Synchronization of laying by great spotted cuckoos and recognition ability of magpies

Brood parasites rely entirely on the parental care of host species to raise the parasitic nestlings until independence. The reproductive success of avian brood parasites depends on finding host nests at a suitable stage (i.e. during egg laying) for parasitism and weakly defensive (i.e. non‐ejector) hosts. Finding appropriate nests for parasitism may, however, vary depending on ecological conditions, including parasite abundance in the area, which also varies from one year to another and therefore may influence coevolutionary relationships between brood parasites and their hosts. In this scenario, we explored: 1) the degree of laying synchronization between great spotted cuckoos Clamator glandarius and magpies Pica pica during two breeding seasons, which varied in the level of selection pressure due to brood parasitism (i.e. parasitism rate); 2) magpie responses to natural parasitism in the pre‐laying period and successfulness of parasitic eggs laid at this stage; and 3) magpie responses to experimental parasitism performed at different breeding stages. We found that, during the year of higher parasitism rate, there was an increase in the percentage of parasitic eggs laid before magpies started laying. However, the synchronization of laying was poor both years regardless of the differences in the parasitism rate. The ejection rate was significantly higher during the pre‐egg‐laying and the post‐hatching stages than during the laying stage, and hatching success of parasitic eggs laid during the pre‐egg‐laying stage was zero. Thus, non‐synchronized parasitic eggs are wasted and therefore poor synchronization should be penalized by natural selection. We discuss four different hypotheses explaining poor synchronization.     

Larval amphibian growth and development under varying density: are parasitized individuals poor competitors?

Population density and infection with parasites often are important factors affecting the growth and development of individuals. How these factors co-occur and interact in nature should have important consequences for individual fitness and higher-order phenomena, such as population dynamics of hosts and their interactions with other species. However, few studies have examined the joint effects of density and parasitism on host growth and development. We examined the co-influences of rearing density and parasitism, by the trematode Echinostoma trivolvis, on the growth and development of larval frogs, Rana (=Lithobates) pipiens. We also examined the potential role of parasite-mediated intraspecific competition by observing how unparasitized individuals performed when housed with other unparasitized tadpoles, versus housing with a combination of unparasitized and parasitized hosts. Mean mass and mean developmental stage were reduced under high rearing densities. The presence of parasitized conspecifics had no significant effect, but there was a significant interaction of density and parasitism presence on host mass, due to the fact that parasitized conspecifics grew poorly at high densities. Unparasitized individuals reared with parasitized and unparasitized conspecifics fared no better than unparasitized individuals reared only with one another. This result indicates that infected hosts compete as much as uninfected hosts for resources, even though infected individuals have reduced mass under high-density conditions. Resource acquisition and resource allocation are different processes, and parasitism, if it only affects the latter, might not have a discernible impact on competitive interactions.     

Parasitism in early life: environmental conditions shape within‐brood variation in responses to infection

Parasites play key ecological and evolutionary roles through the costs they impose on their host. In wild populations, the effect of parasitism is likely to vary considerably with environmental conditions, which may affect the availability of resources to hosts for defense. However, the interaction between parasitism and prevailing conditions is rarely quantified. In addition to environmental variation acting on hosts, individuals are likely to vary in their response to parasitism, and the combined effect of both may increase heterogeneity in host responses. Offspring hierarchies, established by parents in response to uncertain rearing conditions, may be an important source of variation between individuals. Here, we use experimental antiparasite treatment across 5 years of variable conditions to test how annual population productivity (a proxy for environmental conditions) and parasitism interact to affect growth and survival of different brood members in juvenile European shags (Phalacrocorax aristotelis). In control broods, last‐hatched chicks had more plastic growth rates, growing faster in more productive years. Older siblings grew at a similar rate in all years. Treatment removed the effect of environment on last‐hatched chicks, such that all siblings in treated broods grew at a similar rate across environmental conditions. There were no differences in nematode burden between years or siblings, suggesting that variation in responses arose from intrinsic differences between chicks. Whole‐brood growth rate was not affected by treatment, indicating that within‐brood differences were driven by a change in resource allocation between siblings rather than a change in overall parental provisioning. We show that gastrointestinal parasites can be a key component of offspring's developmental environment. Our results also demonstrate the value of considering prevailing conditions for our understanding of parasite effects on host life‐history traits. Establishing how environmental conditions shape responses to parasitism is important as environmental variability is predicted to increase.     

