Maternal Care in the Burrower Bug <Emphasis Type="Italic">Adomerus triguttulus</Emphasis>: Defensive Behavior

Some burrower bugs (Heteroptera: Cydnidae) show complex patterns of maternal care, including defense against predators and the provisioning of food to nymphs. Recently, the subsocial cydnid bugs have attracted the interest of researchers as model systems to study the behavioral ecology of parental investment. However, there have been few attempts to quantify the fitness benefits of maternal behavior other than provisioning. Here, we examined the maternal behavior of Adomerus triguttulus and its adaptive significance in terms of offspring survival in the field. A. triguttulus young depend on fallen nutlets of myrmecophorous mints, Lamium spp. Under field conditions, females attend offspring, from eggs to second instar nymphs, in nests on the ground under the litter. When disturbed, the females showed aggressive responses against the source of disturbance. The females often carried spherical clutches of eggs away from the nest when heavily disturbed. Female-removal experiments in the field demonstrated a defensive function of the female behavior; predators, such as ants, attacked egg clutches without females and the clutches often disappeared during the experiment. Egg clutches without females sometimes also suffered from fungal infection. Selective factors on maternal defensive behavior in A. triguttulus are discussed in terms of habitat properties possibly emerging from insect–plant associations.     

The effects of twinning and maternal experience on maternal-filial social relationships in confined beef cattle

The objective of this investigation was to assess the maternal-filial social relationships of Hereford beef cattle as influenced by maternal experience of the dam (primiparous vs. multiparous) and number of offspring (one vs. two calves). Calves were temporarily separated from their dams during the first week after parturition, and the behavioral responses of mother and young were noted during and following separation.Contact and contact-seeking behaviors between twins and their mothers began to decline by the 5th or 6th day post-partum. Over the same period, contact behaviors exhibited by single calves and their dams remained stable or increased in frequency. Mothers of twins were less responsive to their calves than mothers of singles both during and following separation, and twins interacted with alien females more frequently than single-born young. It is proposed that insufficient milk production by Hereford dams bearing two calves provides an incentive for twins to parasitize the milk supply of alien mothers and, thus, become less dependent on their natural mothers. Social feedback between mother and twins may be further reduced by dams dividing their maternal attentiveness between two offspring.In general, experienced cows were more responsive to separation from their offspring than inexperienced heifers. Cows and their calves exhibited more frequent contact and contact-seeking behavior than heifers and their young.     

Parity-associated reductions in behavioral sensitivity to opiates

Behavioral and physiological responses differ between primiparous and multiparous female rodents. Specifically, multiparous females respond with the full repertoire of maternal behaviors much more rapidly and with greater intensity than their primiparous counterparts. Since opiates inhibit the expression of maternal behavior in postpartum rats and can be reversed by means of the opiate antagonist naloxone, we investigated whether multiparous females would be resistant to the inhibitory effects of opiates on maternal behavior, relative to primiparous females. In Experiment 1 we evaluated the effects of a range of doses of morphine sulfate (MS; 0.625, 1.25, 2.5, 5.0, and 10.0 mg/kg or saline) on maternal behavior in primiparous females on Days 5-6 of lactation. The 5.0 and 10.0 mg/kg doses effectively disrupted maternal behavior, whereas the lower doses were ineffective or only marginally disruptive. In Experiment 2, age-matched female rats were timed-mated and tested for maternal behavior from Day 5 to 13 of lactation, after daily injections of the 5.0 mg/kg dose of MS. On Day 5 of lactation, this morphine treatment eliminated full maternal behavior in 87% of the primiparous animals, but only 37% of the multiparous animals were affected. By Day 10 of lactation, 100% of the multiparous females displayed full maternal behavior after MS treatment, whereas only 69% of primiparous females were responsive. In Experiment 3, analgesic responses were measured both in rats experiencing their initial or second pregnancy, and in postpartum, lactating rats after MS (5.0 mg/kg) administration. Using a tail-flick apparatus to measure analgesia, we found multigravid females to be significantly less analgesic prepartum than primigravid females, suggesting less sensitivity to endogenous opioids.(ABSTRACT TRUNCATED AT 250 WORDS)     

