At this stage, these secretions could have supplemented vitelline nutrients (in much the same way as oviductal secretions do in monotremes), perhaps facultatively. Subsequently, hypertrophy and specialization of cutaneous glands accompanied the controlled production of a copious, nutritious secretion, which eventually evolved into a primary source of energy for development and growth of the offspring. We outline important events in the evolution of milk, and suggest studies likely to provide indirect tests of the evolutionary hypotheses discussed.     

Maternal food restriction delays weaning in the guinea pig, Cavia porcellus

In mammals, the duration of lactation varies much more than other life history parameters in relation to body mass, both within and between species. The causes of this variation are poorly understood and seem to result from varying conditions of mothers and young. We studied the effect of long-term maternal food restriction on litter mass at birth, duration of lactation and offspring development in the precocial guinea pig. Mild experimental food restriction during reproduction resulted in prolonged nursing behaviour of mothers. Evidence for a threshold mass at weaning was, however, equivocal. In the guinea pig, benefits of prolonged lactation prove hard to understand, because nutritional benefits are minor. Independently of maternal food regime, pups terminated suckling attempts several days after mothers ceased nursing behaviour. The time between the last nursing behaviour and the last suckling attempts was not longer in litters with higher need, that is, in litters of food-restricted females, than in litters of females fed ad libitum. Under food restriction, mothers maintained their own body mass, leading in pups to lower mass at birth, reduced postnatal growth and lower body mass at maturity. Guinea pig mothers appear to be selected to value their own condition more than that of a litter. We suggest that lengthening of the nursing period under poor conditions is a life history response primarily of precocial mammals.     

Nutrition, fertility and maternal investment in primates

While the energetics of reproduction have been intensively investigated among women, studies of mother-offspring relationships among non-human primates have tended to neglect the effect of nutrition of the mother on lactational performance and on growth and survival of offspring. Typically fertility has been compared between populations under different nutritional regimes. In this paper, the relations between suckling frequencies, the time of weaning, the survivorship of offspring, the contraceptive effects of lactation and the quality of maternal diets are outlined. Energy transfer from mother to offspring in the form of milk is proposed as a measurable component of maternal investment, and the behavioural causes and consequences of lactational anoestrus are explored using data from free-ranging vervet monkeys. It is suggested that nutrition of the mother is most important during the early phase of rapid infant growth, because at that time the energetic requirements of lactation are high; and that a mother's ability to assess her infant's demands and needs for nutrition for growth leads to alterations in suckling frequencies which result in variation in female fertility.     

The arrangement of the heart chambers and associated blood vessels in the Devonian osteostracan Norselaspis glacialis. A reinterpretation based on recent studies of the circulatory system in lampreys

Food intake and digestion were investigated at four stages in the first 218 days of lactation in tammar wallabies ( Macropus eugenii ) carrying litters of one, and in non-lactating females as a control. This period of lactation in tammars, which includes the phase of exponential growth of the young, is comparable to gestation plus early lactation in ruminant placentals. Food and energy intakes by mothers remained at the non-lactating level while rate of growth of young was slow (up to Day 105 of lactation) but then rose as the growth rate of young increased, keeping pace with the predicted requirements for milk synthesis and export. There was no indication of the energy deficit seen in late gestation and early lactation in many herbivorous placental mammals. The gross efficiency of utilization of ME for growth of offspring was estimated as 13–15%, which is at least as high as values for placentals during gestation. The mean intake of metabolizable energy (ME) at 218 days was 603 kJ.kg^-0.75.d^-1, which represented 136% of ME intake by nonlactating females, or an increment of 159 kJ.kg^-0.75.d^-1. It was estimated that ME intake may rise to 773 kJ.kg^-0.75.d^-1 at peak lactation, which would be 174% of the non-lactating level or an increment of 329 kJ.kg^-0.75. d^-1. This allometrically-scaled increment is similar to values for some ruminants that use body reserves extensively to offset peak lactational food requirements. These and previously-reported trends suggest that ecologically comparable herbivorous marsupials and placentals utilize different physiological strategies to minimize demands on food resources during reproduction, but that both daily and overall demands can be similar.     

