Determinants of parental care and offspring survival during the post-fledging period: males care more in a species with partially reversed sex roles

Sexual conflict is magnified during the post-fledging period of birds when the sexes face different trade-offs between continuing parental care or investing in self maintenance or other mating opportunities. Species with reversed sex roles provide a unique opportunity to study the relationship between mating systems and investment in parental care. Here, we provide the first detailed study of the length of care by males versus females (n = 24 pairs) during the post-fledging period, assessing factors that may promote care within and between the sexes. In the northern flicker Colaptes auratus, a species with partly reversed sex roles, males cared longer than females (average 16 versus 12 days, respectively). Overall, 36 % of females but no males deserted the brood prior to fledgling independence. Parents that provisioned nestlings at a high rate also spent more days feeding fledglings. Among males, age and nestling feeding rates were positively associated with the length of care. Among females, a low level of feather corticosterone (CORT_f) was associated with a longer length of care. About 45 % of fledglings died within the first week, but fledglings with intermediate body mass had the highest survival suggesting stabilizing selection on mass. Fledgling survival was also higher in individuals with larger broods and lower levels of CORT_f. We demonstrate that because females can be polyandrous they often desert the brood before males, and that the sexes respond to different cues relating to their energy balance when deciding the length of care given to their offspring.     

Extreme gender-based post-fledging brood division in the toc-toc

The possibility that parents of one sex may preferentially investin offspring of a certain sex raises profound evolutionary questionsabout the relative worth of sons and daughters to their mothersand fathers. Post-fledging brood division—in which eachparent feeds a different subset of offspring—has beenwell documented in birds. However, a lack of empirical evidencethat this may be based on offspring sex, combined with the theoreticaldifficulty of explaining such an interaction, has led researchersto consider a gender bias in post-fledging brood division highlyunlikely. Here we show that in the toc-toc, Foudia sechellarum,post-fledging brood division is extreme and determined by sex;where brood composition allows, male parents exclusively provisionmale fledglings, whereas female parents provision female fledglings.This is the first study to provide unambiguous evidence, basedon molecular sexing, that sex-biased post-fledging brood divisioncan occur in birds. Male and female parents provisioned at thesame rate and neither offspring nor parent survival appearedto be affected by the sex of the parent or offspring, respectively.The current hypotheses predicting advantages for brood divisionand preferential care for one specific type of offspring arediscussed in the light of our results.     

Successive clutches and parental roles in waders: the importance of timing in multiple clutch systems

Production of successive clutches within the same breeding season has received less attention than many other aspects of avian reproduction. Waders are of particular interest because in these birds, multiple clutches are associated with at least three different breeding systems: double-clutching (uniparental care), monogamous double-brooding (biparental care) and polyandry (uni- or biparental care). Data from eight species and twelve breeding populations suggest that early second clutches, and thus brood overlap, are associated with parental role division and uniparental care, whereas species or populations with biparental care tend to have long intervals between successive clutches. We suggest that ecological factors influencing the relative timing of the second clutch will have consequences for the parental care system. In particular, conditions that favour early laying of the second clutch (large brood overlap) are likely to lead to parental role division, as found in double-clutching species. Factors determining the timing of second clutches are discussed, as are possibilities for testing these ideas.     

Allocation of Male Parental Care in Relation to Paternity Within and Among Broods of the Common Yellowthroat (Geothlypis trichas)

The relationship between male parental care and paternity has been investigated in a number of avian species, but in many cases the influences of confounding factors, such as variation in male and territory quality, were not addressed. These sources of variation can be controlled for by making within-male comparisons between successive broods or within-brood comparisons between groups of fledglings in a divided brood. We studied the relationship between male parental care and paternity in the common yellowthroat ( Geothlypis trichas ) at three levels: between groups of fledglings in divided broods, between first and second broods of the same pair, and among all broods in the population. In this study we proposed three hypotheses: first, males in double-brooded pairs should provide relatively more parental care to broods in which they have higher paternity; secondly, after fledging and brood division, males should provide more care to related offspring; and finally, among all broods in the population, paternity should be related positively to male parental care. Brood division occurred in many of the broods studied; however, broods were not divided according to fledgling size or paternity. Furthermore, within divided broods, males fed within-pair and extra-pair fledglings at similar rates. For sequential broods of the same pair, male feeding rates were not associated with differences in paternity between broods. Among all broods in the population, males did not provide relatively less care to broods containing unrelated young. The lack of a relationship between male parental care and paternity suggests that either males cannot assess their paternity or the costs of reducing male parental care outweigh the benefits.     

