Variation in body composition of female big brown bats (Eptesicus fuscus) during lactation

Most small mammals support the nutritional requirements of milk production by increasing food intake. However, when nutrient intake is low, maternal body reserves may be mobilized to maintain adequate milk output. We examined patterns of body composition, including dry matter, fat, protein, and mineral content in big brown bats, Eptesicus fuscus, during lactation. Concentrations of fat and phosphorus were markedly lower in lactating mothers during week three of lactation than during the first two weeks, but these constituents rebounded to previous levels in the fourth and fifth week. Rapid recovery from fat depletion suggests that females are able to adjust to changes in demands for energy. The decrease in phosphorus during mid-lactation suggests bone demineralization, but an interspecific comparison of adult concentrations of minerals prevalent in bone suggests that mineral concentrations may never reach critically low levels in reproductively active females.     

The energetics of lactation in cooperatively breeding meerkats Suricata suricatta

Species may become obligate cooperative breeders when parents are unable to raise their offspring unassisted. We measured the daily energy expenditure of mothers, helpers and offspring during peak lactation in cooperatively breeding meerkats Suricata suricatta using the doubly labelled water technique. Lactating mothers expended more energy per day than allo-lactating subordinate females, non-lactating females or suckling offspring. Metabolizable energy intakes of lactating mothers were calculated from isotope-based estimates of offspring milk energy intake, and were not significantly different from the previously suggested maximal limit for mammals. Allo-lactating females were the only category of animals that lost weight during the period of study, probably because they spent more time babysitting than non-lactating females. Daily energy expenditure (DEE) of lactating mothers increased with litter size but decreased with the number of helpers. Calculations show that for every 10 helpers, even in the absence of allo-lactators, mothers are able to reduce their DEE during peak lactation by an amount equivalent to the energy cost of one pup. These results indicate that helpers have beneficial energetic consequences for lactating mothers in an obligate cooperatively breeding mammal.     

Review: Nutrient requirements of the modern high-producing lactating sow,with an emphasis on amino acid requirements

Sow productivity improvements continue to increase metabolic demands during lactation. During the peripartum period, energy requirements increase by 60%, and amino acid needs increase by 150%. As litter size has increased, research on peripartum sows has focused on increasing birth weight, shortening farrowing duration to reduce stillbirths and improving colostrum composition and yield. Dietary fibre can provide short-chain fatty acids to serve as an energy source for the uterus prior to farrowing; however, fat and glucose appear to be the main energy sources used by the uterus during farrowing. Colostrum immunoglobulin G concentration can be improved by increasing energy and amino acid availability prior to farrowing; however, the influence of nutrient intake on colostrum yield is unequivocal. As sows transition to the lactation period, nutrient requirements increase with milk production demands to support large, fast-growing litters. The adoption of automated feed delivery systems has increased feed supply and intake of lactating sows; however, sows still cannot consume enough feed to meet energy and amino acid requirements during lactation. Thus, sows typically catabolise body fat and protein to meet the needs for milk production. The addition of energy sources to lactation diets increases energy intake and energy output in milk, leading to a reduction in BW loss and an improvement in litter growth rate. The supply of dietary amino acids and CP close to the requirements improves milk protein output and reduces muscle protein mobilisation. The amino acid requirements of lactating sows are variable as a consequence of the dynamic body tissue mobilisation during lactation; however, lysine (Lys) is consistently the first-limiting amino acid. A regression equation using published data on Lys requirement of lactating sows predicted a requirement of 27 g/day of digestible Lys intake for each 1 kg of litter growth, and 13 g/day of Lys mobilisation from body protein reserves. Increases in dietary amino acids reduce protein catabolism, which historically leads to improvements in subsequent reproductive performance. Although the connection between lactation catabolism and subsequent reproduction remains a dogma, recent literature with high-producing sows is not as clear on this response. Many practical aspects of meeting the nutrient requirements of lactating sows have not changed. Sows with large litters should approach farrowing without excess fat reserves (e.g. <18 mm backfat thickness), be fed ad libitum from farrowing to weaning, be housed in a thermoneutral environment and have their skin wetted to remove excess heat when exposed to high temperatures.     

