Dynamics of evolutionary succession and coordination between opposite adaptations in cuckoo hosts under antagonistic coevolution.

Adaptations are driven by specific natural selection pressures throughout biological evolution. However, these cannot inherently align with future shifts in selection dynamics, thus manifesting in opposing directions. We performed field experiments on cuckoo hosts to investigate the coexistence and conflict between two evolutionarily successive but opposing behavioral adaptations-egg retrieval and rejection. Our findings provide key insights. (1) Egg rejection against brood parasites in hosts reshapes egg retrieval to flexible reactions-retrieval, ignoring, or outright rejection of foreign eggs outside the nest cup, departing from instinctual retrieval. (2) Parasitism pressure and egg mimicry by parasites remarkably alter the proportions of the three host reactions. Host species with higher parasitism pressure exhibit frequent and rapid rejection of non-mimetic foreign eggs and reduced ignoring or retrieval responses. Conversely, heightened egg mimicry enhances retrieval behaviors while diminishing ignoring responses. (3) Cuckoos employ consistent mechanisms for rejecting foreign eggs inside or outside the nest cup. Direct rejection of eggs outside the nest cup shows that rejection precedes retrieval, indicating prioritization of specific adaptation over instinct. (4) Cuckoo hosts navigate the conflict between the intentions and motivations associated with egg rejection and retrieval by ignoring foreign eggs, a specific outcome of the rejection-retrieval tradeoff.

Comparison of Reproductive Strategies between Two Sympatric Copsychus Passerines.

Reproduction plays a crucial role in determining the development, fate, and dynamics of bird populations. However, reproductive strategies vary among species and populations. In this study, we investigated the reproductive strategies of the Oriental Magpie Robin (Copsychus saularis) and White-rumped Shama (C. malabarica), which are closely related passerines that reproduce in sympatric areas. We found that although these two species were both cavity nesting, their nest-site selection differed; the Shama preferred nesting close to trees and forests, whereas the Magpie Robin nested close to human residential areas. Furthermore, their egg incubation patterns differed; the Shama increased daily incubation frequency with incubation time, but the Magpie Robin maintained its daily incubation time regardless of changes in incubation frequency. However, the nestling heating patterns of these two species were similar, indicating a critical demand for regulating hatchling body temperature during this crucial stage. The feeding frequencies of male parents were strongly correlated with those of females in both species, suggesting equal contribution and good synchronization between the sexes. Nestling feeding frequency was also correlated with nest cleaning frequency, implying coordination between feeding and defecation by parents and offspring, respectively. This research explored the divergence and convergence of reproductive strategies between these two sympatric species, providing valuable insights into the niche differentiation theory.

Revealing the roles of egg darkness and nest similarity for a cryptic parasite egg versus host's cognition: an alternate coevolutionary trajectory.

As a text-book example of coevolution, the escalating interactions between egg mimicry by parasitic cuckoos and egg recognition by their hosts constitute a key battlefield for parasitism and anti-parasitism strategies. However, some parasite-host systems have deviated from this coevolutionary trajectory because some cuckoos do not lay mimetic eggs, while the hosts do not recognize them, even under the high costs of parasitism. The cryptic egg hypothesis was proposed to explain this puzzle, but the evidence to date is mixed and the relationship between the two components of egg crypticity, egg darkness (dim egg coloration) and nest similarity (similarity to host nest appearance), remains unknown. Here, we developed a 'field psychophysics' experimental design to dissect these components while controlling for undesired confounding factors. Our results clearly show that both egg darkness and nest similarity of cryptic eggs affect recognition by hosts, and egg darkness plays a more influential role than nest similarity. This study provides unambiguous evidence to resolve the puzzle of absent mimicry and recognition in cuckoo-host systems and explains why some cuckoo eggs were more likely to evolve dim coloration rather than similarity to host eggs or host nests.

Egg rejection based on egg size recognition as a specific strategy against parasitic cuckoos.