Paternal care and male mate-attraction effort in the European starling is adjusted to clutch size

In facultative polygynous birds with biparental care, a trade-off may occur between male parental care and attraction of additional mates. If there is a cost associated with reduced male parental care, the relative benefit of mate attraction may be predicted to decrease as the size of a male's clutch or brood increases. We tested this prediction in monogamous pairs of facultatively polygynous European starlings (Sturnus vulgaris). The larger the clutch, the more time the male spent incubating and the less time he spent attracting an additional female (i.e. singing near and carrying green nesting material into adjacent empty nest-boxes). Reduced paternal incubation resulted in lower overall incubation (the female did not compensate) and lower hatching success. Immediately after experimental reduction of clutches, males spent significantly less time incubating and more time singing and carrying greenery, and vice versa for experimentally enlarged clutches. Males with experimentally reduced clutches attracted a second female more often than males with experimentally enlarged clutches. This is the first study, to our knowledge, to provide experimental evidence for an adjustment of paternal care and male mate-attraction effort to clutch size. However, a trade-off between paternal nestling provisioning and mate attraction was not revealed, probably due to the absence of unpaired females by that time in the breeding season. Experiments showed that the relative contribution of the male and female to nestling provisioning was unrelated to brood size.     

Brood division in robins

Broods of fledgling robins Erithacus rubecula are sometimes divided between their parents so that each parent feeds only some of the chicks. These associations between a parent and certain of its young (‘family units’) are shown to be stable over periods of days. Brood division is most frequent in broods that are not followed by another nesting attempt. Experimental manipulation of the food supply suggests that brood division is relaxed when food is readily available. An analysis of the interactions between parents and chicks demonstrates that both adults and fledglings play a role in brood division. The possible functions of brood division are discussed with reference to ‘other types of care’, ‘parental efficiency’, ‘cheat countermeasure’ and ‘two types of chick’ hypotheses. Male parents feed chicks with shorter winglengths than do females: since females tend to have shorter winglengths than males, this suggests that chicks are cared for by parents of the opposite sex. Possible causes and consequences of this observation are discussed.     

Sexual conflict and parental care in magnificent frigatebirds: full compensation by deserted females

Parental care is a cooperative venture between a male and a female in many socially monogamous birds. Care is costly, and thus, sexual conflict arises between the parents about how much effort they should invest into rearing their young. The sexual conflict over care is most apparent when one parent abandons the brood before the offspring are independent. The deserted parent has three options: (1) desert the brood because a single parent is unable to raise the young on its own; (2) continue care provision at the same level as during biparental care, and thus do not compensate for the absence of mate; or (3) increase care and compensate partially or totally. We investigated these options in the magnificent frigatebird, Fregata magnificens, a species in which the male deserts his mate and brood before the chick is independent. During biparental care, females fed the chick more often than the males. After their mate deserted, the females nearly doubled their feeding rate and thus, fully compensated for the lost care. Consistent with these observations, growth rates of chicks provided with biparental and female-only care did not differ. These results support recent theoretical models of parental care, and suggest that females may withhold care during biparental care to manoeuvre their mates into prolonged care provision. A female only provides at her full capacity once her mate has deserted.     

Ecological factors regulating brood attendance patterns of the Western Sandpiper Calidris mauri

Parental brood attendance patterns vary greatly among shorebird species. For monogamous calidridine species, biparental care with female-first brood departure is most common. It is believed that adult sandpipers balance potential individual survival costs associated with extended parental care against the benefit gained by their brood of prolonged parental care. These costs and benefits are difficult to quantify and factors affecting the termination of parental brood attendance are unclear. We compared clutch size, nesting phenology, and parental attendance patterns of Western Sandpipers Calidris mauri at Nome and Kanaryarmiut, Alaska, sites separated by three degrees of latitude. The sites differed in breeding density and duration of breeding season, but the distribution of clutch sizes did not differ between sites or between nesting attempts. Parental attendance patterns were similar between sites, suggesting that parental attendance is a highly conserved life-history trait in Western Sandpipers. Male Western Sandpipers attended broods longer than females, and the duration of parental attendance decreased at a similar rate for both sexes as the season progressed. Male and female Western Sandpipers undertake differential migrations to their non-breeding grounds, with males typically settling at more northerly locations and females at more southerly sites, a migration pattern shared by certain other monogamous calidridine species. These same species exhibit similar parental brood attendance patterns, suggesting the strong role of overall migration distance in shaping the expression of parental attendance behaviours. A contrast of more geographically disjunct sites coupled with a better understanding of the migratory connectivity between Western Sandpiper breeding and non-breeding populations would elucidate the role of cross-seasonal effects on parental brood attendance decisions.     