Maternal condition influences phenotypic selection on offspring

1. Environmentally induced maternal effects are known to affect offspring phenotype, and as a result, the dynamics and evolution of populations across a wide range of taxa. 2. In a field experiment, we manipulated maternal condition by altering food availability, a key factor influencing maternal energy allocation to offspring. We then examined how maternal condition at the time of gametogenesis affects the relationships among early life-history traits and survivorship during early development of the coral reef fish Pomacentrus amboinensis. 3. Maternal condition did not affect the number of embryos that hatched or the number of hatchlings surviving to a set time. 4. We found no significant difference in egg size in relation to the maternal physiological state. However, eggs spawned by supplemented mothers were provisioned with greater energy reserves (yolk-sac and oil globule size) than nonsupplemented counterparts, suggesting that provision of energy reserves rather than egg size more closely reflected the maternal environment. 5. Among offspring originating from supplemented mothers, those with larger yolk-sacs were more likely to successfully hatch and survive for longer periods after hatching. However, among offspring from nonsupplemented mothers, yolk-sac size was either inconsequential to survival or offspring with smaller yolk-sac sizes were favoured. Mothers appear to influence the physiological capacity of their progeny and in turn the efficiency of individual offspring to utilize endogenous reserves. 6. In summary, our results show that the maternal environment influences the relationship between offspring characteristics and survival and suggest that energy-driven selective mechanisms may operate to determine progeny viability.     

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.     

Effects of quinestrol and levonorgestrel on prolactin serum concentration in lactating Mongolian gerbils (Meriones unguiculatus) and reproductive parameters of their offspring

The effects of the two sterilants, quinestrol (QE) and levonorgestrel (LNG) on serum prolactin (PRL) level in lactating Mongolian gerbils and reproductive parameters of their offspring were examined in the study. Both sterilants increased the serum PRL level in lactating gerbils. The body weight as well as weights of the ovary, testis, epididymides, and seminal vesicles were lower, whereas that of the uterus was higher in the pups originating from QE-treated mothers in comparison to controls. Histological ovarian sections of the offspring from QE-treated mothers contained only growing follicles, whereas their uterine sections showed a thinner endometrium, thicker myometrium, and greater epithelial-cell height than in controls. The histometrical testis characteristics as well as sperm concentration and motility of male pups from QE-treated mothers were lower compared to those of the control group. The serum gonadotropin levels of female pups from mothers treated with QE were lower, whereas the serum estradiol (E₂) and progesterone (P₄) levels were higher than in control gerbils. In contrast, serum gonadotropin and testosterone (T) levels of male pups from QE-treated mothers were lower compared to controls. LNG did not affect the examined parameters of the offspring. The offspring from QE-treated mothers was infertile, whereas the offspring from LNG-treated mothers was fertile. In summary, QE and LNG have a stimulatory effect on PRL level in lactating gerbils. It also appears that QE administered via milk to mothers affects reproductive processes of their offspring.     

Suckling ability and maternal prolactin levels in hypothyroid rats

Long-Evans rats and their offspring were made hypothyroid by addition of the antithyroid goitrogen 6-N-propylthiouracil (PTU) to the drinking water (0.1%) from the day of parturition. Serum concentrations of prolactin (PRL), thyroid-stimulating hormone (TSH) and thyroxine (T4) were determined by double radioimmunoassay (RIA). From the fifth postnatal day, body weight of PTU-treated pups was significantly lower than that of control rats, and a strikingly elevated serum TSH level and nondetectable amount of T4 were measured both in PTU-exposed mothers and their offspring at Day 10 postpartum. To test the youngs' suckling capability and the amount of maternal milk production, 10- and 15-day-old normal and PTU-treated pups were separated from their mothers for 4 hr in the morning and then reunited and allowed to suckle. Normal pups gained body weight at the end of both the first and second hour postreunion, while PTU pups gained only during the first hour and lost weight in the second hour of testing. When the pups were exchanged between normal and PTU mothers, opposite results were obtained, indicating that the reduced gain in hypothyroid rats was not due to impaired suckling capability, or insufficient sensory stimulation for milk secretion but to a decreased milk production of PTU mothers. In accordance with this, in lactating hypothyroid rats both the basal (presuckling) level and the suckling-induced rise of serum PRL were found significantly depressed.     

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.     

Relationship between reproductive resource allocation and resource capacity in the matriphagous spider, <Emphasis Type="Italic">Chiracanthium japonicum </Emphasis>(Araneae: Clubionidae)

Females of the Japanese foliage spider, Chiracanthium japonicum, are eaten by their offspring at the end of the maternal care period. To examine the patterns of allocation of maternal investment to their offspring associated with female resource capacity, the amounts of female body reserves accumulated before oviposition, reproductive components at the egg-production phase and those at the matriphagy phase were measured using an artificial breeding nest. Regardless of size, female bodies were completely consumed by the offspring, and larger females, i.e. those having larger reserves, produced a larger number of offspring, but not larger offspring. Furthermore, the proportion of reserves allocated to egg production was not affected by the total amount of the reserves, which indicated that the females systematically divided the resources for individual offspring between egg yolk and food for the growth and survival of the offspring. These results suggest that C. japonicum females adjust egg production to their own resource capacity so that they can achieve an investment per individual offspring which is not dependent on resource capacity. Electronic Publication     

