Don'T put all your eggs in one nest: spread them and cut time at risk

Abstract In many egg-laying animals, some females spread their clutch among several nests. The fitness effects of this reproductive tactic are obscure. Using mathematical modeling and field observations, we analyze an unexplored benefit of egg spreading in brood parasitic and other breeding systems: reduced time at risk for offspring. If a clutch takes many days to lay until incubation and embryo development starts after the last egg, by spreading her eggs a parasitic female can reduce offspring time in the vulnerable nest at risk of predation or other destruction. The model suggests that she can achieve much of this benefit by spreading her eggs among a few nests, even if her total clutch is large. Field data from goldeneye ducks Bucephala clangula show that egg spreading enables a fecund female to lay a clutch that is much larger than average without increasing offspring time at risk in a nest. This advantage increases with female condition (fecundity) and can markedly raise female reproductive success. These results help explain the puzzle of nesting parasites in some precocial birds, which lay eggs in the nests of other females before laying eggs in their own nest. Risk reduction by egg spreading may also play a role in the evolution of other breeding systems and taxa-for instance, polyandry with male parental care in some birds and fishes.     

Public information and conspecific nest parasitism in goldeneyes: targeting safe nests by parasites

Conspecific nest parasitism (CNP) is a widespread alternativereproductive tactic in birds. Several hypotheses have been putforward to explain the evolution and occurrence of CNP, butno generally applicable hypothesis exists. Recent experimentalresults from the common goldeneye (Bucephala clangula), a cavity-nestingduck, have revealed that parasitic females preferentially layeggs in safe nest-sites, implying that nest predation risk isan important ecological determinant of CNP. The present studyfocuses on the mechanisms by which parasites identify safe nest-sites.Predation risk of a given nest-site was predictable betweensuccessive breeding seasons. At the end of the nesting season,females prospected active nest-sites more frequently than nest-sitesthat did not have a nest in the current season. Nest-sites thathad been prospected more frequently by females in year t hada higher probability to be parasitized in year t + 1. The resultssuggest that the use of public information, derived throughnest-site prospecting, enabled parasites to target safe nests.These findings provide a new and potentially generally applicableperspective to understand the evolution and occurrence of CNP.     

Colony kin structure and host‐parasite relatedness in the barnacle goose

Conspecific brood parasitism (CBP), females laying eggs in the nest of other ‘host’ females of the same species, is a common alternative reproductive tactic among birds. For hosts there are likely costs of incubating and rearing foreign offspring, but costs may be low in species with precocial chicks such as waterfowl, among which CBP is common. Waterfowl show strong female natal philopatry, and spatial relatedness among females may influence the evolution of CBP. Here we investigate fine‐scale kin structure in a Baltic colony of barnacle geese, Branta leucopsis, estimating female spatial relatedness using protein fingerprints of egg albumen, and testing the performance of this estimator in known mother‐daughter pairs. Relatedness was significantly higher between neighbour females (nesting ≤ 40 metres from each other) than between females nesting farther apart, but there was no further distance trend in relatedness. This pattern may be explained by earlier observations of females nesting close to their mother or brood sisters, even when far from the birth nest. Hosts and parasites were on average not more closely related than neighbour females. In 25 of 35 sampled parasitized nests, parasitic eggs were laid after the host female finished laying, too late to develop and hatch. Timely parasites, laying eggs in the host’s laying sequence, had similar relatedness to hosts as that between neighbours. Females laying late parasitic eggs tended to be less related to the host, but not significantly so. Our results suggest that CBP in barnacle geese might represent different tactical life‐history responses.     

