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.     

Ecological constraints on breeding system evolution: the influence of habitat on brood desertion in Kentish plover

1. One of the fundamental insights of behavioural ecology is that resources influence breeding systems. For instance, when food resources are plenty, one parent is able to care for the young on its own, so that the other parent can desert and became polygamous. We investigated this hypothesis in the context of classical polyandry when females may have several mates within a single breeding season, and parental duties are carried out largely by the male. 2. We studied a precocial wader, the Kentish plover Charadrius alexandrinus, that exhibits variable brood care such that the chicks may be raised by both parents, only by the female or, more often, only by the male. The timing of female desertion varies: some females desert their brood at hatching of the eggs and lay a clutch for a new mate, whereas other females stay with their brood until the chicks fledge. Kentish plovers are excellent organisms with which to study breeding system evolution, as some of their close relatives exhibit classical polyandry (Eurasian dotterel Eudromias morinellus, mountain plover Charadrius montanus), whereas others are polygynous (northern lapwing Vanellus vanellus). 3. Kentish plovers raised their broods in two habitats in our study site in southern Turkey: saltmarsh and lakeshore. Food intake was higher on the lakeshore than in the saltmarsh as judged from feeding behaviour of chicks and adults. As the season proceeded and the saltmarsh dried out, the broods moved toward the lakeshore. 4. As the density of plovers increased on lakeshore, the parents spent more time defending their young, and female parents stayed with their brood longer on the lakeshore. 5. We conclude that the influence of food abundance on breeding systems is more complex than currently anticipated. Abundant food resources appear to have profound implications on spatial distribution of broods, and the social interactions between broods constrain female desertion and polyandry.     

Brood desertion by female shorebirds: a test of the differential parental capacity hypothesis on Kentish plovers.

The aim of this study was to examine whether the energetic costs of reproduction explain offspring desertion by female shorebirds, as is suggested by the differential parental capacity hypothesis. A prediction of the hypothesis is that, in species with biparental incubation in which females desert from brood care after hatching, the body condition of females should decline after laying to a point at which their body reserves are too low for continuing parental care. We tested this prediction on Kentish plovers (Charadrius alexandrinus) in which both sexes incubate but the females desert from brood care before the chicks fledge. We found no changes in either the body masses or body compositions of both individual male and female plovers from early incubation and throughout early chick rearing. Furthermore, the timing of brood desertion by females was not affected by their body condition. Neither did we find gender differences in the energetic costs of incubation. There were no differences in the timing of brood desertion between experimental and control females in an experiment in which we lengthened or shortened the duration of incubation by one week. These results indicate that energetic costs do not explain offspring desertion by female Kentish plovers and that the needs of chicks for parental care rather than cumulative investment by females is what determines the timing of brood desertion.     

Parental behaviour in the Lapwing Vanellus vanellus

Parental behaviour of monogamous and polygynous Lapwings was studied during incubation and brood care. Both parents attended the nest in 86% of monogamous pairs ( n = 29 pairs). In 14% of pairs, only the male parent continued incubation until the eggs hatched, whereas the female deserted the clutch before or at the end of incubation. There was a clear division of parental roles during incubation. Females spent more time incubating (64% of time) than their mates (27%), whereas males spent more time defending the nest (3%) than females (>1%). Time spent incubating did not differ between monogamous and polygynous males. However, polygynous females spent more time incubating (primary females: 95%; secondary females: 97%) than monogamous females. Biparental care was the most common pattern of post-hatching care, although in some broods either the male or the female parent deserted before the chicks fledged. Division of sex roles was less pronounced in brood care than during incubation. Females spent more time brooding (21%) than males (3%), and females attended their chicks more closely than males. Nevertheless, males and females spent similar amounts of time defending the brood from predators and conspecifics. We suggest that the apparent division of parental roles may be explained by sexual selection, i.e. the remating opportunities for male Lapwings might be reduced if they increase their share in incubation. However, the different efficiency of care provision, for example in ability to defend offspring, may also influence the roles of the sexes in parental care.     

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.     

Experimental mate-removal increases the stress response of female house sparrows: the effects of offspring value?

