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.     

Sex-specific defence behaviour against brood parasitism in a host with female-only incubation

Nest protection against intruders is an indispensable component of avian parental care. In species with biparental care, both mates should evolve nest defence behaviour to increase their reproductive success. In most host-parasite systems, host females are predicted to have more important roles in nest defence against brood parasites, because they typically are primarily responsible for clutch incubation. Male antiparasitic behaviour, on the other hand, is often underestimated or even not considered at all. Here we investigated sex-specific roles in four aspects of great reed warbler (Acrocephalus arundinaceus) nest defence against a brood parasite—the cuckoo (Cuculus canorus), namely (1) mobbing, (2) nest attendance/guarding, (3) nest checking and (4) egg ejection. Using dummy experiments, simulating brood parasitism and by video-monitoring of host nests we found that males took the key roles in cuckoo mobbing and nest guarding, while females were responsible for nest checking and egg ejection behaviours. Such partitioning of parental roles may provide a comprehensive clutch protection against brood parasitism.     

To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti‐parasite strategies

Hosts either tolerate avian brood parasitism or reject it by ejecting parasitic eggs, as seen in most rejecter hosts of common cuckoos, Cuculus canorus, or by abandoning parasitized clutches, as seen in most rejecter hosts of brown‐headed cowbirds, Molothrus ater. What explains consistent variation between alternative rejection behaviours of hosts within the same species and across species when exposed to different types of parasites? Life history theory predicts that when parasites decrease the fitness of host offspring, but not the future reproductive success of host adults, optimal clutch size should decrease. Consistent with this prediction, evolutionarily old cowbird hosts, but not cuckoo hosts, have lower clutch sizes than related rarely‐ or newly parasitized species. We constructed a mathematical model to calculate the fitness payoffs of egg ejector vs. nest abandoner hosts to determine if various aspects of host life history traits and brood parasites’ virulence on adult and young host fitness differentially influence the payoffs of alternative host defences. These calculations showed that in general egg ejection was a superior anti‐parasite strategy to nest abandonment. Yet, increasing parasitism rates and increasing fitness values of hosts’ eggs in both currently parasitized and future replacement nests led to switch points in fitness payoffs in favour of nest abandonment. Nonetheless, nest abandonment became selectively more favourable only at lower clutch sizes and only when hosts faced parasitism by a cowbird‐ rather than a cuckoo‐type brood parasite. We suggest that, in addition to evolutionary lag and gape‐size limitation, our estimated fitness differences based on life history trait variation provide new insights for the consistent differences observed in the anti‐parasite rejection strategies between many cuckoo‐ and cowbird‐hosts.     

Host nest defense against a color-dimorphic brood parasite: great reed warblers (Acrocephalus arundinaceus) versus common cuckoos (Cuculus canorus)

We tested great reed warbler (Acrocephalus arundinaceus) discrimination against two common cuckoo (Cuculus canorus) female color morphs (gray and rufous) in two areas with different parasitism rates and proportions of the two morphs. Hosts recognized the two cuckoo morphs from a control, the feral pigeon (Columba livia), at Apaj, Hungary (where brood parasitism was heavy), whereas no significant differences among the models were recorded at Lužice, Czech Republic (where the parasitism rate was moderate). At Apaj, the hosts discriminated the rufous morph (which is slightly predominant there) better than the gray morph from the control. Between-site comparison (after controlling for background aggression) revealed that great reed warblers were more aggressive towards the rufous morph at Apaj than at Lužice, whereas their responses to the gray morph did not differ, corresponding with much higher between-site difference in the relative abundance of the rufous morph. Our results suggest that both local parasitism pressure and relative abundance of two female color morphs of a brood parasite may significantly influence host nest defenses.     

Evidence for aggressive mimicry in an adult brood parasitic bird,and generalized defences in its host

Mimicry of a harmless model (aggressive mimicry) is used by egg, chick and fledgling brood parasites that resemble the host''s own eggs, chicks and fledglings. However, aggressive mimicry may also evolve in adult brood parasites, to avoid attack from hosts and/or manipulate their perception of parasitism risk. We tested the hypothesis that female cuckoo finches (Anomalospiza imberbis) are aggressive mimics of female Euplectes weavers, such as the harmless, abundant and sympatric southern red bishop (Euplectes orix). We show that female cuckoo finch plumage colour and pattern more closely resembled those of Euplectes weavers (putative models) than Vidua finches (closest relatives); that their tawny-flanked prinia (Prinia subflava) hosts were equally aggressive towards female cuckoo finches and southern red bishops, and more aggressive to both than to their male counterparts; and that prinias were equally likely to reject an egg after seeing a female cuckoo finch or bishop, and more likely to do so than after seeing a male bishop near their nest. This is, to our knowledge, the first quantitative evidence for aggressive mimicry in an adult bird, and suggests that host–parasite coevolution can select for aggressive mimicry by avian brood parasites, and counter-defences by hosts, at all stages of the reproductive cycle.     

