Egg ejection cost can limit defence strategies against brood parasitism

A cost associated with the evolution of antiparasite strategies is the failure to recognize parasitic eggs, leading the host to evict its own eggs. However, there is evidence that birds recognize their own eggs through imprinting. This leads to the question of why birds accept parasitic eggs if such eggs can be identified. Here, we tested whether egg ejection per se can be costly due to increased predation risk to the remaining clutch and whether olfactory or visual cues of egg ejection increase predation. We carried out three field experiments to answer the following questions: (a) Does ejecting an egg increase nest predation risk? (b) Does the presence of olfactory cues, such as the smell of a broken egg, increase nest predation risk? And (c) Does the presence of visual cues, such as an egg shell below the nest, increase nest predation risk? We found evidence that egg ejection increases nest predation and that olfactory cues alone also increase nest predation. The presence of visual cues did not change predation rates. These data indicate that egg ejection is costly for both host and parasitic eggs that may remain in the nest. Our results suggest why host and parasite eggs are commonly found within the same nests, despite the possibility that hosts recognize and could possibly eject the parasite’s egg.     

Brood parasitism selects for no defence in a cuckoo host

In coevolutionary arms races, like between cuckoos and their hosts, it is easy to understand why the host is under selection favouring anti-parasitism behaviour, such as egg rejection, which can lead to parasites evolving remarkable adaptations to ‘trick’ their host, such as mimetic eggs. But what about cases where the cuckoo egg is not mimetic and where the host does not act against it? Classically, such apparently non-adaptive behaviour is put down to evolutionary lag: given enough time, egg mimicry and parasite avoidance strategies will evolve. An alternative is that absence of egg mimicry and of anti-parasite behaviour is stable. Such stability is at first sight highly paradoxical. I show, using both field and experimental data to parametrize a simulation model, that the absence of defence behaviour by Cape bulbuls (Pycnonotus capensis) against parasitic eggs of the Jacobin cuckoo (Clamator jacobinus) is optimal behaviour. The cuckoo has evolved massive eggs (double the size of bulbul eggs) with thick shells, making it very hard or impossible for the host to eject the cuckoo egg. The host could still avoid brood parasitism by nest desertion. However, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg, a strategy aided by the fact that many cuckoo eggs are incorrectly timed, so do not hatch in time and hence do not reduce host fitness to zero. Selection will therefore prevent the continuation of any coevolutionary arms race. Non-mimetic eggs and absence of defence strategies against cuckoo eggs will be the stable, if at first sight paradoxical, result.     

Escape from parasitism: spatial and temporal strategies of a sphecid wasp against a specialised cuckoo wasp

Parasites and parasitoids exert an important selection pressure on organisms and, thus, play an important role for both population dynamics and evolutionary responses of host species. We investigated host-parasite interactions in a brood-caring wasp, the European beewolf, Philanthus triangulum (Hymenoptera, Sphecidae), and asked whether females of this species might employ temporal or spatial strategies to reduce the rate of attack by a specialised brood parasitoid, the cuckoo wasp Hedychrum rutilans (Hymenoptera, Chrysididae). Females of the host species might shift their activity to periods of low parasitoid activity both in the course of the season and in the course of the day. On a spatial scale, aggregated or dispersed nesting might be favoured depending on the form of the density dependence of parasitism. The beginning and end of the flight season of host and parasitoid were nearly identical. Activity of chrysidids relative to beewolves did not change significantly during the flight season. However, relative parasitoid activity declined in the course of the day, suggesting the existence of temporal enemy-free space in the evening hours. Shifting the main activity to the evening hours might be a flexible response of beewolves to the presence of chrysidids. Activity of cuckoo wasps per nest was independent of nest density but the actual rate of parasitism as revealed by nest excavations indicated direct density dependence. Total mortality, however, was inversely density dependent. Thus, in the study population aggregated nesting did not reduce parasitism but minimised total mortality.     

