Maternal Care Strategies Research Articles

Altered Patterns of Maternal Behavior Transitions in Rats Exposed to Limited Bedding and Nesting Material Paradigm.

Maternal care plays a fundamental role in early life, and the alteration of its patterns can negatively affect the developmental course of the offspring in a myriad of domains in both rats and humans. The limited bedding and nesting (LBN) protocol is an extensively used paradigm in rodents to address the impact of altered maternal behavior patterns on infants' neurodevelopment. Here, we explore the altered patterns of maternal care in rats in LBN conditions by describing sequences of transition between maternal behavior components using network analysis. Using this technique, we capture how often maternal behavior transitions take place during the LBN period and which behaviors play central roles in those transitions over time. Female rats and their pups were placed in standard and LBN housing conditions from Postpartum Days 2 to 9, during which maternal behavior was observed during the light and dark phases. We used inferential statistical analysis to compare the maternal behavior profiles of control and LBN dams, and network analysis was used to capture the altered sequence of maternal behavior transitions during the period of LBN. Compared to control dams, LBN dams significantly increased their high crouch nursing posture during light/dark phases (p=0.018), and the number of behavioral transitions increased only during the dark phase (p=0.0004). Network analysis revealed specific altered patterns of behavioral transitions in LBN dams, characterized by the predominance of switches between active nursing postures during the first five days of the LBN protocol. Nursing behavior was the most disrupted component of maternal behavior under the LBN protocol, mainly during the dark phase. Network analysis can complement and extend traditional methods to gain a more thorough understanding of maternal care strategies and behavioral patterns in LBN conditions and potential consequences for the offspring.

Genotypic sex shapes maternal care in the African pygmy mouse, Mus minutoides.

Sexually dimorphic behaviours, such as parental care, have long been thought to be mainly driven by gonadal hormones. In the past two decades, a few studies have challenged this view, highlighting the direct influence of the sex chromosome complement (XX versus XY or ZZ versus ZW). The African pygmy mouse, Mus minutoides, is a wild mouse species with naturally occurring XY sex reversal induced by a third, feminizing X* chromosome, leading to three female genotypes: XX, XX* and X*Y. Here, we show that sex reversal in X*Y females shapes a divergent maternal care strategy (maternal aggression, pup retrieval and nesting behaviours) from both XX and XX* females. Although neuroanatomical investigations were inconclusive, we show that the dopaminergic system in the anteroventral periventricular nucleus of the hypothalamus is worth investigating further as it may support differences in pup retrieval behaviour between females. Combining behaviours and neurobiology in a rodent subject to natural selection, we evaluate potential candidates for the neural basis of maternal behaviours and strengthen the underestimated role of the sex chromosomes in shaping sex differences in brain and behaviours. All things considered, we further highlight the emergence of a third sexual phenotype, challenging the binary view of phenotypic sexes.

Maternal stress and vulnerability to depression: coping and maternal care strategies and its consequences on adolescent offspring

Depressive mothers often find mother-child interaction to be challenging. Maternal stress may further impair mother-child attachment, which may increase the risk of negative developmental consequences. We used rats with different vulnerability to depressive-like behavior (Wistar and Kyoto) to investigate the impact of stress (maternal separation-MS) on maternal behavior and adolescent offspring cognition. MS in Kyoto dams increased pup-contact, resulting in higher oxytocin levels and lower anxiety-like behavior after weaning, while worsening their adolescent offspring cognitive behavior. Whereas MS in Wistar dams elicited higher quality of pup-directed behavior, increasing brain-derived neurotrophic factor (BDNF) in the offspring, which seems to have prevented a negative impact on cognition. Hypothalamic oxytocin seems to affect the salience of the social environment cues (negatively for Kyoto) leading to different coping strategies. Our findings highlight the importance of contextual and individual factors in the understanding of the oxytocin role in modulating maternal behavior and stress regulatory processes.

