Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism

Parasites may, in multi-parasite systems, block the defenses of their hosts and thus thwart host recognition of parasites by frequency-dependent selection. Nest defenses as frontline may block or promote the subsequent stage of defenses such as egg recognition. We conducted comparative studies of the defensive strategies of a host of the Oriental cuckoo Cuculus optatus, the yellow-bellied prinia Prinia flaviventris, in mainland China with multiple species of cuckoos and in Taiwan with a single cuckoo species. Cuckoo hosts did not exhibit aggression toward cuckoos in the presence of multiple cuckoo species but showed strong aggressive defenses of hosts directed toward cuckoos in Taiwan. Furthermore, the cuckoo host in populations with a single cuckoo species was able to distinguish adults of its brood parasite, the Oriental cuckoo, from adult common cuckoos (Cuculus canorus). This represents the first case in which a cuckoo host has been shown to specifically distinguish Oriental cuckoo, from other Cuculus species. Hosts ejected eggs at a higher rate in a single cuckoo species system than in a multi-species cuckoo system, which supports the strategy facilitation hypothesis. Granularity analysis of variation in egg phenotype based on avian vision modeling supported the egg signature hypothesis in hosts because Taiwanese prinias increased consistency in the appearance of their eggs within individual hosts thus favoring efficient discrimination against cuckoo eggs. This study significantly improves our knowledge of intraspecific variation in antiparasitism behavior of hosts between single- and multi-cuckoo systems.     

First evidence of regular common cuckoo, <Emphasis Type="Italic">Cuculus canorus</Emphasis>, parasitism on eastern olivaceous warblers, <Emphasis Type="Italic">Hippolais pallida elaeica</Emphasis>

Coevolution is defined as specialized relationships between species that lead to a reciprocal evolutionary change. A particularly suitable model system for studying coevolution is the interactions between obligate avian brood parasites and their hosts. The common cuckoo (Cuculus canorus, hereafter cuckoo) is a well-known brood parasite, which utilizes a range of smaller passerines as hosts. However, warblers of the genus Hippolais have rarely been reported as being victims of cuckoos, and furthermore, few data exist on the occurrence of antiparasite defenses in these hosts. In this study, we examined possible host–parasite coevolution between cuckoos and eastern olivaceous warblers (Hippolais pallida elaeica, hereafter olivaceous warblers) in three closely situated areas in northwestern Bulgaria. The olivaceous warbler has never been reported to be a regular cuckoo host. However, the present study, carried out in 2001–2003 shows that the olivaceous warbler is regularly and heavily parasitized by the cuckoo in this area. Parasitism rate was high (26.6%, 34/128) and consistent among years, with some variation between areas. The cuckoo egg mimicry was moderately good, and olivaceous warbler rejection rate of such eggs was 50%. Cuckoo eggs laid in olivaceous warbler nests had a whitish to whitish-green ground color, and the majority appeared to be distinctly different from cuckoo eggs found in other host species in the area. The olivaceous warbler proved to be a rather good host for cuckoos as 20.6% (7/34) of cuckoo eggs laid produced fledglings, a breeding success comparable to other suitable hosts in Europe. This is the first in-depth study of brood parasitism in a warbler of the genus Hippolais, and cuckoos parasitizing olivaceous warblers probably represent a previously unknown gens.     

Host genotype and age have no effect on rejection of parasitic eggs

Egg rejection belongs to a widely used host tactic to prevent the costs incurred by avian brood parasitism. However, the genetic basis of this behaviour and the effect of host age on the probability of rejecting the parasitic egg remain largely unknown. Here, we used a set of 15 polymorphic microsatellite loci, including a previously detected candidate locus (Ase64), to link genotypes of female great reed warblers (Acrocephalus arundinaceus), a known rejecter, with their egg rejection responses in two host populations. We also tested whether host female age, as a measure of the experience with own eggs, plays a role in rejection of common cuckoo (Cuculus canorus) eggs. We failed to find any consistent association of egg rejection responses with host female genotypes or age. It seems that host decisions on egg rejection show high levels of phenotypic plasticity and are likely to depend on the spatiotemporal variation in the parasitism pressure. Future studies exploring the repeatability of host responses towards parasitic eggs and the role of host individual experience with parasitic eggs would greatly improve our understanding of the variations in host behaviours considering the persistence of brood parasitism in host populations with rejecter phenotypes.     

