Brood desertion in Kentish plover: the value of parental care

To understand the evolution of parental care, one needs to estimatethe payoffs from providing care for the offspring and from terminatingcare and deserting them. In this study we estimated the payofffrom care provision, and in a companion paper we analyze thepayoff from offspring desertion. In the current study we experimentallyinvestigated the influence of the number and sex of attendingparents on growth and survival of offspring in the Kentish ploverCharadrius alexandrinus, in two sites (A and B). Either the maleor the female parent was removed from some broods at hatchingof the chicks (female-only and male-only broods, respectively),whereas in control broods both parents were allowed to attendtheir young. At site A survival of the chicks was lower in uniparental(male-only and female-only) broods than in control broods, whereaswe found no difference in brood survival at site B. Brood survivaldecreased over the season. Removal of either parent did not influencethe growth of the young, although growth varied over the breeding season,and it was significantly different between the sites. Theseresults suggest that the payoff from parental care decreasesover the breeding season and that the value of parental care(i.e., the contribution of parents to the survival of theiryoung) may depend on the environment.     

Brood desertion in Kentish plover: sex differences in remating opportunities

To understand the evolution of parental care, one needs to estimatethe payoffs from providing care for the offspring and the payoffsfrom terminating care and deserting them. These payoffs arerarely known. In this study we experimentally estimated therewards from brood desertion in a species that has a variablepattern of parental care. In particular, either the female or themale parent may desert the brood in Kentish plover Charadrius alexandrinus,so some broods are attended by one parent of either sex, whereasin other broods both parents stay with the brood until the chicks fledge.We created single males and single females by experimentallyremoving the other parent and the clutch. The expected rematingtime of males was significantly higher (median: 25.4 days) thanthat of the females (5.3 days, p <.0001). The expected rematingtime tended to increase over the breeding season in both sexes,although the increase was significant only in females. The newnest of remated males was closer to their previous territory (mean± SE, 46 ± 8 m) than that of the remated females(289 ± 57 m, p <.001). Hatching success of new nestswas not different between remated males and females. Our resultsdemonstrate that the remating opportunities are different formale and female Kentish plovers and these opportunities varyover the season. We propose that the remating opportunitieswere influenced by the male-biased adult sex ratio and the seasonaldecrease in the number of breeders. However, we stress thatmeasuring remating times is a more direct measure of matingopportunities than calculating the operational sex ratio.     

The effect of partial brood loss on male desertion in a cichlid fish: an experimental test

There is little experimental evidence testing whether currentbrood size and past brood mortality influence mate desertion.In the cichlid Aequidens coeruleopunctatus both parents initiallydefend offspring. In a field study, all experimental broods,irrespective of initial brood size (222.9 ± 60.4, mean± SD), were manipulated to a size of 100 fry. Neitherthe duration nor investment of females in parental care differed between control and brood reduced pairs, even though care seemedcostly. On average, females lost 5.1 ± 4.8% of initialweight while guarding a brood until independence. In contrast,males with experimentally reduced broods guarded fry for significantlyfewer days before deserting their mate than did males fromcontrol pairs with natural-sized broods (20.5 ± 7.5 vs. 14.2 ± 6.2 days). In at least 20% of cases (n = 9/45),the deserting male immediately mated with another female. Maleswith experimentally reduced broods also spent less time guardingfry before deserting and attacked fewer brood predators thandid males with control broods. For broods manipulated to have100 fry, there was a significant negative relationship betweenthe days until male desertion and the proportion of the initialbrood removed. This indicates that male assessment of the futuresuccess of the current brood (hence its reproductive value)is based on past mortality and/or that there is variation amongmales in the expected size of future broods. Both current broodsize and brood size relative to initial brood size are thereforepredictors of male, but not female, parental behavior and matedesertion. Female care may be unaffected by brood reductiondue to limited breeding opportunities and partial compensationfor reduced male care.     