Brood parasitism,female condition and clutch reduction in the common eider Somateria mollisima

Conspecific brood parasitism (CBP) is an alternative reproductive tactic found in many animals with parental care. Parasitizing females lay eggs in the nests of other females (hosts) of the same species, which incubate and raise both their own and the foreign offspring. The causes and consequences of CBP are debated. Using albumen fingerprinting of eggs for accurately detecting parasitism, we here analyse its relation to female condition and clutch size in High Arctic common eiders Somateria mollissima borealis. Among 166 clutches in a Svalbard colony, 31 (19%) contained eggs from more than one female, and 40 of 670 eggs (6%) were parasitic. In 6 cases an active nest with egg(s) was taken over by another female. Many suitable nest sites were unoccupied, indicating that CBP and nest takeover are reproductive tactics, not only consequences of nest site shortage. Similarity in body mass between female categories suggests that condition does not determine whether a nesting female becomes parasitised. There was no evidence of low condition in parasites: egg size was similar in hosts and parasites, and parasitism was equally frequent early and late in the laying season. Meta‐analysis of this and 3 other eider studies shows that there is a cost of being parasitised in this precocial species: host females laid on average 7% fewer eggs than other females.     

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.     

Conspecific nest parasitism is associated with inequality in nest predation risk in the common goldeneye (Bucephala clangula)

Previous studies of the role of nest predation in conspecificnest parasitism have not taken into account the possibilitythat predation risk may not be randomly distributed among nestsites and that breeding individuals may use different cues toassess the risk and adjust their reproductive tactic betweenyears accordingly. Especially in cavity-nesting species, therole of nest predation in conspecific nest parasitism has beendownplayed, while the role of nest site limitation has beenhighlighted. Using both observational and experimental data,I show that in the common goldeneye (Bucephala clangula), acavity-nesting species in which conspecific nest parasitism iscommon, predation risk varies considerably between nest sitesand does not follow a random expectation. The inequality inpredation risk between nest sites also showed up in the occurrenceof parasitized nests in an experimental setup. Nests parasitizedin year t were more frequent in those nest sites that were notdepredated during the previous nesting attempt in year t - nthan in nest sites that were depredated and in control nestsites that had not been used for nesting before. A nest siteaddition experiment revealed that conspecific nest parasitismwas not associated with nest site limitation. My findings givesupport for the hypothesis that nest predation is an importantecological factor explaining conspecific nest parasitism ingoldeneyes.     

Conspecific brood parasitism and population dynamics

Conspecific brood parasitism (CBP), defined as parasitic laying of eggs in a conspecific nest without providing parental care, occurs in insects, fishes, amphibians, and many birds. Numerous factors have been proposed to influence the evolution of CBP, including nest site limitation; effects of brood size, laying order, or parasitic status on offspring survival; randomness of parasitic egg distribution; adult life-history trade-offs; and variation in parental female quality or risk of nest predation. However, few theoretical studies consider multiple possible types of parasitism or the interplay between evolution of parasitism and population dynamics. We review existing theory of CBP and develop a synthetic modeling approach to ask how best-of-a-bad job parasitism, separate-strategies parasitism (in which females either nest or parasitize), and joint-strategies parasitism (in which females can both nest and parasitize) differ in their evolutionary conditions and impacts on population dynamics using an adaptive dynamics framework including multivariate traits. CBP can either stabilize or destabilize population dynamics in different scenarios, and the role of comparable parameters on evolutionarily stable strategy parasitism rate, equilibrium population size, and population stability can differ for the different modes of parasitism.     

Do parasitic common goldeneye Bucephala clangula females choose nests on the basis of host traits or nest site traits?

Conspecific brood parasitism (CBP) is an important alternative breeding strategy for gaining reproductive output in birds. While interactions between hosts and parasites and consequences of CBP to breeding success of both parties have been studied a lot, the roles of host characteristics and nest site characteristics in CBP have received less attention. We studied the relative importance of host‐related traits, such as female condition and breeding experience, and nest‐site‐related factors, such as overall nest site preference and occupation rate, in explaining the occurrence of CBP in a common goldeneye Bucephala clangula population. We used spatially and temporally extensive data sets, analysed the data with generalized linear mixed models that allowed us to account for the non‐independency of individual nesting attempts across females and nesting sites, and used an information theoretic approach in model selection and inference. About half of the nests were parasitized annually during the seven year study period. The occurrence of CBP decreased with advancement of the breeding season but late nests were also frequently parasitized. We found that the occurrence of CBP was better explained by nest‐site characteristics than host traits, implying that parasitic females target a given nest based on factors related to the nest site itself rather than on the host. Our results suggest that more attention should be paid to factors associated with nest site attractiveness and quality when studying laying decisions of parasites and the occurrence of CBP in general.     

