Negotiation of parental care when the stakes are high: experimental handicapping of one partner during incubation leads to short-term generosity

1. Most game theoretical models of biparental care predict that a reduction in care by one partner should not be fully compensated by increased work of its mate but this may not be true for incubating birds because a reduction in care could cause the entire brood to fail.
2. I performed the first handicapping experiment of both males and females during incubation, by placing small lead weights on the tails of male and female northern flickers Colaptes auratus , a woodpecker in which males do most of the incubation.
3. Females responded to the acute stressor (handling and handicapping) by tending to abandon more readily than males and staying away from the nest longer in the first incubation bout. Among pairs that persisted, both males and females compensated fully for a handicapped partner, keeping the eggs covered nearly 100% of the time.
4. Partners did not retaliate by forcing their handicapped mate to sit on the eggs with a long incubation bout length subsequent to having a long bout length themselves. Instead, during the 24 h immediately after handicapping, males behaved generously by relieving handicapped females early.
5. Such generosity was probably not energetically sustainable as these male partners took on less incubation in the 72 h following handicapping compared to female partners of handicapped males. Males and females are probably generous in the short-term because of the high cost of nest failure during incubation but maintaining increased work loads in the longer term is probably limited by body condition and abandonment thresholds consistent with game theory models.     

Biparental care in house sparrows: negotiation or sealed bid?

We explored the responses of monogamous house sparrow parentsto deviations in their mates' contributions to nestling provisioning.Following 1-2 days of baseline measurement of parental fooddelivery rates, we applied small lead fishing weights to thetail feathers of either male or female parents. Weighting hadmuch greater immediate impact on male parental care than on female care, but the handicapping had little long-term effecton either male or female provisioning behavior. When parentalperformance of handicapped males was most impaired, their matesdid not show significant increases in parental care as compensation,nor did females mated to handicapped males reduce their provisioningas their mates recovered from weighting. Similarly, males matedto handicapped females did not respond to their partners' recovery with declines in their own efforts; paradoxically, these malesshowed a sustained elevation of provisioning throughout thepost-treatment interval, despite no significant reduction inprovisioning by weighted females. The apparent insensitivityof both males and females to changes in their mates' parentalbehavior, and the ineffectiveness of current partner behaviorat predicting an individual's provisioning effort, fail toconform to assumptions of biparental care models that requirefacultative responses to partner deviations in effort. Instead,the remarkable consistency of each individual's behavior supportsthe notion of "sealed bids" and suggests that variation innestling provisioning is largely attributable to factors thatare independent of the mate's current behavior, such as differencesin individual quality.     

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.     

Sex Allocation in Response to Maternal Condition: Different Tactics of Care-Giving by Male and Female Zebra Finches

While behavioral ecologists have studied sex allocation for 30 yr, almost nothing is known about the roles of male vs. female parents in making secondary allocation decisions in species with bi‐parental care. To investigate possible sex differences in tactics in zebra finches, we manipulated the condition of one cohort of females by trimming their flight feathers; a second cohort of females and all males were left intact. Focal observations of feeding behavior revealed that manipulated females did not reduce their feeding time, but rather focused their efforts on rearing sons, while control females allocated effort to rearing daughters. Males mated to manipulated females tended to focus effort to daughters, while control males showed no consistent response. Manipulated females experienced a lower reproductive rate, primarily because of a low daughter rate, relative to control females. Manipulated females also laid smaller clutches and had longer inter‐clutch intervals, which suggest that their ability to metabolize and allocate essential proteins from pectoral muscle mass during the egg‐laying period was impaired. To our knowledge, this study is the first to show that parents of both sexes make active sex allocation decisions when the physiological condition of one parent is manipulated; males do not simply adopt female allocation patterns, but make complementary adjustments. Our results have implications for interpretation of handicapping studies that seek to understand the dynamics of inter‐sexual negotiations of care‐giving. Investigation of sex differences in sex allocation tactics in species with limited dietary protein, such as granivorous birds, is a potentially important direction for future research.     