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.     

Contrasting Parental Tasks Influence Parental Roles for Paired and Single Biparental Cichlid Fish

Biparental care of young occurs when both parents provide some sort of care for offspring and can include a wide variety of behaviors, yet often studies focus on single aspects of parental care when trying to determine how each parent contributes. Here, we presented the biparental convict cichlid fish (Amatitlania nigrofasciata) with two conflicting parental behaviors: retrieval of non‐swimming offspring that have been displaced from the nest and defense against a conspecific intruder, a potential brood predator. We examined single males, single females, and pairs of parents to determine how males and females each contributed to overall parental care. Traditionally in this species, parents exhibit a division of labor (in which each parent contributes to all parental activities), but also exhibit a division of roles (in which males tend to favor the role of defense and females tend to favor more direct care, spending more time with offspring). We hypothesized that single parents would compensate for their absent mate, but that males and females would still favor preferred roles. Additionally, we hypothesized that there would be an asymmetrical expansion of roles, with females being more flexible. Our results show that the preferred roles of both parents were evident even when parents were without their mates and that males and females differed in their compensatory levels, at least when compared to the behaviors of the intact pair. Contrary to our prediction, females seem unable to fully compensate for the defensive behaviors usually exhibited by males, while males shifted completely to retrieve displaced offspring.     

The Effect of an Experimental Brood Reduction on Male Desertion in the Panamanian Blue Acara Cichlid Aequidens coeruleopunctatus

Investment in present vs. future reproduction is a life-history trade-off faced by many animals. Because males generally pay a higher cost from lost mating opportunities than females, males are expected to react more strongly to changes in brood value. We examined the effect of an experimental brood reduction on male desertion in the substrate-brooding biparental cichlid Aequidens coeruleopunctatus under field conditions. We tested the prediction that brood reduction should decrease the duration of male care and examined the effect of brood reduction on the quality of male and female parental care. Our results show that males with reduced broods stopped providing parental care earlier than males with control broods. Males with reduced broods, however, also stayed longer with their broods as the season progressed. Brood reduction did not decrease daily investment in male or female parental care. We conclude that males trade off present and future reproduction by changing the duration but not the quality of parental care. The longer duration of male care in the experimental group later in the season suggests that the trade-off between present and future reproduction changes as the season progresses because the payoffs of desertion progressively decrease.     

Females compensate for moult‐associated male nest desertion in Hooded Warblers

Uniparental offspring desertion occurs in a wide variety of avian taxa and usually reflects sexual conflict over parental care. In many species, desertion yields immediate reproductive benefits for deserters if they can re‐mate and breed again during the same nesting season; in such cases desertion may be selectively advantageous even if it significantly reduces the fitness of the current brood. However, in many other species, parents desert late‐season offspring when opportunities to re‐nest are absent. In these cases, any reproductive benefits of desertion are delayed, and desertion is unlikely to be advantageous unless the deserted parent can compensate for the loss of its partner and minimize costs to the current brood. We tested this parental compensation hypothesis in Hooded Warblers Setophaga citrina, a species in which males regularly desert late‐season nestlings and fledglings during moult. Females from deserted nests effectively doubled their provisioning efforts, and nestlings from deserted nests received just as much food, gained mass at the same rate, and were no more likely to die from either complete nest predation or brood reduction as young from biparental nests. The female provisioning response, however, was significantly related to nestling age; females undercompensated for male desertion when the nestlings were young, but overcompensated as nestlings approached fledging age, probably because of time constraints that brooding imposed on females with young nestlings. Overall, our results indicate that female Hooded Warblers completely compensate for male moult‐associated nest desertion, and that deserting males pay no reproductive cost for desertion, at least up to the point of fledging. Along with other studies, our findings support the general conclusion that late‐season offspring desertion is likely to evolve only when parental compensation by the deserted partner can minimize costs to the current brood.     

