Further evidence for sex differences in suckling behaviour of captive plains zebra foals

Sex differences in suckling behaviour could be explained either by different maternal investment or by different behaviour of young. Previously, we found sex differences in rejection and termination of suckling bouts in captive plains zebras (Equus burchellii). In this study, we analysed the length of suckling bout interruptions and unsuccessful subsequent attempts which followed a successful suckling bout in plains zebra foals at Dvůr Králové Zoo. When a suckling bout was interrupted, male foals resumed the bout sooner than female foals. The probability of a subsequent attempt decreased with increasing age in female foals but did not change in male foals. These results demonstrate higher effort in suckling interest by male foals, who tried to suckle more than female foals. Although we found sex bias in the effort to suckle, which suggested higher parent–offspring conflict in male offspring, we cannot omit a sex bias in milk supply by the mother.     

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.     

A case of adoption and allonursing in captive plains zebra (Equus burchellii)

Although allonursing (allowing non-filial offspring to suckle) can be a costly behaviour, it has been reported for many mammals including ungulate species. However, such behaviour is very rare in equids. This is the first report on adoption and allonursing in captive plains zebra (Equus burchellii), recorded in the Dv?r Králové Zoo, Czech Republic. We observed a case of adoption of an orphaned foal by a lactating mare, who then regularly nursed two foals (filial and non-filial). The allonursing mare rejected more suckling attempts, terminated suckling bouts more often, and had a shorter suckling bout duration than other mares. When nursing both foals at the same time, the suckling bout lasted for less time than when nursing a single foal, regardless of whether it was filial or non-filial. The allonursing mare apparently did not discriminate between the filial and non-filial foal.     

Maternal care and foal social relationships in a herd of Sorraia horses: Influence of maternal rank and experience

The influence of maternal rank and experience on patterns of maternal care and social relationships of foals were investigated in a managed herd of Sorraia horses, Equus caballus. Social interactions and spatial relationships of 13 foals (seven females and six males) born to seven mares were examined from birth to 10 months of life, within the three major periods of foal development. Conflict over suckling between dam and foal was not generally affected by rank and experience, but higher-ranking mothers allowed more suckling during late lactation than lower-ranking mothers. Foals of higher-ranking mares spent more time in proximity to the mother during socialization. Maternal rank and experience did not significantly affect maternal protectiveness, foal independence from the mother or the development of affiliative relationships between foals and group members. Foals of higher-ranking mares received lower frequencies of aggression from other horses only in the first month of life. Dominance relationships among foals depended mainly on aggressiveness and were not associated with maternal rank. The large variability in maternal behaviour, the absence of a significant association between maternal rank and body condition at parturition and the stable social environment within this herd may partly account for the reported results.     

Suckling behavior in goitered gazelle: do females invest more in twins or singletons?

The mother–offspring social unit is a universal feature in the social life of all mammals and nursing is the most direct and vital component of maternal investment in young. Living in diverse environments, various ungulate species have different strategies for rearing offspring, from bearing a single, relatively large newborn and supplying only limited amounts of milk, to bearing several relatively small newborns with intensive post-partum lactation. In this paper, we consider the rearing strategy of goitered gazelle with a focus on suckling behavior, which, until now, has never been a subject of special investigation. Adult females of this species in their reproductive prime typically bear twins when environmental conditions are favorable, but the proportion of singletons increases when conditions are unfavorable. We expected that in goitered gazelles suckling intensity would be maximal during the first weeks after birth, and then decrease with the growth of the young; we also expected that twins would demand more energy, but receive significantly less maternal investment per young than singletons. We found that, indeed, suckling behavior had similar dynamics as typical of all bovid species, but our expectation for less maternal investment in twins vs. singletons was wrong. In reality, female goitered gazelles suckled twins significantly more intensively and terminated suckling less often compared to singletons. We concluded that in favorable situations females of high quality have the ability to show significantly more maternal investment in each twin, while singletons are typically born to weaker females. This ability of females to produce mostly twins allows goitered gazelles to take advantage of any favorable opportunity to quickly increase their population in an environment with unpredictable and abrupt yearly changes typical of the arid regions of Central Asia.     

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.     

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.     