No evidence for sex biases in milk macronutrients,energy, or breastfeeding frequency in a sample of filipino mothers

Maternal reproductive investment includes both the energetic costs of gestation and lactation. For most humans, the metabolic costs of lactation will exceed those of gestation. Mothers must balance reproductive investment in any single offspring against future reproductive potential. Among mammals broadly, mothers may differentially invest in offspring based on sex and maternal condition provided such differences investment influence future offspring reproductive success. For humans, there has been considerable debate if there are physiological differences in maternal investment by offspring sex. Two recent studies have suggested that milk composition differs by infant sex, with male infants receiving milk containing higher fat and energy; prior human studies have not reported sex‐based differences in milk composition. This study investigates offspring sex‐based differences in milk macronutrients, milk energy, and nursing frequency (per 24 h) in a sample of 103 Filipino mothers nursing infants less than 18 months of age. We found no differences in milk composition by infant sex. There were no significant differences in milk composition of mothers nursing first‐born versus later‐born sons or daughters or between high‐ and low‐income mothers nursing daughters or sons. Nursing frequency also showed no significant differences by offspring sex, sex by birth order, or sex by maternal economic status. In the Cebu sample, there is no support for sex‐based differences in reproductive investment during lactation as indexed by milk composition or nursing frequency. Further investigation in other populations is necessary to evaluate the potential for sex‐based differences in milk composition among humans. Am J Phys Anthropol 152:209–216, 2013. © 2013 Wiley Periodicals, Inc.     

Trade-offs in Energy Allocation During Lactation

SYNOPSIS. During lactation, mothers require energy to meet bothmaternal and offspring requirements. If a mother exports toomuch energy to dependent offspring (in milk), her weight lossmay be excessive and maternal risk may increase. Conversely,too little energy allocation to offspring may reduce the growthrate or induce mortality of dependent offspring. This paradigmwas evaluated in cotton rats (Sigmodon hispidus) supportingsmall (3 pup) and large (6 pup) litters from early to late lactation.Several types of evidence indicate that physiological constraintslimit the ability of mothers with large litters to provide resourcesto offspring. Mothers with large litters produced a dilute,energy-poor milk and their rates of food intake, weight lossand energy export per litter appeared to approach physiologicalmaxima. Whereas the energy exported to pups in small littersincreased from early to late lactation, the energy flow perpup in large litters was consistently low; consequently, offspringin large litters had low growth rates. An increase in eithermaternal food intake or weight loss (catabolism of maternaltissue) could have provided additional energy to offset thelow growth rate of pups in large litters. However, mothers withlarge litters did not substantially increase their food intakeor weight loss compared with mothers supporting small litters.These results indicate that the maternal support of offspringin large litters is limited. The pattern of energy allocationshown by cotton rats with large litters likely reflects a compromisebetween meeting maternal and offspring energy requirements (cf.,Parker and Macnair, 1979). The energy flow is greater than optimalfor the parent but less than optimal for the offspring. Lessmaternal-offspring conflict occurs in small than large littersbecause offspring in small litters maintain a high growth rateat a relatively low maternal cost. Yet, under favorable environmentalconditions, the reduction in maternal-offspring conflict hasno apparent fitness benefit.     

Is tissue maturation necessary for flight? Changes in body composition during postnatal development in the big brown bat

Patterns of offspring development reflect the availability of energy and nutrients, limitations on an individual’s capacity to use available resources, and tradeoffs between the use of nutrients to support current metabolic demands and tissue growth. To determine if the long period of offspring dependency in bats is associated with the need for an advanced state of tissue maturation prior to flight, we examined body composition during postnatal growth in the big brown bat, Eptesicus fuscus. Despite their large size at birth (22% of maternal mass), newborn bats are relatively immature, containing 82% body water in fat-free mass. However, the total body water content of newborn bat pups decreases to near-adult levels in advance of weaning, while concentrations of total body fat and protein exceed adult values. In contrast to many other mammals, postnatal growth of bat pups was characterized by relatively stable concentrations of calcium and phosphorus, but declining concentrations of magnesium. These levels remained stable or rebounded in late postnatal development. This casts doubt on the hypothesis that low rates of mineral transfer necessitate an extended lactation period in bats. However, our finding of near-adult body composition at weaning is consistent with the hypothesis that extended lactation in bats is necessary for the young to achieve sufficient tissue maturity to undertake the active flight necessary for independent feeding. In this respect, bats differ from most other mammals but resemble birds that must engage in active flight to achieve nutritional independence.     

Body weight,energy metabolism,and time in the life of birds

The breeding of birds, both large and small, is affected by two specific factors: (1) hypometry of egg weight relative to female body weight and (2) seasonality of breeding, with the favorable period being limited and almost equal for birds of different body sizes. Dozens of published allometric formulas describing the dependence of energy parameters of eggs and nestlings at different growth stages and the energy cost of parental care on the body weight of parents, eggs, and nestlings, respectively, are reviewed. It is shown that birds, especially species with a large body weight, repeatedly change their metabolic parameters during ontogeny in order to shorten the period of breeding and growth. In most species, the energy costs of breeding in both sexes are approximately equal. Bringing food in the bill allows birds to supply nestlings with the amount of energy that is dozens of times greater than that expended for obtaining the food. In placental mammals, only females are involved in offspring development. Therefore, the growth rate of embryos and energy expenditures for milk feeding are limited by the metabolic potential of the mother. As a consequence, mammalian offspring grow ten times slower than bird nestlings, the body weights of females being equal.     