Transgenerational effects of poor elemental food quality on Daphnia magna

Environmental effects on parents can strongly affect the phenotype of their offspring, which alters the heritability of traits and the offspring’s responses to the environment. We examined whether P limitation of the aquatic invertebrate, Daphnia magna, alters the responses of its offspring to inadequate P nutrition. Mother Daphnia consuming P-poor algal food produced smaller neonates having lower body P content compared to control (P-rich) mothers. These offspring from P-stressed mothers, when fed P-rich food, grew faster and reproduced on the same schedule as those from P-sufficient mothers. In contrast, offspring from P-stressed mothers, when fed P-poor food, grew more slowly and had delayed reproduction compared to their sisters born to control mothers. There was also weak evidence that daughters from P-stressed mothers are more susceptible to infection by the virulent bacterium, Pasteuria ramosa. Our results show that P stress is not only transferred across generations, but also that its effect on the offspring generation varies depending upon the quality of their own environment. Maternal P nutrition can thus determine the nature of offspring responses to food P content and potentially obfuscates relationships between the performance of offspring and their own nutrition. Given that food quality can be highly variable within and among natural environments, our results demonstrate that maternal effects should be included as an additional dimension into studies of how elemental nutrition affects the physiology, ecology, and evolution of animal consumers.     

Testing hypotheses for maternal effects in Daphnia magna

Maternal effects are widely observed, but their adaptive nature remains difficult to describe and interpret. We investigated adaptive maternal effects in a clone of the crustacean Daphnia magna, experimentally varying both maternal age and maternal food and subsequently varying food available to offspring. We had two main predictions: that offspring in a food environment matched to their mothers should fare better than offspring in unmatched environments, and that offspring of older mothers would fare better in low food environments. We detected numerous maternal effects, for example offspring of poorly fed mothers were large, whereas offspring of older mothers were both large and showed an earlier age at first reproduction. However, these maternal effects did not clearly translate into the predicted differences in reproduction. Thus, our predictions about adaptive maternal effects in response to food variation were not met in this genotype of Daphnia magna.     

Provisioning control during maternal care by the earwig Anisolabis maritima (Dermaptera: Anisolabididae): Do mothers adjust provisioning according to offspring need?

Provisioning offspring is an important form of parental care for the improvement of offspring survival and growth. Because provisioning can be costly for parents, parents may change their investment levels in response to offspring need and begging signals. Anisolabis maritima is a cosmopolitan species of earwig that shows subsocial behavior. Females progressively provision their young in soil burrows. The present study investigated whether A. maritima mothers carry food to the nest for their offspring (nymphs) and whether the mothers adjust the amount of food carried to the burrow according to the degree of the nymphs’ hunger. Through laboratory experiments, I found that mothers carried food to sites where more nymphs were present, and more food to broods of more hungry nymphs. These results have revealed that mothers recognize the presence of offspring and the degree of their hunger. This study, therefore, indicates the presence of offspring begging signals in A. maritima.     

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.     

Estimates of milk constituents from lactating bonnet macaque (Macaca radiata) mothers between two and seven months post‐partum

Background The literature regarding milk composition in non‐human primates collected across offspring development is limited. We assayed milk samples from bonnet macaque (Macaca radiata) mothers as part of studies characterizing development of this species. Methods Milk was obtained when possible longitudinally from seven lactating bonnet macaque mothers. Samples were frozen until analysis. Individual samples were analyzed to determine the concentrations of electrolytes including sodium, potassium, calcium, chloride, and magnesium, as well as urea, protein, lipids, glucose, and lactose. Results A trend for increased lipids as well as protein percentage was noted with increasing infant age. Chloride and calcium showed an increase with age, whereas other electrolytes remained relatively stable across development. Conclusions The composition of the milk of this particular macaque species was similar to other Old World primates as well as humans. These data add to the limited information available on milk constituents among mammals.     

