Hosts improve the reliability of chick recognition by delaying the hatching of brood parasitic eggs

The reliability of information that animals use to make decisions has fitness consequences. Accordingly, selection should favor the evolution of strategies that enhance the reliability of information used in learning and decision making. For example, hosts of avian brood parasites should be selected to increase the reliability of the information they use to learn to recognize their own eggs and chicks. The American coot (Fulica americana), a conspecific brood parasite, uses cues learned from the first-hatched chicks of each brood to recognize and reject parasitic chicks. However, if parasitic eggs are among the first to hatch, recognition cues are confounded and parents then fail to distinguish parasitic chicks from their own chicks. Therefore, hosts could ensure correct chick recognition by delaying parasitic eggs from hatching until after the first host eggs. Here we demonstrate that discriminatory incubation, whereby coots specifically delay the hatching of parasitic eggs, improves the reliability of parasitic chick recognition. In effect, coots gain fitness benefits by enhancing the reliability of information they later use for learning. Our study shows that a positive interaction between two host adaptations in coots--egg recognition and chick recognition--increases the overall effectiveness of host defense.     

Nestling competition,rather than supernormal stimulus,explains the success of parasitic brown-headed cowbird chicks in yellow warbler nests

Interspecific parasitic chicks are usually fed more than the smaller host young with whom they share the nest. This could be due to parasitic chicks having evolved exaggerated features that are preferred by the adults to the features present in their own young (the supernormal stimulus hypothesis). Alternatively, the success of parasitic chicks could be due to them being better competitors. We tested these hypotheses by studying the interaction between brown-headed cowbird chicks, Molothrus ater, and a common small host, the yellow warbler, Dendroica petechia. Parasitic chicks begged more intensively than the host''s young and received most of the feeds. The relative height reached by the begging chicks of both species was the most important variable in determining their feeding success. Being larger and begging intensively, brown-headed cowbirds were better able to reach higher than the host''s young, but at equal heights parasitic chicks were no better than the host''s young at gaining feeds. It is suggested that the success of the brown-headed cowbirds when parasitizing yellow warblers is due to them physically out-competing the smaller young of their hosts, and not to them evoking a stronger response from the hosts by being a supernormal stimulus.     

Adoption Behaviour in Little and Common Terns (Aves; Sternidae): Chick Benefits and Parents' Fitness Costs

Adoption seeking by semi-precocial chicks of some bird species can be adaptive since it provides an alternative tactic to permit poorly cared-for young to survive despite their neglectful parents' behaviour. Moreover, own-nest desertion may enhance inclusive fitness of fugitive chicks by increasing survival prospects of siblings. On the other hand, adoption by breeding adults can be detrimental to foster parents' fitness if they invest resources in promoting survival of others' offspring at the expense of their own. In this study we report on the proximate causes and survival consequences of adoption seeking by chicks, and on the presumed costs of adoption sustained by foster parents in two colonial, ground-nesting tern species: the little tern (Sterna albifrons) and the common tern (Sterna hirundo). Adoptions were frequent in little tern and, notably, in common tern colonies. Chicks that deserted their original brood were poorly fed compared with resident chicks, but crowding in the brood and age rank relative to nest companions did not influence the chances of desertion. Deserting their original brood was risky for little tern chicks since stray chicks experienced higher mortality than resident ones. Common tern chicks deserted their original nest significantly more often than little tern chicks. Adoptees of both species benefited by the same survival prospects as resident chicks. A negative correlation existed between the proportion of food given to strange chicks and seasonal fitness or chick survival rate of breeding pairs. This was not predictable because: (1) foster parents could have increased their parental efforts, thus ensuring the same survival prospects to their own chicks, and (2) chicks of foster parents could have been, in turn, adopted thus obliterating the negative fitness effects of adoption. The sexes were identical with respect to their proneness to provide food to strange chicks. We suggest that adoption seeking by little and common tern chicks has evolved as an alternative tactic that is pursued to counter the effects of poor parental care. Adoption behaviour seems maladaptive since it is accompanied by a reduction in seasonal fitness in both species. Possible alternative explanations for nest desertion and adoption behaviour are also discussed.     

Co-evolutionary arms race between brood parasites and their hosts at the nestling stage

Traditionally it was thought that the arms race between brood parasites and their hosts was confined to the egg stage of the breeding cycle because many host species are able to reject mimetic parasitic eggs but they are unable to reject strongly different parasitic chicks. However, recently, new cases of chick rejection, discrimination, or mimicry, have been published confirming the possibility that an equivalent arms race to that found at the egg stage could ever be played out at the chick stage. Here, I review the evidence for the existence of a co-evolutionary arms race at the nestling stage. Recent findings include new deceiving strategies used by brood parasitic chicks, defensive strategies used by foster parents and adaptive strategies of host nestlings. This review shows that both chick discrimination and relationships between brood parasites and their hosts at the nestling stage are much more complicated than previously believed. At least in some brood parasite-host systems, an arms race at the nestling stage is working.     