Brood sex ratio in the Kentish plover

How and why do the mating opportunities of males and femalesdiffer in natural population of animals? Previously we showedthat females have higher mating opportunities than males inthe Kentish plover Charadrius alexandrinus. Both parents incubatethe eggs, and males provide more brood care than females; thusit is not obvious why the females find new mates sooner thanthe males. In this study we investigated whether the sex-biasedmating opportunities stem from biased offspring sex ratios.We determined the sex of newly hatched, precocial chicks usingCHD gene markers. Among fully sexed broods, 0.461 ± 0.024(SE) of chicks (454 chicks in 158 broods) were male, and thissex ratio was not significantly different from unity. The proportionof males at hatching decreased significantly over the breedingseason, which occurred consistently in all 3 years of the study.Large chicks were more likely to be males than females. Neitherparental age nor body size of male and female parents was relatedto brood sex ratio. We also sexed a number of chicks that werecaught after they left their nest (range of estimated ages 0–17days) and found that the proportion of males increased withbrood age. This relationship remained highly significant whencontrolling statistically for hatching date. As brood size decreaseddue to mortality after the chicks left their nest, these resultssuggest that the mortality of daughters was higher than thatof the sons shortly after hatching. Taken together, our resultsshow that the female-biased mating opportunities in the Kentishplover are not due to biased brood sex ratio at hatching but,at least in part, are due to female-biased chick mortality soonafter hatching.     

Synchronous provisioning increases brood survival in cooperatively breeding pied babblers

1.  Behavioural synchrony typically involves trade-offs. In the context of foraging, for example, synchrony may be suboptimal when individuals have different energy requirements but yield net benefits in terms of increased foraging success or decreased predation risk.
2.  Behavioural synchrony may also be advantageous when individuals collaborate to achieve a common goal, such as raising young. For example, in several bird species, provisioners synchronize nest-feeding visits. However, despite the apparent prevalence of provisioning synchrony, it is not known whether it is adaptive or what its function might be.
3.  Here, we propose a novel explanation for provisioning synchrony: it increases brood survival by decreasing the number of temporally separate nest visits and accordingly the chance that the nest will be detected by predators. Using cooperatively breeding pied babblers, we showed experimentally that provisioners synchronized nest visits by waiting for another provisioner before returning to the nest. Brood survival increased with provisioning synchrony. Provisioners were more likely to synchronize feeding visits for older nestlings as they were louder and possibly more conspicuous to predators. Finally, provisioners in large groups were more likely to wait for other provisioners and synchronized a higher proportion of all visits than those in smaller groups. Thus, provisioning synchrony may be one mechanism by which large groups increase brood survival in this species.
4.  This study highlights a novel strategy that birds use to increase the survival of young and demonstrates the advantages of coordinated behaviour in social species.     

Farming-out of offspring is a predominantly male tactics in a biparental mouthbrooding cichlid <Emphasis Type="BoldItalic">Perrisodus mircolepis</Emphasis>

Synopsis Intraspecific brood-mixing of a Tanganyikan biparental cichlid fish Perissodus microlepis has been attributed to farming-out, a behaviour in which a parent transport some or all of their free-swimming young in the mouth and put them under the care of other guarding parents. We conducted observations under natural conditions to understand how often farming-out occurs and which sex is the primary performer. At most brooding sites, young in a school entirely disappeared before attaining to the size of independence. At many of these sites, farming-out and its precursory behaviours by males preceded disappearance of their young. Females never performed farming-out. We proposed that farming-out by males is an alternative tactics to brood desertion to evade paternal roles for remating.     

Offspring desertion and parental care in the Whiskered Tern Chlidonias hybrida

In species with biparental care, a conflict of interest can arise if one mate tries to maximize its own reproductive success at the expense of the other's. One of the mates can desert the brood to accrue a number of benefits to enhance its own fitness, leaving parental care to the remaining parent. This study is the first to describe the desertion pattern in a tern species (Sternidae). We investigated offspring desertion in the Whiskered Tern Chlidonias hybrida, a species with semi‐precocial chicks. Offspring desertion was recorded in 52% of nests prior to fledging (n = 131 nests). Females also deserted during the post‐fledging period. Of the deserters, 97% were females. Desertions started when chicks were 5 days old and no longer required intense brooding. Desertions before fledging did not affect fledging success. Provisioning rates between pair members differed, and females supplied much less food than males. Female provisioning rate affected the chances of nest desertion significantly: daily desertion rates were lower when females supplied more food. After females had deserted, males increased their provisioning rates but compensated for the loss of female care only partly in two‐ and three‐chick broods. Only in small (one‐chick) broods was compensation full. We conclude that male and female Whiskered Terns adopt different reproductive strategies in the population studied here. Females invest much less in parental care than males, providing less food and deserting more frequently. Given the ready availability of food and low predation pressure, benefits appear to accrue to females that desert; selection forces may therefore not be acting against female desertion.     