To Compensate or Not? Caring Parents Respond Differentially to Mate Removal and Mate Handicapping in the Burying Beetle,Nicrophorus quadripunctatus

Game theoretical models predict that when one parent reduces its care, the mate should adjust its care facultatively to compensate partially. To test these models, mate-removal and mate-handicapping techniques have been used. However, there have been few experimental studies comparing results from mate removal and mate handicapping, and there has been no study on insects employing handicapping. Male and female burying beetles both maintain the nest and regurgitate to young. We examined how burying beetle parents adjust their level of care when their mates are removed or handicapped. Males increased their frequency of provisioning significantly after female removal, whereas females showed no response to male removal. However, neither sex showed a response to the handicapping of its partner, although handicapped mates decreased the frequency of their care. This result showed that burying beetle parents respond differentially to mate removal and handicapping, and suggests that parents do not respond to a change in the behavior of their mates.     

State‐dependent cooperation in burying beetles: parents adjust their contribution towards care based on both their own and their partner's size

Handicapping experiments on species with biparental care show that a focal parent increases its contribution when its partner is handicapped. Such results are interpreted as evidence for negotiation, whereby each parent adjusts its amount of care to that of its partner. However, it is currently unclear whether the focal parent responds to a change in its handicapped partner's behaviour or state. To address this gap, we conducted an experiment on the burying beetle Nicrophorus vespilloides where we first generated different‐sized males and females by varying the duration of larval development. We then used a 2 × 2 factorial design in which a small or large male was paired with a small or large female. Small females provided less direct care (food provisioning and interactions with larvae) than large females, and both males and females provided less direct care when paired with a small partner. Thus, the focal parent adjusted its contribution towards care based on both its own state and that of its partner. There was also evidence for negotiation between the two parents as the focal parent adjusted its contribution based on the amount of care by its partner. However, there was no evidence that negotiation accounted for how the focal parent responded to its partner's size. Our results have important implications for our understanding of biparental cooperation as they show that each parent adjusts its contribution not only based on the amount of care provided by its partner but also based on its own state and its partner's state.     

Conflict between parents over care

Conflict between parents over care of young arises when the young benefit from the effort of both parents, but each parent suffers a reduction in future reproductive success as a consequence of its own effort. Here, we review existing models and argue that they fail to capture many important components of parental conflict. For example, we lack adequate models of how a parent should compensate for a reduction in the effort of its mate. These models should incorporate the process by which decisions are reached. Recent theory suggests that a parent benefits by handicapping itself, and more experimental and theoretical work on this topic could be fruitful. We also need more theoretical work on attractiveness that incorporates consistent interactions between males and females.     

Parental care behavior in the monogamous,sexually dimorphic Madagascar paradise flycatcher: sex differences and the effect of brood size

I studied the parental care behavior of the Madagascar paradise flycatcher Terpsiphone mutata in northwestern Madagascar. I especially focused on feeding, brooding and vigilance behaviors. Feeding rate did not differ between males and females, but females spent more time at the nest than males. Females dedicated their time to brooding, while males perched on the nest and were vigilant. Both parents changed the feeding rate in relation to brood size, so the feeding rate per nestling was not different among nests of different brood size. Duration of brooding by females increased with decreasing brood size, suggesting that the Royama effect, the pattern of lower feeding rate per nestling in larger broods, did not apply in this study. Males spent more time on vigilance than females. Anti-predator vigilance by males should be important for nestling survival given the high predation pressure typical of this population. In conclusion, males provide considerable parental care probably to minimize nestling starvation and to avoid nest predation. My results are not consistent with the general pattern of less parental effort by males in monogamous, sexually dimorphic species.     