The effect of host developmental stage at parasitism on sex‐related size differentiation in a larval endoparasitoid

• 1 For their larval development, parasitoids depend on the quality and quantity of resources provided by a single host. Therefore, a close relationship is predicted between the size of the host at parasitism and the size of the emerging adult wasp. This relationship is less clear for koinobiont than for idiobiont parasitoids.
• 2 As size differentiation in host species exhibiting sexual size dimorphism (SSD) is likely to occur already during larval development, in koinobiont larval endoparasitoids the size of the emerging adult may also be constrained based on the sex of the host caterpillar.
• 3 Sex‐specific growth trajectories were compared in unparasitised Plutella xylostella caterpillars and in second and fourth instar hosts that were parasitised by the solitary larval koinobiont endoparasitoid Diadegma semiclausum. Both species exhibit SSD, where females are significantly larger than males.
• 4 Healthy female P. xylostella caterpillars developed significantly faster than their male conspecifics. Host regulation induced by D. semiclausum parasitism depended on the instar attacked. Parasitism in second‐instar caterpillars reduced growth compared to healthy unparasitised caterpillars, whereas parasitism in fourth‐instar caterpillars arrested development. The reduction in growth was most pronounced in hosts producing male D. semiclausum.
• 5 Parasitism itself had the largest impact on host growth. SSD in the parasitoid is mainly the result of differences in growth rate of the parasitoid–host complex producing male and female wasps and differences in exploitation of the host resources. Female wasps converted host biomass more efficiently into adult biomass than males.

     

Diadegma mollipla parasitizing Plutella xylostella: host instar preference and suitability

Oviposition decisions (i.e., host selection and sex allocation) of female parasitoids are expected to correspond with host quality, as their offspring fitness is dependent on the amount and quality of resources provided by a single host. The host size model assumes that host quality is a linear function of host size, with larger hosts believed to contain a greater quantity of resources, and thus be more profitable than smaller hosts. We tested this assertion in the laboratory on a solitary larval–pupal parasitoid Diadegma mollipla (Holmgren) (Hymenoptera: Ichneumonidae) developing on three instars (second–fourth) of one of its hosts, the diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). In a no‐choice test, parasitism levels and sex ratio (i.e., proportion of female progeny) were significantly high in hosts attacked in the second instar followed by third then fourth instars. However, the few parasitoids that completed a generation from the fourth instars did so significantly faster than conspecifics that started development in the other two instars. In direct observations, however, the parasitoids (i) randomly attacked the various host instars, (ii) spent a similar period examining the various host instars with their ovipositors, (iii) subdued all three host instars with about the same effort, and (iv) no statistical differences were observed in the attack rates on the three host instars. In a choice test, the females parasitized significantly more third instars followed by second then fourth instars. However, total parasitism in this experiment was 43% lower compared to parasitism of only second instars in the no‐choice test. No significant differences were detected in progeny sex ratios. In both choice and no‐choice tests, significantly more fourth instars died during the course of the experiments than second instars, while third instars were intermediate. The higher parasitism of third than second instars in the choice test indicates that the females perceived larger hosts as higher quality than smaller hosts, despite their lower suitability for larval development.     

Pre‐Patch Experience Affects the Egg Distribution Pattern in a Polyembryonic Parasitoid of Moth Egg Batches

According to foraging theory, female parasitoids should alter their host choice in response to cues that indicate a limitation of resources. We tested whether females of the polyembryonic parasitoid Ageniaspis fuscicollis (Hymenoptera: Encyrtidae), which attack egg batches of small ermine moths (Lepidoptera: Yponomeutidae), would alter their host acceptance pattern in response to different pre‐patch experience. We kept females of the parasitoid prior to a patch visit under different conditions, which should indicate different levels of competition for hosts. With increased competition as pre‐patch experience, females laid more eggs per host egg and self‐superparasitized more often, and the resultant egg distributions showed a trend from more regular distributions to increasingly Poisson and aggregated distributions. Consequently, females with a pre‐patch experience that would indicate low competition for hosts had the most even egg distributions. We conclude that pre‐patch experience of competitors may lead to a significant change of mutual interference patterns in egg‐laying A. fuscicollis wasps.     