Of mammals and milk: how maternal stress affects nursing offspring

1. A large body of research shows that maternal stress during an offspring’s early life can impact its phenotype in both the short and long term. In the Vertebrata, most research has been focused on maternal stress during the prenatal period. However, the postnatal period is particularly important in mammals because maternal milk provides a conduit by which maternal hormones secreted in response to stressors (glucocorticoids, GCs) can reach offspring. Moreover, lactation outlasts gestation in many species.
2. Though GCs were first detected in milk over 40 years ago, few studies have explored how they affect nursing offspring, and no reviews have been written on how maternal stress affects nursing offspring in the natural world.
3. We discuss the evolution of milk and highlight its importance in each of the three mammalian lineages: monotremes (subclass Monotremata), marsupials (infraclass Marsupialia), and eutherians (infraclass Placentalia). Most research on the effects of milk GCs on offspring has been focused on eutherians, but monotremes and marsupials rely on their mothers’ milk for a proportionally longer period of time, and so research on these taxa may yield more insight.
4. We show that GCs are important for milk production, both during an individual nursing bout and over the entire lactation period, and review evidence of GCs moving from maternal blood to milk, and eventually to nursing offspring. We examine evidence from rodents and primates of associations between GC levels in lactating females (either blood or milk) and offspring behaviour and growth rates. We discuss ways that maternal stress may impact these offspring phenotypes outside of milk GCs, such as changes to: (1) milk output, (2) other milk constituents (e.g. macronutrients, growth factors, cytokines), and (3) maternal care behaviour.
5. Critical to understanding the fitness impacts of elevated maternal GC levels during lactation is to place this within the context of the natural environment. Species-specific traits and natural histories will help us to understand why such maternal stress produces different offspring phenotypes that equip them to cope with and succeed in the environment they are about to enter.

     

Maternal effort and male quality in the bank vole, Clethrionomys glareolus.

Parental investment in reproduction is adjusted according to potential benefits in terms of offspring survival and/or mating success. If male quality affects the reproductive success of a female, then females mating with high-quality males should invest more in reproduction. Although the subject has been of general interest, further experimental verification of the hypothesis is needed. We studied whether female bank voles (Clethrionomys glareolus) adjusted their maternal effort according to male quality, measured as mating success. To enable the measurement of maternal effort during nursing separately from male genetic effects the litters were cross-fostered. Further, the genetic background of male quality was examined. Male quality did not correlate with litter size or offspring size at birth. Offspring growth was positively related to food consumption and milk production of mothers. However, these direct measurements of maternal effort were independent of male quality. Male mating success appeared to be significantly heritable indicating that there are genetic benefits. Still, females did not adjust maternal effort according to the genetic quality of their offspring. We suggest that female bank voles gain significant genetic benefits from mating with high-quality males whereas they cannot improve their reproductive success by increasing maternal effort.     

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.     

Maternal effects in Daphnia: what mothers are telling their offspring and do they listen?

Maternal effects can significantly impact offspring performance. Provisioning of offspring with energy stores can quantitatively alter their growth rates, survivorship, and future fecundity, and influence population regulatory mechanisms. In this paper, we show that maternal effects can also qualitatively affect offspring reproduction (i.e. their mode of reproduction). The freshwater herbivore Daphnia pulex can change the amount of energy allocated between asexual and ephippial egg production. Our experiments on individuals, experiencing “step‐up” or “step‐down” food manipulations, reveal that offspring qualitatively shift their energy allocation away from asexual reproduction to ephippial egg production when there is a simple mismatch between maternal and offspring food environments. We show that the response is asymmetric with respect to changes in food level, ephippial egg production is higher with a greater mismatch between environments, and that the effect can be observed in dynamic experimental populations. These results point to a “generational memory” that could challenge our interpretation of field patterns and mechanisms influencing population dynamics in Daphnia–algal systems.     

Adaptive responses at the whole lactation scale of Baladi dairy goats according to feed supply and level of body reserves in agro-pastoral feeding system

Two diets were tested on Baladi lactating goats during mid-lactation in order to determine their adaptive capacities facing feed restrictions: a low nutritive value pasture (LP) and a high nutritive value pasture (HP). During early lactation on natural pastures, goats’ body condition (BCS) degraded, as initially fat goats lost more weight (BW) and were subject to a greater body reserves mobilization (BCS and NEFA) than lean ones. An intense compensation for all goats followed their transfer to the HP whereas the mobilization continued in LP, but only for fat goats. The lean goats managed to maintain their body condition by increasing their feed intake. When moved to mixed agricultural pastures at late lactation, all goats showed a full reconstitution of body reserves, particularly intense for those coming from LP, showing their strong capacities to recover their body reserves at this period. In parallel, milk production decreased for all goats on natural pastures, as the milk fat and milk proteins content. After transfer to HP, the high lactation rebound (+36%) showed the good reactivity of the Baladi goat in response to a feed improvement. Another rebound appeared in groups coming from LP after being transferred to a better feeding condition. However, during the reproduction phase, the milk yields decrease showing the highest priority given to the body reserves recovery.     

Altered gravity effects on mothers and offspring: the importance of maternal behavior

In this paper, I review and discuss recent studies of pregnant, parturient and lactating rat mothers and neonates exposed to hypo- and hypergravity. These studies are revealing new insights into how deviations form Earth-normal gravity may affect fundamental reproductive and ontogenetic processes in mammals. By way of background, I will first briefly summarize the spaceflights that have carried mammalian mothers and their offspring into space.