Effect of Mate Removal on Current and Subsequent Parental Care in the Convict Cichlid (Pisces: Cichlidae)

In most biparental, substrate-brooding species of cichlid fishes, female and male roles differ. Females are usually more involved in direct care of the young while males spend more time away patrolling the territory. This study tested the flexibility of these sex roles with removal experiments in the convict cichlid, Cichlasoma nigrofasciatum. When males were removed, female fanning activity increased. When females were removed, males spent more time fanning and less time away from the brood. Other behavioural variables (frequency of digging, mouthing, foraging and retrieving) were not affected. Being alone or paired during a first breeding episode did not affect parental behaviour during a subsequent episode in which all fish were paired. Observations were carried out during the day and at night, and nocturnal fanning of fry is reported here for the first time. Female role appears less flexible than male role, as befits the more direct care normally given by females.     

Sequential Polygyny During Egg Attendance is Rare in a Tree Frog and Does not Increase Male Fitness

Sequential polygyny is a reproductive strategy that allows males to continue to mate and compensates for the loss of future breeding opportunities incurred by parental care (i.e. egg attendance). Using the frog Kurixalus eiffengeri, we tested predictions that (1) attending males fathered two, overlapping clutches; and (2) that double clutching leads to improved offspring numbers. Using five microsatellite DNA markers, we genotyped 15 pairs of overlapping clutches, which differed slightly in developmental stage at a single egg‐laying site. Parentage analyses showed at least 12 of 15 pairs of overlapping egg clutches were sired by the attending male mated with different females, providing the first genetic evidence to support an earlier prediction that attending males sired both egg clutches. Field surveys found a low incidence of overlapping clutches (4.9% of 263 egg‐occupied stumps), suggesting sequential polygyny is uncommon. Stumps with multiple clutches contained significantly more eggs than stumps with single clutches but hatched similar number of tadpoles. Results suggest that continuous calling that attracts females during egg attendance is a reproductive tactic that maximizes mating opportunities. However, adoption of the sequential polygyny tactic may only result in marginal fitness gains for males that are traded off against average higher egg mortality in larger egg clutches.     

Why are males more attractive after brood care? Proximate causes of enhanced sex pheromone emission in a burying beetle

Recent studies demonstrate that pheromones can be costly to produce and emit and, therefore, the types and quantities that they express are likely to covary with individual condition. Previous experiments reveal that, when given the opportunity to breed and care for young, male burying beetles Nicrophorus vespilloides go on to produce a higher amount of their sex pheromone and attract more females than control males that do not exhibit parental care. This finding is surprising because parental care is usually assumed to be energetically costly, reducing the future capacity to invest in sexual signalling. However, burying beetles reproduce on dead vertebrates and the carrion meal might enable males to acquire resources that can subsequently be allocated to pheromone signalling. Alternatively, males might accumulate pheromone precursors because they do not emit their sex pheromone during brood care. To shed light on the mechanisms of enhanced pheromone emission after brood care, in the present study, we test the effect of diet quality, social condition during care (biparental versus uniparental care) and an experimentally enforced calling pause on subsequent male pheromone emission, body weight and energy storage components. The experimentally enforced calling pause and social condition during brood care demonstrate no impact on pheromone quantity. However, the results of the present study suggest that the vertebrate carrion meal during brood care partly explains enhanced pheromone release after care. Unravelling the biosynthetic pathways of the pheromone components and analyzing the impact of potential microbial symbionts on pheromone production represents a fruitful avenue for future research.     

Females Paired with More Attractive Males Show Reduced Oxidative Damage: Possible Direct Benefits of Mate Choice in Pied Flycatchers

Direct benefits of female mate choice may concern female fertility and fecundity but also physiological status. In birds with biparental care, males may contribute to improve the condition and health of their pair‐mates through help in constructing nests, incubation or incubation feeding and nestling provisioning. They may also reduce harassment of females by non‐pair males. A consequence of these male activities could be expressed in terms of oxidative damage, which may depend on metabolic effort and social stress. Here, we have related male contribution to parental and territorial duties to female oxidative status in the pied flycatcher Ficedula hypoleuca, a species where preferred males present darker dorsal plumage and, in Iberian populations, a large white forehead patch. Darker males were paired with females with high incubation attendance and reduced nestling provisioning rates, which may lead to reduced female exertion. These males owned nest boxes at which there were fewer visits by non‐pair males. Although females paired with dark mates worked less hard, they were able to raise more fledglings. Female oxidative damage measured as malondialdehyde (MDA) level in plasma declined with increasing incubation attendance and male incubation feeding. Moreover, levels of MDA in females declined with both darkness of male dorsal plumage and male forehead patch size when controlling for female forehead patch size and male age. The effect of male plumage darkness was especially strong. Females paired with middle‐aged males (2–3 yr) showed reduced levels of MDA compared with those paired with 1‐yr‐old and more than 3‐yr‐old males. Male age could not explain the effects of male attractiveness. Females paired with attractive males were more successful in reproduction while suffering reduced oxidative damage, possibly mediated by help during incubation and nestling rearing from their pair‐mates. Although correlative, the evidence suggests direct benefits of females paired with more attractive males.     