Vertebrates secrete elevated levels of glucocorticoids in response to various stressors, which mobilize energetic reserves but concurrently interfere with reproduction. In accordance with life-history theory, recent evidence suggests that the corticosterone response to stress is modulated according to the value of the brood. Since brood value is positively related to parental care, the stress response modulation may be either the consequence of offspring value (e.g. large broods have high fitness potential - the brood value hypothesis) or the consequence of parental workload (e.g. large broods are energetically demanding for the parents - the workload hypothesis). In this experiment, we aimed at experimentally separating the effects of brood value and workload and to confront the latter two hypotheses. To do so, we captured the male parents from breeding pairs of house sparrows (Passer domesticus) and took them in captivity for 48 h. During the absence of males, mate-removed females made more food deliveries than controls (increased workload) but were unable to fully compensate the lack of their mate, thus their chicks were in worse condition (reduced brood value) than control chicks. After the experimental period, mate-removed females responded more strongly to the standardized stressor than controls. In both groups, the corticosterone response to stress was negatively related to the nestlings' mass gain. These results provide experimental support for the brood value hypothesis, i.e. that individuals may actively modulate their stress response (either down- or upwards) with respect to the value of their current reproduction.     

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.     

The mating system of Kentish Plovers Charadrius alexandrinus

Kentish Plover Charadrius alexandrinus pairs generally re-nest together after the loss of a clutch. In contrast, two females who hatched clutches changed mates before re-nesting, thus proving sequential polyandry. Observations of adults accompanying broods show that females normally desert the brood about a week after hatching. The majority of birds change mates between seasons, even if their partner from the previous season is alive.     

Prolactin stress response does not predict brood desertion in a polyandrous shorebird

One of the fundamental principles of the life-history theory is that parents need to balance their resources between current and future offspring. Deserting the dependent young is a radical life-history decision that saves resources for future reproduction but that may cause the current brood to fail. Despite the importance of desertion for reproductive success, and thus fitness, the neuroendocrine mechanisms of brood desertion are largely unknown. We investigated two candidate hormones that may influence brood desertion in the Kentish plover Charadrius alexandrinus: prolactin ('parental hormone') and corticosterone ('stress hormone'). Kentish plovers exhibit an unusually diverse mating and parental care system: brood desertion occurs naturally since either parent (the male or the female) may desert the brood after the chicks hatch and mate with a new partner shortly after. We measured the hormone levels of parents at hatching using the standard capture and restraint protocol. We subsequently followed the broods to determine whether a parent deserted the chicks. We found no evidence that either baseline or stress-induced prolactin levels of male or female parents predicted brood desertion. Although stress-induced corticosterone levels were generally higher in females compared with males, individual corticosterone levels did not explain the probability of brood desertion. We suggest that, in this species, low prolactin levels do not trigger brood desertion. In general, we propose that the prolactin stress response does not reflect overall parental investment in a species where different parts of the breeding cycle are characterized by contrasting individual investment strategies.     

Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers.

Why do some parents care for their young whereas others divorce from their mate and abandon their offspring? This decision is governed by the trade-off between the value of the current breeding event and future breeding prospects. In the precocial Kentish plover Charadrius alexandrinus females frequently, but not always, abandon their broods to be cared for by their mate, and seek new breeding partners within the same season. We have shown previously that females'' remating opportunities decline with date in the season, so brood desertion should be particularly favourable for early breeding females. However, the benefits are tempered by the fact that single-parent families have lower survival expectancies than those where the female remains to help the male care for the young. We therefore tested the prediction that increasing the value of the current brood (by brood-size manipulation) should increase the duration of female care early in the season, but that in late breeders, with reduced remating opportunities, desertion and thus the duration of female care should be independent of current brood size. These predictions were fulfilled, indicating that seasonally modulated trade-offs between current brood value and remating opportunities can be important in the desertion decisions of species with flexible patterns of parental 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.     

Brood mixing and reduced polyandry in a maternally mouthbrooding cichlid with elevated among-breeder relatedness

Uniparental maternal brood care often coincides with multiple paternity and single maternity of broods, possibly reflecting benefits of polyandry and costs of uniparental care. Genetic data from the maternally mouthbrooding cichlid fish Simochromis pleurospilus revealed the opposite pattern--low polyandry and allomaternal care. More than 70% of the investigated females had mated with a single male, and 14% of the females had unrelated fry in their broods. Broods with foreign fry were in the late stage of brood care, in which females guard free-swimming fry and recall the broods into their mouths for protection. With one exception, fostering females were related to their adopted fry at the level of first cousins (R(QG) > 0.12), but relatedness between fosters and adopted fry was not significantly higher than between fosters and fry tended by other females. Relatedness among breeders extended to the level of first-order relatives. Mean relatedness among contemporaneously breeding dams (R(QG) = 0.08) was significantly higher than among dams breeding in different seasons (R(QG) = -0.04), which suggests a temporal or spatial concentration of mouthbrooding relatives. Indeed, females sometimes brood in small groups. This behaviour may reduce brood predation but will increase the risk of brood mixing, which is possibly mitigated by low costs of brood care and indirect benefits accrued by relatedness among the breeders in the group. Remarkably, the apparent inbreeding potential did not give rise to bet-hedging polyandry or active avoidance of relatives, as half of the mated individuals were related at R(QG) > 0.13 and polyandry did not coincide with high within-pair relatedness.     