Does contrast between eggshell ground and spot coloration affect egg rejection?

Obligate avian brood parasitic species impose the costs of incubating foreign eggs and raising young upon their unrelated hosts. The most common host defence is the rejection of parasitic eggs from the nest. Both egg colours and spot patterns influence egg rejection decisions in many host species, yet no studies have explicitly examined the role of variation in spot coloration. We studied the American robin Turdus migratorius, a blue-green unspotted egg-laying host of the brown-headed cowbird Molothrus ater, a brood parasite that lays non-mimetic spotted eggs. We examined host responses to model eggs with variable spot coloration against a constant robin-mimetic ground colour to identify patterns of rejection associated with perceived contrast between spot and ground colours. By using avian visual modelling, we found that robins were more likely to reject eggs whose spots had greater chromatic (hue) but not achromatic (brightness) contrast. Therefore, egg rejection decision rules in the American robin may depend on the colour contrast between parasite eggshell spot and host ground coloration. Our study also suggests that egg recognition in relation to spot coloration, like ground colour recognition, is tuned to the natural variation of avian eggshell spot colours but not to unnatural spot colours.     

Parental conflict and blue egg coloration in a seabird

When both parents provide offspring care, equal sharing of costly parental duties may enhance reproductive success. This is crucial for longlived species, where increased parental effort in current reproduction profoundly affects future reproduction. Indication of reproductive value or willingness to invest in reproduction may promote matching responses by mates, thus reducing the conflict over care. In birds with biparental care, blue-green eggshell color may function as a signal of reproductive value that affects parental effort, as predicted by the signaling hypothesis of blue-green eggshell coloration. However, this hypothesis has not been explored during incubation, when the potential stimulus of egg color is present, and has been little studied in longlived birds. We experimentally studied if egg color affected incubation patterns in the blue-footed booby, a longlived species with biparental care and blue eggs. We exchanged fresh eggs between nests of the same laying date and recorded parental incubation effort on the following 4 days. Although egg color did not affect male effort, original eggshell color was correlated with pair matching in incubation. Exchanged eggshell color did not affect incubation patterns. This suggests that biliverdin-based egg coloration reflects female quality features that are associated with pair incubation effort or that blue-footed boobies mate assortatively high-quality pairs incubating more colorful clutches. An intriguing possibility is that egg coloration facilitates an equal sharing of incubation, the signal being functional only during a short period close to laying. Results also suggest that indication of reproductive value reduces the conflict over care.     

Effects of maternal diet and host quality on oviposition patterns and offspring performance in a seed beetle (Coleoptera: Bruchidae)

In seed beetles, oviposition decisions may influence the offspring phenotype because eggs constitute the initial resources available for larval development. We tested the effects of host quality variations (small vs. large seeds of the host plant Calystegia sepium, Convolvulaceae) on oviposition patterns and offspring performance of the seed beetle Megacerus eulophus. We also manipulated the maternal diet: high diet quality vs. low diet quality to evaluate possible interactive effects of the maternal nutritional environment and host quality on oviposition patterns. We further assessed the consequences of egg size variation in offspring size. Female M. eulophus fed with high-quality diet (H-diet) laid more eggs and lived longer than females fed with low-quality diet (P-diet). Fecundity decreased under a low-quality host for both maternal diets. The occurrence of maternal environmental effects on egg size plasticity was detected. Under conditions of low-quality host, mothers fed with the high-quality diet produced bigger eggs in comparison with a high-quality host, whereas females fed with the low-quality diet produced smaller ones. Regardless of these differences observed in egg size depending on the maternal diet, progeny emerging from small seeds (low-quality host) showed a similar performance at emergence. Offspring traits were only significantly affected by host quality. Beetles emerging from large seeds had greater body weight and length than those reared on small seeds. Variations in oviposition patterns in response to host quality are discussed.     