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.     

Antagonistic antiparasite defenses: nest defense and egg rejection in the magpie host of the great spotted cuckoo

Brood parasites dramatically reduce the reproductive successof their hosts, which therefore have developed defenses againstbrood parasites. The first line of defense is protecting thenest against adult parasites. When the parasite has successfullyparasitized a host nest, some hosts are able to recognize andreject the eggs of the brood parasite, which constitutes the secondline of defense. Both defense tactics are costly and would be counteractedby brood parasites. While a failure in nest defense implies successfulparasitism and therefore great reduction of reproductive successof hosts, a host that recognizes parasitic eggs has the opportunityto reduce the effect of parasitism by removing the parasiticegg. We hypothesized that, when nest defense is counteractedby the brood parasite, hosts that recognize cuckoo eggs shoulddefend their nests at a lower level than nonrecognizers becausethe former also recognize adult cuckoos. Magpie (Pica pica) hoststhat rejected model eggs of the brood parasitic great spottedcuckoo (Clamator glandarius) showed lower levels of nest defensewhen exposed to a great spotted cuckoo than when exposed toa nest predator (a carrion crow Corvus corone). Moreover, magpiesrejecting cuckoo eggs showed lower levels of nest defense againstgreat spotted cuckoos than nonrecognizer magpies, whereas differencesin levels of defense disappeared when exposed to a carrion crow.These results suggest that hosts specialize in antiparasitedefense and that different kinds of defense are antagonistically expressed.We suggest that nest-defense mechanisms are ancestral, whereasegg recognition and rejection is a subsequent stage in the coevolutionaryprocess. However, host recognition ability will not be expressedwhen brood parasites break this second line of defense.     

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     

Nest desertion cannot be considered an egg‐rejection mechanism in a medium‐sized host: an experimental study with the common blackbird Turdus merula

Two main mechanisms of egg rejection, the main defence of hosts against brood parasites, have been described: ejection and desertion. Desertion of the parasitized nest is much more costly and is usually exhibited by small‐sized host species unable to remove the parasitic egg. However, nest desertion is frequently assumed to be an anti‐parasite strategy even in medium or large‐sized host species. This assumption should be considered with caution because: 1) large‐sized hosts able to eject the parasitic egg should eject it rather than desert the nest, and 2) breeding birds may desert their nests in response to different disturbances other than brood parasitism. This problem is especially important in the common blackbird Turdus merula because this is a medium‐sized species, potential host of the common cuckoo Cuculus canorus, in which desertion has been frequently reported as a response to cuckoo egg models. Here, we seek to determine whether nest desertion can be considered a response unequivocally directed to the parasitic egg in medium‐sized hosts using the blackbird as the study species. In an experimental study in which we have manipulated levels of mimicry and size of experimental eggs, we have found that both colour (mimetic and non‐mimetic; at least for human vision) and size (small, medium, and large) significantly affected ejection rates but not nest desertion rates. In fact, although large eggs disproportionally provoked nest desertion more frequently than did small or medium‐sized eggs, cuckoo‐sized parasitic eggs were not deserted allowing us to conclude that desertion is unlikely to be an adaptive response to brood parasitism at least for this species.     

Nestling sex predicts susceptibility to parasitism and influences parasite population size within avian broods

Vertebrate hosts differ in their level of parasite susceptibility and infestation. In avian broods, variation in susceptibility of nestlings to ectoparasites may be associated with non‐uniform distributions of parasites among brood mates, with parasites concentrating feeding on the most vulnerable hosts. The presence of a highly susceptible nestling in a brood can benefit the remaining young by reducing the parasite pressure they experience; however, from a parasite’s perspective, broods with fewer susceptible hosts may provide effectively fewer resources than broods of the same size containing a greater abundance of susceptible hosts, and this could limit the number of parasites that a host brood can sustain. To test whether variation in number of susceptible hosts affects the number of parasites in bird nests, we first examined the role of host sex and induced immunity (via methionine supplementation) on susceptibility of mountain bluebirds Sialia currucoides to parasitism by blow flies Protocalliphora spp. We then assessed the effect of variation in number of susceptible hosts on the number of parasites inhabiting the nest. Only females showed a benefit of methionine supplementation, gaining mass more rapidly following supplementation compared to males. This suggests that females are more susceptible to parasites in this system; this was further supported by parasite feeding trials, in which parasites extracted larger blood meals from female than male hosts. Finally, the abundance of parasites in nests was predicted by brood sex ratio: broods containing more female young harboured more parasites. Hence, within‐brood variation in host susceptibility to parasites can not only influence the costs of parasitism for individual nestlings, but may also have consequences for the size of parasite populations within nests. If patterns of maternal investment affect the abundance of nest‐dwelling parasites, these interactions may be important for understanding fitness consequences of maternal resource allocation in many vertebrate hosts.     

