Why cuckoos remove host eggs: Biting eggs facilitates faster parasitic egg-laying.

Brood parasitism by cuckoos relies on manipulating hosts to raise their offspring and has evolved stunning adaptations to aid in their deception. The fact that cuckoos usually but not always, remove one or two host eggs while laying their eggs has been a longstanding focus of intensive research. However, the benefit of this behavior remains elusive. Moreover, the recently proposed help delivery hypothesis, predicting that egg removal by cuckoos may decrease the egg-laying duration in the parasitism process caused by biting action, lacks experimental verification. Therefore, in this study, we examined the effects of egg removal/biting on the egg-laying speed in the common cuckoo (Cuculus canorus) to experimentally test this hypothesis. We compared the duration of cuckoo egg-laying in empty nests, nests with host eggs, and nests with artificial blue stick models to test whether cuckoos biting an egg/stick can significantly hasten the egg-laying speed than no biting action. Our results showed that biting an egg or an object is associated with cuckoos laying approximately 37% faster than when they do not bite an egg or an object. This study provides the first experimental evidence for the help delivery hypothesis and demonstrates that when cuckoos bite eggs or other objects in the nest, they lay eggs more quickly and thereby avoid suffering the hosts' injurious attack.

Nest desertion as an anti-parasitism strategy in hosts selects for late egg-laying behavior in cuckoos.

Studies have shown that brood parasites lay their eggs early in the egg-laying sequence of their hosts, providing them with the advantage of earlier hatching. However, common cuckoos (Cuculus canorus) appear to parasitize the nests of gray bushchat (Saxicola ferreus) during the late egg-laying stage. The bushchat often abandons parasitized nests in the early stages, but not in the late egg-laying stages, thus favoring late egg-laying by cuckoos. In this study, four experiments were conducted to determine whether gray bushchats employ a nest desertion strategy targeted at cuckoo parasitism. The results showed that nest desertion was significantly correlated with parasitism cues and occurred mainly during the hosts' early egg-laying stage. Our study provides the first experimental evidence that nest desertion is an anti-parasitic strategy used by hosts in response to cuckoos. Additionally, our experiments demonstrated that the nest desertion is influenced by the trade-offs of investments in different egg-laying stages.

Brood parasitism and egg recognition in three bunting hosts of the cuckoos.

Comparative studies of egg recognition and rejection between various sympatric hosts provide insight into the coevolutionary history of the hosts and parasites, as well as the degree of antagonism between the species. Although buntings are widely considered to be a suitable host taxon for cuckoos, there has been relatively little research on this example of parasitism and host antiparasitic behaviour. Here we provided the first report on brood parasitism and egg recognition in three sympatric ground-nesting bunting hosts of the common cuckoo (Cuculus canorus), namely the yellow-throated bunting (Emberiza elegans), south rock bunting (E. yunnanensis), and crested bunting (E. lathami). The results show that for the five breeding seasons during 2018-2022, the parasitism rate by common cuckoos was 0.87% and 0.45% in yellow-throated buntings and south rock buntings, respectively, whereas the parasitism rate by an unidentified parasite was 4% during 2018-2023 in the crested bunting. The rejection rates of the three bunting hosts for blue non-mimetic eggs were 89.3%, 88.9%, and 100% for yellow-throated buntings, south rock buntings, and crested buntings, respectively. The rejection rates for red non-mimetic eggs by yellow-throated buntings and south rock buntings were lower at 76.9% and 82.4%, respectively. All three sympatric bunting hosts examined had high levels of egg recognition and egg rejection, suggesting that it may have been subjected to high parasitic history and that egg recognition ability was retained after the loss of parasitism, which needs to be further verified by future experiments.

Defense behavior of two closely related but geographically distant host species against cuckoo parasitism: A next test for the parallel coevolution.