Aphid egg protection by ants: a novel aspect of the mutualism between the tree-feeding aphid Stomaphis hirukawai and its attendant ant Lasius productus

Aphids often form mutualistic associations with ants, in which the aphids provide the ants with honeydew and the ants defend the aphids from predators. In this paper, we report aphid egg protection by ants as a novel aspect of the deeply interdependent relationship between a tree-feeding aphid and its attendant ant. The ant Lasius productus harbours oviparous females, males, and eggs of the hinoki cypress-feeding aphid Stomaphis hirukawai in its nests in winter. We investigated the behaviour of ants kept with aphid eggs in petri dishes to examine whether the ants recognise the aphid eggs and tend them or only provide a refuge for the aphids. Workers carried almost all of the aphid eggs into the nest within 24 h. The ants indiscriminately tended aphid eggs collected from their own colonies and those from other ant colonies. The ants cleaned the eggs and piled them up in the nest, and egg tending by ants dramatically increased aphid egg survival rates. Starving the ants showed no significant effect on aphid egg survivorship. Without ants, aphid eggs were rapidly killed by fungi. These results suggested that grooming by the ants protected the aphid eggs, at least, against pathogenic fungi. This hygienic service afforded by the ants seems indispensable for egg survival of these aphids in an environment rich in potentially pathogenic microorganisms.Electronic supplementary material  Supplementary material is available for this article at and is accessible for authorized users.     

Decision rules for egg recognition are related to functional roles and chemical cues in the queenless ant Dinoponera quadriceps

The capacity to distinguish colony members from strangers is a key component in social life. In social insects, this extends to the brood and involves discrimination of queen eggs. Chemical substances communicate colony affiliation for both adults and brood; thus, in theory, all colony members should be able to recognize fellow nestmates. In this study, we investigate the ability of Dinoponera quadriceps workers to discriminate nestmate and non-nestmate eggs based on cuticular hydrocarbon composition. We analyzed whether cuticular hydrocarbons present on the eggs provide cues of discrimination. The results show that egg recognition in D. quadriceps is related to both age and the functional role of workers. Brood care workers were able to distinguish nestmate from non-nestmate eggs, while callow and forager workers were unable to do so. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A Myanmar amber cockroach with protruding feces contains pollen and a rich microcenosis

Several hypotheses have been proposed to explain the mechanisms responsible for maintenance of host-specific gentes in the common cuckoo (Cuculus canorus). Some of them expect that when adult cuckoos return to lay their eggs to their natal site (natal philopatry hypothesis) or habitat in which they were reared (habitat-imprinting hypothesis), there is a higher probability of finding nests of the host species by which they were reared. Since published evidence is ambiguous, we here evaluate the natal philopatry and habitat-imprinting hypotheses using information on habitat homogeneity and cross-continental long-term ringing data. We found no evidence for the natal philopatry hypothesis—instead of returning to their natal site, juvenile cuckoos exhibited longer dispersal movements than adults, and the difference was even larger in comparison with a wide array of cuckoo host species. On the contrary, we found support for the habitat-imprinting hypothesis—juvenile cuckoos followed similar levels of natal habitat homogeneity at 5- and 25-km scale when returning to breed in the next years. Our results suggest that preference for the particular habitat structures may help cuckoos to find appropriate hosts.