Sex-related parental care strategies in the lesser spotted woodpecker Picoides minor: of flexible mothers and dependable fathers

We investigated sex-specific parental care behaviour of lesser spotted woodpeckers Picoides minor in the low mountain range Taunus, Germany. Observed parental care included incubation, nest sanitation as well as brooding and feeding of nestlings. Contributions of the two sexes to parental care changed in progress of the breeding period. During incubation and the first half of the nestling period, parental care was divided equally between partners. However, in the late nestling stage, we found males to feed their nestlings irrespective of brood size while females considerably decreased feeding rate with the number of nestlings. This behaviour culminated in desertion of small broods by females shortly before fledging. The fact that even deserted nests were successful indicates that males were able to compensate for the females' absence. Interestingly, the mating of one female with two males with separate nests could be found in the population, which confirms earlier findings of polyandry in the lesser spotted woodpecker. We conclude that biparental care is not essential in the later stage and one partner can reduce effort and thus costs of parental care, at least in small broods where the mate is able to compensate for that behaviour. Reduced care and desertion appears only in females, which might be caused by a combination of two traits: First, females might suffer higher costs of investment in terms of mortality and secondly, male-biased sex ratio in the population generally leads to higher mating probabilities for females in the following breeding season. The occurrence of polyandry seems to be a result of these conditions.     

Blood metabolite levels in normal and handicapped pied flycatchers rearing broods of different sizes

We measured levels of select metabolites (glucose, triglycerides, free fatty acids, glycerol, uric acid) and corticosterone in the blood plasma of adult pied flycatchers Ficedula hypoleuca while they were rearing broods whose sizes were modified experimentally. We also made it more difficult than normal for some pairs of birds to forage by removing certain wing and tail feathers (handicapping them). Both procedures have been shown previously to change parental workload. We did this in order to determine if the birds alter their use of nutrients in response to differences in their workload. Metabolite levels were not influenced by handicapping or brood size. However, the concentration of free fatty acids in the plasma of females and of triglycerides in the plasma of males was directly related to the frequency with which the adults fed their nestlings. These findings suggest that the two sexes have different ways of coping with the work associated with rearing the brood: females apparently undergo brief daily fasts while feeding their chicks, whereas males take more time to feed themselves while providing food for their young, and spend more time doing so as their workload increases. The flycatchers exhibited high concentrations of uric acid and corticosterone in the blood plasma; corticosterone and glycerol were positively correlated in females; and corticosterone and triglyceride levels were negatively correlated in males; all of which suggest that gluconeogenesis provides some of the energy required for their parental activities.     

Sexual division of antibacterial resource defence in breeding burying beetles, Nicrophorus vespilloides

1.  A key component of parental care involves defending resources destined for offspring from a diverse array of potential interspecific competitors, such as social parasites, fungi and bacteria.
2.  Just as with other aspects of parental care, such as offspring provisioning or brood defence, sexual conflict between parents may arise over how to share the costs of this form of care. There has been little previous work, however, to investigate how this particular burden might be shared.
3.  Here, we describe a hitherto uncharacterized form of parental care in burying beetles Nicrophorus vespilloides , a species which prepares carrion for its young and faces competition from microbes for this resource. We found that parents defend the carcass with antibacterial anal exudates, and that the antibacterial activity of these exudates is only upregulated following the discovery of a corpse. At the same time, phenoloxidase activity in the anal exudates is downregulated, indicating parallels with the internal insect immune system.
4.  In unmanipulated breeding pairs, females had higher antibacterial activity in their anal exudates than males, suggesting sex-specific roles in this aspect of parental care.
5.  When we experimentally widowed males, we found that they increased levels of antibacterial activity in their anal exudates. Experimentally widowing females, however, led them to decrease levels of antibacterial activity in their anal exudates. Widowed beetles of each sex thus produced anal exudates of comparable antibacterial activity. We suggest that this flexible division of antibacterial activity may be coordinated by Juvenile Hormone.     