On the evolutionary pathway of parental care in mouth-brooding cichlid fishes

Evolutionary theory predicts that differences in parental care patterns among species arose from interspecific differences in the costs and benefits of care for each sex. In Galilee St Peter''s fish, Sarotherodon galilaeus (Cichlidae), male care, female care and biparental care all occur in the same population. We exploit this unusual variability to isolate conditions favouring biparental versus uniparental mouth-brooding by males or females. We first review a game-theoretic model of parental care evolution, predictions of which we test experimentally in this paper. Manipulations of the operational sex ratio show that males and females desert their offspring more frequently when the costs of care are high (in terms of lost mating opportunities). Breeding trials with males of different sizes show that small fathers desert more frequently than large fathers. We attribute this to the associated difference in the fitness benefit of biparental care relative to female-only care. Our experimental results confirm that in St Peter''s fish the probability of caring is determined facultatively according to current conditions at each spawn. The experiments and model together suggest that interspecific variation in remating opportunities and clutch size may be responsible for differences in care patterns within the sub-family Tilapiini. Our results support the hypothesis that biparental mouth-brooding was the ancestral state of both male and female uniparental mouth-brooding in cichlid fishes.     

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.     

Brood Reduction in White Storks Mediated through Asymmetries in Plasma Testosterone Concentrations in Chicks

We hypothesized that increasing chick plasma testosterone concentrations, transmitted from the mothers via their eggs, enhances survival of their offspring and that the fitness of the young, depending on the maternal hormones, is influenced by parental quality. To test our hypotheses we distinguished the broods of white storks Ciconia ciconia L. where chicks died and those where all chicks survived. We analysed the plasma testosterone concentrations in the chicks, the ability of the chicks to be first to receive food and the mass of chicks before fledging in relation to their hatching order and recorded the body mass of parents and food mass delivered by them.
Female storks used the asymmetries in testosterone concentrations within a brood to control brood size and adjusted the number of young hatched to match the parental ability to rear offspring. Females of poor condition altered the testosterone concentrations to produce large differences between the chicks: The first-hatched chicks, which had high plasma testosterone levels, responded faster to the feeding parent and received more food than did their younger siblings. One or two later-hatched chicks, which had lower testosterone levels, died in these broods. Females in good condition produced small differences in testosterone concentrations between the chicks and all chicks survived in their brood. Chicks that were raised by the females of poor condition in reduced broods were heavier than chicks that were raised by females of good condition in broods where all chicks survived.
We suggest that the control of brood size by testosterone concentration, transmitted by the mother to the chicks, is a hormonal means of condition-dependent reproductive strategy in the white stork.     

EVOLUTION OF OBLIGATE SIBLICIDE IN BOOBIES. 2: FOOD LIMITATION AND PARENT–OFFSPRING CONFLICT

Proximate limitation on parental food delivery has long been invoked to explain the evolution of single-chick broods of pelagic seabirds such as masked boobies (Sula dactylatra). A second possible proximate limit on brood size is siblicide driven by genetic parent–offspring conflict (POC) over brood size, if siblicidal offspring can reduce brood size to one even if the parents' optimal brood size is greater than one. I tested these two hypotheses by experimentally suppressing obligate siblicide in masked booby broods and comparing breeding parameters of these broods with unmanipulated single-chick control broods. Per capita mortality rate of experimental nestlings was higher than that of controls, but this deficit was more than made up by larger brood size. Parents of experimental broods brought more food to offspring, had higher fledging success, and apparently incurred no additional major short-term cost of reproduction, relative to parents of control broods, thus refuting the food limitation hypothesis. Estimates of inclusive fitness of chicks in experimental broods were higher than were those of control nestlings, a result inconsistent with the POC hypothesis that the siblicidal offspring's optimal brood size is one while the parents' optimum is greater than one. This discrepency between natural brood size and apparent brood size optima might be resolved in several ways: experimental artifacts may give misleading estimates of optimal brood size; experimental and control offspring may have different reproductive values at the time of fledging; nestling masked boobies may face a special frequency-dependent case of POC in which the high risk of sharing a nest with a siblicidal sibling makes invasion of other behavioral genotypes difficult even when offspring and parent inclusive fitnesses are higher from a nonsiblicidal brood of two than from a brood of one.     