     

Foraging scent marks of bumblebees: footprint cues rather than pheromone signals

In their natural habitat foraging bumblebees refuse to land on and probe flowers that have been recently visited (and depleted) by themselves, conspecifics or other bees, which increases their overall rate of nectar intake. This avoidance is often based on recognition of scent marks deposited by previous visitors. While the term 'scent mark' implies active labelling, it is an open question whether the repellent chemicals are pheromones actively and specifically released during flower visits, or mere footprints deposited unspecifically wherever bees walk. To distinguish between the two possibilities, we presented worker bumblebees (Bombus terrestris) with three types of feeders in a laboratory experiment: unvisited control feeders, passive feeders with a corolla that the bee had walked over on its way from the nest (with unspecific footprints), and active feeders, which the bee had just visited and depleted, but which were immediately refilled with sugar-water (potentially with specific scent marks). Bumblebees rejected both active and passive feeders more frequently than unvisited controls. The rate of rejection of passive feeders was only slightly lower than that of active feeders, and this difference vanished completely when passive corollas were walked over repeatedly on the way from the nest. Thus, mere footprints were sufficient to emulate the repellent effect of an actual feeder visit. In confirmation, glass slides on which bumblebees had walked on near the nest entrance accumulated hydrocarbons (alkanes and alkenes, C23 to C31), which had previously been shown to elicit repellency in flower choice experiments. We conclude that repellent scent marks are mere footprints, which foraging bees avoid when they encounter them in a foraging context.     

Pre- and post-hatch trophic egg production in the subsocial burrower bug, Canthophorus niveimarginatus (Heteroptera: Cydnidae)

In recent years, three terrestrial bugs, Adomerus triguttulus and Sehirus cinctus (Cydnidae) and the closely related Parastrachia japonensis (Parastrachiidae), have been the focus of several fascinating studies because of the remarkable, extensive parental care they were found to display. This care includes egg and nymph guarding, production of trophic eggs, unfertilized, low cost eggs that are used as food by newly hatched nymphs, and progressive provisioning of the host seed. In this study, we have investigated yet a third related Asian cydnid, Canthophorus niveimarginatus, with regard to the possible occurrence of some or all of these complex traits in order to assess how widespread these maternal investment patterns are in this group of insects and to better understand the implications of their manifestations from an evolutionary context. Manipulative experiments were carried out in the lab to determine whether females provision nests. Observational and egg removal studies were carried out to determine whether trophic eggs are produced, and, if they are, their possible impact on nymphal success. The findings revealed that C. niveimarginatus does, in fact, progressively provision young, and this species also displays all of the other behaviors associated with extended parental care in subsocial insects. Moreover, unlike the other two related species, which place trophic eggs on the surface of the original egg mass, C. niveimarginatus produces both pre- and post-hatch trophic eggs. Nymphs deprived of access to post-hatch trophic eggs had significantly lower body weight and survival rate than those that fed on them. To our knowledge, this is the first time the production of both pre- and post-hatch trophic eggs has been demonstrated in insects outside the Hymenoptera. In this paper, we qualitatively and quantitatively demonstrate the provisioning behavior and patterns of trophic egg production in C. niveimarginatus. When and how trophic eggs are produced and delivered to young should have important correlations with the ecological and life history constraints under which a species has evolved. Thus, we also discuss the possible ecological and life history factors that favor the evolution of post-hatch trophic eggs.     

An absence of aggression between non-nestmates in the bull ant <Emphasis Type="Italic">Myrmecia nigriceps</Emphasis>

The ability of social insects to discriminate against non-nestmates is vital for maintaining colony integrity, and in most social insect species, individuals act aggressively towards non-nestmates that intrude into their nest. Our experimental field data revealed that intra-colony aggression in the primitive bulldog ant Myrmecia nigriceps is negligible; our series of bioassays revealed no significant difference in the occurrence of aggression in trials involving workers from the same, a close (less than 300 m) or a far (more than 1.5 km) nest. Further, non-nestmate intruders were able to enter the nest in 60% of our trials; a similar level was observed in trials involving nestmates. These results suggest that workers of M. nigriceps are either unable to recognize alien conspecifics or that the costs of ignoring workers from foreign colonies are sufficiently low to favor low levels of inter-colony aggression in this species.     