A brood parasite selects for its own egg traits

Many brood parasitic birds lay eggs that mimic their hosts'' eggs in appearance. This typically arises from selection from discriminating hosts that reject eggs which differ from their own. However, selection on parasitic eggs may also arise from parasites themselves, because it should pay a laying parasitic female to detect and destroy another parasitic egg previously laid in the same host nest by a different female. In this study, I experimentally test the source of selection on greater honeyguide (Indicator indicator) egg size and shape, which is correlated with that of its several host species, all of which breed in dark holes. Its commonest host species did not discriminate against experimental eggs that differed from their own in size and shape, but laying female honeyguides preferentially punctured experimental eggs more than host or control eggs. This should improve offspring survival given that multiple parasitism by this species is common, and that honeyguide chicks kill all other nest occupants. Hence, selection on egg size in greater honeyguides parasitizing bee-eaters appears to be imposed not by host defences but by interference competition among parasites themselves.     

Food availability modulates the effects of maternal antibodies on growth and immunity in young feral pigeons

It is now widely acknowledged that mothers can transfer their own immune experience to their progeny through the allocation of specific maternal antibodies (hereafter referred as MatAb) that can shape offspring phenotype and affect their fitness. However, the importance of environmental variability in modulating the effects of MatAb on offspring traits is still elusive. Using an experimental approach, we investigated how food availability interacted with MatAb to solve the trade‐off between humoral immunity and growth in young feral pigeons Columba livia. Results show that the inhibitory effect of MatAb on the humoral response of chicks was detected regardless of the food treatment. In addition, body mass growth was higher in chicks receiving lower amounts of maternal antibodies but only in chicks of the ad libitum food treatment. This contradicts previous studies and suggests that the transfer of MatAb could entail some costs for chicks and reduce their growth. Taken together these results reinforce the idea that the maternal antibodies play a central role in shaping offspring life‐history traits but that their adaptive value is highly dependent on the environmental context in which they are transmitted by the mother.     

Great Spotted Cuckoo Nestlings but not Magpie Nestlings Starve in Experimental Age‐Matched Broods

Nestlings of non‐evicting avian brood‐parasites have to compete for food with foster parents' own nestlings. The outcome of these competitive contests is determined mainly by body size differences between parasitic and host nestlings. As part of the coevolutionary arms race between brood parasites and their hosts at the nestling stage, it has been reported that some host foster parents discriminate against parasitic chicks and are reluctant to feed them. Here, by experimentally creating size‐matched broods of different composition (only magpie Pica pica chicks, only great spotted cuckoo Clamator glandarius chicks or mixed broods), we show that great spotted cuckoo chicks starved in 20.2 per cent (17 of 84) of the parasitized magpie nests even in absence of size asymmetries, while in none (0 of 72) of the nests a magpie chick starved. As far as we know, this is the first record of non‐evictor brood parasitic nestlings starving without being smaller than their host nestmates in a frequently used host species. Nest composition had no effect on chick starvation. The cuckoo nestling starved even in two of the nests occupied by only one cuckoo chick. Our results could be explained by (1) magpies being reluctant to feed cuckoo chicks; (2) parasitic chicks receiving lower‐quality food items or cuckoo nestlings being sensitive to some particular component of the diet (e.g. cereal grains); and (3) the existence of cuckoo chick discrimination ability by magpie foster parents.     

Brood parasite eggs enhance egg survivorship in a multiply parasitized host

Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests. We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this 'dilution effect', comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection.     

Cuckoos and parasitic ants: Interspecific brood parasitism as an evolutionary arms race

Each summer thousands of nesting birds feed cuckoo chicks that have killed the hosts' own young. Likewise, worker ants rear the brood of other ants that have killed the workers' queen or even induced the workers to kill their queen themselves. In both cases the hosts spend time and energy raising offspring that, to them, are of no genetic value. Such exploitation involves intricate parasitic adaptations for deceiving hosts. It should also provoke host defences. Brood and social parasites and their hosts therefore provide excellent opportunities for the study of evolutionary arms races.     