Effects of Intraspecific Competition and Host-Parasitoid Developmental Timing on Foraging Behaviour of a Parasitoid Wasp

In a context where hosts are distributed in patches and susceptible to parasitism for a limited time, female parasitoids foraging for hosts might experience intraspecific competition. We investigated the effects of host and parasitoid developmental stage and intraspecific competition among foraging females on host-searching behaviour in the parasitoid wasp Hyposoter horticola. We found that H. horticola females have a pre-reproductive adult stage during which their eggs are not mature yet and they forage very little for hosts. The wasps foraged for hosts more once they were mature. Behavioural experiments showed that wasps’ foraging activity also increased as host eggs aged and became susceptible to parasitism, and as competition among foraging wasps increased.     

A koinobiont parasitoid mediates competition and generates additive mortality in healthy host populations

Insects are subject to attack from a range of natural enemies. Many natural enemies, such as parasitoids, do not immediately, or ever, kill their victims but they are nevertheless important in structuring biological communities. The lag that often occurs between attack and host death results in mixed populations of healthy and parasitised hosts. However, little is understood about how the effects of parasitism during this lag period affect the competitive ability of parasitised hosts and how this, in turn, affects the survival and dynamics of the surviving healthy host populations. Here we investigate the impact of the timing of introduction, and the strength of that introduction, of a parasitoid natural enemy Venturia canescens (Gravenhorst) on the outcome of intraspecific competition between larvae of the Indian meal moth, Plodia interpunctella (Hübner). In contrast to healthy hosts alone, we find reduced survival of healthy larvae with increasing periods of exposure to greater numbers of parasitised conspecifics. This represents indirect mortality of the host, which is in addition to that imposed by parasitism itself. Furthermore, longer periods of exposure to parasitised larvae resulted in an increase in development time of healthy individuals and they were larger when they emerged as adults. These results are relevant to both insect–parasitoid and insect–pathogen systems where there is a lag in host death following infection or attack.     

Host choice decisions in the polyembryonic wasp Copidosoma koehleri (Hymenoptera: Encyrtidae)

Female parasitoids often reject hosts of poor quality, where the survival and fitness of their offspring are expected to be low. In polyembryonic parasitoid wasps, a clone of genetically identical embryos develops from one egg in a host. In the wasp Copidosoma koehleri, each female clone produces one soldier larva that attacks competing clones inside the host. Aggression by soldiers is directed usually towards unrelated clones. Accordingly, it may be predicted that females will prefer nonparasitized over parasitized hosts, especially if the latter have been parasitized previously by a mated unrelated female, as a result of the reduced chances of survival for their offspring inside these hosts. In accordance with these predictions, females prefer nonparasitized hosts over self‐parasitized hosts when they are presented simultaneously. By contrast to the predictions, females prefer hosts parasitized by an unrelated conspecific over nonparasitized hosts when presented simultaneously. Females do not distinguish hosts parasitized by conspecifics from self‐parasitized hosts when presented simultaneously. They reject self‐parasitized hosts significantly more often than hosts parasitized by conspecifics when each host type is presented alone. Females faced with two previously parasitized hosts are not affected in their choice by the mating status (i.e. virgin or mated) of the previous parasitizing females. The combined results suggest that females are limited in their ability to assess the risk that their offspring will be attacked by a soldier, or that this risk is balanced by the relative advantages of ovipositing in a host parasitized by conspecifics. A possible advantage may be increased out‐breeding opportunities for the emerging offspring.     