Hawk mimicry in cuckoos and anti‐parasitic aggressive behavior of barn swallows in Denmark and China

Hosts of brood parasites defend their nests against parasitism by aggression and subsequently, if parasitized, by rejection of the parasite egg or nestling. Cuckoos have evolved plumage mimicry with convergence towards the phenotype of Accipiter hawks that are common predators of cuckoo hosts. Here we tested two alternative hypotheses 1) whether barn swallows Hirundo rustica have evolved less aggressive behavior towards cuckoos in areas of sympatry with more abundant Accipiter hawks; and 2) whether barn swallows have evolved more aggressive anti‐parasite behavior in areas with a single species of cuckoo. We presented dummies of common cuckoo Cuculus canorus, sparrowhawk Accipiter nisus and Oriental turtledove Streptopelia orientalis (a benign control) at the nests of barn swallows during breeding, while recording intensity of response and proximity of barn swallows to the dummy. We demonstrated that cuckoos moved away when attacked aggressively and approached more closely by barn swallows showing that barn swallow behavior was efficient at driving away cuckoos. Barn swallows were significantly more aggressive and approached cuckoo and sparrowhawk dummies more closely in Denmark than in China, despite sparrowhawks being relatively more common in Denmark. Responses towards cuckoo dummies differed from responses towards sparrowhawk dummies, showing that barn swallows distinguished between the two different causes of danger. These findings are inconsistent with a less aggressive response towards cuckoo dummies in areas of sympatry with more abundant Accipiter hawks, but consistent with the alternative hypothesis that barn swallows have evolved more aggressive behavior towards cuckoos in areas with a single species of brood parasite, but not in areas with multiple species of parasites, where it is harder for hosts to tell the difference.     

Behaviour in usurpers and late joiners ofPolistes biglumis bimaculatus (Hymenoptera,Vespidae)

Summary During the late pre-emergence phase, a foundress of the paper waspPolistes biglumis bimaculatus may be expelled by a conspecific female from her own nest (usurpation) or, less frequently, joined by another female of the same species (late association). The behaviour of femalePolistes biglumis bimaculatus, when usurping a conspecific colony or joining another foundress, is compared with that of foundresses on non-usurped colonies. The most conspicous difference is the intense abdomen stroking behaviour the usurper performs over the comb surface on the first days after usurpation. As observed in otherPolistes species, once usurpers and joiners arrive on a strange nest they will destroy most of the immature brood of the previous nest owner. Although host workers are not aggressive towards the intruder females, reproductive success of usurpers and joiners is low compared with that of legitimate foundresses. The same behaviours observed on usurped colonies are found in the obligate social parasites ofPolistes. These behaviours are therefore discussed in the context of the evolution of intra- and inter-specific parasitism.     

No change in common cuckoo Cuculus canorus parasitism and great reed warblers’ Acrocephalus arundinaceus egg rejection after seven decades

The coevolutionary process among avian brood parasites and their hosts involves stepwise changes induced by the antagonistic selection pressures of one on the other. As long‐term data on an evolutionary scale is almost impossible to obtain, most studies can only show snapshots of such processes. Information on host behaviour, such as changes in egg rejection rates and the methods of rejection are scarce. In Hungary there is an interesting case between the common cuckoo Cuculus canorus and the great reed warbler Acrocephalus arundinaceus, where the level of parasitism is unusually high (around 50%). We compared host rejection rates and methods of rejection from within our own project to that of an early study carried out and published almost 70 yr ago in the same region. Our comparisons revealed high and stable rates of parasitism (range: 52–64%), and marked fluctuations in the ratio of multiply parasitized nests (range: 24–52%). No difference was revealed in egg rejection rates after 7 decades (34–39%). Linear mixed‐effects modelling revealed no year effect on the type host responses toward the parasitic egg(s) during the years of study (categorized as acceptance, ejection, burial, and nest desertion). Cuckoo egg rejection was primarily affected by the type of parasitism, as more cuckoo eggs were rejected during single parasitism than from multiply parasitized nests. Our comparison did not reveal any directional changes in this cuckoo–host relationship, except a slight decrease in the frequency of multiple parasitism, which is likely to be independent from coevolutionary processes.     