Variation in milk production and lactation performance in grey seals and consequences for pup growth and weaning characteristics

Phocid seals are one of the few groups of mammals capable of sustaining the energetic demands of lactation entirely through body nutrient stores while fasting. Lactation performance of the female in turn influences the rate and pattern of pup growth. We examined variation in and patterns of milk composition and production, maternal energy output, and pup growth and energy deposition over the entire lactation period in 18 grey seal mother-pup pairs using hydrogen isotope (3H2O and D2O) dilution. Milk composition was independent of maternal mass and nutrient stores, indicating dependence on other physiological and genetic factors. Heavier females lactated longer (r2=0.653, P<0.001), had higher total milk outputs (r2=0.652, P<0.001), and produced larger pups at weaning (r2=0.417, P=0.005). While fatter females lactated for longer periods of time (r2=0.595, P<0.001), females with a larger lean body mass at parturition produced more milk (r2=0.579, P<0.001). Total milk energy output was the strongest predictor of pup weaning mass, which, along with the pup's efficiency of energy storage, accounted for 91% of the variation in weaning mass. Nevertheless, there was sufficient plasticity in milk composition and energy output that some smaller females produced relatively large pups. Few females appeared to deplete body nutrients to the point where it might limit the duration of lactation.     

The coordination and interaction between respiration and deglutition in young pigs

The anatomical pathways for inspired air and ingested food cross in the pharynx of mammals, implying that breathing and swallowing must be separated either in space or in time. In this study we investigated the time relationship between swallowing and respiration in young pigs, as a model for suckling mammals. Despite the high morphological position of the larynx in young mammals, allowing liquid to pass in food channels lateral to the larynx, respiration and swallowing are not wholly independent events. Although, when suckling on a veterinary teat, the swallows occurred at various points in the respiratory cycle, there was always a period of apnea associated with the swallow. Finally, an increase in the viscosity of the milk altered this coordination, changing respiratory cycle length and also restricting the relative rate at which swallows occurred in some parts of the respiratory cycle. These results suggest that the subsequent changes in respiratory activity at weaning, associated with passage of a solid bolus over the larynx, is preceded by the ability of the animal to alter coordination between respiration and swallowing for a liquid bolus. Accepted: 29 September 1997     

Primate milk: proximate mechanisms and ultimate perspectives

To understand the evolutionary forces that have shaped primate lactation strategies, it is important to understand the proximate mechanisms of milk synthesis and their ecological and phylogenetic contexts. The lactation strategy of a species has four interrelated dimensions: the frequency and duration of nursing bouts, the period of lactation until weaning, the number and sex ratio of infants that a mother rears simultaneously, and the composition and yield of the milk that mothers synthesize. Milk synthesis, arguably the most physiologically costly component of rearing infants, remains the least studied. Energy transfer becomes energetically less efficient, transitioning from placental support to milk synthesis just as the energy requirements for infant growth, development, and behavioral activity substantially increase. Here we review primate lactation biology and milk synthesis, integrating studies from anthropology, biology, nutrition, animal science, immunology, and biochemistry, to identify the derived and ancestral features of primate milks and enhance our understanding of primate life history.     

Lactation in the tammar wallaby (Macropus eugenii). II. Intake of milk components and maternal allocation of energy

The intake of milk components (total solids, carbohydrate, protein, lipid, energy) by suckling tammar wallabies ( Macropus eugenii ), from peak lactation to independence, was measured using a double-isotope dilution technique and chemical analysis of milk samples. The time of peak intake of milk solids (day 256 of lactation or 1126 g of offspring weight) was similar to that for whole milk. Peak intake of carbohydrate occurred earlier than this (235 days) and peak intakes of protein and lipid occurred later (262 days and 266 days, respectively). Intake of gross energy peaked at 262 days and represented a maternal yield of about 207 KJ.Kg^-0.75.d^-1. This is much lower than peak lactational energy yields in most other mammals, but the duration of lactation is longer in tammars than in other mammals. Total output of energy in milk by tammar mothers was 63 MJ, and this would require an intake of about 98 MJ of metabolizable energy in food. This requirement, which is equivalent to 21 MJ/kg of maternal weight, is similar to those calculated for sheep and cattle, suggesting that there are not large differences between marsupial and placental herbivores in terms of weight-related allocation of energy to reproduction. We suggest that a strategy of minimizing the peak energetic demand of lactation may be an important adaptation for a small, primarily grazing mammal due to size-related physiological constraints on elevating herbage intake and the increasing risk from predators when grazing time is increased.