Flexible parents: joint effects of handicapping and brood size manipulation on female parental care in Nicrophorus vespilloides

Parental care is highly variable, reflecting that parents make flexible decisions in response to variation in the cost of care to themselves and the benefit to their offspring. Much of the evidence that parents respond to such variation derives from handicapping and brood size manipulations, the separate effects of which are well understood. However, little is known about their joint effects. Here, we fill this gap by conducting a joint handicapping and brood size manipulation in the burying beetle Nicrophorus vespilloides. We handicapped half of the females by attaching a lead weight to their pronotum, leaving the remaining females as controls. We also manipulated brood size by providing each female with 5, 20 or 40 larvae. In contrast to what we predicted, handicapped females spent more time provisioning food than controls. We also found that handicapped females spent more time consuming carrion. Furthermore, handicapped females spent a similar amount of time consuming carrion regardless of brood size, whereas controls spent more time consuming carrion as brood increased. Females spent more time provisioning food towards larger broods, and females were more likely to engage in carrion consumption when caring for larger broods. We conclude that females respond to both handicapping and brood size manipulations, but these responses are largely independent of each other. Overall, our results suggest that handicapping might lead to a higher investment into current reproduction and that it might be associated with compensatory responses that negate the detrimental impact of higher cost of care in handicapped parents.     

Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care

Partial filial cannibalism, the act of cannibalizing some offspring, has been explained as a response to the high energetic cost of care. I tested this hypothesis by manipulating the cost-to-benefit ratio of care in the scissortail sergeant, Abudefduf sexfasciatus, a tropical damselfish with male care. Background egg mortality was lower than the incidence of cannibalism, confirming that males did not just dispose of dead eggs. Investment in the current brood affected future investment, because males forced to skip a brood cycle put more effort into courtship during the following cycle and obtained larger broods than did unmanipulated males. Any factor influencing the cost-to-benefit ratio of parental care should also affect the incidence of cannibalism. I reduced the cost of care by supplementary feeding and reduced the benefit of care by simulating a decrease in paternity certainty through simulated intrusions by non-nesting males. Supplementary feeding significantly reduced partial filial cannibalism by parental males, a result compatible with the hypothesis that eggs are consumed to cover the energetic costs of parental care. Cannibalism decreased regardless of whether males were fed with conspecific eggs or crabmeat. Cannibalism was only reduced but not fully eliminated by supplementary feeding, and residual levels of cannibalism after feeding were similar to the background rate of egg mortality. Simulated intrusions by non-nesting males led to an increase in filial cannibalism and a decrease in parental effort.     

Male age mediates reproductive investment and response to paternity assurance

Theory predicts that male response to reduced paternity will depend on male state and interactions between the sexes. If there is little chance of reproducing again, then males should invest heavily in current offspring, regardless of their share in paternity. We tested this by manipulating male age and paternity assurance in the burying beetle Nicrophorus vespilloides. We found older males invested more in both mating effort and parental effort than younger males. Furthermore, male age, a component of male state, mediated male response to perceived paternity. Older males provided more prenatal care, whereas younger males provided less prenatal care, when perceived paternity was low. Adjustments in male care, however, did not influence selection acting indirectly on parents, through offspring performance. This is because females adjusted their care in response to the age of their partner, providing less care when paired with older males than younger males. As a result offspring, performance did not differ between treatments. Our study shows, for the first time, that a male state variable is an important modifier of paternity–parental care trade-offs and highlights the importance of social interactions between males and females during care in determining male response to perceived paternity.     

Males paving the road to polyandry? Parental compensation in a monogamous nesting cuckoo and a classical polyandrous relative