Sexual conflict over care: antagonistic effects of clutch desertion on reproductive success of male and female penduline tits

A fundamental tenet of sexual conflict theory is that one sex may increase its reproductive success (RS) even if this harms the other sex. Several studies supported this principle by showing that males benefit from reduced paternal care whereas females suffer from it. By investigating penduline tits Remiz pendulinus in nature, we show that parental conflict may be symmetric between sexes. In this small passerine a single female (or male) cares for the offspring, whereas about 30% of clutches are deserted by both parents. Deserting parents enhance their RS by obtaining multiple mates, and they reduce the RS of their mates due to increased nest failure. Unlike most other species, however, the antagonistic interests are symmetric in penduline tits, because both sexes enhance their own RS by deserting, whilst harming the RS of their mates. We argue that the strong antagonistic interests of sexes explain the high frequency of biparental desertion.     

Quantifying the costs and benefits of parental care in female treehoppers

Parental protection of eggs represents one of the most basicforms of parental care. Theory suggests that even such basicparental investment represents a trade-off between current offspringsurvival and future reproductive success. However, few studieshave quantified the underlying costs and benefits of parentalcare for marked individuals across an entire lifetime. I markedand followed 370 females of Publilia concava (Hemiptera: Membracidae)that exhibited a range of guarding durations for their firstclutch. Greater hatching success was correlated with longerguarding durations, and a removal experiment verified that femalepresence was responsible for a twofold increase in hatchingsuccess. On the other hand, females that remained to guard eggshad a lower number and size of future broods, suggesting thatparental care may reduce lifetime fecundity. Marked femalesexhibited a bimodal distribution of guarding durations, reflectingthe extreme tactics of immediate abandonment or remaining throughhatching. Estimates of lifetime number of nymphs produced byfemales that abandon eggs early versus guard eggs through hatchingrevealed roughly equivalent levels of fitness. I discuss theconditions under which we might expect a female to adopt eachof the alternative tactics, given the costs and benefits ofparental care that were quantified in this study.     

The function of habitat change during brood-rearing in the precocial Kentish plover <Emphasis Type="Italic">Charadrius alexandrinus</Emphasis>

Food availability is often variable during the breeding season. Parents with nonmobile, altricial young have no choice but to accept changes in local food availability, whereas in precocial animals, the parents may lead their young away from poor sites to areas that have rich resources and/or are safe from predators. We investigated the latter hypotheses in the Kentish plover Charadrius alexandrinus, a precocial shorebird that raises its young in two habitats: on lakeshore and in saltmarsh. Parents move with their broods from saltmarsh to lakeshore, especially late in the breeding season, and we hypothesized that lakeshores provide more food than the saltmarsh. Consistent with our hypotheses, plover chicks grew faster on the shore, and the difference in growth rates between the two habitats was amplified later in the breeding season. In addition, brood survival was higher on lakeshore than in saltmarsh and decreased with hatching date. Taken together, our results suggest that Kentish plover parents increase their reproductive success by switching brood-rearing habitats strategically.     

Distribution and breeding ecology of the Ferruginous Duck Aythya nyroca in Algeria

We conducted a survey of the distribution of Ferruginous Duck Aythya nyroca across Algeria and analysed the influence of nest-site characteristics on nesting success at a Ramsar site, Lake Tonga. The species was found to occupy different wetlands (freshwater lakes, brackish marshes and salt lakes) across three major climatic belts (subhumid coastal strip, semi-arid Hauts Plateaux and arid Sahara). Mean clutch size of successful nests was 13.3 ± 6.0 eggs (N = 26) with a hatching rate of 74% for successful clutches. Nesting success was recorded for 44% of nests with clutch desertion (72.7%) accounting for the majority of failed clutches. Egg size of the study population, which breeds at the southern limit of the species’ range, was significantly smaller than that of its northerly counterparts. Clutch size was negatively related to egg size and positively associated with depth of water below the nest, suggesting that older, more experienced or high-quality birds monopolised the safest sites. Successful clutches were significantly associated with tall vegetation, suggesting that when nesting is carried out mainly on offshore floating islets, protection against aerial predators and heat stress determine nesting outcome. Conspecific brood parasitism was significantly and positively associated with deferred egg-laying and smaller egg size, suggesting an age-dependent mechanism.     

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.     

Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism

All parental hosts of heterospecific brood parasites must paythe cost of rearing non-kin. Previous research on nest parasitismby brown-headed cowbirds (Molothrus ater) concluded that competitivesuperiority of the typically more intensively begging and largercowbird chick leads to preferential feeding by foster parentsand causes a reduction in the hosts' own brood. The larger sizeof cowbird nestlings can be the result of at least two causes:(1) cowbirds preferentially parasitize species with smallernestlings and lower growth rates; and/or (2) cowbirds hatchearlier than hosts. I estimated the cost of cowbird parasitismfor each of 29 species by calculating the difference betweenhosts' published brood sizes in nonparasitized and parasitizednests and using clutch size to standardize values. In this analysis,greater incubation length and lower adult mass, surrogate measuresof the hatching asynchrony and size difference between parasiteand hosts, were both related to greater costs of cowbird parasitismwithout bias owing to phylogeny. To establish causality, I manipulatedclutch contents of eastern phoebes (Sayornis phoebe) and examinedwhether earlier hatching by a single cowbird or phoebe egg reducesthe size of the rest of the original host brood. As predicted,greater hatching asynchrony increased the proportion of theoriginal phoebe brood that was lost. This measure of the costof parasitism was partially owing to increased hatching failureof the original eggs in asynchronous broods but was not at allrelated to the size differences of older and younger conspecificnestmates. However, proportional brood loss owing to an earlierhatching conspecific was consistently smaller than brood lossowing to asynchronous cowbirds in both naturally and experimentallyparasitized phoebe nests. These results imply that althoughhatching asynchrony is an important cause of the reduction ofhost broods in parasitized clutches, competitive features ofcowbird nestlings remain necessary to explain the full extentof hosts' reproductive costs caused by interspecific brood parasitism.     

Vocal matching and intensity of begging calls are associated with a forebrain song circuit in a generalist brood parasite

Vocalizations produced by developing young early in life have simple acoustic features and are thought to be innate. Complex forms of early vocal learning are less likely to evolve in young altricial songbirds because the forebrain vocal‐learning circuit is underdeveloped during the period when early vocalizations are produced. However, selective pressure experienced in early postnatal life may lead to early vocal learning that is likely controlled by a simpler brain circuit. We found the food begging calls produced by fledglings of the brown‐headed cowbird (Molothrus ater), a generalist avian brood parasite, induced the expression of several immediate early genes and early circuit innervation in a forebrain vocal‐motor pathway that is later used for vocal imitation. The forebrain neural activity was correlated with vocal intensity and variability of begging calls that appears to allow cowbirds to vocally match host nestmates. The begging‐induced forebrain circuits we observed in fledgling cowbirds were not detected in nonparasitic passerines, including species that are close relatives to the cowbird. The involvement of forebrain vocal circuits during fledgling begging and its association with vocal learning plasticity may be an adaptation that provides young generalist brood parasites with a flexible signaling strategy to procure food from a wide range of heterospecific host parents. © 2015 Wiley Periodicals, Inc. Develop Neurobiol 76: 615–625, 2016     

Inter‐specific brood parasitism and the evolution of avian reproductive strategies

Avian brood parasitism is a potent selective agent modulating host behaviors and morphology, although its role in determining diversification of avian breeding strategies remains elusive. Hitherto, the study of selection of brood parasites on host breeding strategies has been based on single reproductive trait approaches, which neglect that evolutionary responses to brood parasites may involve co‐ordinated changes in several aspects of reproduction. Here I consider covariation among reproductive traits to test whether parental breeding strategies of hosts of brown headed cowbird (BHC hereafter) in North America and the common cuckoo (CC hereafter) in Europe, two parasites with contrasting level of virulence, have evolved in response to brood parasitism. The effect of parasitism on avian breeding strategies differed between continents. Long term exposure to BHC parasitism selected for a lower breeding investment in North America, but not so CC parasitism in Europe. These results suggest a key role of parasite virulence on the evolution of avian breeding strategies and that brood parasitism has selected for a co‐ordinated breeding strategy of reducing parasitism costs by shortening and fractioning reproductive events within a single season in North America.     

