Parental care of a cowbird host: caught between the costs of egg-removal and nest predation

Avian brood parasites reduce host fitness through the addition of parasitic eggs and the removal of host eggs. Both parasitic egg-addition and host egg-removal may be important sources of selection on host behaviour, creating fitness trade-offs with selection imposed by nest predation. However, the relative costs hosts suffer from egg-addition and host egg-removal and the responses to these costs are largely unstudied. Through experimental manipulations and observations, we demonstrate that increased nest attentiveness by female yellow warblers (Dendroica petechia) reduces the cost of brood parasitism by reducing egg-removal by brown-headed cowbirds (Molothrus ater). However, female attentiveness does not reduce the addition of parasitic eggs. Experimentally parasitized females respond to the threat of egg-removal by increasing nest attentiveness. Increased attentiveness, however, reduces time for females to gather food and requires males to visit the nest more often to feed incubating females. This increased activity in turn increases the risk of nest predation. Thus, brood parasitism (specifically egg-removal) and nest predation produce conflicting selection on incubation strategies, as parasitized hosts are caught between the costs of egg-removal by brood parasites, and the costs of increased nest predation if the female spends more time on the nest to reduce egg-removal.     

Avoidance,tolerance, and resistance to ectoparasites in nestling and adult tree swallows

We examined avoidance, tolerance, and resistance strategies of nestling and adult tree swallows Tachycineta bicolor in response to ectoparasitic blowflies Protocalliphora sialia. Tree swallows avoided settling in north‐facing nest boxes early in the breeding season. These boxes were more likely to be parasitized later in the season, suggesting that box selection may facilitate blowfly avoidance. After experimentally manipulating blowfly intensity, we found that nestlings were generally tolerant of parasitism. Parasites significantly reduced nestling blood hemoglobin but had no effect on nestling body mass, primary feather growth, age at fledging, or fledging success. Parents of parasitized nestlings did not increase their food provisioning rate to promote nestling tolerance. Adult female tree swallows demonstrated both tolerance and resistance: blowfly parasitism had no effect on adult hemoglobin and body mass, and those with higher P. sialia‐binding antibody levels had fewer blowfly larvae in their nests. Nestling antibodies were unrelated to blowfly intensity. Despite considerable variation among years, our results suggest that the costs of blowfly parasitism to nestling and adult tree swallows are modest, and limited to blood loss in nestlings. Future work should examine the effects of reduced blood hemoglobin on fledgling survival and the importance of parasite‐specific antibodies.     

Intraspecific nest parasitism in the European starling Sturnus vulgaris

Biochemical genetic markers were used along with conventional methods (abnormal laying sequence/clutch size, unusual egg shape/pigmentation) to identify intraspecific nest parasitism at two British nestbox colonies of the European starling. Between 11 and 37% of first clutches were parasitized during 1977–1979. Parasitic females probably comprised all of the following categories: (1) paired females contesting a nestbox occupied by another pair; (2) previously paired females who had laid a clutch but had been unsuccessful; (3) unpaired females who had copulated with males that already had a mate and nest site; and (4) ‘professional’ nest parasites who distributed at lest some of their eggs in one or more nests other than their own. Although parasitized nests had higher clutch sizes, parasitism led to fewer host young fledging per egg laid, mainly through the eviction of eggs and subsequent nest desertion. Number of parasitic young fledged per egg laid was highest when eggs were laid synchronously with the host, when host clutches were larger, or a smaller number of parasite eggs were added to a nest, thus favouring parasites that distribute their eggs amongst a number of nests. A greater pressure on nest sites may have accounted for the higher levels of parasitism at the Aberdeen colony and for the greater number of parasite eggs laid in a nest. Although most parasitic female starlings appeared to be much less successful than non-parasitic ones, nest parasitism in the starling might evolve directly when one or more of the following advantages are present. (1) There are no constraints on the number of eggs a female may lay but there are constraints on the number of young she may feed adequately. (2) Female survival is increased by having fewer or no eggs/young to care for. (3) Current feeding conditions favour the survival of more young than would be produced by the most common clutch size. Intraspecific nest parasitism is considered to be a first stage in the evolution of interspecific nest parasitism.     

