Variation In Parental Care Research Articles

Integrative Studies of the Effects of Mothers on Offspring: An Example from Wild North American Red Squirrels.

Animal species vary in whether they provide parental care or the type of care provided, and this variation in parental care among species has been a common focus of comparative studies. However, the proximate causes and ultimate consequences of within-species variation in parental care have been less studied. Most studies about the impacts of within-species variation in parental care on parental fitness have been in primates, whereas studies in laboratory rodents have been invaluable for understanding what causes inter-individual variation in parental care and its influence on offspring characteristics. We integrated both of these perspectives in our long-term study of North American red squirrels (Tamiasciurus hudsonicus) in the Yukon, Canada, where we have focused on understanding the impacts of mothers on offspring. This includes documenting the impacts that mothers or the maternal environment itselfhas on their offspring, identifying how changes in maternal physiology impact offspring characteristics, the presence of individual variation in maternal attentiveness toward offspring before weaning and its fitness consequences, and postweaning maternal care and its fitness consequences. We provide an overview of these contributions to understanding the impacts mothers have on their offspring in red squirrels using an integrative framework and contrast them with studies in the laboratory.

Daily Rhythms of Female Self-maintenance Correlate with Predation Risk and Male Nest Attendance in a Biparental Wader

Parents make tradeoffs between care for offspring and themselves. Such a tradeoff should be reduced in biparental species, when both parents provide parental care. However, in some biparental species, the contribution of one sex varies greatly over time or between pairs. How this variation in parental care influences self-maintenance rhythms is often unclear. In this study, we used continuous video recording to investigate the daily rhythms of sleep and feather preening in incubating females of the Northern Lapwing (Vanellus vanellus), a wader with a highly variable male contribution to incubation. We found that the female's sleep frequency peaked after sunrise and before sunset but was low in the middle of the day and especially during the night. In contrast, preening frequency followed a 24-h rhythm and peaked in the middle of the day. Taken together, incubating females rarely slept or preened during the night, when the predation pressure was highest. Moreover, the sleeping and preening rhythms were modulated by the male contribution to incubation. Females that were paired with more contributing males showed a stronger sleep rhythm but also a weaker preening rhythm. If more incubating males also invest more in nest guarding and deterring daylight predators, their females may afford more sleep on the nest during the day and preen more when they are off the nest. Whether the lack of sleep in females paired with less caregiving males has fitness consequences awaits future investigation.

Prairie vole offspring only prefer mothers over fathers when mothers are a unique resource, yet fathers are the primary source of variation in parental care

In biparental species, each parent represents a semi-independent source of variable caregiving. The nature of care may differ between parents, and the type of care offspring seek is likely to change across development. We asked if caregiving differed between prairie vole (Microtus ochrogaster) mothers and fathers, and which parent pups prefer over development. We categorized parents as high- or low-contact based on daily recordings of grooming and brooding behavior. Pups were tested for their preferences between parents on postnatal days 10, 14, 18, 22, and 26. We expected individual parents would vary in the amount of care they gave, with pups preferring the parent that gives the most care and/or that most meets their needs at each developmental timepoint. Mothers spent more time in contact with pups than fathers. Mothers were consistent in the amount of care they gave, whereas fathers were variable caregivers. Pups never preferred fathers over mothers, but only demonstrated a preference for mothers before weaning. Lastly, the amount of contact did not influence pup preferences. Our data indicate that mothers are consistent sources of caregiving relative to fathers, and pups show little evidence of attachment to a specific parent beyond meeting its own immediate needs.