Nest defence by Magpies(Pica pica) and the brood parasitic Great Spotted Cuckoos(Clamator glandarius) in parasitized and unparasitized nests

Summary Nest defence is a frequent and widespread parental behaviour which enhances brood survival. We have found that in a Spanish Magpie population which is heavily parasitized by the brood parasitic Great Spotted Cuckoo, Magpies defend (1) unparasitized more frequently than parasitized nests, and (2) at the end of the nestling period more frequently than in other stages of the breeding cycle. Great Spotted Cuckoos are brood parasites, which means that their eggs are incubated and their nestlings are raised by members of a host species. Brood parasites are not thought to take care of their own offspring. However, we have found that Great Spotted Cuckoos sometimes scolded us on our regular visits to parasitized magpie nests (but never on those to unparasitized nests). Frequency of nest defence by cuckoos differed significantly among years, being significantly higher at the beginning of the study. Although sporadic observations of adult brood parasites feeding juveniles have been recorded, nest defence has not previously been suggested for any brood parasite.

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Nestverteidigung von durch den Häherkuckuck(Clamator glandarius) parasitierten und unparasitierten Nestern bei Elstern(Pica pica)

Zusammenfassung Nestverteidigung ist ein häufiges und weit verbreitetes elterliches Verhalten zur Erhöhung des Bruterfolges. In einer spanischen Elsterpopulation, die sehr intensiv vom Häherkuckuck parasitiert ist, wurden unparasitierte Nester häufiger verteidigt als parasitierte, und zum Ende der Nestlingsperiode wurden Nestern häufiger verteidigt als zu früheren Phasen des Brutzyklus. Häherkuckucke sind Brutparasiten, deren Eier von den Wirtseltern bebrütet und die Nestlinge von ihnen aufgezogen werden. Solche Brutparasiten kümmern sich im allgemeinen nicht selbst um ihre Nachkommen. Manchmal jedoch haßten Häherkuckuck auf uns, wenn wir parasitierte Nester der Elster kontrollierten, während an unparasitierten Nestern ein solches Hassen niemals erfolgte. Die Häufigkeit dieser Nestverteidugung der Kuckucke variierte zwischen Jahren und war signifikant häufiger zu Beginn unserer Untersuchung. Zwar wurde gelegentlich schon Füttern der Jungvögel durch elterliche Brutparasiten beobachtet, die hier festgestellte Nestverteidung ist bisher aber von keinem Brutparasiten beschrieben.

     

An experimental test of the prolonged brood care model in the tufted titmouse (Baeolophus bicolor)

The prolonged brood care model rests on the assumption thatretaining an offspring through the winter months in the faceof a limited food supply should have a cost for parents. Wetested this idea with a New World permanent-resident bird,the tufted titmouse (Baeolophus bicolor). Using DNA fingerprinting,we assessed the degree of relatedness between adult and juvenilebirds in 17 winter groups, finding that in 8 of the groups no young bird was the offspring of the territorial pair. We comparedthe nutritional condition of territorial adult birds in smallforest fragments from which their own offspring and other younghad been removed with the nutritional condition of controlbirds from unmanipulated fragments. Contrary to the model'sassumption, the nutritional condition of adults in treatment groups (young removed) appeared to be worse, not better, thanin groups where a related juvenile was present. These resultssuggest that the prolonged brood care model may not be universalin its application and that under some ecological conditions,retaining offspring through the winter can result in a netbenefit for territorial adults despite the necessity of sharing resources.     

Body mass dynamics during incubation and duration of parental care in Pacific Dunlins Calidris alpina pacifica: a test of the differential parental capacity hypothesis

Breeding is energetically expensive and individuals face a trade‐off between current and future breeding investment. Due to their production of large eggs, female birds are thought to have substantially higher initial energetic investments than males, which decrease the female's offspring rearing capacity. The differential parental capacity hypothesis argues that this large initial investment limits the ability of female shorebirds to provide extended parental care, which can ultimately lead to offspring desertion. This hypothesis predicts that (1) during early incubation females will be in poorer condition than males, (2) both sexes will lose condition during incubation, but the decline in females will be slower than the decline in males and (3) there will be a positive relationship between female condition and the duration of maternal brood care. These predictions were tested using data on body mass adjusted for body size (as a proxy for condition) and parental care from Pacific Dunlins Calidris alpina pacifica nesting on the Yukon Kuskokwim Delta, Alaska. None of the predictions received support: females were heavier than males in early incubation, the overall pattern during incubation was that males gained mass while female mass remained relatively constant, and there was no relationship between female mass and maternal brood care duration. These results suggest that the factors influencing parental care decisions are more complex than a parent simply caring until it is physiologically unable to do so.