In the coevolutionary interactions between avian brood parasites and their hosts, egg recognition based on color and/or pattern is a common and effective defense to counter parasitism. However, for egg recognition based on size, only a few studies have found affirmative results, and they do not provide unambiguous evidence that egg size recognition in hosts has evolved as an important and specific anti-parasite adaptation against parasite eggs. We studied the brood parasite system between the Asian emerald cuckoo Chrysococcyx maculatus and its host, the chestnut-crowned warbler Phylloscopus castaniceps. The cuckoo parasitizes the warbler using non-mimetic and larger eggs at a parasitism rate of 12.9%. The warbler nests used in this experiment were built in a dark environment with the nest illuminance near 0 lux. Experiments with 2 types of model eggs with colors and patterns resembling cuckoo eggs of different sizes (cuckoo egg size or host egg size) showed that the warblers were able to reject 63.6% of cuckoo model eggs under these dim light conditions. However, model eggs with the same color and pattern similar to the warbler egg size were always accepted. This study provides strong evidence supporting the theory that egg size recognition can be evolved in hosts as a specific anti-parasite adaptation against cuckoos. We suggest that the egg size recognition of the warbler is an outcome of the tradeoff between the costs of violating the parental investment rule and suffering cuckoo parasitism.

Illegal and Exploitative Sand-Digging Activities Could Be Managed to Create Suitable Nesting Habitats for Blue-Tailed Bee-Eaters (Merops philippinus).

The development of human society often interferes with wild animals and their natural habitats. Interference during resource exploitation is mostly negative; however, in some cases, it can be positive and even have significance for some species. In this study, we investigated the number of blue-tailed bee-eaters (Merops philippinus), a species under 'state protection category II' in China, between controlled and manipulated nesting habitats from 2017 to 2022. Our results indicated that commercial sand-digging activities, either illegal or approved, initially created suitable nesting habitats to attract blue-tailed bee-eaters but subsequently led to damage of nests or nesting habitats. However, sand digging can be modified by avoiding the breeding season to provide safe and suitable nesting habitats for bee-eaters. The number of breeding birds more than tripled when digging during the breeding season was avoided. We also found that conventional conservation strategies, which strictly prohibited sand-digging activities, did not contribute to the nesting habitats of bee-eaters. This study enriches the theories of conservation biology and emphasizes the importance of dialectical thinking regarding exploitative and seemingly destructive activities.

Egg Rejection and Nest Sanitation in an Island Population of Barn Swallows (Hirundo rustica): Probability, Response Latency, and Sex Effects.

Bird nests function as vessels for eggs and nestlings, and an environment for rearing offspring. However, foreign objects falling into bird nests and nestling eggshells may be harmful. Moreover, the smell of fecal sacs increases the risk of detection by predators. Many bird species have evolved nest sanitation to prevent damage to their nests. Furthermore, egg rejection evolved in some birds to thwart brood parasites that lay eggs in their nests. We studied 133 nests of barn swallows (Hirundo rustica) in an island population through a nest content manipulation experiment to determine nest sanitation and egg rejection behaviors and their relationship. Swallows rejected non-egg foreign objects more frequently (100% vs. 58.6%) and sooner than parasite eggs, which supports the hypothesis that nest sanitation is a pre-adaptation to egg rejection. However, nest sanitation did not increase egg rejection, either in probability or latency. Furthermore, both sexes incubated the eggs, cleaned the nests, and removed parasite eggs, implying that both are confronted with natural selection related to nest sanitation and brood parasitism. However, females invested more time in these behaviors than males. This provides evidence for the evolutionary relationship of nest sanitation and egg rejection behaviors in barn swallows.

Anti-Predation Responses to Conspecific versus Heterospecific Alarm Calls by the Nestlings of Two Sympatric Birds.

Predation is generally the main cause of bird mortality. Birds can use acoustic signals to increase their predation survival. Bird response to mobbing alarm calls is a form of anti-predation behavior. We used a playback technique and acoustic analysis to study the function of mobbing alarm calls in the parent-offspring communication of two sympatric birds, the vinous throated parrotbill (Sinosuthora webbianus) and oriental reed warbler (Acrocephalus orientalis). The chicks of these two species responded to conspecific and heterospecific mobbing alarm calls by suppressing their begging behavior. The mobbing alarm calls in these two species were similar. Mobbing alarm calls play an important role in parent-offspring communication, and chicks can eavesdrop on heterospecific alarm calls to increase their own survival. Eavesdropping behavior and the similarity of alarm call acoustics suggest that the evolution of alarm calls is conservative and favors sympatric birds that have coevolved to use the same calls to reduce predation risk.

Female Cuckoo Calls Deceive Their Hosts by Evoking Nest-Leaving Behavior: Variation under Different Levels of Parasitism.