Reassessing the role of the honeybee (Apis mellifera) Dufour's gland in egg marking

Dufour's gland secretion may allow worker honeybees to discriminate between queen-laid and worker-laid eggs. To investigate this, we combined the chemical analysis of individually treated eggs with an egg removal bioassay. We partitioned queen Dufour's gland into hydrocarbon and ester fractions. The bioassay showed that worker-laid eggs treated with either whole gland extract, ester fraction or synthetic gland esters were removed more slowly than untreated worker-laid eggs. However, the effect only lasted up to 20 h. Worker-laid eggs treated with the hydrocarbon fraction were removed at the same rate as untreated eggs. The amount of ester which reduced the egg removal rate was far higher than that naturally found on queen-laid or worker-laid eggs, and at natural ester levels no effect was found. Our results indicate that esters or hydrocarbons probably do not function as the signal by which eggs can be discriminated.     

Keeping eggs warm: thermal and developmental advantages for parasitic cuckoos of laying unusually thick-shelled eggs

Obligate brood parasites have evolved unusually thick-shelled eggs, which are hypothesized to possess a variety of functions such as resistance to puncture ejection by their hosts. In this study, we tested the hypothesis that obligate brood parasites lay unusually thick-shelled eggs to retain more heat for the developing embryo and thus contribute to early hatching of parasite eggs. By doing so, we used an infrared thermal imaging system as a non-invasive method to quantify the temperature of eggshells of common cuckoos (Cuculus canorus) and their Oriental reed warbler (Acrocephalus orientalis) hosts in an experiment that artificially altered the duration of incubation. Our results showed that cuckoo eggshells had higher temperature than host eggs during incubation, but also less fluctuations in temperature during incubation disturbance. Therefore, there was a thermal and hence a developmental advantage for brood parasitic cuckoos of laying thick-shelled eggs, providing another possible explanation for the unusually thick-shelled eggs of obligate brood parasites and earlier hatching of cuckoo eggs compared to those of the host.     

Kin recognition and cannibalistic behaviours by adult male fathead minnows (<Emphasis Type="Italic">Pimephales promelas</Emphasis>)

Parental care is an energetically demanding activity that ensures genes are efficiently passed from one generation to the next. According to evolutionary theory, the greatest energetic investment should be directed towards offspring that are most closely related to the parent. Male fathead minnows, Pimephales promelas, provide this parental investment to developing embryos but not newly hatched larvae. Therefore, selection should favour recognition of embryonic kin to ensure energetic expenditure is optimally invested. In this study, adult male fathead minnows were tested using behavioural assays, with egg cannibalism as an endpoint, to determine whether adult males could discriminate between related and unrelated embryos. Egg cannibalism was highest when adult male fathead minnows were presented with unrelated eggs and lowest when presented with eggs fertilized by the test subject (related eggs). The degree of cannibalism was also a function of breeding status. Unrelated males in breeding condition showed an intermediate response between the low cannibalism demonstrated by related males and the high cannibalism demonstrated by unrelated males in a nonbreeding condition. These results suggest that although male fathead minnows can discriminate between unrelated and related embryos, at least some component of parental investment is a simple function of breeding status.     

“Winter” aggregations, colony cycle, and seasonal phenotypic change in the paper wasp Polistes versicolor in subtropical Brazil

Social wasps from temperate zones have clear annual colony cycles, and the young queens hibernate during winter. In the subtropics, the only previously reported evidence for the existence of “hibernation” is the facultative winter aggregations of females during harsh climate conditions. As in temperate-zone species analyzed so far, we show in this study that in the paper wasp, Polistes versicolor, a subtropical species, body size increases as an unfavorable season approaches. Our morphological studies indicate that larger females come from winter aggregations—that is, they are new queens. Multivariate analyses indicate that size is the only variable analyzed that shows a relationship to the differences. Given the absence of a harsh climate, we suggest that the occurrence of winter aggregations in tropical P. versicolor functions to allow some females to wait for better environmental conditions to start a new nest, rather than all being obliged to start a new nest as soon as they emerge.     