The evolution of cuckoo parasitism: a comparative analysis

Cuckoos (family Cuculidae) show the highest diversity of breeding strategies within one bird family (parental care, facultative and obligate brood parasites). We used independent contrasts from two phylogenies to examine how this variation was related to 13 ecological and life-history variables. The ancestral state was probably tropical, resident, forest cuckoos with parental care. The evolution of brood parasitism was correlated with a shift to more open habitats, a change in diet, increases in species breeding-range size and migration, and a decrease in egg size. Once parasitism had evolved, more elaborate parasitic strategies (more harmful to host fitness) were correlated with decreased egg size, a change in diet, increased breeding-range size and migration, a shortened breeding season and a decrease in local abundance. Establishing the most probable evolutionary pathways, using the method of Pagel, shows that changes in ecological variables (such as migration, range size and diet type) preceded the evolution of brood parasitism, which is likely to be a later adaptation to reduce the cost of reproduction. By contrast, brood parasitism evolved before changes in egg size occurred, indicating that egg size is an adaptive trait in host--parasite coevolution. Our results suggest that the evolution of cuckoo brood parasitism reflects selection from both ecological pressures and host defences.     

Fluctuation of body temperature and cuckoo brood parasitism

Body temperatures of 11 bird species, including cuckoos, were measured in an artificial meteorological room. Ratios of change in body temperature to that in air temperature were thereby obtained for each species. Cuckoos demonstrate a remarkably high value, indicating a particularly low ability to regulate body temperature. Viewed in this light, the cuckoo's parasitic behavior is very likely an adaptation to overcome a physiological disadvantage. This in turn might be expected to reinforce delay in evolution of temperature homeostasis.     

Diet specialization and brood parasitism in cuckoo species

1. Brood parasitism is a breeding strategy adopted by many species of cuckoos across the world. This breeding strategy influences the evolution of life histories of brood parasite species.
2. In this study, we tested whether the degree on diet specialization is related to the breeding strategy in cuckoo species, by comparing brood parasite and nonparasite species. We measured the gradient of diet specialization of cuckoos, by calculating the Gini coefficient, an index of inequality, on the multiple traits describing the diet of species. The Gini coefficient is a measure of statistical dispersion on a scale between 0 and 1, reflecting a gradient from low to high specialization, respectively. First, we tested the strength of the phylogenetic signal of diet specialization index among cuckoo species worldwide. Then, we ran phylogenetic generalized least square (PGLS) models to compare diet specialization, distribution range, and body mass of parasitic and nonparasitic cuckoo species, considering the phylogenetic signal of data.
3. After adjusting for the phylogenetic signal of the data and considering both, species distribution range and species body mass, brood parasitic cuckoos were characterized by higher diet specialization than nonbrood parasitic species. Brood parasitic species were also characterized by a larger breeding distribution range than nonparasitic species.
4. The findings of this study provide an additional understanding of the cuckoos’ ecology, relating diet and breeding strategies, information that could be important in conservation ecology.

     

Sex-specific defence behaviour against brood parasitism in a host with female-only incubation

Nest protection against intruders is an indispensable component of avian parental care. In species with biparental care, both mates should evolve nest defence behaviour to increase their reproductive success. In most host-parasite systems, host females are predicted to have more important roles in nest defence against brood parasites, because they typically are primarily responsible for clutch incubation. Male antiparasitic behaviour, on the other hand, is often underestimated or even not considered at all. Here we investigated sex-specific roles in four aspects of great reed warbler (Acrocephalus arundinaceus) nest defence against a brood parasite—the cuckoo (Cuculus canorus), namely (1) mobbing, (2) nest attendance/guarding, (3) nest checking and (4) egg ejection. Using dummy experiments, simulating brood parasitism and by video-monitoring of host nests we found that males took the key roles in cuckoo mobbing and nest guarding, while females were responsible for nest checking and egg ejection behaviours. Such partitioning of parental roles may provide a comprehensive clutch protection against brood parasitism.     