Interactions between avian brood parasites, such as common cuckoos (Cuculus canorus), and their hosts are one of the best-studied examples of the coevolutionary arms race. Different stages of this arms race can be seen in different races of common cuckoos and their hosts across their range. However, little is known whether selected populations of two closely related but geographically distant species with probably different coevolutionary histories with the common cuckoo are also at different stages of the arms race. In this study, we tested this prediction experimentally using the same non-mimetic model eggs and three-dimensional (3D) printed models of the gray adult common cuckoo (Cuculus canorus). We examined egg recognition and egg rejection and aggression against the common cuckoo in the great reed warbler (Acrocephalus arundinaceus) and Oriental reed warbler (Acrocephalus orientalis), in Slovakia of Europe and northeast China of Asia. The results showed that the great reed warbler exhibited stronger responses to experimental model eggs and 3D models of the common cuckoo than the Oriental reed warbler. We conclude that both the great reed warbler and Oriental reed warbler have well-developed antiparasitic behaviors against common cuckoos in the studied populations, but with different levels of defense intensity, which may be due to local differences in parasitic pressure and the risk of parasitism. This provides an opportunity to study coevolutionary processes between the brood parasite and its hosts together in both species at large geographical scales.

Predation of Daurian redstarts offspring in nest boxes by the Oriental magpie-robin and tree sparrow.

Birds select suitable nest sites for breeding to ensure their own and offspring's survival; however, they inevitably suffer some potential predation risk. We studied the breeding ecology of Daurian redstarts (Phoenicurus auroreus) by providing nest boxes for their breeding from March to August of 2022. We recorded the predation of both Daurian redstarts eggs or nestlings by Oriental magpie-robins (Copsychus saularis) and tree sparrow (Passer montanus). Oriental magpie-robin were recorded attacking a feeding female adult and depredating nestlings. After the nestling predation event, the Daurian redstarts abandoned the nest. This video evidence provide a better understanding of the potential predators of cavity-nesting birds.

Importance of cooperation: How host nest defenses effectively prevent brood parasitism from the cuckoos.

As the frontline defense against avian brood parasitism, nest defense is important in reducing nest parasitism and increasing host fitness. However, systematic studies on its effectiveness (i.e., on whether it successfully prevents cuckoo parasitism) are scarce. Based on 214 video recordings from 10 years of field observations, we evaluated the effectiveness of nest defenses of the Oriental reed warbler (Acrocephalus orientalis) in deterring common cuckoo (Cuculus canorus) parasitism. Under a breeding pair situation (≤ 2 hosts individuals), warblers were hardly effective in resisting the egg-laying of the cuckoo and many of the cuckoos under attack were able to complete the parasitic process without being harmed. However, when hosts ≥ 3 individuals, the warblers could effectively thwart the cuckoos and cause lethal damage to the cuckoo in partial cases. This indicated that the host group effectively resisted the cuckoo, demonstrating the importance of cooperation among host neighbors in resisting cuckoo parasitism.

First description of injury feigning behavior in Godlewski's buntings.

Nest defense behavior helps ground-nesting birds improve their breeding success. Among such behaviors, injury feigning behavior (IFB) is one of the better ways to attract predators and protect birds' nests. IFB is generally associated with shorebirds in general and plovers in particular, however, through field observation, it has been found this behavior is also exhibited in bunting species when they facing the risk of predation. We attempt to explore the detailed description of this behavior in buntings and the factors that affect this behavior. Based on video-recordings of the nest defense behavior by the ground-nesting bird Godlewski's bunting (Emberiza godlewskii) against nest invaders, we explored the characteristic of IFB and differences in nest defense behavior during their brooding seasons. The results showed that female buntings had a distinct IFB: the wings of buntings incited within 60°-90° of the body, ran and called rapidly, pretending to be injured and unable to fly. The nest stage had significant and extremely significant effects on IFB and movement distance (MD), respectively. And IFB was more likely to occur in brooding (34.62%) than incubation period (16.42%). This indicates that there are significant differences in the IFB of buntings at different breeding stages.

Fatal mobbing and attack of the common cuckoo by its warbler hosts.