Maternal Lineage of Warmblood Mares Contributes to Variation of Gestation Length and Bias of Foal Sex Ratio

Maternal lineage influences performance traits in horses. This is probably caused by differences in mitochondrial DNA (mtDNA) transferred to the offspring via the oocyte. In the present study, we investigated if reproductive traits with high variability—gestation length and fetal sex ratio—are influenced by maternal lineage. Data from 142 Warmblood mares from the Brandenburg State Stud at Neustadt (Dosse), Germany, were available for the study. Mares were grouped according to their maternal lineage. Influences on the reproduction parameters gestation length and sex ratio of offspring were analyzed by simple and multiple analyses of variance. A total of 786 cases were included. From the 142 mares, 119 were assigned to six maternal lineages with n≥10 mares per lineage, and 23 mares belonged to smaller maternal lineages. The mean number of live foals produced per mare was 4.6±3.6 (±SD). Live foal rate was 83.5%. Mean gestation length was 338.5±8.9 days (±SD) with a range of 313 to 370 days. Gestation length was affected by maternal lineage (p<0.001). Gestation length was also significantly influenced by the individual mare, age of the mare, year of breeding, month of breeding and sex of the foal (p<0.05). Of the 640 foals born alive at term, 48% were male and 52% female. Mare age group and maternal lineage significantly influenced the sex ratio of the foals (p<0.05). It is concluded that maternal lineage influences reproductive parameters with high variation such as gestation length and foal sex ratio in horses. In young primiparous and aged mares, the percentage of female offspring is higher than the expected 1:1 ratio.     

Individual mares bias investment in sons and daughters in relation to their condition

The Trivers-Willard hypothesis (TWH) predicts that a mother will treat a son or daughter differently depending on her ability to invest and the impact of her investment on offspring reproductive success. Although many studies have investigated the hypothesis, few have definitively supported or refuted it because of confounding factors or an inappropriate level of analysis. We studied maternal investment in sons and daughters in feral horses, Equus caballus, which meet the assumptions of the TWH with a minimum of confounding variables. Population level analyses revealed no differences in maternal behaviour towards sons and daughters. When we incorporated mare condition, we found that sons were more costly to mares in good condition, whereas daughters were more costly to mares in poor condition, although no differences in maternal behaviour were found. However, since the TWH makes predictions about individual mothers, we examined investment by mares who reared both a son and a daughter in different years of the study. Mares in good condition invested more in their sons in terms of maternal care patterns, costs to maternal body condition and costs to future reproduction. Conversely, mares in poor condition invested more in daughters. Therefore, with an appropriate level of analysis in a species in which confounding variables are minimal, the predictions of the Trivers-Willard hypothesis are supported. Copyright 2000 The Association for the Study of Animal Behaviour.     

Sucking motivation and related problems in calves

Since survival of the young mammals depends on sucking success, it is assumed that sucking motivation must be strong and that sucking deprivation would result in frustration which could have a negative impact on their welfare. This concern as well as that regarding cross-sucking between calves and intersucking between older animals has stimulated research on the motivation of calves for non-nutritive sucking. Non-nutritive sucking is elicited by the ingestion of milk, and the lactose concentration in milk, rather than that of fat or protein, is the main factor stimulating non-nutritive sucking. Every time a calf drinks milk, it is stimulated to suck and deprivation of sucking may interfere with digestive processes or satiety. To understand the behaviour of the calf during nutritive sucking, we examined the effects of milk flow on calves' sucking and butting an artificial feeding system. Slowing and stopping the flow rate stimulates butting and can lengthen the duration of sucking for the meal. It also stimulates the calf to switch teats when a second teat is available. These findings are well correlated to our observations of the calf suckling a cow in experimental manipulations. The duration of the meal is not correlated with milk intake, but it is influenced by milk availability and how hungry the calf is. Furthermore, calves will butt more often when there is less milk available in the dam's udder, presumably because milk flow is slower. Consequently, it is the occurrence of butting rather than sucking duration that would be a good indicator of milk intake when the calf is suckling the dam. Finally, we recommend a combination of slower milk flow and hay feeding and the provision of a non-nutritive artificial teat to reduce the occurrence of cross-sucking following a milk meal.     

On lactation and associated behaviour in a natural herd of horses

Developmental changes in time spent suckling and related mother-foal behaviour are described in an unmanaged herd of Camargue horses. Male foals spent about 40% more time suckling than females during the first 8 weeks. Body weight did not differ between the sexes but time-budgets did: males grazed less and were more active. If pregnant, the typical multiparous mare nursed her foals for 35–40 weeks, males and females alike, and weaned them 15 weeks before the next foaling. Primiparae lactated longer and weaned closer to the next foaling by 5 weeks. The mares played an active role in regulating the time spent suckling in early, and particularly in late lactation.     

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.     