Temporal patterns, benefits, and defensive behaviors associated with male parental care in the glassfrog Centrolene savagei

Anurans are good study models for a better understanding of the behavioral ecology of parental care in vertebrates because such behavior evolved multiple times independently in frogs and toads; moreover, forms of parental care are highly diverse in those vertebrates and according to the species is performed by the male, the female, or both sexes. In this study, we first recorded variations in parental care by males of the glassfrog Centrolene savagei at two temporal scales (day vs night, and throughout embryo development). Second, we compared levels of embryo mortality in egg clutches attended and naturally unattended by males. Third, we performed field experiments to simulate the risk of predation by small invertebrates to test the level of male commitment to providing parental care. During 65 field trips (1–2 nights each) we recorded 87 males and 154 egg clutches in a population of C. savagei from the Central Andes of Colombia. Parental care (measured as male egg brooding) was higher at night than at day, and it decreased from oviposition towards egg hatching as embryos developed. Embryo mortality was greater in naturally abandoned clutches, compared to those receiving male care. Most males caring for eggs but none of the solitary males exhibited defensive behavior, such as biting and kicking the predator stimulus. Preliminary results also suggest that caring males have a higher tolerance toward threatening stimuli before fleeing than did solitary males. Altogether, rates of natural mortality suggest that male care for eggs is likely adaptive in this species. Males protect their offspring from at least two causes of mortality: desiccation and predation. However, when and how much males care for the offspring varies between night and day, and through embryonic development.

Linking genetic merit to sparse behavioral data: behavior and genetic effects on lamb growth in Soay sheep

AbstractWild quantitative genetic studies have focused on a subset of traits (largely morphological and life history), with others, such as behaviors, receiving much less attention. This is because it is challenging to obtain sufficient data, particularly for behaviors involving interactions between individuals. Here, we explore an indirect approach for pilot investigations of the role of genetic differences in generating variation in parental care. Variation in parental genetic effects for offspring performance is expected to arise from among-parent genetic variation in parental care. Therefore, we used the animal model to predict maternal breeding values for lamb growth and used these predictions to select females for field observation, where maternal and lamb behaviors were recorded. Higher predicted maternal breeding value for lamb growth was associated with greater suckling success, but not with any other measures of suckling behavior. Though our work cannot explicitly estimate the genetic basis of the specific traits involved, it does provide a strategy for hypothesis generation and refinement that we hope could be used to justify data collection costs needed for confirmatory studies. Here, results suggest that behavioral genetic variation is involved in generating maternal genetic effects on lamb growth in Soay sheep. Though important caveats and cautions apply, our approach may extend the ability to initiate more genetic investigations of difficult-to-study behaviors and social interactions in natural populations.

Compensatory and additive helper effects in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis).

In cooperatively breeding species, care provided by helpers may affect the dominant breeders’ investment trade‐offs between current and future reproduction. By negatively compensating for such additional care, breeders can reduce costs of reproduction and improve their own chances of survival. Alternatively, helper care can be additive to that of dominants, increasing the fledging fitness of the current brood. However, the influence helpers have on brood care may be affected by group size and territory quality. Therefore, the impact of helping needs to be disentangled from other factors determining offspring investment before conclusive inferences about the effect of help on additive and compensatory care can be made. We used 20 years of provisioning data to investigate the effect of helping on provisioning rates in the facultative cooperatively breeding Seychelles warbler Acrocephalus sechellensis. Our extensive dataset allowed us to statistically disentangle the effects of helper presence, living in larger groups and different food availability. We show compensatory and additive care (i.e., partial compensation) in response to helper provisioning. Helpers lightened the provisioning load of the dominant male and female and increased total provisioning to nestlings. This was irrespective of group size or territory quality (food availability). Moreover, our results illustrate sex‐specific variation in parental care over the course of the breeding event. We discriminate between temporal variation, group size, and territory quality processes affecting cooperative care and as such, gain further insight into the importance of these factors to the evolutionary maintenance of helping behavior.

Fathers favour sons, mothers don't discriminate: Sex-biased parental care in northwestern Tanzania.