Silk threads function as an 'adhesive cleaner' for nest space in a social spider mite

Individuals of the social spider mite Stigmaeopsis longus live communally in narrow, humid nests made from silk threads and display nest sanitation behaviour through the coordinated deposition of faeces. We used artificial dust to experimentally determine that females of this species use silk threads to perform regular cleaning of the nest space and eggs. We first learned that silk-weaving behaviour is not a by-product of nest building (nest reinforcement); rather, it is actively performed as a function of cleaning the living space and eggs. Furthermore, we determined the effectiveness of the attending females by artificially manipulating their natural habitat, which is clearly connected to the cleaning behaviour by parental females. As such, we have uncovered an extraordinary new role of silk threads as devices for cleaning the nest space and/or eggs. These results strongly indicate that special adaptations for maintaining clean habitats are essential for animals to evolve aggregative social lives.     

Behaviour of African turdid hosts towards experimental parasitism with artificial red-chested cuckoo Cuculus solitarius eggs

The red-chested cuckoo Cuculus solitarius parasitises many passerines in Africa, but some common species sympatric with this brood parasite are rarely used as hosts. We tested the responses of three turdid hosts to parasitism with artificial cuckoo eggs. The kurrichane thrush Turdus libonyana , which is not regularly parasitized by the cuckoo, rejected 60% of mimetic model eggs and 81% of non-mimetic eggs. We observed female thrush behaviour during the first visit after parasitism, and thrushes appeared to be initially fooled by mimetic eggs in completed clutches in all cases, and incubated. By contrast, in half of the experiments with non-mimetic eggs, these were ejected by the thrushes, with the host grasping the egg and flying away with it. The time spent nest checking prior to ejection was only one third of the time spent nest checking when females decided to incubate the clutch, suggesting that females were immediately aware of a foreign egg in the nest. By contrast, southern olive thrushes T. olivaceous rejected all non-mimetic and accepted all mimetic model eggs, whereas cape robins Cossypha caffra accepted all model eggs, irrespective of whether or not they were mimetic. Our results support the hypothesis that rejection behaviour in these two thrush species evolved as a defence against interspecific nest parasitism, with thrushes appearing to be ahead in this particular host-parasite arms race. The cape robin, by contrast, appears not to reject cuckoo eggs, either because it is to unable to recognize them, or because the costs associated with removal may be too high.     

Nest Sanitation as the Evolutionary Background for Egg Ejection Behaviour and the Role of Motivation for Object Removal

Higher interclutch colour variation can evolve under the pressure of brood parasitism to increase the detection of parasitic eggs. Nest sanitation could be a prerequisite for the evolution of anti-parasite defence in terms of egg ejection. In this respect, we used nest sanitation behaviour as a tool to identify: i) motivation and its underlying function and, ii) which features provoke ejection behaviour. Therefore, we experimentally tested whether size, colour or shape may influence ejection behaviour using artificial flat objects. We found a high interclutch variation in egg colouration and egg size in our tree sparrow (Passer montanus) population. Using colour and size we were in fact able to predict clutch affiliation for each egg. Our experiments further revealed the existence of direct anti-parasite behaviours and birds are able to recognise conspecific eggs, since only experimentally-deposited eggs have been removed. Moreover, experiments with different objects revealed that the motivation of tree sparrows to remove experimental objects from their nests was highest during egg laying for objects of varying size, most likely because of parasitism risk at this breeding stage. In contrary, motivation to remove white objects and objects with edges was higher during incubation stage as behavioural patterns connected to hatching started to emerge. The fact that rejection rate of our flat objects was higher than real egg ejection, suggests that egg ejection in tree sparrows and probably more general in small passerines, to be limited by elevated costs to eject eggs with their beaks. The presence of anti-parasite behaviour supports our suggestion that brood parasitism causes variation in egg features, as we have found that tree sparrows can recognise and reject conspecific eggs in their clutch. In conclusion, in tree sparrows it seems that nest sanitation plays a key role in the evolution of the removal of parasitic eggs.     

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.     

