Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand (original) (raw)
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Birds use eggshell UV reflectance when recognizing non-mimetic parasitic eggs
Brood parasitism generally has detrimental effect on host fitness. To avoid the negative consequences of brood parasitism, hosts have often evolved an effective counter-adaptation-recognition and rejection of parasitic eggs. Because eggshells of the Eurasian reed warbler (Acrocephalus scirpaceus) and its brood parasite, the common cuckoo (Cuculus canorus), differ significantly in their ultraviolet (UV) reflectance, one would expect that the ability of the hosts to see UV light will play an important role in recognition and rejection of parasitic eggs. To test this assumption, we performed 3 sets of experiments differing in the level of mimicry of the parasitic egg. In the first 2 experiments, we parasitized host nests by conspecific eggs (either own or from other females with perfect and good mimicry, respectively) coated either with a UV blocker (completely reducing UV reflectance of the eggshell) or with Vaseline as a control treatment. Although the UV blocker significantly decreased eggshell UV reflectance, hosts accepted most of these conspecific eggs and the type of coating did not significantly affect the probability of rejection. In the third experiment, we parasitized clutches with 2 types of non-mimetic eggs differing only in UV reflectance (UV− and UV+). We found that hosts rejected UV+ eggs at a significantly higher rate than UV− eggs, probably due to their lower mimicry in the UV spectrum. Here, we demonstrated that hosts use UV signals during egg recognition. Moreover, we suggest that such signals may play a more important role when the parasitic egg is non-mimetic rather than mimetic, when hosts can use additional cues, such as spotting pattern.
Visual discrimination of polymorphic nestlings in a cuckoo-host system
Scientific Reports, 2018
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. The interactions between brood parasites and their hosts are a classic example of a co-evolutionary process in which adaptation on one side leads to counter-adaptation on the other and so on 1. Phenotypic polymorphism is an example of such an adaption with an important role in the host-parasite co-evolutionary arms race 2. For example, European Cuckoo Cuculus canorus females have two alternative plumage phenotypes that can help evading detection by the host 3-5 , while polymorphism in egg appearance may allow hosts to escape brood parasitism 6,7. The evolution of successful host defences against brood parasitism, which involve the ability to detect and discriminate the brood parasite, is the fundamental driver in the arms race 1. Thus, cognitive and perceptual abilities of the host are essential in the evolution and maintenance of phenotypic variation in both the host and parasite 2. Variation in egg colour and pattern is an example of such defence strategy. In response to egg discrimination by hosts, brood parasites evolve egg mimicry 8-12 , which in turn favours the evolution of distinct egg signatures 13-15 or distinct polymorphism in host clutches 6,7,16,17. However, in a given host population, the success of such a defence strategy depends on phenotypic variation among clutches, which makes it difficult for the parasite to target a particular egg type, and on egg uniformity within clutches, which allows host parents to better discriminate a parasite against their own egg template 18-23. In some host-cuckoo systems the arms race has reached the nestling stage, and host parents discriminate parasite nestlings from their own 24-33 , which led to improved mimicry by cuckoo nestlings 34,35 (but see 36). In theory, the same mechanisms that determine egg polymorphism should also apply to nestling polymorphism 2 and a recent study showed that polymorphism does indeed occur at the nestling stage in a cuckoo-host system in New Caledonia 37. In this Pacific island, the local subspecies of the Fan-tailed Gerygone, Gerygone flavolateralis flavolateralis, is the exclusive host of the local subspecies of the Shining Bronze-cuckoo, Chalcites lucidus layardi. Mimicry by bronze-cuckoo nestlings is common in Chalcites-Gerygone systems 34,38 and it also occurs in New Caledonia 37. Despite the mimicry, two Australian Gerygone species 25,26 and the Fan-tailed Gerygone from New
Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host
Behavioral Ecology, 2013
Many hosts have evolved diverse cognitive mechanisms to recognize and reduce the cost of social parasitism. For example, great reed warblers Acrocephalus arundinaceus can accurately reject closely mimetic eggs of brood parasitic common cuckoos Cuculus canorus. Yet, these same hosts are less effective at identifying and rejecting parasitism when the clutch is parasitized by multiple cuckoo eggs, suggesting a role for discordancy (the rejection of the egg type in the minority of the clutch) and/or online self-referent phenotype matching (the simultaneous viewing of cuckoo and own eggs in the nest) to reject foreign eggs. We tested whether the presence of host's own eggs is required for the discrimination of foreign eggs by dyeing hosts' own eggs with one of several colors so that clutches contained (a) 1 dyed and 4 unmanipulated eggs, (b) 3 dyed and 2 unmanipulated eggs, or 5 eggs dyed either (c1) differently or (c2) similarly. Rejection rates of dyed eggs varied widely between different colors and were highest in treatment (a), with 1 dyed egg, compared with treatments with the majority (b) or all (c1 and c2) dyed eggs. However, relative rejection rates of dyed eggs were also consistent among specific colors across treatments, including (c1) and (c2), where no unmanipulated own eggs were available for viewing and irrespective of whether eggs were dyed all different colors (c1) or the same colors (c2). We conclude that these hosts can rely on comparisons of foreign egg colors against an internal recognition template of acceptable (own) egg phenotypes.
Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines
Journal of Comparative Physiology A, 2012
Ultraviolet (UV) light-transmitted signals play a major role in avian foraging and communication, subserving functional roles in feeding, mate choice, egg recognition, and nestling discrimination. Sequencing functionally relevant regions of the short wavelength sensitive type 1 (SWS1) opsin gene that is responsible for modulating the extent of SWS1 UV sensitivity in birds allows predictions to be made about the visual system's UV sensitivity in species where direct physiological or behavioral measures would be impractical or unethical. Here, we present SWS1 segment sequence data from representative species of three avian lineages for which visually based cues for foraging and communication have been investigated to varying extents. We also present a preliminary phylogenetic analysis and ancestral character state reconstructions of key spectral tuning sites along the SWS1 opsin based on our sequence data. The results suggest ubiquitous ultraviolet SWS1 sensitivity (UVS) in both paleognaths, including extinct moa (Emeidae), and parrots, including the nocturnal and flightless kakapo (Strigops habroptilus), and in most, but not all, songbird (oscine) lineages, and confirmed violet sensitivity (VS) in two suboscine families. Passerine hosts of avian brood parasites were included both UVS and VS taxa, but sensitivity did not co-vary with egg rejection behaviors. The results should stimulate future research into the functional parallels between the roles of visual signals and the genetic basis of visual sensitivity in birds and other taxa.
Proceedings of the Royal Society B: Biological Sciences, 2006
Owing to the conspicuousness of ultraviolet (UV) colour in dark environments, natural selection might have selected UV egg coloration because it would enhance egg detectability by parents in murky nests. Here, we tested this hypothesis by using comparative and experimental approaches. First, we studied variation in egg coloration of 98 species of European passerines measured using UV-visible reflectance spectrometry (300-700 nm) in relation to nesting habits. Analyses based on raw data and controlling for phylogenetic distances both at the species and the family levels revealed that hole-nester species produced eggs with higher UV reflectance than those nesting in open habitats. The experimental approach consisted of the manipulation of UV reflectance of the experimental eggs introduced outside the nest-cup of the hole-nester spotless starling Sturnus unicolor and the study of the retrieval of these eggs. Ultraviolet-reflecting eggs (controls) were more frequently retrieved to the nest-cup than nonreflecting (-UV) eggs. These results were not due to '-UV' eggs being recognized by starlings as parasitic because when a parasitic egg is detected, starlings removed it from the nest-box. Therefore, these results are consistent with the hypothesis that UV egg colours are designed to provide highly detectable targets for parent birds in dark nest environments.
Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo
Biological Journal of the Linnean Society, 2003
Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.
Experimental support for the use of egg uniformity in parasite egg discrimination by cuckoo hosts
Behavioral Ecology and Sociobiology, 2008
Common cuckoo (Cuculus canorus) parasitism drastically reduces the reproductive success of their hosts and selects for host discrimination of cuckoo eggs. In a second stage of anti-parasite adaptation, once cuckoos can lay eggs that mimic those of their hosts, a high uniformity of host egg appearance within a clutch may favour cuckoo egg discrimination. Comparative evidence provides indirect support for this hypothesis although experimental support is currently lacking. Here, we studied the effect of experimentally decreased uniformity of host egg appearance on cuckoo egg discrimination by great reed warbler (Acrocephalus arundinaceus) hosts in a population in which long-term cuckoo parasitism has led to high levels of cuckoo-host egg mimesis. We manipulated host clutch uniformity by adding extra spots to fresh host eggs just after they were laid. Rejection of non-mimetic experimental eggs added to these nests was compared with those in control nests in which uniformity was not altered. Previously, by over-painting real spots in a control group of nests, we showed a negligible effect of our paints on hosts' perception of their eggs. We show that for the great reed warbler, non-mimetic experimental eggs were relatively more tolerated in experimental nests, i.e. with lower uniformity (40%) than in control nests (5%). This is the first experimental study, to our knowledge, which demonstrates a reduced discrimination of foreign eggs as a consequence of an increase of egg phenotypes variation perception in a cuckoo host.