Host density predicts presence of cuckoo parasitism in reed warblers

In some hosts of avian brood parasites, several populations apparently escape parasitism, while others are parasitized. Many migratory specialist brood parasites like common cuckoos, Cuculus canorus , experience a short breeding season, and in order to maintain local parasite populations host densities should be sufficiently high to allow efficient nest search. However, no studies have investigated the possible effect of host density on presence of cuckoo parasitism among populations of a single host species. Here, we investigated possible predictors of common cuckoo parasitism in 16 populations of reed warblers, Acrocephalus scirpaceus , across Europe. In more detail, we quantified the effect of host density, number of host breeding pairs, habitat type, mean distance to nearest cuckoo vantage point, predation rate and latitude on the presence of cuckoo parasitism while controlling for geographical distance among study populations. Host density was a powerful predictor of parasitism. We also found a less pronounced effect of habitat type on occurrence of parasitism, while the other variables did not explain why cuckoos utilize some reed warbler populations and not others. This is the first study focusing on patterns of common cuckoo-host interactions within a specific host species on a large geographic scale. The results indicate that if host density is below a specific threshold, cuckoo parasitism is absent regardless of the state of other potentially confounding variables.     

Does Brood Parasitism Induce Paternal Care in a Polygynous Host?

Red‐winged blackbirds (Agelaius phoeniceus) are a polygynous songbird with facultative biparental care, and a common host for brown‐headed cowbirds (Molothrus ater), an obligate brood parasite. We examined brood parasitism and paternal care in a long‐term study of parental care in red‐winged blackbirds. The presence of a cowbird nestling was associated with a higher likelihood of paternal care by the host male redwing in both naturally and experimentally parasitized nests. This result indicates that it was the presence of the brood parasite that was important and not simply that brood parasites chose hosts where paternal care was more likely. Both male and particularly female redwings increased provisioning to parasitized broods. Our work suggests that brood parasites raise the cost of parental care and push a polygynous host species toward monogamy.     

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.     

Adjustment of incubation according to the threat posed: a further signal of enemy recognition in the Blackcap Sylvia atricapilla?

Nest predation and brood parasitism are costly for nest owners, and natural selection should therefore favour the evolution of parental counterdefences. We addressed the question of whether Blackcaps Sylvia atricapilla change their incubation behaviour in response to various nest intruders and whether this adjustment matches the intensity of mobbing exhibited towards these intruders. Near focal nests, we successively exposed a dummy of a brood parasite, nest predator and an innocuous species. After the parents had responded, we removed the dummy and filmed their incubation. The most aggressive response towards the Common Cuckoo Cuculus canorus and high nest attendance after its disappearance indicated recognition of the brood parasite. Low-intensity response to the Jay Garrulus glandarius, together with reduced subsequent parental care, suggested that Blackcaps perceived it either as less deleterious at the egg stage than the Cuckoo or as a danger to themselves. Almost no aggression towards the Turtle Dove Streptopelia turtur, along with the resumption of incubation after its removal, implied that Blackcaps recognised it as harmless. In addition, we found that the level of aggression positively correlated with nest attendance, suggesting a link between the intensity of mobbing and subsequent parental care. Altogether, our results demonstrate that the issue of enemy recognition may be viewed as a complex of both aggressive and post-presentation behaviours.     

Micro-evolutionary change and population dynamics of a brood parasite and its primary host: the intermittent arms race hypothesis

A long-term study of the interactions between a brood parasite, the great spotted cuckoo Clamator glandarius, and its primary host the magpie Pica pica, demonstrated local changes in the distribution of both magpies and cuckoos and a rapid increase of rejection of both mimetic and non-mimetic model eggs by the host. In rich areas, magpies improved three of their defensive mechanisms: nest density and breeding synchrony increased dramatically and rejection rate of cuckoo eggs increased more slowly. A stepwise multiple regression analysis showed that parasitism rate decreased as host density increased and cuckoo density decreased. A logistic regression analysis indicated that the probability of changes in magpie nest density in the study plots was significantly affected by the density of magpie nests during the previous year (positively) and the rejection rate of mimetic model eggs (negatively). These results are consistent with a hypothesis (the intermittent arms race hypothesis) of spatially structured cyclic changes in parasitism. During periods of parasitism, host defences continuously improve, and as a consequence, the fitness gains for parasites decrease. When host defences against parasites reach a high level, dispersing parasites have a selective advantage if they are able to emigrate to areas of low resistance. Once parasites have left an area hosts will lose their defensive adaptations due to their cost in the absence of parasitism. The scene is then set for re-colonization by great spotted cuckoos. Received: 7 May 1998 / Accepted: 24 August 1998     

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.