Egg morphology fails to identify nests parasitized by conspecifics in common pochard: a test based on protein fingerprinting and including female relatedness

Conspecific brood parasites lay eggs in nests of other females of the same species. A variety of methods have been developed and used to detect conspecific brood parasitism (CBP). Traditional methods may be inaccurate in detecting CBP and in revealing its true frequency. On the other hand more accurate molecular methods are expensive and time consuming. Eadie developed a method for revealing CBP based on differences in egg morphology. That method is based on Euclidean distances calculated for pairs of eggs within a clutch using standardized egg measurements (length, width and weight). We tested the applicability of this method in the common pochard Aythya ferina using nests that were identified as parasitized (39 nests) or non‐parasitized (16 nests) based on protein fingerprinting of eggs. We also analyzed whether we can distinguish between parasitic and host eggs in the nest. We found that variation in MED can be explained by parasitism but there was a huge overlap in MED between parasitized and non‐parasitized nests. MED also increased with clutch size. Using discriminant function analysis (DFA) we found that only 76.4% of nests were correctly assigned as parasitized or non‐parasitized and only 68.3% of eggs as parasitic or host eggs. Moreover we found that MED in parasitized nests increased with relatedness of the females that laid eggs in the nest. This finding was supported by positive correlation between MED and estimated relatedness in female–female pairs. Although variation in egg morphology is associated with CBP, it does not provide a reliable clue for distinguishing parasitized nests from non‐parasitized nests in common pochard.     

Factors influencing the risk of common cuckoo Cuculus canorus parasitism on marsh warblers Acrocephalus palustris

Using multiple logistic regression analysis, we investigated the influence of nest site characteristics, laying date and nest size in marsh warblers Acrocephalus palustris on the risk of parasitism by common cuckoos Cuculus canorus . Marsh warblers breed in more diverse and dense herbaceous vegetation than other cuckoo hosts investigated in comparable studies. The "perch proximity" hypothesis was supported as parasitized nests were situated closer to trees than non-parasitized ones. Furthermore, demonstrated for the first time in a cuckoo host, tree height was an important predictor of parasitism, with higher trees increasing the parasitism odds ratio. The "nest exposure" hypothesis was also supported since parasitized nests had a shorter stand of vegetation in the close vicinity than non-parasitized nests. However, visibility of the nest from the nearest potential cuckoo perch (cuckoo view) was not selected by the model, probably because most nests were well concealed. Laying date, height of nest above ground and the distance from the nest to the nearest edge of the vegetation were not important predictors of parasitism. Though smaller nests tended to be parasitized more frequently than larger ones, nest size only approached significance, making its importance unclear.     

Reliability of egg morphology to detect conspecific brood parasitism in goldeneyes Bucephala clangula examined using protein fingerprinting

Eadie (1989) developed a method based on variation between females in egg length, width and weight to detect conspecific brood parasitism in the field: using these three egg measures, Euclidean distance between all pairs of eggs within a clutch is calculated, and if maximum Euclidean distance (MED) between any two eggs exceeds a threshold value the nest is considered parasitized. The MED method has been tested in Finnish and Scottish common goldeneye Bucephala clangula populations but the results have been contradicting. Here we use protein fingerprinting to assess the validity of the MED method. Data comprised 35 clutches of which we knew, based on protein fingerprinting, how many different females laid the clutch (range 1–5 females). The mean MED of non-parasitized clutches (laid by 1 female only) was 1.470 (95% CI: lower 1.169, upper 1.771; n=21) and that of parasitized clutches (laid by 2 or more females) was 3.654 (95% CL: lower 3.083, upper 4.225; n=14). Using a MED>3.0 as a criterion to identify parasitized clutches 89% of all clutches were classified correctly either parasitized or non-parasitized when compared to the identification based on protein fingerprinting. Clutch size and the number of females (beyond 2 females) did not affect the clutch MED, whereas the status of parasitism did. Repeatability of egg length, width and weight were: 0.63, 0.76 and 0.80, respectively, implying that, variation in these egg measures occurs among rather than within females. Our new results confirm that the MED method is reliable enough to detect parasitism in common goldeneye.     