Evidence for Sex-Biased Behavioral Maternal Investment in the Gray Mouse Lemur (Microcebus murinus)

To study sex-differential allocation of maternal behavior in Microcebus murinus, I recorded behavioral patterns on 21 litters from parturition to the weaning period. After a pregnancy of 61.5 ± 0.9 days, females may produce from one to four young per litter. Litters were weaned in 40 days by mothers. Behavioral observations at the beginning of the nocturnal activity period demonstrated that close contacts between mothers and infants were more frequent in multiparous mothers than in primiparous ones (p < .01). Time in close contact with offspring aged >15 days old compared to contacts with neonates is significantly lower only in single-sex litters and is more marked for all-female litters (p < .01). Mother's approaches toward mixed litters or all-male litters were always significantly greater than approaches toward all-female litters (p = .04). However, mother's approaches within mixed sex litters were not biased toward either sex (p = .7). Males in a litter may be interpreted as a stimulator of maternal behavior. Similarly, using retrieving tests of 15-min duration, a significant maternal preference for male neonates is evident. Latency to first retrieval is significantly shorter in multiparous females than in primiparous ones (p < .05) independent of size and sex ratio of the litter. For multiparous females only, male neonates were chosen first for retrieval more often than females (p < .05). Finally, the calls of young played a stimulator effect on maternal retrieving (p < .001). Accordingly multiparous mothers exhibit more interest in their young, which appears to be biased toward male neonates.     

Reproductive experience differentially affects spatial reference and working memory performance in the mother

The transition to motherhood results in a number of hormonal, neurological, and behavioral changes necessary to ensure offspring survival. Once motherhood is established, further neurological and behavioral changes may result with additional parity and mothering. Recent research has shown that motherhood enhances both hippocampal-dependent learning and memory and oxytocin-induced long-term potentiation, suggesting that the hippocampus is affected by mothering. In turn, degree of maternal behavior, either high or low, has been shown to affect spatial learning and memory performance in adult offspring. The present experiment aimed to investigate the effect of reproductive experience (nulli-, primi-, and multiparity and mothering) and degree of maternal behavior on hippocampus-dependent learning and memory in the mother. Results show that regardless of error type, primiparous rats make fewer errors compared to nulliparous rats, while multiparous rats show a trend towards making fewer errors compared to nulliparous rats. In addition, mothers who spend less time licking and nursing offspring had fewer reference memory errors. Perhaps the enhanced learning and memory in the inexperienced, new mother allows her to effectively acquire the suite of maternal behaviors necessary to ensure offspring survival and achieve reproductive success with subsequent reproductive experience.     

ADAPTIVE MATERNAL ADJUSTMENTS OF OFFSPRING SIZE IN RESPONSE TO CONSPECIFIC DENSITY IN TWO POPULATIONS OF THE LEAST KILLIFISH, HETERANDRIA FORMOSA

Given a trade-off between offspring size and number and an advantage to large size in competition, theory predicts that the offspring size that maximizes maternal fitness will vary with the level of competition that offspring experience. Where the strength of competition varies, selection should favor females that can adjust their offspring size to match the offspring's expected competitive environment. We looked for such phenotypically plastic maternal effects in the least killifish, Heterandria formosa , a livebearing, matrotrophic species. Long-term field observations on this species have revealed that some populations experience relatively constant, low densities, whereas other populations experience more variable, higher densities. We compared sizes of offspring born to females exposed during brood development to either low or high experimental densities, keeping the per capita food ration constant. We examined plastic responses to density for females from one population that experiences high and variable densities and another that experiences low and less-variable densities. We found that, as predicted, female H. formosa produced larger offspring at the higher density. Unexpectedly, we found similar patterns of plasticity in response to density for females from both populations, suggesting that this response is evolutionarily conserved in this species.     