Recognition of foreign oviposition-marking pheromone in a multi-trophic context

Both phytophagous and parasitic insects deposit oviposition-marking pheromones (OMPs) following oviposition that function to inform conspecifics of a previously utilized host of reduced suitability. The blueberry maggot fly, Rhagoletis mendax Curran (Diptera: Tephritidae), deposits eggs individually into blueberries and then marks the fruit surface with an OMP which reduces acceptance of fruit for oviposition by conspecifics. Diachasma alloeum (Muesebeck) (Hymenoptera: Braconidae) is a parasitic wasp attacking larval R. mendax which also deposits an OMP, signaling conspecifics of a wasp-occupied host. Behavioral studies were conducted testing the hypothesis that the OMP of the parasitic wasp modifies the oviposition behavior of its host fly. In this study, we show that the OMP of D. alloeum is recognized by R. mendax, and female flies will reject wasp-marked fruit for oviposition. Thus, we present a rare demonstration of pheromonal recognition between animals occupying different taxonomic orders and trophic levels. This chemical eavesdropping may enhance the ability of the fly to avoid fruit unsuitable for larval development.     

Moorhens have an internal representation of their own eggs

How do birds recognize their own eggs? Do they have a stored template for their own egg characteristics, or do they use another mechanism? Intraspecific brood parasitism is considered to be an additional reproductive tactic where females can increase their own reproductive success. Because of the costs involved in rearing young that are not their own, it will pay females to detect and reject the eggs of a parasite, although it is not known how they do this. Here, we show experimentally that moorhens will cease laying in a nest when their first egg is replaced with another hen’s egg but not when it is replaced with their own egg taken from an earlier clutch. This provides good evidence that birds have an internal representation of their own eggs and use this in decisions about whether to reject foreign eggs.     

Alternative mating behaviors of the queen polymorphic ant <Emphasis Type="Italic">Temnothorax longispinosus</Emphasis>

Mating behaviors of ants fall into two categories: female calling, in which a female alate releases pheromones that attract males, and male swarming, in which large male aggregations attract females. Female calling is common in species with queens that return to their natal nest to found colonies dependently after mating, while male swarming is common in species with queens that disperse to found independently. In some species that display both founding strategies, a queen-size polymorphism has evolved in which dependent-founding queens are smaller than independent-founding queens. Dependent founding is likely difficult if gynes (virgin queens) are mating in distant swarms. Therefore, a queen may adopt one or the other mating strategy based on its size and founding behavior. We investigated mating behaviors in the queen-polymorphic ant, Temnothorax longispinosus. Observations in laboratory mating arenas indicated that small gynes exhibited significantly lower flight activity than large gynes. Both forms mated in male swarms, and neither form exhibited female calling. The reduced flight activity of the small morph may facilitate returning to the natal nest after mating, provided the mating swarm is located nearby. Therefore, alternative colony-founding behaviors may be possible without the evolution of female-calling behavior; however, the reduced flight activity of small morphs may require that mating swarms are not distant from the natal nest.     

Mechanical defence in seeds to avoid predation by a granivorous ant

Harvester ants have traditionally been considered as seed predators that negatively affect plants. In some cases, however, they can also act as positive seed dispersers. During field observations, we noted that a portion of Psoralea bituminosa seeds that were collected and carried to the nest by the granivorous harvester ant Messor barbarus were discarded intact in refuse piles outside the nest. We analyzed and compared the physical characteristics of size, mass and toughness in P. bituminosa seeds from two different origins: intact seeds found in the ant's refuse piles and seeds collected directly from the plants. Seeds from refuse piles were similar in width but lighter and tougher than seeds from the plant. Our results point to a mechanical defence based on seed toughness to avoid predation by M. barbarus and suggest that an elevated proportion (~69%) of the seeds produced by P. bituminosa could be too tough to be consumed by this ant. These transported but uneaten seeds could benefit by being moved far from the mother plant and this could act as a selective evolutionary pressure towards tough seeds.