Common Cuckoos Cuculus canorus change their nest‐searching strategy according to the number of available host nests

In recent decades, numerous studies have examined factors affecting risk of host nest parasitism in well‐known avian host–parasite systems; however, little attention has been paid to the role of host nest availability. In accordance with other studies, we found that nest visibility, reed density and timing of breeding predicted brood parasitism of Great Reed Warblers Acrocephalus arundinaceus by the Common Cuckoo Cuculus canorus. More interestingly, hosts had a greater chance of escaping brood parasitism if nesting was synchronized. Cuckoo nest searching was governed primarily by nest visibility at high host‐nest density. However, even well‐concealed nests were likely to be parasitized during periods when just a few hosts were laying eggs, suggesting that Cuckoos adjust their nest‐searching strategy in relation to the availability of host nests. Our results demonstrate that host vulnerability to brood parasitism varies temporally and that Cuckoo females are able to optimize their nest‐searching strategy. Moreover, our study indicated that Cuckoos always manage to find at least some nests to parasitize. Thus, in this case, the co‐evolutionary arms race should take place mainly in the form of parasitic egg rejection rather than via frontline pre‐parasitism defence.     

INTRASPECIFIC NEST PARASITISM IN BIRDS

(1) The incidence of intraspecific nest parasitism in birds is reviewed. This phenomenon can be identified by various methods, ranging from biochemical examination of protein and enzyme polymorphisms to observations on the sequence of appearance of eggs in the nest as well as on the shape and colour of the eggs. The phenomenon has been reported for at least 53 species (Table I), mostly among precocial birds.
(2) The evidence suggests that the parasites are ( a ) young, unmated birds, ( b ) females which have lost their nests and (c) mated females which also lay in the nests of other females. High proportions of such females, and scarcity of suitable nest sites increase the rate of parasitism.
(3) Breeding success in parasitized nests is reduced by factors such as egg loss, desertion, inefficient incubation, reduced clutch size and late layings. The upper limit of the rate of intraspecific parasitism is discussed. It is argued that its incidence will be higher in the tropics than in extreme zones, for example, high latitudes and deserts, because there is higher synchronization of breeding in the latter, and increased predation in the former zones. Also, it will be more common in species which lay large clutches, such as precocial species.     

Impact of mating status on egg-laying and superparasitism behaviour in a parasitoid wasp

Most parasitoid female wasps can distinguish between unparasitized and parasitized hosts and use this information to optimize their progeny and sex allocation. In this study, we explored the impact of mating on oviposition behaviour (parasitism and self‐ and conspecific superparasitism) on both unparasitized and already parasitized hosts in the solitary parasitoid wasp Eupelmus vuilleti (Crw.) (Hymenoptera: Eupelmidae). Virgin and mated females had the same oviposition behaviour and laid eggs preferentially on unparasitized hosts. The sex ratio (as the proportion of females) of eggs laid by mated females in parasitism and conspecific superparasitism was 0.67 ± 0.04 and 0.57 ± 0.09, respectively. Likewise, females laid more eggs in conspecific superparasitism than self‐superparasitism under our experimental conditions. These experiments demonstrate that E. vuilleti females can (i) discriminate between unparasitized and parasitized hosts and adapt the number of eggs they lay accordingly, and (ii) probably discriminate self from conspecific superparasitized hosts. Finally, mating does not appear to influence the host discrimination capacity, the ovarian function, or the oviposition behaviour.     

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.     

Different mate preferences by parasitized and unparasitized females potentially reduces sexual selection

Parasite‐mediated models of sexual selection predict that females should avoid parasitized mates, thereby generating selection on male traits revealing health. The strength of this selection, however, may depend on the prevalence of parasitism among females if their infection status alters their mate preferences. We evaluated the effects of a socially transmitted parasite on male traits and female behaviour in spadefoot toads. Parasitized males were larger and in better condition than unparasitized males. Moreover, better condition males produced longer calls. Unparasitized females preferred longer calls indicative of good‐condition males that are more likely parasitized. By contrast, parasitized females as a group possessed no preference for call duration. Presumably because of reduced selection by these parasitized females, male mating success was not associated with any measured traits. Thus, when females are parasitized, sexual selection on condition‐dependent traits is potentially reduced.     

Consistency in Egg Rejection Behaviour: Responses to Repeated Brood Parasitism in the Blackcap (Sylvia atricapilla)

To evaluate host responses towards repeated brood parasitism we experimentally parasitized and continuously videotaped blackcap nests in two consecutive trials. The ejection of a foreign egg was the most common response (94.5%) in both trials, but desertion (4.1%) and acceptance (1.4%) also occurred. The general method of ejection was puncturing. In 9.8% of identified ejections, already punctured eggs stuck to the abdominal feathers of the incubating bird and were carried out of the nest. Females were responsible for the majority of ejections in both trials and their response time was significantly shorter than that of males. Blackcaps exhibited consistency in the sex responsible for egg ejection over the two trials; but in five (20.8%) experiments individuals changed their behaviour. Repeatability for host responses within the nest was very high. In ejections accomplished by the same bird, the response was significantly quicker in the second trial, indicating the presence of certain learning abilities. Our results suggest that cuckoo hosts are quite consistent in their responses towards parasitic eggs when parasitized repeatedly within one breeding attempt.     

Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study

Nests of cavity‐nesting birds usually harbor some species of haematophagous ectoparasites that feed on the incubating adults and nestlings. Given the negative impact of ectoparasites on nestlings there will be selection on hosts to reduce parasite infestations through behavioural means. We have experimentally reduced the abundance of all ectoparasites in nests of pied flycatchers Ficedula hypoleuca to explore both whether there are changes in the frequency and duration of putative anti‐parasite behaviours by tending adults, as well as whether such anti‐parasite behaviours are able to compensate for the deleterious effects that parasites may have on nestlings. Heat treatment of nests substantially decreased the density of ectoparasites, and thereby positively affected nestling growth. The frequency and intensity of female grooming and nest sanitation behaviours during the incubation and nestling periods decreased as a consequence of the experimental reduction of ectoparasite infestation. Although nestlings begged more intensely in infested nests, the experiment had no significant effect on parental provisioning effort. Reduction of parasites resulted in larger nestlings shortly before fledging and increased fledging success. This study shows a clear effect of a complete natural nest ectoparasite fauna on parental behaviour at the nest and nestling growth in a cavity‐nesting bird. Although ectoparasites induce anti‐parasite behaviours in females, these behaviours are not able to fully remove parasite's deleterious effects on nestling growth and survival.     

Nest sanitation behavior does not increase the likelihood of parasitic egg rejection in herring gulls

Birds’ behavioral response to brood parasitism can be influenced not only by evolution but also by context and individual experience. This could include nest sanitation, in which birds remove debris from their nests. Ultimately, nest sanitation behavior might be an evolutionary precursor to the rejection of parasitic eggs. Proximately, the context or experience of performing nest sanitation behavior might increase the detection or prime the removal of parasitic eggs, but evidence to date is limited. We tested incubation-stage nests of herring gulls Larus argentatus to ask whether nest sanitation increased parasitic egg rejection. In an initial set of 160 single-object experiments, small, red, blocky objects were usually rejected (18 of 20 nests), whereas life-sized, 3D-printed herring gull eggs were not rejected whether red (0 of 20) or the olive-tan base color of herring gull eggs (0 of 20). Next, we simultaneously presented a red, 3D-printed gull egg and a small, red block. These nests exhibited frequent nest sanitation (small, red block removed at 40 of 48 nests), but egg rejection remained uncommon (5 of those 40) and not significantly different from control nests (5 of 49) which received the parasitic egg but not the priming object. Thus, performance of nest sanitation did not shape individuals’ responses to parasitism. Interestingly, parents were more likely to reject the parasitic egg when they were present as we approached the nest to add the experimental objects. Depending on the underlying mechanism, this could also be a case of experience creating variation in responses to parasitism.     

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     

An experimental analysis of joint nesting in the salamander Hemidaetylium scutatum (Caudata: Plethodontidae): the effects of population density

Three nesting behaviour patterns are documented in the plethodontid salamander Hemidactylium scutatum. A female may lay eggs (1) in a solitary nest and brood them, (2) in a joint nest and brood them as well as eggs of other females, or (3) in a joint nest that is brooded by another female. The hypothesis that population density was positively associated with joint nesting was tested by following two populations for 5 years and by experimentally manipulating the population density of nesting females in artificial habitats for the latter 2 years. The proportion of joint nests did not vary with density, although joint nests tended to contain eggs of more females at the high population density. Joint nests were usually brooded by one female; thus, most females that laid eggs in joint nests did not brood them at high density. The reproductive success, as measured by survival of embryos, of solitary and joint nesters was equivalent. Joint nests were deserted less often, however, which decreased the probability of catastrophic mortality. The number of days of brooding was significantly positively correlated with loss of body mass of females, suggesting a cost to brooding behaviour. Joint nesting with solitary brooding is not explained by aggressive usurpation of nests or by brood parasitism.