Cuckoo-host System Research Articles

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 mimicry and host selection by common cuckoos among four sympatric host species breeding within a reed habitat

AbstractIn the case of cuckoo parasitism, the maintenance of host specificity may be closely related to active host selection. In the reed wetlands of the Yongnian National Wetland Park, China, four host species of common cuckoos (Cuculus canorus) with similar nest structures breed sympatrically, namely, the Oriental reed warbler (Acrocephalus orientalis) (ORW), vinous-throated parrotbill (Sinosuthora webbiana) (VP), reed parrotbill (Paradoxornis heudei) (RP) and blunt-winged warbler (Acrocephalus concinens) (BW). Cuckoo parasitism rates on ORW (14.5%) and BW (18.2%) were found to be significantly higher than those on two species of parrotbills (RP 1.4% and VP 0%), and cuckoo eggs mimicked the size and coloration of ORW eggs significantly more closely than those of the eggs of the other three hosts. Egg recognition experiments revealed that the ability of ORW and VP to recognize nonmimetic eggs was significantly greater than that of BW and RP. Different life history strategies of the four hosts, including antiparasitic strategy, breeding time period and population density may partly explain the difference of parasitism in this multiple cuckoo-host system. Our study suggests that determining host life history traits and antiparasitic strategies are important for a better understanding of the specificity of host selection in common cuckoos.

Visual discrimination of polymorphic nestlings in a cuckoo-host system

Mimicry by avian brood parasites favours uniformity over variation within a breeding attempt as host defence against parasitism. In a cuckoo-host system from New Caledonia, the arms race resulted in both host (Gerygone flavolateralis) and parasite (Chalcites lucidus) having nestlings of two discrete skin colour phenotypes, bright and dark. In our study sites, host nestlings occurred in monomorphic and polymorphic broods, whereas cuckoo nestlings only occurred in the bright morph. Irrespective of their brood colour, host parents recognised and ejected parasite nestlings but never ejected their own. We investigated whether host parents visually recognised their own nestlings by using colour, luminance and pattern of multiple body regions. We found that the parasite mimicked multiple visual features of both host morphs and that the visual difference between host morphs was larger than the difference between the parasite and the mimicked host morph. Visual discrimination alone may result in higher chances of recognition errors in polymorphic than in monomorphic host broods. Host parents may rely on additional sensorial cues, not only visual, to assess nestling identity. Nestling polymorphism may be a trace of evolutionary past and may only have a marginal role in true-recognition of nestlings in the arms race in New Caledonia.

Egg shape mimicry in parasitic cuckoos.

Parasitic cuckoos lay their eggs in nests of host species. Rejection of cuckoo eggs by hosts has led to the evolution of egg mimicry by cuckoos, whereby their eggs mimic the colour and pattern of their host eggs to avoid egg recognition and rejection. There is also evidence of mimicry in egg size in some cuckoo-host systems, but currently it is unknown whether cuckoos can also mimic the egg shape of their hosts. In this study, we test whether there is evidence of mimicry in egg form (shape and size) in three species of Australian cuckoos: the fan-tailed cuckoo Cacomantis flabelliformis, which exploits dome nesting hosts, the brush cuckoo Cacomantis variolosus, which exploits both dome and cup nesting hosts, and the pallid cuckoo Cuculus pallidus, which exploits cup nesting hosts. We found evidence of size mimicry and, for the first time, evidence of egg shape mimicry in two Australian cuckoo species (pallid cuckoo and brush cuckoo). Moreover, cuckoo-host egg similarity was higher for hosts with open nests than for hosts with closed nests. This finding fits well with theory, as it has been suggested that hosts with closed nests have more difficulty recognizing parasitic eggs than open nests, have lower rejection rates and thus exert lower selection for mimicry in cuckoos. This is the first evidence of mimicry in egg shape in a cuckoo-host system, suggesting that mimicry at different levels (size, shape, colour pattern) is evolving in concert. We also confirm the existence of egg size mimicry in cuckoo-host systems.