Comparative studies have established the necessity for biparental care as an important factor for monogamy in freshwater fish and birds. However, whether two parents are really needed for offspring care remains an open question in many cases. I experimentally studied female and male contributions to offspring care in the white-browed coucal (Centropus superciliosus), a monogamous and biparental cuckoo with a balanced adult sex ratio, and contrasted it with the sympatric black coucal (C. grillii), a classically polyandrous species with a male-biased adult sex ratio and male-only care. To study the necessity for biparental care, I temporarily removed one partner for 2 days to see whether the remaining parent compensated for the absence of its partner. Both female and male white-browed coucals approximately doubled their feeding rates when their partner was absent, thus fully compensating the number of feeding visits to the nest. However, nestlings maintained their growth only, when males were present and females were removed. When males were removed and only females were present, nestling growth declined. Hence, only male white-browed coucals fully compensated for the temporary loss of the partner, suggesting that females could benefit most from nesting with additional males—if these should become available. Removing female black coucals had no consequence for nestling feeding rates of male black coucals. But male black coucals had to be returned to their territories within a few hours to avoid harming the brood because female black coucals typically would not commence feeding their offspring. In conclusion, the breeding system of white-browed coucals seems quite flexible and the relatively balanced adult sex ratio may stabilize monogamy in this species. Should ecological factors ever favour a stronger bias in the adult sex ratio towards males, female white-browed coucals may easily become polyandrous and relinquish parental care entirely to males.     

Morphological and genetic predictors of parental care in the North American barn swallow Hirundo rustica erythrogaster

Sexually dimorphic traits often signal the fitness benefits an individual can provide to potential mates. In species with altricial young, these signals may also predict the level of parental care an individual is expected to provide to shared offspring. In this study, we tested three hypotheses that traditionally relate sexually dimorphic traits to parental care in two populations of North American barn swallows Hirundo rustica erythrogaster. The good parent hypothesis predicts a positive relationship between an individual's ornamentation and his or her care whereas the differential allocation (more care given by individuals when paired to high quality mates) and reproductive compensation (more care given by individuals when paired to low quality mates) hypotheses predict that an individual's level of parental investment is relative to the quality of their mate. Male and female North American barn swallows have colorful ventral feathers and elongated tail streamers, but there is evidence that ventral color, not tail streamer length, predicts measures of seasonal reproductive success. Accounting for the positive correlation between within‐pair feeding rates and other potentially confounding variables in all of our models, we found no support for the good parent hypothesis because in both males and females, traits shown to be under sexual selection did not predict feeding rates in either sex. However, our data reveal that male coloration, and not streamer length, predicted a female's provisioning rate to shared offspring (females fed more when paired with darker individuals) in two separate populations, supporting the differential allocation, but not the reproductive compensation hypothesis. Because genetic traits have also been shown to affect parental investment, we evaluated this variable as well and found that a male's paternity did not have significant effects on either male or female feeding rates. Overall, our results suggest that females do not pair with darker males in order to gain direct benefits in terms of his expected levels of parental care to shared offspring, but do themselves invest greater levels of care when paired to darker males. Further, our results are consistent with previous studies which suggest that ventral feather color, not streamer length, is a target of sexual selection in North American populations of barn swallow because females invested more in their offspring when paired to darker mates.     

Altitudinal and environmental variation in lifespan in the Copper butterfly Lycaena tityrus

1.  Variation in longevity within and between natural populations is widespread, and understanding the relative importance of environmental and genetic factors as well as their interactions in mediating such variation is crucial in longevity research.
2.  In this study lifespan of adult copper butterflies was examined in relation to altitude, temperature (20 and 27 °C), sex and adult feeding.
3.  As expected, longevity increased with decreasing temperature, and sucrose-fed butterflies had longer lifespans compared to water-fed and finally non-fed individuals. The impact of feeding, especially of having access to water or not, was larger at the higher compared to the lower temperature.
4.  Regarding altitudinal patterns, increased lifespan in high-altitude populations was largely restricted to beneficial feeding conditions, while under carbohydrate deprivation low-altitude animals lived longer, suggesting that low-altitude butterflies do better under food stress.
5.  Differences in longevity between sexes were small at 20 °C, while females lived substantially longer than males at the higher temperature. Consequently, females may be less susceptible to high temperature stress than males. Further, males suffered more from food stress than females, suggesting that females are generally more stress resistant than males.
6.  Using a full factorial design, this study demonstrates that variation in longevity is caused by several factors, and additionally by substantial interactive effects. Consequently, patterns of variation in longevity are complex, and one needs to be cautious when neglecting this source of variation, by focussing on individual factors only.     