Female Response to Reduced Male Parental Care in Birds: An Experiment in Tree Swallows

In biparental species, parental-investment theory generally predicts an inverse relationship between the level of parental care provided by each parent and incomplete compensation by one parent in response to reduced parental care by their partner. The factors that influence the magnitude of this compensation have rarely been examined in birds. For example, the level of compensation may differ between a widowed bird that receives no assistance from its partner and a mated bird whose partner is still present but providing less than its normal share of parental care. This study compares the compensatory response of female tree swallows (Tachycineta bicolor) without their mate's parental assistance (when females are widowed) and with reduced male parental care (when males are handicapped by cutting some feathers). When compared with control females, experimental females compensated more in terms of nest visits for the absence than the reduction of male parental care. In addition, widowed females had significantly reduced brood mass and fledging success compared with control females. Although handicapped males reduced their nest-visit rate significantly, females with handicapped mates did not significantly increase their nest-visit rate nor was there reduced brood mass or reduced fledging success at their nests. Total nest-visit rate was similar for all groups, yet widowed females fledged fewer and lighter young, suggesting that they brought less food per nest visit. We suggest that fledging success and measures of offspring quality are probably better indicators of the level of compensatory parental care than nest-visit rate. We suggest that for widowed females the benefits of a relatively large compensatory response outweighed the costs; whereas, for females with a handicapped mate the benefits of higher feeding rates were not greater than the cost. The results of this study help to explain the differences among experimental studies of compensatory parental care and point to a new method of testing models of parental care.     

Parental Investment and Division of Labor in the Midas Cichlid (Cichlasoma citrinellum)

The Midas cichlid (Cichlasoma citrinellum) is an aggressive, monogamous fish living in the Great Lakes of Nicaragua. Its breeding success rates are low due to intense competition for breeding sites and high levels of predation on the young. Male Midas cichlids devote a small portion of body weight to gonads and gametes compared with females. Males produce relatively small amounts of sperm perhaps because cichlid fertilization is very efficient and the male has a high certainty of paternity. While pair members invest equal amounts of time in parental care over the course of the breeding cycle, there is a clear division of labor. Males invest more in territorial protection than do females, whereas females provide more nurturance. Both parents are active over the course of the cycle but the male invests more intensely in the early stages of the cycle. About the time the eggs hatch, the burden of care shifts to the female and she continues to invest significantly more than the male over the remainder of the cycle. Females invest much more than do males when tissue investment and parental behavior are combined. Females also assume more of the burden of care as the brood matures. The male is not free to take advantage of this and leave his mate to initiate other broods because two parents are needed to defend the breeding site and brood. Monogamy with biparental care results.     

Who Cares? Males Provide Most Parental Care in a Monogamous Nesting Cuckoo

Cuckoos hold a prominent position in the study of parental care, because they show the greatest variation of any bird family in the way they care for their offspring. Despite this, few data are available on cuckoos with biparental care even though it is the most common form of parental care in cuckoos and birds in general. Here I describe the breeding behaviour of the pheasant coucal, Centropus phasianinus , an old-world nesting cuckoo. I show that males almost exclusively build the nest and incubate and brood the young alone both at night and during the day. The incubation pattern of short, c . 40 min bouts on the nest interspersed with 20 min frequent recesses is well suited to incubation by a single parent and is widespread amongst birds. Males also defend the nestlings and deliver 80% of the feeds to the young consisting of insects (65%), frogs and reptiles. Females did not compensate for their fewer feeding visits by delivering more vertebrates than males. Although coucal males get little help feeding, the hourly feeding rate of 3.8 feeds per brood (1.4 feeds/nestling) exceed that of the few nesting cuckoos studied to date and matches that of other tropical non-passerines. Predominantly male care is found in less than 5% of birds, mainly species with reversed sexual size dimorphism or reversed sex-roles. Its evolution, especially in monogamous species, remains puzzling. The breeding behaviour of pheasant coucals illustrates a possible transitional stage in the evolution of polyandry and interspecific brood parasitism in cuckoos.