Variation in parental care by child's sex is evident across cultures. Evolutionary theory provides a functional explanation for this phenomenon, predicting that parents will favour specific children if this results in greater fitness payoffs. Here, we explore evidence for sex-biased parental care in a high-fertility, patriarchal and polygynous population in Tanzania, predicting that both mothers and fathers will favour sons in this cultural setting. Our data come from a cross-sectional study in rural northwestern Tanzania, which included surveys with mothers/guardians of 808 children under age 5. We focus on early childhood, a period with high mortality risk which is fundamental in establishing later-life physical and cognitive development. Examining multiple measures of direct/physical care provision (washing, feeding, playing with, supervising, co-sleeping and caring when sick), we demonstrate that fathers favour sons for washing, feeding and supervising, while maternal care is both more intensive and unrelated to child sex. We find no difference in parental care between girls and boys regarding the allocation of material resources and the duration of breastfeeding; or in terms of parental marital and co-residence status. This bias towards sons may result from higher returns to investment for fathers than mothers, and local gender norms about physical care provision.

Offspring growth and mobility in response to variation in parental care: a comparison between populations

Life history theory emphasizes the importance of trade‐offs in how time and energy are allocated to the competing demands of growth, fecundity, and survival. However, avian studies have historically emphasized the importance of resource acquisition over resource allocation to explain geographic variation in fecundity, parental care, and offspring development. We compared the brood sizes and nestling mass and feather growth trajectories between orange‐crowned warblers Oreothlypis celata breeding in Alaska versus California, and used 24‐h video recordings to study the relationship between parental care and growth rates. Per‐offspring provisioning rates were highest in the smallest broods, and food delivery was positively correlated with nestling growth over the 24‐h period only in Alaska. Females in Alaska spent more time brooding, and juveniles there showed faster feather growth and earlier mobility compared with those in California. We also found differences in the energetic and nutritional content of insect larvae that could facilitate the observed differences in nestling growth relative to food provisioning. Our results point to the potential importance of food quality and parental provisioning of warmth, in addition to food, for explaining avian growth patterns. We highlight the need to quantify multiple dimensions of parental care and of offspring growth and development, and to better understand the relationships between feather growth, nestling period length, and fledgling mobility.

Plasticity and personality of parental care in the clown anemonefish

Characterizing individual variation in parental care is critical to understanding how selection shapes and maintains patterns of care, yet little is known about how individual parents vary in their responses to the environment. Reaction norms, functions that describe how phenotypes change across an environmental gradient, provide an elegant framework for studying individual variation in behavioural responses. We use a reaction norm approach to investigate how studying plasticity, which describes variation within an individual through time, and personality, which describes repeatable variation among individuals, together explain individual variation in the parental behaviour of the anemonefish Amphiprion percula. More specifically, we test how resource availability influences individual parental responses to the environment and discuss the consequences for our understanding of plasticity and personality in parental care. Breeding pairs of A. percula were fed either a high or a low food ration and their parental behaviours were monitored. Individuals exhibited plasticity in parental behaviour across the two resource environments. Furthermore, individuals were repeatable in their behaviour through time, as evidenced by significant among-individual variation in intercept. Finally, the slope and elevation of individual reaction norms varied, revealing a level of variation not captured at the population level and providing insight into the potential mechanisms generating individual variation.

Age-related parental care in a long-lived bird: implications for offspring development

In long-lived species, behaviour is expected to vary across the lifespan, first improving with maturation and experience and then declining with senescence, but measurement is rare, particularly during old age. Measuring nest defence intensity in 255 known-age blue-footed boobies (Sula nebouxii) of 19 age classes confirmed the inverted-U pattern: intensity of nest defence increased in young males and females until roughly 11–12 years and declined progressively afterwards. We discuss the processes that may generate this distinctive pattern. Regardless of the underlying processes, this study establishes the existence of age-related variation in parental care in a long-lived species. Natural variation in natal conditions has recently been shown to have long-term impacts on development, so this study raises the question whether age-related changes in parental care generate systematic variation in offspring phenotypes. In theory, age-related change in parental care can result in differences among offspring produced at different ages. However, parental behaviour has never been measured over the whole age-span of any long-lived species because of the difficulty of sampling very old animals in the field. We measured intensity of nest defence over the age-span and confirmed that blue-footed boobies exhibit an age-related quadratic pattern in this parental behaviour: defence intensity increases in early life and declines progressively afterwards. Our results imply that similar-shaped patterns may exist in other components of parental care, such as feeding and social interaction, potentially affecting the long-term development of offspring.