Nest defense is an effective strategy of hosts against parasites. Typically, hosts will aggressively attack brood parasites that approach or visit their nests, which can prevent the parasites from laying eggs or may even lead to the death of the parasites. Few previous studies have specifically reported such fatal cases involving brood parasites and have attributed the cause of death to either drowning or hypothermia after falling into the water following an attack from hosts. In this study, we recorded the process of multiple host individuals of the Oriental reed warbler (Acrocephalus orientalis) mobbing and attacking a female common cuckoo (Cuculus canorus) in the field. We discovered that the immediate cause of the cuckoo's death was the fatal physical damage resulting from the aggressive defense from the hosts, suggesting that frantic pecking and scratching by the hosts is the most proximate cause of mortality among egg-laying female cuckoos. This finding enhances our essential understanding of the effectiveness of host attacks.

Defensive adaptations to cuckoo parasitism in the black-browed reed warbler (Acrocephalus bistrigiceps): recognition and mechanism.

Hosts of avian brood parasites suffer a high cost of reproductive loss due to parasitism, driving them to evolve a variety of anti-parasitic defenses. These defenses comprise a series of components, including the recognition of brood parasites and the eggs laid by the parasites, cues used for recognition, and the mechanisms on which these behaviors are based. In this study, we conducted egg recognition and nest intruder experiments to examine these components of anti-parasitic behavior in the black-browed reed warbler (Acrocephalus bistrigiceps), a rare host of the common cuckoo (Cuculus canorus). We found that the host possessed strong recognition capacity, rejecting 100% of parasitic eggs, and used a template-based mechanism for egg recognition. The host birds also rejected 80% of their own eggs on which artificial markings were added to the blunt pole; however, they accepted all eggs with the same manipulation on the sharp pole, implying that the blunt pole was an important recognition cue. Furthermore, the host exhibited stronger aggression to cuckoos than to harmless controls; a behavior specific to the incubation stage rather than the nestling stage. Therefore, the host was able to distinguish the cuckoo from other nest intruders as being a brood parasite. These results together help explain the near absence of cuckoo parasitism in black-browed reed warblers and provide new information concerning anti-parasitic defenses in this host species.

Nest size matters: common cuckoos prefer to parasitize larger nests of Oriental reed warblers.

Avian brood parasites leave parental care of their offspring to foster parents. Theory predicts that parasites should select for large host nests when they have sufficient available host nests at a given time. We developed an empirical experimental design to test cognitive ability of female cuckoos in nest size by studying nest choice of common cuckoos (Cuculus canorus) among nests of its Oriental reed warbler (Acrocephalus orientalis) hosts. We presented three groups of experimental nests: 1) nest dyads tied together including one large and one small artificial nest from reed leaves, 2) nest triads tied together used the old modified warbler's own nests including enlarged, reduced and medium-sized nests, and 3) nest dyads are similar to group 1, but not tied together to elicit parasitism by common cuckoos. We predict that cuckoos prefer larger nest than medium one, the next is smaller nest. Our findings showed that common cuckoo females generally prefer large nests over medium or small sized nests in all three experimental groups. Furthermore, cuckoo parasitism was significantly more common than in previous studies of the same warbler population, implying that larger, higher and more exposed host nests effectively increased the probability of cuckoo parasitism.

Cryptic eggs are rejected less frequently by a cuckoo host.

Obligate brood parasitism is associated with huge reproduction costs, forcing hosts to evolve various anti-parasitic strategies against brood parasites, among which egg recognition and rejection is the most effective defense strategy. According to the crypsis hypothesis, non-mimetic yet cryptic eggs in a nest can also deceive their hosts and eventually be accepted. To validate this hypothesis, we conducted field experiments on Oriental reed warblers (Acrocephalus orientalis), a common host for common cuckoos (Cuculus canorus). We firstly tested the egg recognition and rejection abilities of Oriental reed warblers, using black and white model eggs in natural nests. Then we designed a comparison test where the cryptic effects of the two groups of experimental eggs were different. We manipulated the nest lining color and added relatively cryptic and bright model eggs to test warblers' rejection behaviors against cryptic and bright foreign eggs. The results showed that warblers have strong egg recognition and rejection abilities. There is a significant tendency for warblers to prefer to peck and reject relatively distinguishable foreign eggs, which supports the crypsis hypothesis. These findings indicate that even in the host-parasite system of open nests, parasitic eggs that are cryptic enough are prevented from being discovered and rejected by the host, and thus obtain the possibility of successful parasitism.

Common cuckoo females remove more conspicuous eggs during parasitism.