Testing hypotheses about the function of repeated nest abandonment as a life history strategy in a passerine bird

Nest structures are essential for successful reproduction in most bird species. Nest construction costs time and energy, and most bird species typically build one nest per breeding attempt. Some species, however, build more than one nest, and the reason for this behaviour is often unclear. In the Grey Fantail Rhipidura albiscapa, nest abandonment before egg‐laying is very common. Fantails will build up to seven nests within a breeding season, and pairs abandon up to 71% of their nests before egg‐laying. We describe multiple nest‐building behaviour in the Grey Fantail and test four hypotheses explaining nest abandonment in this species: cryptic depredation, destruction of nests during storm events, and two anti‐predatory responses (construction of decoy nests to confuse predators, and increasing concealment to ‘hide’ nests more effectively). We found support for only one hypothesis – that abandonment is related to nest concealment. Abandoned nests were significantly less concealed than nests that received eggs. Most abandoned nests were not completely built and none received eggs, thus ruling out cryptic predation. Nests were not more likely to be abandoned following storm events. The decoy nest hypothesis was refuted as abandoned nests were constructed at any point during the breeding season and some nests were dismantled and the material used to build the subsequent nest. Thus, Grey Fantails are flexible about nest‐site locations during the nest‐building phase and readily abandon nest locations if they are found to have deficient security.     

Experimental support for the role of nest predation in the evolution of brood parasitism

In 1965, Hamilton and Orians (HO) hypothesized that the starting point for the evolution of obligate interspecific brood parasitism in birds was the facultative laying of physiologically committed eggs in neighbouring active nests of con‐ and heterospecifics, following predation of a bird’s own nest during the laying stage. We tested this prediction of the HO hypothesis by using captive pairs of zebra finches (Taeniopygia guttata), a species with evidence for intraspecific parasitism both in the wild and in captivity. As predicted, in response to experimental nest removal, subjects laid eggs parasitically in simulated active conspecific nests above chance levels. Across subsequent trials, we detected both repeatability and directional change in laying patterns, with some subjects switching from parasitism to depositing eggs in the empty nest. Taken together, these results support the assumptions and predictions of the HO hypothesis, and indicate that the zebra finch is a potential model species for future behavioural and genetic studies in captive brood parasite research.     

Molecular identification of brood‐parasitic females reveals an opportunistic reproductive tactic in ruddy ducks

In many taxa, females lay eggs in the nests of other conspecifics. To determine the conditions under which conspecific brood parasitism develops, it is necessary to identify parasitic offspring and the females who produce them; however, for most systems parasitism can be difficult to observe and most genetic approaches have relatively low resolving power. In this study, we used protein fingerprinting from egg albumen and 10 microsatellite loci to genetically match parasitic ducklings to their mothers in a population of ruddy ducks (Oxyura jamaicensis). We found that 67% of nests contained parasitic offspring, and we successfully identified their mothers in 61% of the cases. Of the parasitic females identified, 77% also had nests of their own (i.e. a dual tactic, where females both nest and lay parasitically), and we found no evidence that parasitic females pursued a specialist (parasitism only) tactic. We also found that parasitic egg laying was not influenced by nest loss, predation or female condition. Thus, in contrast to most waterfowl studied to date, female ruddy ducks appear to lay parasitic eggs whenever the opportunity arises.     