Male mate choice in a sexually cannibalistic species: male escapes from hungry females in the praying mantid <Emphasis Type="Italic">Tenodera angustipennis</Emphasis>

While competing males and choosy females may be common in animal mating systems, male choice can evolve under certain conditions. Sexual cannibalism is such a condition because of the high mortality risk for males. In mantids, female body condition is associated with male mate preference, with fat females preferred, due to at least two reasons: females in poor nutritional condition are likely to attack and predate males, and fat females can potentially increase the number of offspring. Thus, the risk of cannibalism and female fecundity can influence male mating behavior. In this study, we attempted to separate these factors by using the praying mantid Tenodera angustipennis to examine whether male preference for fat female mantids was based on avoiding sexual cannibalism (cannibalism avoidance hypothesis) or preference for female fecundity (fecundity preference hypothesis). The feeding regimes were experimentally manipulated to discriminate between the effects of female fecundity and female hunger status on male and female mating behaviors. We found that recently starved females more frequently locomoted toward the male, and that male abdominal bending was less intensive and escape was sooner from recently starved females. These female and male behavioral responses to female hunger condition may reveal male avoidance of dangerous females in this mantid.     

The influence of reproductive experience on milk energy output and lactation performance in the grey seal (Halichoerus grypus)

Although evidence from domestic and laboratory species suggests that reproductive experience plays a critical role in the development of aspects of lactation performance, whether reproductive experience may have a significant influence on milk energy transfer to neonates in wild populations has not been directly investigated. We compared maternal energy expenditures and pup growth and energy deposition over the course of lactation between primiparous and fully-grown, multiparous grey seal (Halichoerus grypus) females to test whether reproductive experience has a significant influence on lactation performance. Although there was no difference between primiparous females in milk composition and, thus, milk energy content at either early or peak lactation primiparous females had a significantly lower daily milk energy output than multiparous females indicating a reduced physiological capacity for milk secretion. Primiparous females appeared to effectively compensate for lower rates of milk production through an increased nursing effort and, thus, achieved the same relative rate of milk energy transfer to pups as multiparous females. There was no difference between primiparous and multiparous females in the proportion of initial body energy stores mobilised to support the costs of lactation. Although primiparous females allocated a greater proportion of energy stores to maternal maintenance versus milk production than multiparous females, the difference was not sufficient to result in significant differences in the efficiency of energy transfer to pups. Thus, despite a lower physiological capacity for milk production, primiparous females weaned pups of the same relative size and condition as multiparous females without expending proportionally more energy. Although reproductive experience does not significantly affect the overall lactation performance of grey seals, our results suggest that increases in mammary gland capacity with reproductive experience may play a significant role in the age-related increases in neonatal growth rates and weaning masses observed in other free-ranging mammals.     

Habituation to humans affects yolk steroid levels and offspring phenotype in quail

In the field as well as in the laboratory, human-generated stress responses are reduced in adult animals previously habituated to humans in comparison to non-habituated individuals. In birds, yolk steroid levels vary with maternal environment and condition. We tested the hypothesis that the experience of female birds with humans could affect yolk steroids levels and offspring phenotype. Two groups of Japanese quail, one habituated to humans (H) and a second non-habituated (NH), were exposed daily to brief human disturbances. We analysed egg quality, offspring growth, and offspring emotional reactivity. NH females produced eggs with less androgens (testosterone and androstenedione) and more immunoreactive progesterone compared to birds habituated to humans. NH females produced eggs with less yolk, heavier shell and chicks hatching later and being smaller as compared to habituated individuals. A lower emotional reactivity was found in young of NH females compared to young of H females. Thus, human disturbance of the mother triggered different effects on chick phenotype depending on previous experience of mother birds with humans. In addition, we describe for the first time the influence of environmental stimuli on yolk immunoreactive progesterone levels. Our results show that a relatively minor difference in behavioral habituation may have substantial effects on eggs and offspring. This has obvious implications for keeping and handling laboratory animals, for conservation biology and for animal welfare.     