Host nutritional status mediates degree of parasitoid virulence

Parasitic organisms rely on the resources of their hosts to obtain nutrients essential for growth and reproduction. Insect parasitoids constitute an extreme condition since they develop in a single host from which they typically consume all available resources. As a result, the host is killed following parasitism. However, a few intriguing cases of host survival have been reported wherein hosts resume foraging and may even reproduce following parasitoid emergence. Yet, the ultimate and proximate mechanisms responsible for host recovery remain unresolved. We tested the impact of host nutrition on host fate and parasitoid fitness, using the association between Dinocampus coccinellae and the spotted lady beetle Coleomegilla maculata. Under laboratory conditions, we fed parasitized ladybirds on different aphid diets, with or without pollen. In the field, we followed the fate of parasitized ladybirds during seasonal variations in pollen and aphid abundance. We found that ladybirds fed on aphids or a combination of aphids and pollen recovered more frequently from parasitism (from 65 to 81%) than those eating only pollen (48%). Field data suggest that the fate of parasitized ladybirds is also related to food availability. On the other hand, when hosts fed on a combination of aphids and pollen, consequences for parasitoid fitness were often ‘all‐or‐nothing’: parasitoid emergence rate was the lowest of all host nutrition regimes (～50%), but parasitoids that did emerge were larger than individuals emerging from other host nutrition regimes. Laboratory and field results concur to show that host nutritional status during parasitoid development significantly influences both host fate and parasitoid fitness.     

The Population Dynamics and Community Ecology of Root Hemiparasitic Plants

Root hemiparasitic plants and their host plants interact directly, through parasitism, as well as indirectly, through scramble competition for resources. To understand the population dynamics and community ecology of root hemiparasitic plants and their hosts, models of resource-based competition have been extended to include resource parasitism. Parasitism provides a mechanism for parasitic plants to overcome deficits in their ability to compete for soil resources. The interaction ranges from competitive to exploiter-victim, depending on whether the benefits of parasitism overshadow the costs of competition. These models predict that as productivity in the system increases, parasitic plants should become more abundant. In diverse host communities, differences in the impact that parasites have on their hosts and the benefits that they receive from parasitizing different hosts may lead to nontransitive competitive relationships and a sort of apparent competition. The possible dynamics include paper-rock-scissors oscillations and indirect mutualisms between parasitic plants and their hosts that allow them to form coalitions that can exclude competitive dominants.     

THE PARASITOID,Cotesia flavipes (CAMERON) (HYMENOPTERA: BRACONIDAE), INFLUENCES FOOD CONSUMPTION AND UTILIZATION BY LARVAL Diatraea saccharalis (F.) (LEPIDOPTERA: CRAMBIDAE)

Parasitoids exploit host insects for food and other resources; they alter host development and physiology to optimize conditions to favor parasitoid development. Parasitoids influence their hosts by injecting eggs, along with a variety of substances, including venoms, polydnaviruses, ovarian fluids, and other maternal factors, into hosts. These factors induce profound changes in hosts, such as behavior, metabolism, endocrine events, and immune defense. Because endoparasitoids develop and consume tissues from within their hosts, it is reasonable to suggest that internal parasitization would also influence host food consumption and metabolism. We report on the effects of parasitism by Cotesia flavipes on the food consumption and utilization of its host, Diatraea saccharalis. Cotesia flavipes reduces the host food consumption, but parasitized larvae considered a unit with their parasitoid's attained the same final weight as the nonparasitized larvae. Nutritional indices, midgut activities of carbohydrases, and trypsin of parasitized and nonparasitized D. saccharalis were assessed. Parasitized larvae had reduced relative food consumption, metabolic and growth rates, coupled with higher efficiency for conversion of the digested, but not ingested, food into body mass. Parasitism also affected food flux through the gut and protein contents in the midgut of parasitized larvae. The activity of α‐amylase and trehalase in parasitized host was enhanced in the first day after parasitism relative to control larvae. Saccharase activity remained unchanged during larval development. Trypsin activity was reduced from the fifth to ninth day after parasitism. We argue on the mechanisms involved in host food processing after parasitism.     