Decreasing parental task specialization promotes conditional cooperation

How much to invest in parental care and by who remain puzzling questions fomented by a sexual conflict between parents. Negotiation that facilitates coordinated parental behaviour may be key to ease this costly conflict. However, understanding cooperation requires that the temporal and sex-specific variation in parental care, as well as its multivariate nature is considered. Using a biparental bird species and repeated sampling of behavioural activities throughout a major part of reproduction, we show a clear division of tasks between males and females in provisioning, brooding and foraging. Such behavioural specializations fade with increasing nestling age, which stimulates the degree of alternated feeding visits, as a recently promoted form of conditional cooperation. However, such cooperation is thought to benefit offspring development, which is not supported by our data. Thus, from a proximate point of view, conditional cooperation via alternation critically depends on the division of parental tasks, while the ultimate benefits have yet to be shown.

Exploration in a dispersal task: Effects of early experience and correlation with other behaviors in prairie voles (Microtus ochrogaster)

Socially monogamous prairie voles (Microtus ochrogaster) display remarkable individual variation in social behaviors, which has been associated with differences in early life experience and neuropeptide receptor densities. These differences are also seen in the wild, where approximately 70% of young voles remain in their natal group as non-breeding alloparents, while the other 30% disperse. We investigated whether natural variation in early parental care could contribute to offspring’s willingness to “disperse” (willingness to explore) in a laboratory context. Behavioral differences between dispersers and residents could also provide a way to interpret individual variation in other behaviors commonly observed under laboratory conditions. Breeder pairs ranked as high, medium or low-contact, according to the amount of early parental care they provided to offspring, were used to produce and rear experimental subjects. Effects of early parental care on the offspring’s willingness to disperse were seen at post-natal day 21, with high-contact offspring spending more time in the start cage and low-contact offspring spending more time exploring. Variations in parental care were also associated with differences in juvenile and adult behaviors that could potentially encourage philopatry or dispersal behavior in the wild. High-contact offspring displayed less anxiety-like behavior compared to low-contact animals. Low-contact offspring displayed the lowest amount of alloparental care. High-contact offspring spent more time in side-by-side contact with a potential partner compared to medium and low-contact offspring. These results suggest that variations in early parental care can impact weanlings’ exploratory behavior, but that philopatry is not driven by high anxiety.

Predictably Philandering Females Prompt Poor Paternal Provisioning.

One predicted cost of female infidelity in socially monogamous species is that cuckolded males should provide less parental care. This relationship is robust across species, but evidence is ambiguous within species. We do not know whether individual males reduce their care when paired with cheating females compared with when paired with faithful females (within-male adjustment) or, alternatively, if the males that pair with cheating females are the same males that provide less parental care in general (between-male effect). Our exceptionally extensive long-term data set of repeated observations of a wild passerine allows us to disentangle paternal care adjustment within males-within pairs and between males-while accounting for environmental variables. We found a within-male adjustment of paternal provisioning, but not incubation effort, relative to the cuckoldry in their nest. This effect was mainly driven by females differing consistently in their fidelity. There was no evidence that this within-male adjustment also took place across broods with the same female, and we found no between-male effect. Interestingly, males that gained more extrapair paternity provided less care. Data from a cross-foster experiment suggested that males did not use kin recognition to assess paternity. Our results provide insight into the role of individual variation in parental care and mating systems.

Prolactin is related to individual differences in parental behavior and reproductive success in a biparental passerine, the zebra finch (Taeniopygia guttata)

Variation in parental care can lead to important fitness consequences. The endocrine system is known to regulate physiological and behavioral reproductive traits that are important contributors to lifetime reproductive success. However, the hormonal basis of variation in avian parental care is still not well understood. Plasma prolactin (PRL) concentrations are generally high during post-hatch parental care in birds, and may be a candidate mechanism that regulates variation in parental care and other reproductive success outcomes. Here we analyze the relationship between PRL, parental behavior (chick brooding and feeding) and reproductive success outcomes (clutch size, number of chicks hatched, and chick survival) for the first time in the zebra finch (Taeniopygia guttata). Birds were given cabergoline, a dopamine agonist traditionally used to lower prolactin in mammals, or vehicle in their food. Cabergoline had no effect on prolactin concentrations, but across both groups we found that PRL is positively correlated with parental behavior, number of chicks hatched, and chick survival, but not clutch size. Results from this study will inform hypotheses and predictions for future manipulation studies which test for a causal role for PRL in parental traits.