Effects of prenatal disturbance in the brain testosterone metabolism on anxiety level and behavior of rats in a novel environment

The effects of maternal administration of the aromatase inhibitor 1,4,6-androstatrien-3,17-dione (ATD) during the last week of gestation on formation of behavior in a novel environment were studied in male and female offspring. The "open field" and the elevated plus-maze tests were used. The results showed that there were a significant elevation of the anxiety level and emotionality in ATD-treated 30-day-old female rats, whereas at the age of 90 days, the elevation of these behavioral parameters was observed both in males and females. There was no a sexual dimorphism in behavioral response to a novel environment such as locomotor activity, time of immobilization, total duration of grooming reaction, and anxiety level between adult control male and treated female rats. These data suggest that prenatal inhibition of the brain testosterone metabolism alters the formation of sexual dimorphism of the anxiety and behavioral response to a novel environment in adulthood.     

Hormonal and non-hormonal bases of maternal behavior: The role of experience and epigenetic mechanisms

This article is part of a Special Issue “Parental Care”. Though hormonal changes occurring throughout pregnancy and at the time of parturition have been demonstrated to prime the maternal brain and trigger the onset of mother–infant interactions, extended experience with neonates can induce similar behavioral interactions. Sensitization, a phenomenon in which rodents engage in parental responses to young following constant cohabitation with donor pups, was elegantly demonstrated by Rosenblatt (1967) to occur in females and males, independent of hormonal status. Study of the non-hormonal basis of maternal behavior has contributed significantly to our understanding of hormonal influences on the maternal brain and the cellular and molecular mechanisms that mediate maternal behavior. Here, we highlight our current understanding regarding both hormone-induced and experience-induced maternal responsivity and the mechanisms that may serve as a common pathway through which increases in maternal behavior are achieved. In particular, we describe the epigenetic changes that contribute to chromatin remodeling and how these molecular mechanisms may influence the neural substrates of the maternal brain. We also consider how individual differences in these systems emerge during development in response to maternal care. This research has broad implications for our understanding of the parental brain and the role of experience in the induction of neurobiological and behavior changes.     

Stress early in life leads to cognitive impairments,reduced numbers of CA3 neurons and altered maternal behavior in adult female mice

The hippocampus is a crucial part of the limbic system involved both in cognitive processing and in the regulation of responses to stress. Adverse experiences early in life can disrupt hippocampal development and lead to impairment of the hypothalamic‐pituitary‐adrenal axis response to subsequent stressors. In our study, two types of early‐life stress were used: prolonged separation of pups from their mothers (for 3 hours/day, maternal separation, MS) and brief separation (for 15 minutes/day, handling, HD). In the first part of our study, we found that adult female mice (F0) who had experienced MS showed reduced locomotor activity and impairment of long‐term spatial and recognition memory. Analysis of various hippocampal regions showed that MS reduced the number of mature neurons in CA3 of females, which is perhaps a crucial hippocampal region for learning and memory; however, neurogenesis remained unchanged. In the second part, we measured maternal care in female mice with a history of early‐life stress (F0) as well as the behavior of their adult offspring (F1). Our results indicated that MS reduced the level of maternal care in adult females (F0) toward their own progeny and caused sex‐specific changes in the social behavior of adult offspring (F1). In contrast to MS, HD had no influence on female behavior or hippocampal plasticity. Overall, our results suggest that prolonged MS early in life affects the adult behavior of F0 female mice and hippocampal neuronal plasticity, whereas the mothers' previous experience has effects on the behavior of their F1 offspring through disturbances of mother‐infant interactions.     