Why do hosts with obvious egg polymorphism suffer low parasitism rates under avian brood parasitism? A theoretical consideration

Polymorphism is a general phenomenon in the natural world evolving as a result of frequency-dependent selection. Such polymorphism has recently received increasing attention in parasitic cuckoo-host systems, in which egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to investigate the effect of host egg polymorphism on the rate of successful parasitism (SPR) by cuckoos to help better understand the role of egg polymorphism in cuckoo-host systems. Five key conclusions can be drawn from these calculations: (1) The contrast of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the SPR of cuckoos; (2) hosts can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportion of the two morphs if cuckoos also evolve egg dimorphism as a counter-adaptation; (3) the escalation of egg polymorphism in hosts further reduces the SPR in cuckoos, although the efficiency of such an effect decreases with the number of host egg morphs; (4) cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs; and (5) an increase in the number of cuckoo egg morph does not increase the total SPR of cuckoos for parasitizing hosts with polymorphic eggs. Egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to show that the disruptive evolution of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the rate of successful parasitism by cuckoos (SPR). Hosts with obvious egg polymorphism suffer low parasitism rates and they can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportions of the two morphs if cuckoos also evolve egg dimorphism as a counteradaptation, whilst cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs. Egg polymorphism in hosts is regarded as a specific adaptation against cuckoo parasitism. Here, we provided a theoretical analysis to show that the disruptive evolution of egg phenotypes in hosts significantly reduces cuckoo fitness by reducing the rate of successful parasitism (SPR) by cuckoos. Hosts with obvious egg polymorphism suffer low parasitism rates and they can minimize the SPR of cuckoos by laying polymorphic eggs with equal proportions of the two morphs if cuckoos also evolve egg dimorphism as a counteradaptation, whilst cuckoos can maximize their SPR by laying a ratio of egg morphs equal to the ratio of host egg morphs.

Do common cuckoo chicks suffer nest predation more than host nestlings?

Nestlings of brood parasites exhibit more intensive begging than offspring of their hosts to gain sufficient amount of food or competitive advantage over host nestlings. This begging behaviour should be costly because exuberant acoustic begging may more likely attract nest predators. However, to date, nobody has explored the survival of nests with and without chicks of brood parasites in the common cuckoo (Cuculus canorus) host system. Here, we analysed an extensive dataset of 817 great reed warbler (Acrocephalus arundinaceus) and 788 reed warbler (Acrocephalus scirpaceus) nests to explore the relationships between nest predation and parasitism status (parasitized vs. non-parasitized), nest contents (cuckoo chick vs. host nestlings) and age of nestlings. We found that although parasitized nests had higher predation rate than non-parasitized nests in the incubation stage, the effect of original parasitism status almost disappeared in the nestling stage. In both host species, nests with younger cuckoo chicks survived similarly to nests with host nestlings of the same age (till the ninth day of age). Later on, however, nest contents influenced nest predation in each species differently. While nests with older cuckoo chicks (from the ninth to the 17th day of age) did not survive worse that host nestlings in the great reed warbler, older cuckoos survived much worse than host nestlings in reed warbler nests. Finally, nest survival decreased with nestling age in all three species. Thus, it seems that common cuckoo chicks can be penalized for more intensive begging only in nests of smaller reed warbler hosts. Parental feeding of young is in birds frequently accompanied by striking nestlings begging behaviour serving as a signal of their need. Brood parasites exhibit even more intense food solicitation than their hosts which may attract predators to the nest. However, this hypothesis has never been tested in a widely studied brood parasite species—the common cuckoo. Here, we analysed survival of more than 1600 nests of its two main host species. We found that nests containing older common cuckoo chicks were depredated more frequently than nests with host own nestlings only in the smaller reed warbler hosts but not in the larger and more aggressive great reed warblers. This shows that the intensity of begging could be costly in terms of nest predation at least in some common cuckoo host species.