Common cuckoo Cuculus canorus parasitism,antiparasite defence and gene flow in closely located populations of great reed warblers Acrocephalus arundinaceus

In Hungary an unusually high rate of parasitism on the great reed warbler Acrocephalus arundinaceus by the common cuckoo Cuculus canorus has been maintained for at least the last one hundred years. We evaluated parasitism rate, antiparasite defence and genetic differentiation among Hungarian great reed warblers at three sites located 40–130 km from each other, where hosts suffered from a high (41–68%), moderate (11%), and almost no (<1%) parasitism. We were especially interested in whether the level of antiparasite defence was related to the local parasitism rate, and, if not, to understand why. There was no difference among the three sites in the responses to experimental parasitism by non‐mimetic model cuckoo eggs (rejection rate 71–82%), which can be explained by strong gene flow between populations: there was low level of philopatry and no genetic differentiation in the region. Reproductive success of the host in the heavily parasitised site was about 54% of that in the unparasitised site, indicating that long‐term persistence of host populations in highly exploited areas depends on continuous immigration.     

Host density predicts presence of cuckoo parasitism in reed warblers

In some hosts of avian brood parasites, several populations apparently escape parasitism, while others are parasitized. Many migratory specialist brood parasites like common cuckoos, Cuculus canorus , experience a short breeding season, and in order to maintain local parasite populations host densities should be sufficiently high to allow efficient nest search. However, no studies have investigated the possible effect of host density on presence of cuckoo parasitism among populations of a single host species. Here, we investigated possible predictors of common cuckoo parasitism in 16 populations of reed warblers, Acrocephalus scirpaceus , across Europe. In more detail, we quantified the effect of host density, number of host breeding pairs, habitat type, mean distance to nearest cuckoo vantage point, predation rate and latitude on the presence of cuckoo parasitism while controlling for geographical distance among study populations. Host density was a powerful predictor of parasitism. We also found a less pronounced effect of habitat type on occurrence of parasitism, while the other variables did not explain why cuckoos utilize some reed warbler populations and not others. This is the first study focusing on patterns of common cuckoo-host interactions within a specific host species on a large geographic scale. The results indicate that if host density is below a specific threshold, cuckoo parasitism is absent regardless of the state of other potentially confounding variables.     

Brood parasitism of an open-water spawning cichlid by the cuckoo catfish

The cuckoo catfish Synodontis multipunctatus and S. grandiops are endemic to Lake Tanganyika and the only known nonavian vertebrates that exhibit obligate interspecific brood parasitism. Seven maternal mouth-brooding cichlid fish species are reported to be natural hosts of the parasitic catfish and share a common reproductive behaviour that the catfish exploits: cichlid females spawn eggs on the bottom, allowing the catfish female to place her eggs near the cichlid eggs, and the cichlid females collect the catfish eggs by mouth together with their own eggs. However, so far it has not been reported that the cuckoo catfish exploit different spawning behaviours. The genus Cyprichromis consists of five maternal mouth-brooding species endemic to Lake Tanganyika, most of which spawn and collect eggs in open water. This study reports that the cuckoo catfish also parasitizes the open-water spawning Cyprichromis coloratus, although it may not be a regular host.     

Mycobacterial survival strategies in the phagosome: defence against host stresses

Infections with Mycobacterium tuberculosis remain a major cause of disease and death in humans. Among the factors that contribute to M. tuberculosis 's success as a pathogen is its ability to withstand potentially bactericidal host defences and to resist elimination by an activated immune system. This resistance to killing by the host is in part due to the low permeability of the mycobacterial cell envelope for many toxic molecules. In addition, it depends upon the detoxification of reactive oxygen and reactive nitrogen molecules produced by the host, the repair of the damage these molecules cause and maintenance of a neutral intrabacterial pH within acidic environments. The latter three mechanisms are the focus of this review.     