Integrated Maternal Care Strategies in Low- and Middle-Income Countries: A Systematic Review

Background and aim:Ineffective organisation of care leads to increased morbidity and mortality in neonates and their mothers. We aimed to identify and describe strategies used in low- and middle-income countries that attempt to deliver coherent, coordinated, and continuous services (i.e., integrated care) and how the various strategies affect the organisation of care.Methods:We conducted a systematic literature review to identify, appraise, and synthesise relevant evidence about strategies for integrating maternal care in low- and middle-income countries, searching multiple electronic databases.Results:Fourteen studies met our inclusion criteria. We identified five types of integration strategies: 1) organisational, 2) service/professional, 3) functional, 4) organisational combined with normative strategies, and 5) clinical combined with functional integration strategies. The most frequent types of strategies were organisational, and service/professional integration strategies. We did not identify any publications describing systemic integration strategies implemented in low- and middle-income countries.Conclusions:Most types of strategies described in theory have been implemented and studied in low- and middle-income countries. Our findings suggest that different types of strategies may lead to comparable organisational outcomes. For example, organisational integration strategies and professional or service integration strategies may similarly influence inter-organisational collaboration. Inter-organisational collaboration may play a particularly important role in the context of maternal care integration.

Antipredator tactics are largely maternally controlled in goitered gazelle, a hider ungulate

Predation is usually the primary cause of infant death among ungulate species, with the annual variation in the survival of neonates over their first summer a major factor in the population dynamics of many ungulates. Consequently, the maternal rearing strategy of a species is crucial for its reproductive success. Since the roles mothers and fawns play in the implementation of antipredator strategies in hider species have been poorly understood until now, this paper considers this behavior in the goitered gazelle, which is a typical hider species. I found that within the first month after birth goitered gazelle mothers largely controlled the behavior of their fawns both during the active period (determining the timing of separation and reunion with fawns, movement direction and speed, and bed site location) and the hiding period (keeping the hiding fawns under continuous watch from a distance, especially right after birth). With age the fawns’ mobility increased and cases of independent behavior of fawns apart from their mothers were found more often, though females continued to control their fawns’ behaviors. The main elements of the goitered gazelles’ maternal care strategy − generally related to protecting fawns from potential predator attack − are very similar to other hider species in both bovids and cervids, which demonstrates a standard set of maternal care behaviors, irrespective of predator type or its behavioral peculiarities. Such maternal behaviors, however, likely only decrease the predation losses to a certain extent.

Resin-enabled maternal care is an old evolutionary strategy in New World resin bugs (Hemiptera: Reduviidae)

New World resin bugs (Harpactorinae: Apiomerini) in the genus Apiomerus Hahn, 1831 use plant resins for enhanced prey capture and store resins for maternal care behaviours. The evolutionary history of maternal care strategies across the tribe Apiomerini is unknown because of the lack of a comprehensive phylogeny as well as a lack behavioural data for critical taxa. We here present the first combined morphological and molecular phylogenetic analysis of New World resin bugs that includes representatives of all 13 fossil and extant genera, 112 morphological characters, and 2942 bp of molecular data. Given the lack of direct natural history observations for certain taxa, morphological characters are used as proxies to infer resin-storing and egg-coating maternal behaviours. Phylogenetic hypotheses derived from the combined analyses support three suprageneric clades (Apiomerus, Heniartes, and Manicocoris groups), provide diagnostic features, and place the Dominican amber fossil Apicrenus fossilisMaldonado Capriles, Santiago-Blay & Poinar, 1993 within the Manicocoris clade. Ancestral state reconstruction of characters involved in resin storing and egg coating indicates that this maternal care strategy is not restricted to Apiomerus. Instead, these behaviours are likely to have evolved at the base of the Apiomerus + Manicocoris clade, representing an ancient case of maternal care in this group of insects that originated in the Palaeogene.

Sex-biased parental care and sexual size dimorphism in a provisioning arthropod

The diverse selection pressures driving the evolution of sexual size dimorphism (SSD) have long been debated. Whilst the balance between fecundity selection and sexual selection has received much attention, explanations based on sex-specific ecology have proven harder to test. In ectotherms, females are typically larger than males, and this is frequently thought to be because size constrains female fecundity more than it constrains male mating success. However, SSD could additionally reflect maternal care strategies. Under this hypothesis, females are relatively larger where reproduction requires greater maximum maternal effort—for example where mothers transport heavy provisions to the nests. To test this hypothesis, we focussed on digger wasps (Hymenoptera: Ammophilini), a relatively homogeneous group in which only females provision offspring. In some species, a single large prey item, up to ten times the mother’s weight, must be carried to each burrow on foot; other species provide many small prey, each flown individually to the nest. We found more pronounced female-biased SSD in species where females carry single, heavy prey. More generally, SSD was negatively correlated with the numbers of prey provided per offspring. Females provisioning multiple small items had longer wings and thoraxes, probably because smaller prey are carried in flight. Despite much theorising, few empirical studies have tested how sex-biased parental care can affect SSD. Our study reveals that such costs can be associated with the evolution of dimorphism, and this should be investigated in other clades where parental care costs differ between sexes and species.