Great Spotted Cuckoos Frequently Lay Their Eggs While Their Magpie Host is Incubating

Species that suffer from brood parasitism face a considerable reduction in their fitness which selects for the evolution of host defences. To prevent parasitism, hosts can mob or attack brood parasites when they approach the host nest and block the access to the nest by sitting on the clutch. In turn, as a counter‐adaptation, brood parasites evolved secretive behaviours near their host nests. Here, we have studied great spotted cuckoo (Clamator glandarius) egg‐laying behaviour and defence by their magpie (Pica pica) hosts inside the nest using continuous video recordings. We have found several surprising results that contradict some general assumptions. The most important is that most (71%) of the parasitic events by cuckoo females are completed while the magpie females are incubating. By staying in the nest, magpies force cuckoo females to lay their egg facing the high risk of being attacked by the incubating magpie (attack occurred in all but one of the events, n = 15). During these attacks, magpies pecked the cuckoo violently, but could never effectively avoid parasitism. These novel observations expand the sequence of adaptations and counter‐adaptations in the arms race between brood parasites and their hosts during the pre‐laying and laying periods.     

Rapid laying by Brown-headed Cowbirds Molothrus ater and other parasitic birds

We compared the length of time parasitic and nonparasitic female birds spent on nests while laying eggs (laying bouts) to evaluate the hypothesis that rapid laving by parasitic Brown-headed Cowbirds Molothrus ater and other parasitic birds is a specialization for brood parasitism. Brown-headed Cowbirds typically spent less than 1 min on host nests while laying (41.0 ± 4.58 [mean ± s.e.] s, n = 21). In contrast, mean laving bouts of six nonparasitic icterine species ranged from 21.5 min to 53.4 min, and laying bouts of 13 other passerine species ranged from 20.7 min to 103.7 min. By spending only a few seconds on the nest while laying, brood parasites probably increase their chances of parasitizing nests unnoticed by hosts or, if noticed, are harassed by hosts for less time. Rapid laying may be adaptive if aggression by hosts can thwart attempted parasitism by chasing away the parasite, preventing the parasite from entering the nest or injuring the parasite. Rapid laying may increase the likelihood that the parasitic egg will be accepted. We tested some of these hypotheses by recording the responses of three frequently parasitized species to a stuffed female cowbird placed on their nests for 1 min. All species attacked the model vigorously; however, the mean time for discovery of the model ranged from 3 min to 17 min, ample time for female cowbirds to parasitize the nests. We concluded that rapid laying by parasitic birds is an adaptation for parasitism and, in Brown-headed Cowbirds, reduces the chances that the parasite will be attacked by hosts.     

Relationship Between Nest Predation Suffered by Hosts and Brown-Headed Cowbird Parasitism: A Comparative Study

There are at least four main hypotheses that may explain how the evolution of host selection by avian brood parasites could be linked to nest predation among their potential hosts. First, selection may have favoured parasite phenotypes discriminating among hosts on the basis of expected nest failure. Second, parasitized nests may be more easily detected by predators and extra costs of parasitism may accelerate the evolution of host defences. Third, selection may have favoured predator phenotypes avoiding parasitized nests because parasitism enhances nest defence. Fourth, female brood parasites may directly or indirectly induce host nesting failures in order to enhance future laying opportunities. We collected data on brood parasitism and nest failure due to predation to test these hypotheses in a comparative approach using North American passerines and their brood parasite, the brown-headed cowbird Molothrus ater. Under the hypotheses 1 or 3 we predicted brood parasitism to be negatively associated with nest predation across species, whereas this relation is expected to be positive if hypotheses 2 or 4 are true. We demonstrate that independent of host suitability, nest location, habitat type, length of the nestling period, body mass and similarity among species due to common ancestry, species experiencing relatively high levels of nest predation suffered lower levels of cowbird parasitism. Our results suggest a previously ignored role for nest predation suffered by hosts on the dynamics of the coevolutionary relationships between hosts and avian brood parasites. Co-ordinating editor: Dr. F. Stuefer     

Small hosts infrequently disrupt laying by Brown-headed Cowbirds and Bronzed Cowbirds