Geographic variation in parasitism rates of two sympatric cuckoo hosts in China

Rates of brood parasitism vary extensively among host species and populations of a single host species. In this study, we documented and compared parasitism rates of two sympatric hosts, the Oriental Reed Warbler (Acrocephalus orientalis) and the Reed Parrotbill (Paradoxornis heudei), in three populations in China. We found that the Common Cuckoo (Cuculus canorus) is the only parasite using both the Oriental Reed Warbler and Reed Parrotbill as hosts, with a parasitism rate of 22.4%-34.3% and 0%-4.6%, respectively. The multiple parasitism rates were positively correlated with local parasitism rates across three geographic populations of Oriental Reed Warbler, which implies that higher pressure of parasitism lead to higher multiple parasitism rate. Furthermore, only one phenotype of cuckoo eggs was found in the nests of these two host species. Our results lead to two conclusions: (1) The Oriental Reed Warbler should be considered the major host of Common Cuckoo in our study sites; and (2) obligate parasitism on Oriental Reed Warbler by Common Cuckoo is specialized but flexible to some extent, i.e., using Reed Parrotbill as a secondary host. Further studies focusing on egg recognition and rejection behaviour of these two host species should be conducted to test our predictions.     

Reduced parasitism by retaliatory cuckoos selects for hosts that rear cuckoo nestlings

We present a model to investigate why some bird species rearthe nestlings of brood parasites in spite of suffering largereductions in their own immediate fitness. Of particular interestis the case in which hosts rear only the parasite's young, allof their own offspring having been ejected or destroyed by theparasite. We investigate the conditions for the evolution ofretaliation by brood parasites against hosts that eject theiryoung, as well as the evolution of nonejection by hosts. Retaliationby cuckoos can evolve, despite potentially benefiting otherbrood parasites, if rates of ejection by hosts are neither toohigh nor too low, and if depredated nests are reparasitizedat a high rate by the depredating cuckoo. The presence of aretaliatory cuckoo then eases the conditions for the evolutionof hosts to accept and rear cuckoo offspring. A key conditionfavoring the evolution of non-ejection is that nonejectors enjoylower rates of parasitism in later clutches compared to ejectors.This requires that cuckoos reparasitize the clutches of ejectorsat relatively high rates and that nonejectors can rear a clutchof their own following the rearing of a cuckoo nestling. Ifthese conditions are not met, it pays hosts to eject cuckoonestlings even if the cuckoo retaliates. The model can explainwhy nonejection is relatively easy to evolve in cases in whichthe host young are reared alongside those of the cuckoo, suchas in cowbirds, and shows how hosts can resist invasion by parasiticcuckoos. The model predicts that retaliatory brood parasitessuch as the cuckoo have good memory for the location and statusof nests in their territory. Hosts of retaliatory cuckoos whosenestlings destroy the host clutch are predicted to have longbreeding seasons or the ability to attempt more than one clutchper season. Our model of retaliation may have wider applicationsto host-parasite relationships, virulence, and immunity.     

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.     

Alternative strategies in fungal race-specific parasitism

Summary Based on the gene-for-gene relation in race-specific resistance versus virulence, racial complexity of a pathogen population can be revealed by using host lines each with a single gene for resistance as detector. Such inventories of cereal rusts have shown: i. Genes for virulence may have pleiotropic effects acting on general fitness and their relative prevalence. ii. Genes for virulence are, as most other genes, dependent on genetic background for their general fitness. iii. Specific and general gene erosion in a pathogen population submitted to the assortative function of a race-specific host selection pressure is proportional to the degree of existing recombination and thus ultimately upon mode of reproduction (sexual or asexual). iv. Genetic storage capacity is dependent on ploidy constitution. v. Host alternation for safe annual survival favours a genetic system able to store temporarily unnecessary genes for virulence. — Due to shifting circumstances, pathogens like rusts will even inside the same forma specialis show different strategies. The trend may lead to a process of stabilizing selection and dependence on immediate and provisional flexibility just as typical of true haploids. It may lead to a pattern of preparedness: i.e. accumulation of unnecessary genes for virulence. In the latter case, the modern concept of gene diversification in breeding for disease resistance is less effective. In the former case, gene accumulation can also work.     