Antipredator strategy of female goitered gazelles (Gazella subgutturosa Guld., 1780) with hiding fawn

In ungulates, predation is often a major cause of infant mortality and likely plays an important role in shaping maternal care strategies that favor progeny survival. The anti-predator strategies of ungulates can be broadly categorized into two groups, hiding infants and following infants. We studied the maternal behavioral strategies of goitered gazelle, which is a typical representative of a hiding species. We found that shortly after birth, goitered gazelle mothers (1) stayed at the greatest distances from their hiding fawns; (2) spent the shortest amount of time together with their fawns, and then only for suckling (during the active phase) which was also the longest inter-suckling intervals (during the hiding phase); (3) kept twins separated in different hiding places and suckled them individually one after the other; (4) changed fawns’ hiding places after every active period, travelling with them during the whole suckling bout; (5) oriented their body and muzzle most often toward their hiding young during the fawn’s hiding phase; and (6) demonstrated the highest level of vigilance during their approaches to their hiding fawns. The anti-predator strategy of goitered gazelle females was similar to that observed in some North American (Antilocapra americana, Odocoileus hemionus and Odocoileus virginianus) and Eurasian (Dama dama and Capreolus capreolus) ungulate species that also demonstrate hiding behavior. Females of these species live on different continents with disparate environments and different predatory threats, but share anti-predator strategies, which are likely the result of convergent evolution in Bovids and Cervids.

Stunting at birth: recognition of early-life linear growth failure in the western highlands of Guatemala.

Measurements of length at birth, or in the neonatal period, are challenging to obtain and often discounted for lack of validity. Hence, classical 'under-5' stunting rates have been derived from surveys on children from 6 to 59 months of age. Guatemala has a high prevalence of stunting (49.8%), but the age of onset of growth failure is not clearly defined. The objective of the study was to assess length-for-age within the first 1.5 months of life among Guatemalan infants. As part of a cross-sectional observational study, supine length was measured in young infants. Mothers' height was measured. Length-for-age Z-scores (HAZ) were generated and stunting was defined as HAZ <-2 using WHO growth standards. Eight rural, indigenous Mam-Mayan villages (n 200, 100% of Mayan indigenous origin) and an urban clinic of Quetzaltenango (n 106, 27% of Mayan indigenous origin), Guatemala. Three hundred and six newborns with a median age of 19 d. The median rural HAZ was -1.56 and prevalence of stunting was 38%; the respective urban values were -1.41 and 25%. Linear regression revealed no relationship between infant age and HAZ (r = 0.101, r(2) = 0.010, P = 0.077). Maternal height explained 3% of the variability in HAZ (r = 0.171, r(2) = 0.029, P = 0.003). Stunting must be carried over from in utero growth retardation in short-stature Guatemalan mothers. As linear growth failure in this setting begins in utero, its prevention must be linked to maternal care strategies during gestation, or even before. A focus on maternal nutrition and health in an intergenerational dimension is needed to reduce its prevalence.

Factors influencing egg parasitism in sub-social insects: insights from the treehopperAlchisme grossa(Hemiptera, Auchenorrhyncha, Membracidae)

Subsocial insects rely on maternal care in order to enhance offspring survival. Subsocial Hoplophorionini treehoppers defend their egg masses from predatory and parasitoid attacks. Egg parasitic wasps are important enemies of the Membracidae. We examined parasitism patterns and female defence mechanisms in the Hoplophorionini treehopper Alchisme grossa (Fairmaire). We examined the effect of aggregations of egg-guarding females, spatial aggregations of host plants and female A. grossa, and host plant identity on the incidence of egg mass parasitism. Additionally, we measured the effect of female maternal care strategies on reducing the amount of parasitism on their egg masses. Aggregation of egg-guarding females on a single host plant was the most important factor affecting egg mass parasitism. Increased numbers of aggregated females lowered both parasitism risk and parasitism levels on their egg masses. When spatial clumping of host plants and egg-guarding females occurred simultaneously, parasitism risk was also reduced. Maternal care strategies such as coverage of the egg mass by the females' pronota and intensity of female defensive behaviour also seemed to lower parasitism on egg masses. A reduction of parasitism by female aggregation on host plants can be explained by a selfish herd dilution effect. This dilution effect was potentiated by a possible cooperation between aggregated egg-guarding females on the host plant. The present study provides a new dimension to sub-sociality in Hoplophorionini treehoppers.