The common cuckoo (Cuculus canorus) is an obligate brood parasite that has evolved a series of strategies to trick its hosts. The female cuckoo has been hypothesized to mimic the appearance and sounds of several raptors to deceive the hosts into exhibiting anti-predator behavior. Such behavior would relax the protection of the host nest and thus allow the female cuckoo to approach the host nest unopposed. Many anti-parasite strategies have been found to vary among geographical populations due to different parasitic pressures from cuckoos. However, the effect of female cuckoo calls related to different levels of parasitic pressure has not been examined. Here, we studied the effect of female cuckoo calls on the oriental reed warbler (Acrocephalus orientalis), one of the major hosts of the common cuckoo, in two geographical populations experiencing different levels of parasite pressure. Four kinds of sounds were played back to the hosts: the calls from female common cuckoos, male common cuckoos, sparrowhawks (Accipiter nisus), and oriental turtle doves (Streptopelia orientalis). The results showed that the female cuckoo calls induced the hosts to leave their nests more frequently than the male cuckoo or dove calls in both populations, and two populations of the hosts reacted similarly to the female cuckoo calls, implying that the function of female cuckoo calls would not be affected by the difference in parasitism rate. This study indicates that female cuckoo calls function to distract the hosts' attention from protecting their nests. However, we propose that such a deception by the female cuckoo call may not be due to the mimicry of sparrowhawk calls, but rather that the rapid cadence of the call that causes a sense of anxiety in the hosts.

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.

Parent-offspring and inter-offspring responses to conspecific versus heterospecific distress calls in 2 sympatric birds.

Distress calls, as a type of alarm call, play important roles in expressing bodily condition and conveying information concerning predation threats. In this study, we examined the communication via distress calls in parent-offspring and inter-offspring interactions. First, we used playback of chick distress calls of 2 sympatric breeders, the vinous-throated parrotbill Sinosuthora webbiana and the oriental reed warbler Acrocephalus orientalis, to the adults/chicks of these 2 species, respectively, and measured the responses of conspecifics or heterospecifics. The playback-to-chicks experiment showed that both species of chicks reduced the number of begging calls and begging duration time as a response to conspecific/heterospecific distress calls compared with natural begging and background noise controls. However, reed warbler chicks also reduced beak opening frequency in the response to conspecific distress calls compared with other playback stimuli. Second, the results of the playback-to-adults experiment showed that reed warbler adults could eavesdrop on distress calls of conspecific neighbors and sympatric heterospecifics. Furthermore, the nest-leaving behavior of reed warblers did not differ significantly when they heard the distress calls of conspecifics or parrotbills. Finally, reed warbler adults responded to heterospecific distress calls more quickly than to conspecific distress calls, and parrotbill adults presented the same response. Our results supported the warn-kin hypothesis and show that chick distress calls play an important role in conveying risk and the condition of chicks to enhance individual fitness. In addition, we also found that eavesdropping on distress calls is a congenital behavior that begins in the chick stage.

Coevolution between Himalayan cuckoos and 2 sympatric Pycnonotidae hosts.

Selection due to cuckoo parasitism is responsible for the evolution of anti-parasitism defenses in hosts. Different host species breeding sympatrically with a single parasitic cuckoo may evolve different strategies to reduce the risk of counter cuckoo parasitism, resulting in different interactions between cuckoos and hosts in areas of sympatry. Here, we studied the coevolutionary interactions between Himalayan cuckoos Cuculus saturatus and 2 sympatric and closely related potential hosts belonging to the family Pycnonotidae, the brown-breasted bulbul Pycnonotus xanthorrhous and the collared finchbill Spizixos semitorques. We investigated parasitism rates and nest-site selection (nest height, nest cover, human disturbance, perch height, forest distance, and degree of concealment) related to parasitism risk, nest defense against a cuckoo dummy, and egg rejection against cuckoo model eggs. Bulbuls used specific nest sites that were further away from forests than those of finchbills, and they behaved more aggressively toward cuckoos than finchbills. In contrast, bulbuls possessed moderate egg rejection ability, whereas the finchbill rejected 100% of cuckoo model eggs. We suggest that selection of a nest site away from forests by the bulbul explains the absence of parasitism by Himalayan cuckoos. We suggest that these interspecific differences in nest-site selection and nest defense indicate alternative responses to selection due to cuckoos.

Impact of nest sanitation behavior on hosts' egg rejection: an empirical study and meta-analyses.