Paternity-parasitism trade-offs: a model and test of host-parasite cooperation in an avian conspecific brood parasite

Efforts to evaluate the evolutionary and ecological dynamics of conspecific brood parasitism in birds and other animals have focused on the fitness costs of parasitism to hosts and fitness benefits to parasites. However, it has been speculated recently that, in species with biparental care, host males might cooperate with parasitic females by allowing access to the host nest in exchange for copulations. We develop a cost-benefit model to explore the conditions under which such host-parasite cooperation might occur. When the brood parasite does not have a nest of her own, the only benefit to the host male is siring some of the parasitic eggs (quasi-parasitism). Cooperation with the parasite is favored when the ratio of host male paternity of his own eggs relative to his paternity of parasitic eggs exceeds the cost of parasitism. When the brood parasite has a nest of her own, a host male can gain additional, potentially more important benefits by siring the high-value, low-cost eggs laid by the parasite in her own nest. Under these conditions, host males should be even more likely to accept parasitic eggs in return for copulations with the parasitic female. We tested these predictions for American coots (Fulica americana), a species with a high frequency of conspecific brood parasitism. Multilocus DNA profiling indicated that host males did not sire any of the parasitic eggs laid in host nests, nor did they sire eggs laid by the parasite in her own nest. We used field estimates of the model parameters from a four-year study of coots to predict the minimum levels of paternity required for the costs of parasitism to be offset by the benefits of mating with brood parasites. Observed levels of paternity were significantly lower than those predicted under a variety of assumptions, and we reject the hypothesis that host males cooperated with parasitic females. Our model clarifies the specific costs and benefits that influence host-parasite cooperation and, more generally, yields precise predictions about expected levels of host male paternity. These predictions will enable a more rigorous assessment of field studies designed to test adaptive hypotheses of host-parasite cooperation.     

Interactions between adult robins and chicks belonging to other pairs

Adult robins are able to discriminate between chicks hatched in their own and in other territories. The latter are much less likely to be fed and are more likely to be attacked than the adult's own young. As chicks grow older they become less likely to beg at adults other than their parents. Adults rarely feed chicks from other territories unless they have fledged young of their own. Possible causes of these different responses are discussed and it is emphasized that these need not involve individual recognition. Males appear to be more likely than females to feed chicks hatching in other territories. This could be the result of the females learning about their chicks while brooding them. Males may benefit more, on average, from feeding other pairs' chicks than do females. There has been a previous report that robins are unable to make the discriminations reported in this paper and possible reasons for this discrepancy are discussed. It is conceivable that it reflects a difference between populations.     

Experimental evidence for chick discrimination without recognition in a brood parasite host

Recognition is considered a critical basis for discriminatory behaviours in animals. Theoretically, recognition and discrimination of parasitic chicks are not predicted to evolve in hosts of brood parasitic birds that evict nest-mates. Yet, an earlier study showed that host reed warblers (Acrocephalus scirpaceus) of an evicting parasite, the common cuckoo (Cuculus canorus), can avoid the costs of prolonged care for unrelated young by deserting the cuckoo chick before it fledges. Desertion was not based on specific recognition of the parasite because hosts accept any chick cross-fostered into their nests. Thus, the mechanism of this adaptive host response remains enigmatic. Here, I show experimentally that the cue triggering this 'discrimination without recognition' behaviour is the duration of parental care. Neither the intensity of brood care nor the presence of a single-chick in the nest could explain desertions. Hosts responded similarly to foreign chicks, whether heterospecific or experimental conspecifics. The proposed mechanism of discrimination strikingly differs from those found in other parasite-host systems because hosts do not need an internal recognition template of the parasite's appearance to effectively discriminate. Thus, host defences against parasitic chicks may be based upon mechanisms qualitatively different from those operating against parasitic eggs. I also demonstrate that this discriminatory mechanism is non-costly in terms of recognition errors. Comparative data strongly suggest that parasites cannot counter-evolve any adaptation to mitigate effects of this host defence. These findings have crucial implications for the process and end-result of host-parasite arms races and our understanding of the cognitive basis of discriminatory mechanisms in general.     

Alien eggs in duck nests: brood parasitism or a help from Grandma?