Avian obligate brood parasites gain an advantage by removing the eggs of the cuckoos who have already visited the nest, which can increase the chances of survival for their offspring. Conversely, to prevent their eggs from being picked up by the next parasitic cuckoo, they need to take some precautions. Egg mimicry and egg crypsis are two alternative strategies to prevent the parasitized egg from being picked up by another parasitic cuckoo. Here, we tested whether the egg crypsis hypothesis has a preventative effect when common cuckoos (Cuculus canorus) parasitize their Oriental reed warbler (Acrocephalus orientalis) hosts. We designed two experimental groups with different crypsis effects to induce common cuckoos to lay eggs and observed whether the cuckoos selectively picked up the experimental eggs with low crypsis levels in the process of parasitism. Our results supported the egg crypsis hypothesis; the observed cuckoos significantly preferred to select the more obvious white model eggs. This shows that even in an open nest, eggs that are adequately hidden can also be protected from being picked up by cuckoo females during parasitism so as to increase the survival chance of their own parasitic eggs.

Determining the level of extra-pair paternity in yellow-bellied prinias, a socially monogamous passerine.

Previous work based on molecular evidence has shown that most socially monogamous birds follow a genetic polyandrous mating system. However, our knowledge about avian mating systems is heavily biased toward the north temperate zone, with data on tropical birds remaining relatively scarce. This uneven distribution of both phylogenetic and spatial sampling has hampered our understanding and interpretation of results. In this study, we investigated the frequency of extra-pair paternity (EPP) in a tropical population of yellow-bellied prinias ( Prinia flaviventris) in Guangxi, southern China. A total of 129 individuals belonging to 24 nests were sampled, among which 12 out of 83 chicks (14.46%) in seven nests were found to be EPP offspring. In nests in which all nestlings were sampled, only five out of 56 chicks were EPP offspring, accounting for an unbiased EPP rate of 8.93%. This rate is below the average rate of EPP in the family Sylviidae. The possible causes of EPP in prinias and the occurrence of EPP in birds with high resource investment and intensive parental care are discussed. This study highlights the value of genome-wide markers in determining relatedness in a wild bird species without a reference genome.

Egg polymorphism and highly sensitive egg recognition of cross-phenotypes in rufescent prinias Prinia rufescens as effective defenses against brood parasitism.

Whether escalating egg polymorphism increases the efficiency to reduce the fitness costs of brood parasitism is not supported by empirical studies. Rufescent prinias (Prinia rufescens) laying tetramorphic eggs are highly sensitive to conspecific foreign eggs with different phenotypes that they reject perfectly at 100%, and suffer only 1.4% of plaintive cuckoo (Cacomantis merulinus) parasitism. Our study provided empirical evidence showing that escalation of egg polymorphism in hosts increases their fitness because it reduces successful cuckoo parasitism rate.

Cuckoos use host egg number to choose host nests for parasitism.

To maximize their offspring success common cuckoo (Cuculus canorus) females should lay their eggs into host nests before incubation has begun. This ensures that the parasite chick hatches before all host chicks and can evict its foster siblings to monopolize host parental care. Many studies have demonstrated that most cuckoo eggs are indeed laid before the onset of host incubation. But cues used by female cuckoos to choose the right nest at the right time remain unclear. Here, we combine field observations with a field experiment to test whether female cuckoos use the number of eggs in the nests of their Oriental reed warbler (Acrocephalus orientalis) hosts to direct their choice. Over 8 years of field observations and 5 years of experiments, cuckoo females placed the majority of their eggs in nests with fewer than three host eggs, i.e. early in the laying sequence. For natural nests, the cuckoos may use information gleaned from the activity and behaviour of the host parents to make their choice. In our sets of experimental nests containing different numbers of model eggs, the vast majority of parasitism events occurred in nests containing a single egg. To our knowledge, this is the first field experiment showing that cuckoos choose host nests for parasitism based on the number of host eggs they contain. It appears that cuckoo females use the egg number to estimate the appropriate host nest stage for timely parasitism.

Egg laying behavior of common cuckoos ( Cuculus canorus): Data based on field video-recordings.