Seasonal Variation in Parental Care Drives Sex-Specific Foraging by a Monomorphic Seabird.

Evidence of sex-specific foraging in monomorphic seabirds is increasing though the underlying mechanisms remain poorly understood. We investigate differential parental care as a mechanism for sex-specific foraging in monomorphic Common Murres (Uria aalge), where the male parent alone provisions the chick after colony departure. Using a combination of geolocation-immersion loggers and stable isotopes, we assess two hypotheses: the reproductive role specialization hypothesis and the energetic constraint hypothesis. We compare the foraging behavior of females (n = 15) and males (n = 9) during bi-parental at the colony, post-fledging male-only parental care and winter when parental care is absent. As predicted by the reproductive role specialization hypothesis, we found evidence of sex-specific foraging during post-fledging only, the stage with the greatest divergence in parental care roles. Single-parenting males spent almost twice as much time diving per day and foraged at lower quality prey patches relative to independent females. This implies a potential energetic constraint for males during the estimated 62.8 ± 8.9 days of offspring dependence at sea. Contrary to the predictions of the energetic constraint hypothesis, we found no evidence of sex-specific foraging during biparental care, suggesting that male parents did not forage for their own benefit before colony departure in anticipation of post-fledging energy constraints. We hypothesize that unpredictable prey conditions at Newfoundland colonies in recent years may limit male parental ability to allocate additional time and energy to self-feeding during biparental care, without compromising chick survival. Our findings support differential parental care as a mechanism for sex-specific foraging in monomorphic murres, and highlight the need to consider ecological context in the interpretation of sex-specific foraging behavior.

Variation in parental care in the spectacled tyrant Hymenops perspicillatus is associated with increased nest predation in grassland fragments

Predation risk on birds is often an important source of natural selection that shapes parental care and may promote behavioral changes. Parents can often estimate certain risks and adjust their behavior to reduce the likelihood of nest predation. The fragmentation of habitats is one of the main consequences of loss of habitats, and in general, for birds breeding in smaller patches, their daily nest-survival rate is lower due to increased nest predation. Since nest survival is an estimate of predation risk in the environment, we evaluated the daily survival rate (DSR) for nests of spectacled tyrants (Hymenops perspicillatus) and parental care behavior on fragmented and unfragmented grasslands. We conducted nest searching and monitoring during the 2012–2013 breeding season in small patches and in a continuous patch of grassland. In addition, parental activity was recorded using video monitoring. We found a lower DSR for the spectacled tyrant in fragmented grasslands, associated with increased nest predation risk; females showed a variation in parental care. This variation was evidenced by larger incubation bouts and lower visitation rate during the incubation period, and by a lower food delivery rate to nestlings, compensated by larger prey sizes. The results show that fragmentation not only reduces the fitness of individuals and impacts adversely on population, but individuals are also subjected to a strong selection pressure, and their reproductive success may depend to some extent on the ability of parents to estimate at least certain predation risk and adjust their behavior in this regard.

Maternal sensitivity, infant limbic structure volume and functional connectivity: a preliminary study.