Intraspecific brood parasitism (IBP) is a remarkable phenomenon by which parasitic females can increase their reproductive output by laying eggs in conspecific females' nests in addition to incubating eggs in their own nest. Kin selection could explain the tolerance, or even the selective advantage, of IBP, but different models of IBP based on game theory yield contradicting predictions. Our analyses of seven polymorphic autosomal microsatellites in two eider duck colonies indicate that relatedness between host and parasitizing females is significantly higher than the background relatedness within the colony. This result is unlikely to be a by-product of relatives nesting in close vicinity, as nest distance and genetic identity are not correlated. For eider females that had been ring-marked during the decades prior to our study, our analyses indicate that (i) the average age of parasitized females is higher than the age of nonparasitized females, (ii) the percentage of nests with alien eggs increases with the age of nesting females, (iii) the level of IBP increases with the host females' age, and (iv) the number of own eggs in the nest of parasitized females significantly decreases with age. IBP may allow those older females unable to produce as many eggs as they can incubate to gain indirect fitness without impairing their direct fitness: genetically related females specialize in their energy allocation, with young females producing more eggs than they can incubate and entrusting these to their older relatives. Intraspecific brood parasitism in ducks may constitute cooperation among generations of closely related females.     

Common loon parents defend chicks according to both value and vulnerability

In many territorial breeders, conspecifics that intrude during the chick‐rearing period pose a threat to survival of young. Defense of young from intruders is costly to parents, so it is likely that intense selective pressure has shaped chick defense so as to maximize parental fitness. We simulated territorial intrusion by exposing adult common loons Gavia immer and their chicks to a decoy and used mixed models to investigate responses. We tested two hypotheses: 1) the value hypothesis, which holds that parents should defend large broods of offspring more strongly because of the greater potential fitness benefits they offer, and 2) the vulnerability hypothesis, which predicts vigorous defense of young offspring, whose small size and limited mobility render them vulnerable to sudden attacks from intruders that approach under water. Under natural conditions, parents spent over 80% of their time within 20 m of chicks younger than two weeks (‘young chicks’) but 66% or less of their time close to chicks four weeks or older (‘old chicks’). Parents of young chicks associated less with the decoy but yodelled and penguin danced more during decoy trials than did parents of old chicks, supporting the conclusion that the parents protected young chicks not by engaging intruders directly but by remaining close to chicks and using vocalization and display to keep intruders at a distance. While these findings lent clear support to the vulnerability hypothesis, the value hypothesis too was supported, as males with two‐chick broods were almost three times more likely to yodel than males with singleton chicks. Age of parents was not associated with any aspect of chick defense, but the paucity of known‐aged parents in the oldest age classes makes future investigation of age effects warranted.     

Intraspecific nest parasitism in the Spotless Starling Sturnus unicolor

Intraspecific nest parasitism in two colonies of Spotless Starling Sturnus unicolor breeding in nestboxes was studied in central Spain from 1991 to 1994. Nests were monitored regularly and three criteria were used to detect nest parasitism: the appearance of more than one egg per day during the laying period of the host; the appearance of an egg after the start of incubation; eggs with unusual shape or pigmentation. The proportion of parasitized nests in first clutches (37%) was twice that of intermediate (19%) or second (20%) clutches in colony B, whereas parasitism occurred in first (35%) and intermediate (12%) but not in second clutches in colony A. Most clutches (52–70%) were parasitized during the host's laying period and received one parasitic egg. In 10% of the parasitized clutches in colony B, one of the host's eggs disappeared on the day the parasitic egg was added, suggesting that the parasitic female removed this egg. Although parasitism increased clutch size significantly, it led to a decrease in host breeding success, mainly through the removal of eggs and the loss of host nestlings and the survival of parasitic chicks. Observations suggested that parasitic females were young individuals without their own nests and/or those whose breeding attempt had been disrupted while laying in their own nest.     

Competition with a host nestling for parental provisioning imposes recoverable costs on parasitic cuckoo chick's growth

Chicks of the brood parasitic common cuckoo (Cuculus canorus) typically monopolize host parental care by evicting all eggs and nestmates from the nest. To assess the benefits of parasitic eviction behaviour throughout the full nestling period, we generated mixed broods of one cuckoo and one great reed warbler (Acrocephalus arundinaceus) to study how hosts divide care between own and parasitic young. We also recorded parental provisioning behaviour at nests of singleton host nestlings or singleton cuckoo chicks. Host parents fed the three types of broods with similar-sized food items. The mass of the cuckoo chicks was significantly reduced in mixed broods relative to singleton cuckoos. Yet, after the host chick fledged from mixed broods, at about 10-12 days, cuckoo chicks in mixed broods grew faster and appeared to have compensated for the growth costs of prior cohabitation by fledging at similar weights and ages compared to singleton cuckoo chicks. These results are contrary to suggestions that chick competition in mixed broods of cuckoos and hosts causes an irrecoverable cost for the developing brood parasite. Flexibility in cuckoos' growth dynamics may provide a general benefit to ecological uncertainty regarding the realized successes, failures, and costs of nestmate eviction strategies of brood parasites.     