Milk intake and production curves and allosuckling in captive Iberian red deer, Cervus elaphus hispanicus

In two experiments, we compared milk intake (assessed by weighing calves before and after suckling) and milk production (by hand milking hinds) in Iberian red deer both when calves sucked their mothers together (group-suckling experiment) and when mother and offspring were isolated (isolation-suckling experiment). In both experiments, the general lactation curve for calves increased to a peak and then decreased (type I, standard lactation curve in mammals), whereas the curve for hinds decreased from the start (type II). However, in the experiment on group suckling, calves ingested 17.2% more milk than that produced by their mothers from weeks 6 to 20. In both isolation- and group-suckling experiments, hinds showed an overproduction of milk decreasing from weeks 1 to 5. This decreasing overproduction coincides with a similar trend in calf mortality reported in the literature and might thus be aimed at ensuring calves have sufficient nutrients when mortality is highest. In addition, allosuckling observations in the group-suckling experiment showed an inverse relationship between milk production and percentage of allosucking attempts. Allosucking attempts were also more frequent after the milk overproduction period. Both findings suggest that allosuckling is a response to compensate for a reduced maternal milk supply. Copyright 2000 The Association for the Study of Animal Behaviour.     

Periparturient events in ovariectomized embryo transfer recipient mares

Ovariectomized mares treated with progesterone have established and maintained pregnancy after embryo transfer. This study evaluated the ability of ovariectomized embryo transfer recipients to successfully undergo parturition, raise a foal, and return to a useful reproductive status. Periparturient events in three ovariectomized embryo transfer recipient mares and three intact mares were compared. All mares foaled normally. Mammary scores were similar for both groups and all mares produced sufficient colostrum and milk to allow normal growth of healthy foals. Plasma progesterone levels decreased to < 5 ng/ml by Day 4 post partum in both groups. Progesterone concentrations continued to decrease and remained at <1 ng/ml in ovariectomized mares, but increased after the first postpartum ovulation (Day 9 to 15) in intact mares. Endometrial involution as determined by histological evaluation was complete in ovariectomized mares by Day 10 post partum and in intact mares by Day 11 post partum. As assessed by palpation per rectum and clearance of bacteria from the uterus, uterine involution was similar in all mares. The three ovariectomized mares subsequently received embryos by transcervical transfer and two of them established pregnancy. These results indicate that normal parturition, lactation, maternal behavior and uterine involution are independent of ovarian function.     

Lactation in the tammar wallaby (Macropus eugenii). I. Milk consumption and the algebraic description of the lactation curve

The milk intake of suckling tammar wallabies ( Macropus eugenii ) was estimated between 213 and 339 days of age using a double-isotope procedure in which tritiated water (TOH) was injected into the dams and deuterium oxide (D₂O) injected into the offspring. Recycling of isotopes between mothers and offspring was shown not to be a significant source of error. Estimates of body water (isotope dilution space) in the mothers or offspring, as a proportion of their body weight, were similar to values obtained with other macropodids and with placental mammals (0.73–0.75). Total water inflow in the offspring increased throughout the period, but the proportion of this contributed by milk fell in sigmoid fashion from 95.6% at 213 d to 3.7% at 340 d. Milk intakes reached a peak of about 86 ml/d, which was low compared with placental species. Before the peak, intakes were more closely related to body weight than age. Peak milk intake corresponded with the period of emergence from the pouch. Milk intakes were also in excellent agreement with published data obtained earlier in lactation, in animals drawn from the same population. These data were therefore combined to provide estimates of intake for the whole of lactation in the tammar wallaby, and algebraic models fitted to describe the pattern of milk intake in relation to body weight or age. With body weight, the pattern of milk intake was well described by a rising linear phase to a peak intake of about 86 ml/d near 1110 g body weight, followed by a gradual exponential decline. When related to age, the pattern was well described by a rising logistic phase (peak at 251 d) followed by a sharp exponential decline. It is shown that this latter pattern is markedly similar to the shape of the functions describing the energy requirements for the sum of pregnancy and lactation in a placental species, the sheep.     

Isotope recycling in lactating dogs (Canis familiaris)

Isotope-based techniques for the measurement of water turnover, energy expenditure, and milk intake often assume that there is no recycling of isotopes once they have left the labeled animal. In experiments involving lactating females or their suckling offspring, there are several possible routes of isotope recycling. These include the consumption of labeled milk by offspring, the ingestion of labeled excreta, and the rebreathing of exhaled labeled CO(2) or water vapor by both mother and offspring. Isotope recycling might be especially important during lactation because the offspring are in close contact with each other and their mother for prolonged periods. We show here in 24- to 30-day-old domestic dog Canis familiaris puppies that there was no detectable transfer of (18)O or (2)H from labeled to unlabeled pups in two litters (16 pups, 8 labeled, 8 unlabeled) that were weaned early and independent of their mother. However, there was a significant transfer of both isotopes from labeled to unlabeled pups and from labeled pups to their mothers in nine equivalent nursing litters of the same age (27 labeled, 26 unlabeled pups). The increases in enrichment of isotopes in unlabeled offspring were greater than the increases in enrichment of the mothers. This indicates that maternal ingestion of offspring excreta and subsequent transfer of isotope in milk is not the sole pathway of recycling. Additional routes must also be important, such as exchange of isotope between pups on saliva-coated nipples and perhaps direct ingestion of excreta by unweaned young. Recycling is unlikely to be an important factor when determining maternal metabolic rate during peak lactation in domestic dogs. However, experiments that are designed to assess the energy demands of pups and isotope-based estimates of water turnover in offspring may need to take into account any effects of isotope recycling. In a theoretical example, removing the effects of recycling increased the measured energy expenditure in pups by up to 7% and increased the calculated elimination rates of both isotopes by up to 11.1% in (18)oxygen and 10.9% in (2)hydrogen.     