Stunting at birth: An under‐recognized phenomenon with implications for maternal health and nutrition

BackgroundMeasurements of length at birth or in the neonatal period are challenging to obtain and often discounted for lack of standardization and validity. Classical “under‐five” stunting rates derive from surveys on children from 6 to 59 mo of age.ObjectiveTo assess length‐for‐age (LAZ) within the first 1.5 mo of life among infants from urban (U) and rural (R) sites in the Quetzaltenango Province in the Western Highlands of Guatemala.MethodsSupine length was measured to the nearest 0.5 cm by standardized anthropometrics on a SECA 210 infantometer. 104 infants (39% F) were enrolled in 8 rural Mam‐speaking R villages at 2–46 d of life. 106 infants (50% F) were recruited at an urban U health clinic at 4–33 d of life. Stunting was defined as ≤2 SD of LAZ in relation to the 2006 WHO growth standards.ResultsIn R sites, 100% were indigenous (Mam); in the U site, 27% were of indigenous ascent and 73% non‐indigenous. The median R LAZ was −1.55 and prevalence of stunting was 36.5%; the respective U values were −1.41, and 25.5%. The Pearson correlation coefficient of LAZ vs maternal stature for combined U+R was r=0.202 (n=210, p=0.02).ConclusionAs linear growth failure in this setting begins in utero, its prevention cannot begin at birth, but must be linked to maternal care strategies during gestation, or even before. Funded by the Nestle Foundation, McGill University, and Graduate Women in Science

Predation drives interpopulation differences in parental care expression

Expressing parental care after oviposition or parturition is usually an obligate (evolved) trait within a species, despite evolutionary theory predicting that widespread species should vary in whether or not they express parental care according to local selection pressures. The lizard Eutropis longicaudata expresses maternal care only in a single population throughout its large geographical range, but why this pattern occurs is unknown. We used reciprocal translocation and predator exclusion experiments to test whether this intraspecific variation is a fixed trait within populations and whether predator abundance explains this perplexing pattern. Wild-caught female lizards that were reciprocally translocated consistently guarded or abandoned eggs in line with their population of origin. By contrast, most lizards raised in a common garden environment and subsequently released as adults adopted the maternal care strategy of the recipient population, even when the parents originated from a population lacking maternal care. Egg predation represents a significant fitness cost in the populations where females display egg-guarding behaviour, but guarding eggs outweighs this potential cost by increasing hatching success. These results imply that predators can be a driving force in the expression of parental care in instances where it is normally absent and that local selection pressure is sufficient to cause behavioural divergence in whether or not parental care is expressed.

Delayed onset of vocal recognition in Australian sea lion pups (Neophoca cinerea)

In pinnipeds, maternal care strategies and colony density may influence a species' individual recognition system. We examined the onset of vocal recognition of mothers by Australian sea lion pups (Neophoca cinerea). At 2 months of age, pups responded significantly more to the calls of their own mothers than alien female calls demonstrating a finely tuned recognition system. However, newborn pups did not respond differentially to the calls of their mother from alien female calls suggesting that vocal recognition had not yet developed or is not yet expressed. These findings are in stark contrast to other otariid species where pups learn their mother's voice before their first separation. Variance in colony density, pup movements, and natal site fidelity may have reduced selective pressures on call recognition in young sea lions, or alternatively, another sensory system may be used for recognition in the early stage of life.

Lactation patterns of pinnipeds are not explained by optimization of maternal energy delivery rates

Within pinnipeds, phocids and otariids show differing maternal care strategies. Phocids rear young out of body stores in a yearly cycle with a single stay ashore when the mother fasts while lactating, whereas otariids provision their young by repeated foraging trips to sea alternating with brief stays ashore where they suckle their young. In a previous optimality model, these differences have been interpreted as adaptations based on differing energy requirements of large (phocid) and smaller (otariid) species, and the time budget of the large elephant and the much smaller Antarctic fur seal were correctly predicted. Our refined model—extended to pinniped species of all sizes—predicts lactation strategies to shift from attendance cycles to 1-year cycles with increasing body mass and provides an explanation for the finding that phocid pups are weaned at lower relative mass than otariid pups. However, other predictions do not correspond to empirical findings. In particular, the model does not explain the behavior of large otariids and small phocids. Thus, maternal metabolic requirements alone appear insufficient to explain observed lactation patterns. In the light of our results, we discuss more generally the scope and limitations of optimality models when applied in a comparative framework to a group of related species.