Development of fearfulness in birds: genetic factors modulate non-genetic maternal influences

The development of fearfulness and the capacity of animals to cope with stressful events are particularly sensitive to early experience with mothers in a wide range of species. However, intrinsic characteristics of young animals can modulate maternal influence. This study evaluated the effect of intrinsic fearfulness on non-genetic maternal influence. Quail chicks, divergently selected for either higher (LTI) or lower fearfulness (STI) and from a control line (C), were cross-fostered by LTI or STI mothers. Behavioural tests estimated the chicks' emotional profiles after separation from the mother. Whatever their genotype, the fearfulness of chicks adopted by LTI mothers was higher than that of chicks adopted by STI mothers. However, genetic background affected the strength of maternal effects: the least emotional chicks (STI) were the least affected by early experience with mothers. We demonstrated that young animal's intrinsic fearfulness affects strongly their sensitivity to non-genetic maternal influences. A young animal's behavioural characteristics play a fundamental role in its own behavioural development processes.     

The optimal strategy for brood-parasitism: how many eggs should be laid in the host's nest?

We consider the optimal strategy for intra-specific brood-parasitism, especially with respect to the number of eggs laid by the parasitic individual in the nest of non-parasitic individual, in particular, a host that does not reject the parasite's eggs. With a fundamental mathematical model, assuming that the survival probability of the parasite's offspring in the nest of the host is significantly smaller than that in parasite's own nest, we determine the optimal number of eggs laid in the nest of host that maximizes the expected reproductive fitness of the parasite. We show that the invasion success of brood-parasitism could significantly depend on the total number of eggs laid by the parasite in a breeding season, and that the successfully invading brood-parasitism could realize maximum fitness with a specific number of parasite's eggs laid in the nest of the host.     

The adaptiveness of defence strategies against cuckoo parasitism

Host bird species of the Eurasian Cuckoo, Cuculus canorus, often display egg-discrimination behaviour but chick-rejection behaviour has never been reported. In this paper, we analyse a host-cuckoo association in which both population dynamics and evolutionary dynamics are explored in a discrete-time model. We introduce four host types, each with their own defence behaviour, displaying either egg or chick rejection, neither or both, We also introduce fitness functions for each of these host types. Although we can characterize the long term behaviour in many cases by a simple heuristic argument which is in accordance with common views in ecology, there are a number of other phenomena that are not explained within this framework: we describe stable oscillatory behaviour and coexistence of two defensive host types. We analyse the scenarios in which chick rejection may establish itself and give a first explanation as to why this defence trait has never been recorded in nature. We find that chick rejectors generally are at an intrinsic disadvantage with respect to a host type that rejects eggs. Hosts benefit more from rejecting cuckoo eggs than cuckoo chicks, and our model suggests that this is chiefly responsible for the absence of chick rejection. Moreover, even though it seems that chick rejection must be useful as an extra defence, it is shown that hosts with both defence strategies are less likely to establish themselves in competition with egg-rejectors than hosts which reject chicks only. These results provide insight in the extent to which adaptations may be perfected by natural selection.     

Estimating survival and adoption rates of dependent juveniles

Population growth and fitness are typically most sensitive to adult survival in long‐lived species, but variation in recruitment often explains most of the variation in fitness, as past selection has canalized adult survival. Estimating juvenile survival until age of independence has proven challenging, because marking individuals in this age class may directly affect survival. For Greater Sage‐grouse, uniquely marking juveniles in the first days of life likely results in adverse effects to survival, detection of juveniles is not perfect, and females adopt juveniles from other parents. These challenges are encountered by researchers studying avian and mammalian species with similar life histories, yet methods do not exist that explicitly estimate all these components of the recruitment process. We propose a novel data collection method and demographic model to simultaneously estimate rates of detection, survival, and adoption of juvenile individuals. Using multiple cameras to film the beginning of juvenile activity on specific days, we obtained counts of juveniles associated with marked females. Increases of juveniles to broods provided information that enabled us to estimate rates of adoption that can be applied at the population level. Losses from broods informed apparent survival. These losses could be attributed to death, or they could be chicks that were adopted by other females. We found evidence that apparent survival of juveniles was influenced by localized weather patterns when chicks were young. Similarly, we found that young chicks were more susceptible to the adverse effect of attending females being flushed by an observer. Both of these patterns diminished quickly as chicks aged. We provide the first‐ever estimates of interval‐specific adoption rates. Our results suggest that researchers should be cautious when designing studies to estimate juvenile survival. More importantly, they provide insight into adoption, a behavior that has been known to exist for decades.