Egg Polymorphism and Egg Discrimination in the Daurian RedstartPhoenicurus auroreus, a Host of the Common CuckooCuculus canorus

The evolution of egg polymorphism based on strong egg discrimination by hosts of brood parasites may be a specific adaptation against avian brood parasitism. However, different cuckoo-host systems with egg polymorphism may differ in many other aspects during coevolution. We studied the interaction between the Common Cuckoo Cuculus canorus and its host, the Daurian Redstart Phoenicurus auroreus, and detected that cuckoos use an intermediate degree of egg monomorphism to parasitize contrasting dimorphic eggs laid by redstarts. However, redstarts only possess an intermediate ability of egg recognition of dissimilar egg phenotypes with a high degree of recognition error and long latency to rejection. We discuss possible explanations for these observations and suggest that the intermediate degree of egg mimicry in the cuckoo and egg recognition in the redstart may constitute an early stage of disruptive coevolution in egg phenotypes between cuckoos and hosts. Alternatively, intermediate polymorphism may be maintained as a result of an evolutionary equilibrium between hosts and parasites.

Do common cuckoos (Cuculus canorus) possess an optimal laying behaviour to match their own egg phenotype to that of their Oriental reed warbler (Acrocephalus orientalis) hosts?

Received 20 June 2015; revised 6 August 2015; accepted for publication 7 August 2015Optimality theory suggests that parasitic cuckoos should evolve an optimal laying behaviour aiming to positivelyselect host nests in which the eggs match the phenotype of their own eggs, thus minimizing the rejection riskfrom hosts and, in turn, maximizing the cuckoos’ fitness. We tested this hypothesis by investigating cuckoo-eggmatching between parasitized and nonparasitized nests in a common cuckoo (Cuculus canorus) host, the Orientalreed warbler (Acrocephalus orientalis), by use of Vorobyev–Osorio and Nature-Pattern-Match models to quantifythe matching of egg colour and pattern from avian vision, respectively. The results of our study indicated thatcuckoo-egg matching in parasitized nests was no better than that in nonparasitized nests, and thus we found nosupport for the optimal laying hypothesis in cuckoos. The mixed conclusions from all previous studies, includingthe present study, may be explained by (1) the parallel coevolution in different cuckoo–host systems; (2) theinappropriate methodology; and (3) the deficiency of the assumption itself. We suggest that a better methodologyshould be developed to solve the puzzle of whether cuckoos choose to lay eggs matching those of the host. © 2015The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 00, 000–000.

Egg trait variation in a large hawk-cuckoo (Hierococcyx sparverioides) host population of Chinese babax (Babax lanceolatus).

Mutual interaction between brood parasites and their hosts is a well-known model system for studying host-parasite coevolution. Both parties have acted reciprocally, resembling an evolutionary arms race, in which adaptations and counter-adaptations have evolved as a result of host-parasite dynamics, such as the classical cuckoo-host system. Discrimination among parasite and cuckoo eggs and rejection of foreign eggs is regarded as an important anti-parasitism strategy. The Chinese babax (Babax lanceolatus) is a large hawk-cuckoo (Hierococcyx sparverioides) host distributed in southwest China. A previous study shows that the babax is an intermediate egg rejector, and most cuckoo eggs are accepted by the Chinese babax, although a small proportion of hosts reject cuckoo eggs. Interestingly, the large hawk-cuckoo lays non-mimetic eggs in contrast to the uniform blue eggs of babaxes. Because egg coloration is a critical cue used by host species in favor of the recognition of parasitic eggs by hosts, we used a spectrometer to quantify egg color variation to understand the differentiation in discrimination ability between the egg rejectors and acceptors. We found that the chroma of intra-clutch variation of babax eggs was more consistent in egg rejectors than in acceptors. However, no statistical significance was found in inter-clutch variation between these two types of hosts. Our results suggest that hosts lay eggs with a low level of intra-clutch variation without the necessity of a high level of inter-clutch variation simultaneously as predicted by the egg signature hypothesis. This study may further indicate that selection pressures from evolutionarily recent parasites can drive individual-based differences in an anti-parasitism strategy.