Egg rejection in birds is a specific adaptation toward avian brood parasitism, whereas nest sanitation is a general behavior for cleaning the nest and avoiding predation. However, both behaviors refer to the action of ejecting objects out of the nest, and nest sanitation has been proposed as a pre-adaptation for egg rejection. Here, we tested the eliciting effect of nest sanitation on egg rejection in the red-whiskered bulbul Pycnonotus jocosus, a potential host species that are sympatric with parasitic cuckoos. We conducted meta-analyses of previous studies on both nest sanitation and egg rejection, in order to evaluate the consistency of our conclusions. Our results showed that nest sanitation did not elicit egg rejection in P. jocosus. The conclusions concerning such an eliciting effect from previous studies were mixed, whereas the methodologies were inconsistent, making the studies unsuitable for comparisons. However, the ejection frequency of nest sanitation was consistently higher than the frequency of egg rejection across different host species or populations. These results suggest that nest sanitation, which is an ancient behavior, is more fundamental than egg rejection, but the effect of the former on the latter is complex and needs further study. Standardized methodologies and the integration of behavior, physiology, and modeling may provide better opportunities to explore the relationship between nest sanitation and egg rejection.

Persistent fine-tuning of egg rejection based on parasitic timing in a cuckoo host even after relaxation of parasitism pressure.

Egg rejection is one of the most effective defenses to avoid avian brood parasites by hosts, and reflects avian cognition during parasite-host coevolution. However, egg rejection varies with different populations and species, or under different contexts. Here we studied the egg recognition behavior in a non-parasitized population of the red-whiskered bulbul (Pycnonotus jocosus), which has been recorded as a host of the banded bay cuckoo (Cacomantis sonneratii). By comparing its egg rejection frequency and latency between egg-laying and egg-incubation stages with a variety of nest ages, which represent different costs of cuckoo parasitism, the results show that the hosts rejected parasite eggs more frequently in the egg-laying stage than in the egg-incubation stage without a difference in latency, and accepted parasite eggs with an increase of nest age. These findings indicated that the hosts are able to adjust the intensity of their anti-parasitic responses according to the parasitic timing. A relaxation of parasitism risk and the tradeoff between parasitism risk and egg rejection cost may contribute to explaining our results.

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.

Spatial variation in egg polymorphism among cuckoo hosts across 4 continents.

Although egg color polymorphism has evolved as an effective defensive adaptation to brood parasitism, spatial variations in egg color polymorphism remain poorly characterized. Here, we investigated egg polymorphism in 647 host species (68 families and 231 genera) parasitized by 41 species of Old Word cuckoos (1 family and 11 genera) across Asia, Europe, Africa, and Australia. The diversity of parasitic cuckoos differs among continents, reflecting the continent-specific intensities of parasitic selection pressure on hosts. Therefore, host egg polymorphism is expected to evolve more frequently on continents with higher cuckoo diversity. We identified egg polymorphism in 24.1% of all host species and 47.6% of all host families. The common cuckoo Cuculus canorus utilized 184 hosts (28.4% of all host species). Hosts of the common cuckoo and of Chrysococcyx species were more likely to have polymorphic eggs than hosts parasitized by other cuckoos. Both the number of host species and the host families targeted by the cuckoo species were positively correlated with the frequency of host egg polymorphism. Most host species and most hosts exhibiting egg color polymorphism were located in Asia and Africa. Host egg polymorphism was observed less frequently in Australia and Europe. Our results also suggested that egg polymorphism tends to occur more frequently in hosts that are utilized by several cuckoo species or by generalist cuckoo species. We suggest that selection pressure on hosts from a given continent increases proportionally to the number of cuckoo species, and that this selection pressure may, in turn, favor the evolution of host egg polymorphism.

Sparrows use a medicinal herb to defend against parasites and increase offspring condition.

The incorporation of aromatic plants into nests by birds is suspected to constitute an example of preventative medicine use, whereby the phytochemical compounds within plants reduce infestation by parasites and increase offspring condition [1,2]. In China, russet sparrows (Passer cinnamomeus) incorporate wormwood (Artemisia verlotorum) leaves into their nests around the same time that local people hang wormwood from their doors as a traditional custom during the Dragon Boat Festival. The belief that this behaviour confers protection against ill health [3] is supported by the description of anti-parasite compounds in wormwood [4]. It has been suggested that the incorporation of fresh wormwood leaves into nests may serve a similar function for sparrows. Here we show that sparrows choose nest location and resupply established nests with fresh wormwood leaves using olfactory cues, that nests containing wormwood leaves have lower ectoparasite loads, and that nests with more wormwood leaves produce heavier chicks. Our results indicate that sparrows use wormwood as a preventative medicine to control ectoparasites and improve the body mass of their offspring.