When fathers make the difference: efficacy of male sexually selected antimicrobial glands in enhancing fish hatching success

1.  Egg and offspring resistance to pathogens is a major determinant of survival and has been mainly ascribed to maternal factors. However, paternal production of antimicrobials was recently suggested to increase offspring survival in species where males perform egg care.
2.  In the peacock blenny, Salaria pavo , a demersal spawning species where males exhibit a pair of anal glands producing lysozyme-like compounds, we tested the antimicrobial activity and the egg protection efficacy of these glands. The anal gland secretion (AGS) has an inhibitory effect on the growth of both Gram-negative and Gram-positive bacteria, including those causing the most severe fish diseases in marine culture. The egg clutches cared for by males deprived of anal glands have a significantly lower survival rate than those cared for by sham-operated males and non-viable eggs showed clear signs of bacterial infection.
3.  Anal gland secretion production and its protein content are proportional to gland size. In species where male parental care plays a crucial role in offspring survival, females are expected to assess mates selecting those traits that are reliably associated with parental ability. Hence, we experimentally challenged females with dummy males differing in anal gland size. Females definitely preferred dummy males with larger anal glands, suggesting that their choice is driven by the pursuit of direct fecundity benefits.
4.  These findings indicate that antimicrobial production is a crucial component of male parental care. The contribution of antimicrobials to male performance as fathers suggests that the development of traits devoted to this function may influence male attractiveness and be sexually selected.     

Paternity analysis in the golden egg bug using AFLPs: do the males preferentially accept their true genetic offspring?

Abstract.  1. The evolution of parental care and intraspecific parasitism involve conflicts of interest between mothers and other potential care givers who contribute to enhance offspring survival. In the golden egg bug, Phyllomorpha laciniata Villers (Heteroptera: Coreidae), females lay eggs on conspecifics and on plants. The adaptive significance of egg carrying in this species has been the subject of some controversy, which can only be resolved by determining the genetic relationship between the eggs and the adult who carries them. This study examined whether male acceptance of true genetic offspring occurs with a higher frequency than that expected from random oviposition on conspecifics.
2. Paternity analysis, using Amplified Fragment Length Polymorphism (AFLP) markers, was conducted on eggs carried by males housed with field-mated females.
3. Out of the total number of eggs sired by males in the experimental groups, the proportion of eggs carried by males that were their true genetic offspring was 30.8%.
4. Monte Carlo methods show that the probability of a male accepting an egg that is his true genetic offspring is higher than expected if females dumped eggs on males at random.
5. These results suggest that paternal care plays an important role in the maintenance of male egg carrying in this species. In addition, the methodology developed may become useful in determining true genetic parents in other species in which neither the father nor the mother can be determined by observational methods.     

Sexual differences in moult–breeding overlap and female reproductive costs in pied flycatchers, Ficedula hypoleuca

1. In this study I show that a sexual difference in timing of the post-nuptial moult frequently occurs in a sub-arctic population of the pied flycatcher.
2. Most pairs started to moult after fledging of their young, but an overlap between moult and nestling feeding was more common among males than females. This sexual difference in moult–breeding overlap increased as the season progressed.
3. Females with moult–breeding overlap laid smaller clutches than non-moulting females. In addition to many other factors explaining the seasonal decline in clutch size that has been found for many bird species, it is possible that females adjust their clutch size according to their own risk of having to start moulting while still feeding the nestlings.
4. Nearly 24% of the females were deserted by their mate before the young fledged. Desertion imposed no fitness costs to males in terms of fledgling number or quality, suggesting that their females managed to adjust their care for the loss of male care.
5. Deserted females started moulting later than aided females, which may be a result of their increased reproductive investment.
6. Deserted females and females aided by moulting males had lower survival rate than females aided by non-moulting males.
7. These findings suggests that delayed moult may be one mechanism causing inter-annual reproductive costs in birds, and the relationship between a sexual difference in timing of moult and its fitness consequences may be widespread among passerine birds.