Growth strategies of passerine birds are related to brood parasitism by the brown-headed cowbird (Molothrus ater)

Sibling competition was proposed as an important selective agent in the evolution of growth and development. Brood parasitism by the brown-headed cowbird (Molothrus ater) intensifies sibling competition in the nests of its hosts by increasing host chick mortality and exposing them to a genetically unrelated nestmate. Intranest sibling competition for resources supplied by parents is size dependent. Thus, it should select for high development rates and short nestling periods, which would alleviate negative impacts of brood parasitic chicks on host young. I tested these predictions on 134 North American passerines by comparative analyses. After controlling for covariates and phylogeny, I showed that high parasitism rate was associated with higher nestling growth rate, lower mass at fledging, and shorter nestling periods. These effects were most pronounced in species in which sibling competition is most intense (i.e., weighing over about 30 g). When species were categorized as nonhosts versus old hosts (parasitized for thousands of years) versus new hosts (parasitized the last 100-200 years), there was a clear effect of this parasitism category on growth strategies. Nestling growth rate was the most evolutionarily flexible trait, followed by mass at fledging and nestling period duration. Adjustments during incubation (incubation period length, egg volume) were less pronounced and generally disappeared after controlling for phylogeny. I show that sibling competition caused by brood parasites can have strong effects on the evolution of host growth strategies and that the evolution of developmental traits can take place very rapidly. Human alteration of habitats causing spread of brood parasites to new areas thus cascades into affecting the evolution of life-history traits in host species.     

Great Spotted Cuckoos Frequently Lay Their Eggs While Their Magpie Host is Incubating

Species that suffer from brood parasitism face a considerable reduction in their fitness which selects for the evolution of host defences. To prevent parasitism, hosts can mob or attack brood parasites when they approach the host nest and block the access to the nest by sitting on the clutch. In turn, as a counter‐adaptation, brood parasites evolved secretive behaviours near their host nests. Here, we have studied great spotted cuckoo (Clamator glandarius) egg‐laying behaviour and defence by their magpie (Pica pica) hosts inside the nest using continuous video recordings. We have found several surprising results that contradict some general assumptions. The most important is that most (71%) of the parasitic events by cuckoo females are completed while the magpie females are incubating. By staying in the nest, magpies force cuckoo females to lay their egg facing the high risk of being attacked by the incubating magpie (attack occurred in all but one of the events, n = 15). During these attacks, magpies pecked the cuckoo violently, but could never effectively avoid parasitism. These novel observations expand the sequence of adaptations and counter‐adaptations in the arms race between brood parasites and their hosts during the pre‐laying and laying periods.     

Presence of conspecifics triggers host searching behavior in an egg parasitoid wasp

Parasitoids and predators compete for host or prey species. The efficiency of obtaining prey or host items is reduced by intraspecific competition. As the optimal search behavior depends on the intensity of competition, it is important for the parasitoid or predator to obtain information on this intensity. Previous studies have shown that parasitoids can obtain information regarding competition from encounters with already parasitized hosts. They then change their host searching behavior accordingly. However, whether parasitoids obtain the information directly from observing the presence of conspecifics remains unclear. We used Tiphodytes gerriphagus (Marchal) (Hymenoptera: Scelionidae), the solitary egg parasitoid of water striders, for testing the effect of density of conspecifics on host searching behavior. Females of T. gerriphagus dive into the water to search for hosts and sometimes they dive without hosts present. Thus, we investigated whether T. gerriphagus changed underwater activities in response to the density of conspecifics in the absence of hosts. Four densities (1, 2, 4, and 8 female T. gerriphagus) were investigated. Females in competitive situations (groups of 2, 4, and 8 females) displayed host searching behavior, but the solitary females did not. This indicates that the presence of conspecifics triggers host searching behavior and that T. gerriphagus females obtain information on competition directly from conspecifics and use it for modifying their behavior.     

Common Cuckoos Cuculus canorus change their nest‐searching strategy according to the number of available host nests

In recent decades, numerous studies have examined factors affecting risk of host nest parasitism in well‐known avian host–parasite systems; however, little attention has been paid to the role of host nest availability. In accordance with other studies, we found that nest visibility, reed density and timing of breeding predicted brood parasitism of Great Reed Warblers Acrocephalus arundinaceus by the Common Cuckoo Cuculus canorus. More interestingly, hosts had a greater chance of escaping brood parasitism if nesting was synchronized. Cuckoo nest searching was governed primarily by nest visibility at high host‐nest density. However, even well‐concealed nests were likely to be parasitized during periods when just a few hosts were laying eggs, suggesting that Cuckoos adjust their nest‐searching strategy in relation to the availability of host nests. Our results demonstrate that host vulnerability to brood parasitism varies temporally and that Cuckoo females are able to optimize their nest‐searching strategy. Moreover, our study indicated that Cuckoos always manage to find at least some nests to parasitize. Thus, in this case, the co‐evolutionary arms race should take place mainly in the form of parasitic egg rejection rather than via frontline pre‐parasitism defence.     