The egg laying behavior of brood parasites is at the heart of studies on host co-evolution. Therefore, research on egg laying behavior can improve our understanding of brood parasitism and associated processes. Over a seven year study period, we monitored 455 oriental reed warbler ( Acrocephalus orientalis) nests during the egg laying period, 250 of which were parasitized by common cuckoos ( Cuculus canorus). We collected 53 clear videos of common cuckoo parasitism, analyzed all recorded parasitic behavior in detail, and summarized the process of brood parasitism. Furthermore, based on analyses of the field video recordings, we propose a new explanation for egg removal behavior, namely the delivery hypothesis, i.e., egg pecking and biting by cuckoos may facilitate fast egg-laying and parasitism by reducing host attention and attack, with egg removal a side effect of egg pecking and biting. We concluded that common cuckoos change their behavior when hosts are present at the nest, with a set of behaviors performed to deal with host attack and successfully complete parasitic egg-laying regardless of time of day.

Model eggs fail to detect egg recognition in host populations after brood parasitism is relaxed.

BACKGROUND: Obligate brood parasites exert strong selective pressure on target hosts. In response, hosts typically evolve anti-parasitism strategies, of which egg recognition is one of the most efficient. Generally, host egg-recognition capacity is determined using model eggs. Previous studies have shown that some host species, which are capable of detecting parasite eggs, do not reject model eggs. However, it is unknown that whether the reaction to model eggs varies among distinct populations of the same host in relation to the degree of parasitism pressure. RESULTS: Here, we compared the rejection frequencies of model eggs and real eggs between mainland and island populations of the plain prinia (Prinia inornata), which are respectively sympatric and allopatric with their brood parasite, the common cuckoo (Cuculus canorus). Our results indicated that the mainland and island populations rejected real eggs at similar rates, but rejected model eggs, which were similar in size to real eggs but heavier, at significantly different rates: the island population rejected fewer model eggs, possibly because the rejection motivation of this population was lower due to absence of parasitism. CONCLUSIONS: Our results indicated that some factors affecting the decision to reject, such as rejection motivation, varied according to the degree of parasitism pressure, and thus influenced the frequency of egg rejection. Furthermore, our results suggested that model eggs should be used with caution in comparative studies of egg recognition abilities among species or populations subjected to different intensities of brood parasitism. That is, model eggs may fail to accurately detect egg recognition in host populations with little to no risk of parasitism.

Do swallows (Hirundo daurica) use the visual cue of hatchling down-feathers to discriminate parasite alien nestlings?

Egg recognition is a variable but common anti-parasitism defense among different species of birds with brood parasites. In contrast, nestling recognition is rare. Very few studies have found nestling recognition in brood parasite hosts and determined the rejection mechanism behind this behavior. Hosts may use the number of hatchling down-feathers to reject parasite nestlings. We tested whether hatchling down-feathers is a visual cue for the red-rumped swallow, a host that can recognize and reject parasite nestlings. Our results indicated that red-rumped swallows do not recognize foreign nestlings based on hatchling down-feathers. The closed nest structure and hatchling morph may explain the absence of such a mechanism. None of the rejection mechanisms found in previous studies could explain the nestling recognition in swallows. Olfactory cues, tactile cues, or other visual cues, except for single nestling or hatchling down-feathers, may provide nestling recognition in red-rumped swallows. More study is needed to evaluate these possibilities.

High egg rejection rate in a Chinese population of grey-backed thrush (Turdus hortulorum).

everal previous studies have indicated that nest sanitation behavior is a general adaptation in altricial birds, with egg recognition capacity evolving as a specific response to interspecific brood parasitism (IBP). However, a recent study suggested an alternative hypothesis, concluding that conspecific brood parasitism (CBP) selects for egg rejection in thrushes, with IBP as a by-product. In the present study, we used a spectrophotometer to quantify egg coloration and egg mimicry and performed artificial parasitism experiments in the grey-backed thrush (Turdus hortulorum). We showed that individuals of this species rejected 100% of 12 foreign eggs, without IBP or CBP detected. In a review of previous studies, we also discuss possible explanations for the high egg rejection rate in the grey-backed thrush and suggest areas for future study.