A method for year-round rearing of cuckoo bumblebees (Hymenoptera: Apoidea: Bombus subgenus Psithyrus)

Summary. The study of the social interactions between host bumblebees and their inquiline species requires rearing them. Here we provide a simple method for rearing of cuckoo bumblebees (Bombus subgenus Psithyrus) in the laboratory. Two bumblebee cuckoo-host systems are used: Bombus (Psithyrus) vestalis hosted by B. (Bombus) terrestris and B. (Psithyrus) sylvestris hosted by B. (Pyrobombus) pratorum. First, the invasion of the Psithyrus female is performed in species-specific host colonies containing approximately 10 young workers. On average, a parasitized colony of B. terrestris produced 90 ± 9 young males and 21 ± 3 young females of B. vestalis, whereas a parasitized colony of B. pratorum produced 16 ± 2 young males and 5 ± 1 young females of B. sylvestris. One week after emergence, Psithyrus virgin females are placed in a flight cage exposed to natural light, with Psithyrus males of other colonies. After successful mating, the females are isolated and overwintered in a cold room at 4°C for 2–4 months. This method enables a year-round and mass breeding of Psithyrus species to facilitate studies of these rare species.

Species identification of sympatric cuckoo nestlings in a multiple-cuckoo system, China

Interaction between a parasite and its host could lead to a co-evolutionary arms race. Cuckoo-host system is among the most studied of all brood parasite systems, but the cuckoos of Asia, on the other hand, are much less well known. China has the most abundant cuckoo species in Asia. Many of these co-occur in sympatric areas, posing a potential risk of mis-identification of cuckoo nestlings, especially in <i>Cuculus</i> species. In this study we have provided a practical criterion to identify cuckoo nestlings species in the field and performed molecular phylogeny to confirm our empirical results. These results indicate that two distinct characteristics of cuckoo nestlings, i.e., the gape color pattern and feather traits can be considered as reliable species identification. To our knowledge, this is the first report for species identification of Cuculus nestlings through molecular analysis.

Are cuckoos maximizing egg mimicry by selecting host individuals with better matching egg phenotypes?

BackgroundAvian brood parasites and their hosts are involved in complex offence-defense coevolutionary arms races. The most common pair of reciprocal adaptations in these systems is egg discrimination by hosts and egg mimicry by parasites. As mimicry improves, more advanced host adaptations evolve such as decreased intra- and increased interclutch variation in egg appearance to facilitate detection of parasitic eggs. As interclutch variation increases, parasites able to choose hosts matching best their own egg phenotype should be selected, but this requires that parasites know their own egg phenotype and select host nests correspondingly.Methodology/Principal FindingsWe compared egg mimicry of common cuckoo Cuculus canorus eggs in naturally parasitized marsh warbler Acrocephalus palustris nests and their nearest unparasitized conspecific neighbors having similar laying dates and nest-site characteristics. Modeling of avian vision and image analyses revealed no evidence that cuckoos parasitize nests where their eggs better match the host eggs. Cuckoo eggs were as good mimics, in terms of background and spot color, background luminance, spotting pattern and egg size, of host eggs in the nests actually exploited as those in the neighboring unparasitized nests.Conclusions/SignificanceWe reviewed the evidence for brood parasites selecting better-matching host egg phenotypes from several relevant studies and argue that such selection probably cannot exist in host-parasite systems where host interclutch variation is continuous and overall low or moderate. To date there is also no evidence that parasites prefer certain egg phenotypes in systems where it should be most advantageous, i.e., when both hosts and parasites lay polymorphic eggs. Hence, the existence of an ability to select host nests to maximize mimicry by brood parasites appears unlikely, but this possibility should be further explored in cuckoo-host systems where the host has evolved discrete egg phenotypes.

Evicting cuckoo nestlings from the nest: a new anti-parasitism behaviour

As avian brood parasitism usually reduces hosts' reproductive success, hosts often exhibit strong defence mechanisms. While such host defences at the egg stage (especially egg rejection) have been extensively studied, defence mechanisms at the nestling stage have been reported only recently. We found a previously unknown anti-parasitism behaviour in the large-billed Gerygone, which is a host species of the little bronze-cuckoo, a host-evicting brood parasite. The hosts forcibly pulled resisting nestlings out of their nests and dumped them. Although it has been suggested that defence mechanisms at the nestling stage may evolve when host defence at the egg stage is evaded by the parasite, the studied host seems to lack an anti-parasitism strategy at the egg stage. This suggests that the evolutionary pathway may be quite different from those of previously studied cuckoo-host systems. Future research on this unique system may give us new insights into the evolution of avian brood parasitism.