The evolution of parental care in insects: A test of current hypotheses

Which sex should care for offspring is a fundamental question in evolution. Invertebrates, and insects in particular, show some of the most diverse kinds of parental care of all animals, but to date there has been no broad comparative study of the evolution of parental care in this group. Here, we test existing hypotheses of insect parental care evolution using a literature‐compiled phylogeny of over 2000 species. To address substantial uncertainty in the insect phylogeny, we use a brute force approach based on multiple random resolutions of uncertain nodes. The main transitions were between no care (the probable ancestral state) and female care. Male care evolved exclusively from no care, supporting models where mating opportunity costs for caring males are reduced—for example, by caring for multiple broods—but rejecting the “enhanced fecundity” hypothesis that male care is favored because it allows females to avoid care costs. Biparental care largely arose by males joining caring females, and was more labile in Holometabola than in Hemimetabola. Insect care evolution most closely resembled amphibian care in general trajectory. Integrating these findings with the wealth of life history and ecological data in insects will allow testing of a rich vein of existing hypotheses.     

Can patterns of chromosome inversions in Drosophila pseudoobscura predict polyandry across a geographical cline?

Female multiple mating, known as polyandry, is ubiquitous and occurs in a wide variety of taxa. Polyandry varies greatly from species in which females mate with one or two males in their lifetime to species in which females may mate with several different males on the same day. As multiple mating by females is associated with costs, numerous hypotheses attempt to explain this phenomenon. One hypothesis not extensively explored is the possibility that polyandrous behavior is captured and “fixed” in populations via genetic processes that preserve the behavior independently of any adaptive benefit of polyandry. Here, we use female isolines derived from populations of Drosophila pseudoobscura from three locations in North America to examine whether different female remating levels are associated with patterns of chromosome inversions, which may explain patterns of polyandry across the geographic range. Populations differed with respect to the frequency of polyandry and the presence of inversion polymorphisms on the third chromosome. The population with the lowest level of female remating was the only one that was entirely comprised of homokaryotypic lines, but the small number of populations prevented us investigating this relationship further at a population level. However, we found no strong relationship between female remating levels and specific karyotypes of the various isolines.     

Brood desertion and polygamous breeding in the Kentish Plover Charadrius alexandrinus

In the Kentish Plover Charadrius alexandrinus one of the adults, typically the female, deserts the brood when the chicks are a few days old. Once parental care is terminated, adults may initiate a second nesting attempt if sufficient time remains within the season. For these nests, individuals pair with different mates from those of the first nesting attempt, thus becoming sequentially polygamous. In a small population of Kentish Plovers in Fuente de Piedra lake (southern Spain), the duration of biparental care of broods was longer than in other localities. It also showed considerable variation between years that was evidently related to Gull-billed Tern Gelochelidon nilotica predation pressure on the chicks. There was year-to-year variation in the number of polygamous matings. Both the duration of the breeding season and nesting success in the first half of the season limited the occurrence of polygamy. Despite females deserting broods earlier than males, the interval between the first and second nesting of polyandrous females and polygynous males was similar. The interval was not affected by the body condition of females after the first nesting attempt, nor by problems related to egg formation ability, but was probably due to the availability of potential mates. More females than males initiated second nests, suggesting that polygamous opportunities were more limited for males than for females. In terms of delayed breeding, reduced survivorship or reduced breeding opportunities in years following polygamous breeding, polygamous individuals did not have greater costs than non-polygamous ones. Females with second nests did not seem to be selective in mate choice, mating with any available male. Mates for second nests may therefore be of lower quality than those for first nests, as judged by male plumage characteristics. Clutch sizes and egg characteristics of polyandrous females were similar in first and second nests. Nest success of second nests was only 40% of that of first ones, with nest desertion accounting for 60% of the losses. As the costs of polygamy are apparently low and as breeding success is very variable among years, polygamous breeding of the long-lived Kentish Plover may be an important breeding strategy with which to increase individual lifetime reproductive success.     

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.