Mechanisms underlying the profound parental effects on cognitive, emotional and social development in humans remain poorly understood. Studies with nonhuman models suggest variations in parental care affect the limbic system, influential to learning, autobiography and emotional regulation. In some research, nonoptimal care relates to decreases in neurogenesis, although other work suggests early-postnatal social adversity accelerates the maturation of limbic structures associated with emotional learning. We explored whether maternal sensitivity predicts human limbic system development and functional connectivity patterns in a small sample of human infants. When infants were 6 months of age, 20 mother–infant dyads attended a laboratory-based observational session and the infants underwent neuroimaging at the same age. After considering age at imaging, household income and postnatal maternal anxiety, regression analyses demonstrated significant indirect associations between maternal sensitivity and bilateral hippocampal volume at six months, with the majority of associations between sensitivity and the amygdala demonstrating similar indirect, but not significant results. Moreover, functional analyses revealed direct associations between maternal sensitivity and connectivity between the hippocampus and areas important for emotional regulation and socio-emotional functioning. Sensitivity additionally predicted indirect associations between limbic structures and regions related to autobiographical memory. Our volumetric results are consistent with research indicating accelerated limbic development in response to early social adversity, and in combination with our functional results, if replicated in a larger sample, may suggest that subtle, but important, variations in maternal care influence neuroanatomical trajectories important to future cognitive and emotional functioning.

A high-accuracy, time-saving method for extracting nest watch data from video recordings

Understanding inter- and intraspecific variation in parental care has been an important focus in studies of avian behaviour and evolution. Unfortunately, typical methods for quantifying parental care, such as field observation and video recordings, can be extremely time-consuming. Here, we demonstrate that utilizing behavioural analysis software, such as EthoVision XT, can reduce time required for video data extraction by 37−69 %. This method is highly accurate; results and error rates did not differ from those of manual observation. We suggest this method could be beneficial and time-saving for studies analyzing large amounts of video recordings.

Cortisol administration increases hippocampal activation to infant crying in males depending on childhood neglect.

Animal studies show that exposure to parental neglect alters stress regulation and can lead to neural hyposensitivity or hypersensitivity in response to cortisol, most pronounced in the hippocampus. Cortisol, the end product of the hypothalamic-pituitary-adrenal (HPA) axis, has also been related to parenting more directly, for example, in both sexes, cortisol levels increase when listening to infants crying, possibly to activate and facilitate effective care behavior. Severe trauma is known to negatively affect the HPA-axis in humans; however, it is unknown whether normal variation in parental care in the healthy population can alter sensitivity of the hippocampus to cortisol. Here, we investigate whether variation in experienced neglect changes neural sensitivity to cortisol when humans listen to infant crying, which is an unequivocal signal relevant for care behavior. In a placebo-controlled, within-subject neuroimaging study, we administered 40 mg cortisol to 21 healthy young males without children and used a validated task for measuring neural responses to infant crying. The Dutch version of the Childhood Trauma Questionnaire was used to index participants' early exposure to abuse and neglect. The data show that cortisol markedly increased hippocampal activation toward crying infants, and this effect varied significantly with parental neglect, even in our nonclinical subject sample. Without exposure to severe trauma or neglect, reduced self-experienced quality of parental care in the normal range already substantially increased hippocampal responsivity to cortisol. Altered hippocampal sensitivity to cortisol might be a cross-species marker for the risk of developing later life psychopathology.

The role of social environment on parental care: offspring benefit more from the presence of female than male helpers

Investment in offspring depends on the costs and benefits to the carer, which can vary with sex and social status. Investment also depends on the effort of others by allowing for compensation (load-lightening), with biparental care studies showing that this depends on the state and type of the other carer. By contrast, studies on cooperative breeders have solely focussed on the effects of group size rather than its composition (i.e. social environment). Here we propose and provide the first test of the 'Social Environment' hypothesis, that is, how the characteristics (here the sex) of other helpers present in the group affect parental care and how this in turn affects offspring fitness in cooperatively breeding red-winged fairy-wrens (Malurus elegans). Breeders provisioned nestlings at a higher rate than helpers, but there was no sex difference in provisioning rate. Compensation to increasing group size varied little with sex and status, but strongly depended on social environment. All group members reduced their provisioning rates in response to an increasing number of male (load-lightening), but not female helpers (additive care). As a result, nestlings received more food and grew faster in the presence of female helpers. The increased nestling growth did convey a fitness advantage due to a higher post-fledging survival to adulthood. Our study provides the first evidence that parental care can depend on social environment. This could be an important overlooked aspect to explain variation in parental care in cooperative breeders in general and in particular the enormous variation between the sexes, which we reveal in a literature overview.