Primiparous females do not exhibit reduced maternal care in gray seals (Halichoerus grypus)

We compared the behaviors of primiparous and multiparous gray seal (Halichoerus grypus) females over the course of lactation to examine whether poorly developed maternal behaviors may play a role in the reduced lactation performance observed in primiparous females. Overall, primiparous females spent as much time interacting with their pups as multiparous females. The proportion of time spent nursing their pup increased significantly between early and peak lactation in both primiparous and multiparous females. Although there was no significant difference in the duration of nursing bouts as a function of reproductive status, primiparous females nursed significantly more frequently (bouts/hour) and, therefore, spent a significantly greater proportion of time nursing than multiparous females throughout lactation. Primiparous gray seal females were also significantly more active than multiparous females, however, the difference in activity represented only a small proportion of the overall time budget. We conclude that poorly developed maternal behaviors resulting from a lack of prior reproductive experience are unlikely to account for lower levels of milk energy transfer to pups in primiparous gray seals.     

The effects of pregnancy,lactation, and primiparity on object-in-place memory of female rats

Maternal physiology and behavior change dramatically over the course of pregnancy to nurture the fetus and prepare for motherhood. Further, the experience of motherhood itself continues to influence brain functioning well after birth, shaping behavior to promote the survival of offspring. To meet these goals, cognitive abilities, such as spatial memory and navigation, may be enhanced to facilitate foraging behavior. Existing studies on pregnant and maternal rats demonstrate enhanced cognitive function in specific spatial domains. We adopted a novel object-in-place task to assess the ability of female rats to integrate information about specific objects in specific locations, a critical element of foraging behavior. Using a longitudinal design to study changes in spatial memory across pregnancy and motherhood, an advantage in the object-in-place memory of primiparous female rats compared to nulliparous females emerged during lactation not during pregnancy, and was maintained after weaning at 42 days postpartum. This enhancement was not dependent on the non-mnemonic variables of anxiety or neophobia. Parity did not affect the type of learning strategy used by females to locate a cued escape platform on a dual-solution water maze task. Results indicate that the enhancement of object-in-place memory, a cognitive function that facilitates foraging, emerged after pregnancy during the postpartum period of lactation and persisted for several weeks after weaning of offspring.     

Variability in the development of mother-infant relationships among free-ranging Japanese macaques

Mother-infant relationships were studied during the infant's first year in free-ranging Japanese macaques (Macaca fuscata). Three possible factors controlling the mother-infant relationships were examined using multivariate analysis. Parity was determined to exert the strongest influence on mother-infant relationships. Specifically, during month 1, multiparous mothers showed greater maternal suckling rejection than primiparous mothers, and primparae and multiparae differed in their responses to suckling behavior. During month 6, multiparous mothers prompted independence of their offspring more than primiparous mothers. By month 8, however, parity differences in maternal behavior were substantially reduced. Maternal rank was a less important factor, although during month 1, high-ranking mothers showed greater maternal restriction than low-ranking ones. In the present study, infant gender appeared to have no effect on mother-infant relationships. That most differences were due to parity indicates that mother-infant relations were largely determined by the mothers. This observation conflicts with the “learning-to-mother” hypothesis. Allo-mothering of neonates by nulliparae is rare among Japanese macaques. Primiparous mothers learned appropriate suckling care from handling their own infants.     

Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques

Genetic female fetuses were exposed transplacentally to testosterone propionate injected into their mothers either early (Days 40 through 64) or late (Days 115 through 139) in gestation. Early and late androgenized females (EAFs and LAFs, respectively) were raised with normal males and females that served as criteria for evaluating degree of behavioral masculinization induced by the prenatal androgen. EAFs were genitally virilized and LAFs were not. Males and untreated females differed reliably on five behavioral measures: males showed more mother-mounting, more peer-mounting, more rough play with peers, a preference for initiating play with male partners, and less grooming of mothers. Neither type of prenatally androgenized female showed masculinization of all five types of behavior. Compared with females, EAFs showed more mother-mounting, more peer-mounting, less mother-grooming, did not differ from females in rough play, and did not manifest a preference for male partners. LAFs, like females, groomed but did not mount their mothers, and did not show a preference for male partners; but unlike females they showed elevated rough play and mounting with peers. EAFs showed a statistically significant delay in puberty onset (menarche), but LAFs did not. Mothers inspected genitalia of their offspring more often if they were males than if they were females. Mothers of EAFs inspected their offspring's genitalia as often as mothers of males, but mothers of LAFs did not. No aspect of maternal behavior was associated with either the amount or kind of masculine behavior shown toward peers. We interpret the results to mean that genital virilization is independent of, and largely irrelevant to, the expression of those behavioral traits that characterize the juvenile male social role. Moreover, the individual behavior traits that are components of the juvenile male role are independently regulated by the organizing actions of androgen and have separable critical periods. Of the two major traits, mounting peers and rough play with peers, the latter has a greater requirement for androgenic stimulation late in prenatal life.     