Age of the Jeju pony (Equus caballus) at first reproduction: potential costs for foals and mothers that first reproduce early in life

In a related paper, we showed that mares that reproduced early in life tended to have higher fecundity because of a decrease in the duration of inter-birth intervals relative to mares that reproduced later in life. However, we know that young mares are subordinate to older mares. Hence, costs associated with low dominance rank might offset the benefits of earlier reproduction. We compared harassment of foals of female Jeju ponies that first reproduced at three years of age with that of foals of females that first reproduced at five years of age. As a consequence of their positions in the linear dominance hierarchy, foals born to and guarded by young mares were harassed more frequently than foals whose mothers were older when they first reproduced. A mare that reproduced early in life guarded her offspring more closely and intervened between her foal and neighboring mares more frequently than those mares which first reproduced when older. This need to guard their foals and the harm that might ensue from frequent harassment might counter-balance selection towards earlier reproduction in mares.     

Blood Selenium in Naturally Fed Horses and the Effect of Selenium Administration

Blood Se of adult horses was 26.1, 25.8, and 27.0 ng/ml (mean values at 3 farms), where the Se of food was about 20 ng/g dry substance. Experimental adult horses which received about 41 ng Se/g food showed 45.3 ng/ml blood. At low Se intake suckling foals show higher blood Se than mares, but with high Se intake, the opposite will occur. This is reflected in milk Se, which raises but slowly with rise of mare’s blood Se. Se in blood plasma and in blood corpuscles is on the same level. The effect of various dose levels of Se on blood Se was studied: From 1.5 to 6 mg Se/week, blood Se rose rather linearity; 18 and 30 rag Se/week gave but slightly more effect than 6 mg.     

Relationship between milk energy intake and growth rate in suckling mammalian young at peak lactation: an updated meta-analysis

The milk energy intakes and growth rates of suckling young at peak lactation of 62 mammalian species and subspecies, all measured using either the weigh–suckle–weigh, the isotope dilution or the isotope transfer method, were evaluated. The mean daily gross energy intakes (GEI) were as low as 12 kJ in a small rodent (mouse) to as high as 249 MJ in a phocid seal (hooded seal Cystophora cristata ), while the daily growth rates at peak lactation ranged from 0.4 to 5.9 kg. Several allometric equations were calculated to explore the relationships between gross energy intake via milk and body weight (BW), growth rate and BW, as well as between gross energy intake via milk and growth rate. The results suggest that both GEI via milk and growth rates are proportional to BW to the power of 0.82. Accordingly, the metabolic weight of suckling mammalian young should be expressed as BW^0.82. The predictive values of the calculated equations indicate that suckling young at peak lactation consume c . 883 kJ day⁻¹ kg⁻¹ BW^0.82 and have growth rates of 32 g day⁻¹ kg⁻¹ BW^0.82. However, large deviations for some species and few outliers were found. These equations could be used to predict values for species that have not been studied, provided that the BW falls within the range of weights used to derive the equations.     

Terminal reproductive effort in a marsupial

Life-history theory predicts that as organisms approach the end of their life, they should increase their reproductive effort (RE). However, studies on mammals often find that measures of RE do not vary with maternal age. This might be because offspring have some control over energy transfer which may constrain adaptive variation in RE by mothers, particularly in eutherian mammals where placental function is primarily controlled by offspring. However, in marsupials, energy transfer is primarily by lactation and under maternal control, leaving marsupial mothers free to vary RE. Here, we provide the first analysis, to our knowledge, of age-specific RE in a marsupial, the common brushtail possum. RE, measured as the proportion of maternal mass lost during lactation, was strongly correlated with offspring mass as a yearling. Older females had higher RE, gave birth earlier in the season and were more likely to produce two offspring in a year. Females with high RE in one year were lighter at the beginning of the next breeding season. These results provide the clearest support yet for terminal RE in a mammal.