Bioenergetic theory predicts infection dynamics of human schistosomes in intermediate host snails across ecological gradients

Epidemiological dynamics depend on the traits of hosts and parasites, but hosts and parasites are heterogeneous entities that exist in dynamic environments. Resource availability is a particularly dynamic and potent environmental driver of within‐host infection dynamics (temporal patterns of growth, reproduction, parasite production and survival). We developed, parameterised and validated a model for resource‐explicit infection dynamics by incorporating a parasitism module into dynamic energy budget theory. The model mechanistically explained the dynamic multivariate responses of the human parasite Schistosoma mansoni and its intermediate host snail to variation in resources and host density. At the population level, feedbacks mediated by resource competition could create a unimodal relationship between snail density and human risk of exposure to schistosomes. Consequently, weak snail control could backfire if reductions in snail density release remaining hosts from resource competition. If resource competition is strong and relevant to schistosome production in nature, it could inform control strategies.     

Insights to host discrimination and host acceptance behaviour in a parasitoid (Diptera: Asilidae): Implications for fitness

The robber fly Mallophora ruficauda is one of the principal pests of apiculture in the Pampas region of Argentina. As adults they prey on honey bees and other insects, while as larvae they are solitary ectoparasitoids of third instar scarab beetle larvae. Females of M. ruficauda lay eggs away from the host in tall grasses. After being dispersed by the wind, larvae drop to the ground, where they dig in search of their hosts. It is known that second instar larvae of M. ruficauda exhibit active host searching behaviour towards its preferred host, third instar larva of Cyclocephala signaticollis. Although the means by which host location occurs has been studied and since superparasitism is a frequent scenario in the field, no information about host discrimination and host acceptance is available. We carried out studies in the field and behavioural experiments in the laboratory to determine if M. ruficauda is capable of quality host discrimination. We also studied if this parasitoid is capable of conspecific detection in order to avoid superparasitism. Finally, we analyzed the conditions under which superparasitism occurs in the field. We report here that the second instar larva of M. ruficauda is able to discriminate the parasitism status of the host by means of chemical cues, but is not capable of detecting conspecifics prior to attacking a host. We also found that the host cannot detect the presence of the parasitoid by means of chemical cues, so that no counter-defense against parasitism occurs. Furthermore, we determined that superparasitism occurs on the heavier hosts, i.e. those with more abundant resources which could harbor several parasitoid individuals. Finally, we discuss the possible implications of larval host location and host discrimination decisions on the fitness of this parasitoid.     

植物寄生对生态系统结构和功能的影响

寄生植物是生态系统中的特殊类群之一。植物寄生可以驱动生态系统中生物与非生物因子的变化,在生态系统结构与功能中起关键作用。寄生植物可以通过对寄主营养的集聚、改变凋落物的质量与数量、改变根的周转与分泌物格局、改变土壤水势,从而影响土壤理化特性。寄生植物会改变寄主的行为,改变寄主与非寄主植物之间的相互作用,从而影响植物群落的结构、多样性和动态,进而影响植被演替和植被生产力等。寄生植物与寄主均可被消费者取食,可直接或间接地影响生态系统的食草动物,包括草食昆虫等。寄生植物与寄主的其它寄生物存在竞争关系,可以直接或间接地影响寄主的其它寄生植物或病原真菌。寄生植物可以明显地改变土壤地球化学循环,将固有的不可动的成分转变为可利用的营养成分,改变土壤生物群落的结构与功能,从而显著影响地下生物群落。这些表明,植物寄生对生态系统的结构和功能有重要影响。针对特殊的被入侵的植物群落,该地寄生植物可以通过影响入侵植物寄主的生长、繁殖、生物量分配格局,改变土壤的理化特性,促进非寄主的非优势本地植物的生长,从而改变被入侵植物群落结构与多样性,达到生物防治及生态恢复的目的。