ABSTRACT Brood parasites often must overcome host defenses that may include behaviors that serve other functions, such as deterrence of predators and nest attendance during laying and incubation. Host use by brood parasites may also be influenced by competitors in areas where more than one parasitic species occurs. We identified the degree to which behavior of potential hosts and potential competitors affected laying by Brown‐headed Cowbirds (Molothrus ater) and Bronzed Cowbirds (M. aeneus) at a site in south Texas where they co‐occur. We watched potential host nests during the presunrise period to record cowbird laying and document nest visitation, laying, cowbird‐host encounters, and nest attentiveness by hosts. Hosts were frequently at their nests when cowbirds laid eggs (83% of 121 watches among nests of five host species) and cowbirds regularly encountered hosts (43–74% and 40–77% of watches per species of host for Brown‐headed and Bronzed cowbirds, respectively). Host nest defense infrequently interfered with cowbird laying and cowbirds rarely interacted with one another during laying. Overall, 12% of the 42 cowbird laying attempts that elicited host nest defense failed, resulting in cowbird eggs either laid atop hosts as they sat in nests or laid outside the nest cup. We clearly documented that relatively small hosts can thwart parasitism by cowbirds. Thus, the potential for successful defense of nests should be considered when assessing the evolution of behaviors to deter the removal of host eggs by cowbirds and mechanisms leading to nest abandonment. Regarding the latter, the presence of a cowbird at a nest would be a poor indicator for parasitism as some laying attempts were thwarted and unparasitized broods were reared at those nests. Despite the potential for nest defense to affect host use by cowbirds, we did not detect an effect of nest defense. Because most host defense was ineffective, we examined hypotheses for the timing of cowbird laying and host nest attendance. Our analysis of time of day of laying by Brown‐headed Cowbirds at our site and data compiled from the literature suggests that laying time is best predicted by the time of civil twilight (first light) rather than sunrise.     

Function of egg punctures by Shiny Cowbirds in parasitized and nonparasitized Creamy‐bellied Thrush nests

ABSTRACT Avian brood parasites usually remove or puncture host eggs. Several hypotheses have been proposed to explain the function of these behaviors. Removing or puncturing host eggs may enhance the efficiency of incubation of cowbird eggs (incubation‐efficiency hypothesis) or reduce competition for food between cowbird and host chicks in parasitized nests (competition‐reduction hypothesis) and, in nonparasitized nests, may force hosts to renest and provide cowbirds with new opportunities for parasitism when nests are too advanced to be parasitized (nest‐predation hypothesis). Puncturing eggs may also allow cowbirds to assess the development of host eggs and use this information to decide whether to parasitize a nest (test‐incubation hypothesis). From 1999 to 2002, we tested these hypotheses using a population of Creamy‐bellied Thrushes (Turdus amaurochalinus) in Argentina that was heavily parasitized by Shiny Cowbirds (Molothrus bonariensis). We found that 56 of 94 Creamy‐bellied Thrush nests (60%) found during nest building or egg laying were parasitized by Shiny Cowbirds, and the mean number of cowbird eggs per parasitized nest was 1.6 ± 0.1 (N= 54 nests). At least one thrush egg was punctured in 71% (40/56) of parasitized nests, and 42% (16/38) of nonparasitized nests. We found that cowbird hatching success did not differ among nests where zero, one, or two thrush eggs were punctured and that the proportion of egg punctures associated with parasitism decreased as incubation progressed. Thus, our results do not support the incubation‐efficiency, nest‐predation, or test‐incubation hypotheses. However, the survival of cowbird chicks in our study was negatively associated with the number of thrush chicks. Thus, our results support the competition‐reduction hypothesis, with Shiny Cowbirds reducing competition between their young and host chicks by puncturing host eggs in parasitized nests.     

Increased nest defence of upland‐nesting ducks in response to experimentally reduced risk of nest predation

Parent birds should take greater risks defending nests that have a higher probability of success. Given high rates of mammalian nest predation, therefore, parents should risk more for nests in areas with a lower risk of mammalian predation. We tested this hypothesis using nest defence data from over 1300 nests of six species of dabbling ducks studied in an area where predation risk had been reduced through removal of mammalian predators. When predator removal reduced nest predation, the ducks increased risk taking as predicted. Also as predicted, risk taking varied inversely with body size, an index of annual survival, among species. For ducks to vary nest defence in response to variation in predation risk they must be able to assess the risk of nest predation. Because ducks modified nest defence in the breeding season immediately following predator removal, ducks may be able to assess predator abundance indirectly (e.g. by UV reflection from urine) rather than by seeing or interacting directly with the predators.     