Role of maternal 5‐HT1A receptor in programming offspring emotional and physical development

Serotonin_1A receptor (5‐HT_1AR) deficiency has been associated with anxiety and depression and mice with genetic receptor inactivation exhibit heightened anxiety. We have reported that 5‐HT_1AR is not only a genetic but also a maternal ‘environmental’ factor in the development of anxiety in Swiss‐Webster mice. Here, we tested whether the emergence of maternal genotype‐dependent adult anxiety is preceded by early behavioral abnormalities or whether it is manifested following a normal emotional development. Pups born to null or heterozygote mothers had significantly reduced ultrasonic vocalization (USV) between postnatal day (P) 4 and 12, indicating an influence of the maternal genotype. The offspring's own genotype had an effect limited to P4. Furthermore, we observed reduced weight gain in the null offspring of null but not heterozygote mothers, indicating that a complete maternal receptor deficiency compromises physical development of the offspring. Except a short perinatal deficit during the dark period, heterozygote females displayed normal maternal behavior, which, with the early appearance of USV deficit, suggests a role for 5‐HT_1AR during pre‐/perinatal development. Consistent with this notion, adult anxiety in the offspring is determined during the pre‐/perinatal period. In contrast to heterozygote females, null mothers exhibited impaired pup retrieval and nest building that may explain the reduced weight gain of their offspring. Taken together, our data indicate an important role for the maternal 5‐HT_1AR in regulating emotional and physical development of their offspring. Because reduced receptor binding has been reported in depression, including postpartum depression, reduced 5‐HT_1AR function in mothers may influence the emotional development of their offspring.     

Sexual and maternal behaviour at the postpartum oestrus: The role of experience in time-sharing

The postpartum sexual and maternal behaviour of Norway rats (Rattus norvegicus) was observed in a seminatural habitat. Behavioural decision-making by the female was examined by disrupting the nest and newborn offspring during mating. In experiment 1, multiparous females responded to nest disruption with an increase in maternal behaviour that was largely restricted to the post-ejaculatory intervals. The temporal and frequency measures of copulation were largely unaffected, implicating behavioural time-sharing. In experiment 2, following nest disruption primiparous females did not switch efficiently between maternal and sexual behaviour, showed poor retrieval of pups, and returned to the nest during ejaculatory series. They did not display the characteristics of behavioural time-sharing, indicating that previous experience may play a role in the ability to time-share.     

The influence of rearing conditions on maternal behavior in cynomolgus macaques (Macaca fascicularis)

We studied the influence of rearing on the adequacy of maternal behavior by comparing 20 harem-reared and 15 peer-reared primiparous cynomolgus monkeys. We used them plus 11 wild-caught females to extend this comparison to multiparous subjects and also to compare primiparae with multiparae. We observed no behavioral effect of rearing and parity. Primiparous maternal adequacy amounted to 93% in peer-reared subjects and to 95% in harem-reared monkeys. We extensively discuss theories concerning rearing effects. Leitmotifs throughout the discussion are survival value of maternal behavior immediately after parturition and predictive value of this behavior for the further course of maternal behavior. Support is accumulated for the hypothesis that certain tactile and visual experiences suffice for the development of adequate maternal behavior.