Convergent maternal care strategies in ungulates and macropods.

Mammals show extensive interspecific variation in the form of maternal care. Among ungulates, there is a dichotomy between species in which offspring follow the mother ("following" strategy) versus species in which offspring remain concealed ("hiding" strategy). Here we reveal that the same dichotomy exists among macropods (kangaroos, wallabies and allies). We test three traditional adaptive explanations and one new life history hypothesis, and find very similar patterns among both ungulates and macropods. The three traditional explanations that we tested were that a "following" strategy is associated with (1) open habitat, (2) large mothers, and (3) gregariousness. Our new life-history hypothesis is that a "following strategy" is associated with delayed weaning, and thus with the "slow" end of the slow-fast mammalian life-history continuum, because offspring devote resources to locomotion rather than rapid growth. Our comparative test strongly supports the habitat structure hypothesis and provides some support for this new delayed weaning hypothesis for both ungulates and macropods. We propose that sedentary young in closed habitats benefit energetically by having milk brought to them. In open habitats, predation pressure will select against hiding. Followers will suffer slower growth to independence. Taken together, therefore, our results provide the first quantitative evidence that macropods and ungulates are convergent with respect to interspecific variation in maternal care strategy. In both clades, differences between species in the form of parental care are due to a similar interaction between habitat, social behavior, and life history.

CONVERGENT MATERNAL CARE STRATEGIES IN UNGULATES AND MACROPODS

Mammals show extensive interspecific variation in the form of maternal care. Among ungulates, there is a dichotomy between species in which offspring follow the mother (“following” strategy) versus species in which offspring remain concealed (“hiding” strategy). Here we reveal that the same dichotomy exists among macropods (kangaroos, wallabies and allies). We test three traditional adaptive explanations and one new life history hypothesis, and find very similar patterns among both ungulates and macropods. The three traditional explanations that we tested were that a “following” strategy is associated with (1) open habitat, (2) large mothers, and (3) gregariousness. Our new life-history hypothesis is that a “following strategy” is associated with delayed weaning, and thus with the “slow” end of the slow-fast mammalian life-history continuum, because offspring devote resources to locomotion rather than rapid growth. Our comparative test strongly supports the habitat structure hypothesis and provides some support for this new delayed weaning hypothesis for both ungulates and macropods. We propose that sedentary young in closed habitats benefit energetically by having milk brought to them. In open habitats, predation pressure will select against hiding. Followers will suffer slower growth to independence. Taken together, therefore, our results provide the first quantitative evidence that macropods and ungulates are convergent with respect to interspecific variation in maternal care strategy. In both clades, differences between species in the form of parental care are due to a similar interaction between habitat, social behavior, and life history.Corresponding Editor: B. Crespi

The duration of lactation in feral coypus (Myocastor coypus)

The frequency of consecutive reproductive stages in a post mortem sample of 423 lactating coypus was used to estimate the mean post partum interval (Dpp) and the mean duration of lactation (D1). The estimates required a number of assumptions but the most important involved the validity of making time specific inferences from an “age” series. Variation statistics could not be calculated using conventional techniques and the jacknife method of estimation was used to obtain variances of the means and 95 % confidence intervals. Dpp was estimated as 21 ± 0–8 weeks. Some observations of retrapped wild animals showed that some animals conceived at an oestrus which occurred within a day or two of parturition. Dl was estimated in four different ways, three of which were quite closely related: these averaged 8–4 ± 10 weeks. But the fourth estimate, which is equally valid, was 70 weeks. A weighted average of the four estimates was 7–7 weeks with 95 % confidence limits of c. ± 10. The average suckling period of five captive females was 10–9 weeks. The most likely interpretation of the 42 % difference between this value and the estimate for wild females is attenuation as a result of a reduced nutrient intake in the feral population. DL is substantially longer than predicted from an expression relating maternal weight to DL in other mammals. This may be part of a maternal care strategy that centres on protection of space, and possibly of a food supply for milk production, rather than on defence of the young.