Relative reproductive success of female moorhens using conditional strategies of brood parasitism and parental care

In a population of moorhens (Gallinula chloropus), at least27% of netting females laid one or more eggs in a neighbor'snest Females laid parasitically under three conditions: 56%of parasitic eggs were from nesting females that preceded layinga dutch in their own nest by a parasitic laying bout, 19% werefrom females whose nests were depredated before clutch completionand that laid the following egg parasiticaDy, and 25% were froma small number of females without territories, "non-nesting"parasites, that each laid a series of parasitic eggs. Clutchsizes varied greatly between females, but nesting females eachlaid a consistent clutch size both within and between seasonsfor a given mate and territory. Nesting females that employeda dual strategy of brood parasitism and parental care producedextra eggs that they laid in the nests of neighbors before layinga dutch in their own nests. Two out of ten females whose dutchesI experimentally removed during the laying period were successfullyinduced to lay their next egg in the nest of a neighbor. Nestingfemales that laid parasitically selected their hosts opportunisticallyfrom among the nests dosest to their territories. An experimentin which parasitic eggs were removed and hosts left to rearonly their own young showed that parasites did not choose hoststhat were better parents than pairs with contemporary neststhat were not parasitized. Females that only laid parasiticaDywithin a given season timed their parasitic laying bouts poorlyand achieved no reproductive success. Parasitic young rarelyfledged, and the mean seasonal reproductive success of nestingbrood parasites did not differ from that of nonparasitic females.However, the variance in reproductive success of nesting broodparasites was significantly higher than that of nonparasiticfemales.     

Experimental enlargement of nest size does not increase risk of predation or brood parasitism in the Great Reed Warbler Acrocephalus arundinaceus

We assessed whether nest size affects the probability of nest loss using dyads of large and small (large being twice the size of small) inactive Great Reed Warbler Acrocephalus arundinaceus nests placed at similar sites in Great Reed Warbler territories. Large nests were not predated significantly more frequently than small nests. Experimentally enlarged active Great Reed Warbler nests suffered non‐significantly higher predation compared with non‐manipulated control nests. Our experiments did not support the nest‐size hypothesis and suggested that nest size does not appear to be a factor affecting the risk of nest predation in this species. The probability of brood parasitism by the Common Cuckoo Cuculus canorus was also unaffected by experimental nest enlargement, supporting the commonly accepted hypothesis that the Common Cuckoo searches for suitable host nests by host activity during nest building rather than nest size.     

Brood parasitism is associated with increased bacterial contamination of host eggs: bacterial loads of host and parasitic eggs

Factors related to bacterial environment of nests are of primary interest for understanding the causes of embryo infection and the evolution of antimicrobial defensive traits in birds. Nest visitors such as parasites could act as vectors for bacteria and/or affect the hygienic conditions of nests and hence influence the nest bacterial environment. In the present study, we explored some predictions of this hypothetical scenario in the great spotted cuckoo (Clamator glandarius)–magpie (Pica pica) system of brood parasitism. Great spotted cuckoos visit the nests of their magpie hosts and frequently damage some of the host eggs when laying eggs or on subsequent visits. Therefore, it represents a good system for testing the effect of nest visitors on the bacterial environment of nests. In accordance with this hypothesis, we found that the bacterial load of magpie eggshells was greater in parasitized nests, which may suggest that brood parasitism increases the probability of bacterial infection of magpie eggs. Moreover, comparisons of bacterial loads of cuckoo and magpie eggs revealed that: (1) cuckoo eggshells harboured lower bacterial densities than those of their magpie hosts in the same nests and (2) the prevalence of bacteria inside unhatched eggs was higher for magpies than for great spotted cuckoos. These interspecific differences were predicted because brood parasitic eggs (but not host eggs) always experience the bacterial environments of parasitized nests. Therefore, the results obtained in the present study suggest that parasitic eggs are better adapted to environments with a high risk of bacterial contamination than those of their magpie hosts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 836–848.