Active defence of herbivorous hosts against parasitism: Adult parasitoid mortality risk involved in attacking a concealed stemboring host

Phytophagous insects have several defence strategies to defend themselves against attack by parasitic wasps. Larval lepidopteran hosts can defend themselves actively to prevent oviposition by the parasitoid. Among the aggressive kinds of behaviour exhibited by hosts against parasitoids are violent wriggling, biting and spitting. The behaviour of the braconid parasitoid Cotesia sesamiae attacking stemboring larvae inside their feeding tunnel in the plant stem was investigated in maize and sugarcane stem pieces and transparent artificial tunnels. Attacking a defending stemborer host inside the confined space of a tunnel was shown to be risky for the female parasitoid. A considerable proportion (25%) of female wasps were killed in their attempt to attack the spitting and biting host. No difference was found in the behaviour of C. sesamiae attacking the suitable host Sesamia calamistis or the unsuitable host Eldana saccharina. The consequences of this high mortality risk involved in each host attack is discussed in relation to the ecology of the parasitoid.     

Host plant quality and defence against parasitoids: no relationship between levels of parasitism and a geometrid defoliator immunoassay

Host plant quality has a major influence on the performance, and ultimately on the fitness of an herbivorous insect, but may also have indirect effects on the third trophic level by affecting an herbivore's defensive ability against natural enemies. In a three-year field study, we examined the effects of natural food quality on the ability of autumnal moths, Epirrita autumnata (Lepidoptera, Geometridae), to defend themselves against parasitoids. In each year, we confirmed the variation in quality of host trees (mountain birch, Betula pubescens ssp. czerepanovii ) by determining the mass of pupae reared in mesh bags attached to the trees and the water content of leaves. Individuals grown on high quality trees possessed significantly higher encapsulation rate of a foreign antigen as pupae compared to those on low quality trees during the first and third study years; a parallel trend was also found in the second study year, although this difference was not statistically significant. However, in spite of observed differences in encapsulation rates, individuals reared on high and low quality trees did not differ in their levels of parasitisation when exposed to hymenopteran parasioids in the wild and thus were equally vulnerable. Accordingly, the encapsulation response seems not to play a major role on the population ecology scale in the studied system. Our findings also stress the importance of direct resistance tests, which should be conducted along with tests of insect immune function.     

Host‐specific parasitism in the Central American striped cuckoo,Tapera naevia

Coevolutionary theories of brood parasite strategy and host defense have been informed by research on egg mimicry and host recognition. However, there is no information on the strategies of New World parasitic cuckoos and their hosts. The striped cuckoo Tapera naevia is a New World cuckoo that uses multiple host species and maintains an egg color polymorphism. To investigate if color‐matching influenced rejection behavior in hosts, I conducted an egg rejection experiment on a host that lays blue‐green eggs, the rufous‐and‐white wren Thryophilus rufalbus and a host that lays white eggs, the plain wren Cantorchilus modestus. I used spectrophotometric analysis of egg color to determine the degree of egg color‐matching. I found that at the field site the striped cuckoo lays highly mimetic eggs for the rufous‐and‐white wren, in both color and brightness. The rufous‐and‐white wren was more likely to accept mimetic artificial eggs than non‐mimetic eggs. The plain wren exhibited low rejection rates for both mimetic and non‐mimetic artificial eggs. The evidence from this study indicates that the striped cuckoo lays eggs that are closely color‐matched to those of its preferred host, the rufous‐and‐white wren, and that this mimicry improves acceptance.     

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.