Optimal time allocation in parasitic wasps searching for hosts and food

Many species of parasitic wasp feed on sugar sources such as nectar and honeydew in order to replenish their energy reserves and so extend their life expectancy, which is often correlated with higher reproductive success. Recent research suggests that carbohydrates are also a key component in flight fuel in such insects. The importance of sugar in fuelling locomotion suggests location of sugar-rich food may be more important in parasitoid foraging behaviour than has previously been assumed. If sugar sources and hosts are separated in space, parasitoids have to allocate their time between sugar-searching and host-searching. Using a stochastic dynamic programming model we predict optimal time allocation decisions of parasitoids. Although the model was parameterized using data for Cotesia rubecula , the sensitivity analysis shows that the model predictions are applicable to many parasitoid wasp species. The key prediction of the model is that parasitoids should always search for food if energy reserves drop to low levels, even if the probability of finding food and the average food reward are small. This is in stark contrast to an alternative model proposed by Sirot and Bernstein (1996) which suggests parasitoids should never search for food if food availability is low.     

Host-feeding and oviposition by parasitoids on hosts of different fitness value: Influences of egg load and encounter rate

A dynamic optimization model is presented for the decision to host feed or oviposit on hosts by female parasitoids. Optimal host utilization decisions are compared between two host types with different fitness payoffs for oviposition. The model predicts that hosts of higher fitness value should always be used for oviposition unless the egg load approaches zero. This general prediction is not influenced by levels of host availability or metabolic reserves, the age of the parasitoid, or the magnitude of the fitness difference. An egg-load threshold is predicted above which lower value hosts should be used for oviposition and below which they are used for host feeding. The position of this egg-load threshold is higher when the difference in fitness between host types is larger. The threshold is also higher when overall host availability is high or metabolic reserves for the production of new eggs are low. The threshold for oviposition on low-value hosts decreases to zero near the end of the parasitoid’s life. Under conditions where high-value hosts are rarely encountered compared to low-value hosts, the model predicts that lower value hosts should be accepted for oviposition at a lower egg-load threshold.     

Host‐searching responses to herbivory‐associated chemical information and patch use depend on mating status of female solitary parasitoid wasps

1. In a tritrophic interaction system consisting of plants, herbivores, and their parasitoids, chemicals released from plants after herbivory are known to play important roles for many female parasitoids to find their hosts efficiently. On the plant side, chemical information associated with herbivory can act as an indirect defence by attracting the natural enemies of the host herbivores. 2. However, mated and virgin females of haplodiploid parasitoids might not necessarily respond to such chemical cues in the same way. Since virgin females can produce only sons, they might refrain from searching for hosts to invest eggs until copulation, in order to produce both sexes. 3. Here, we investigated differential host‐searching behaviours shown by mated and virgin females in the solitary parasitoid wasp, Cotesia vestalis, in response to herbivory‐associated chemical information from cruciferous plants infested by their host larvae, Plutella xylostella. 4. Mated females showed a significantly higher flight preference for host‐infested plants over intact plants, while no preference was observed with virgin females. Mated females also showed more intensive antennal searching and ovipositor probing behaviours to leaf squares with wounds caused by hosts than did virgin females. Furthermore, mated females stayed longer in host patches with higher parasitism rates than virgin females. 5. These results indicate that mating status of C. vestalis females clearly influences their host‐searching behaviour in response to herbivory‐associated chemical information and patch exploitation. Female parasitoids seem to forage for hosts depending on their own physiological condition in a tritrophic system.     

寄生蜂寻找隐蔽性寄主害虫的行为机制

林木蛀干类害虫具有高度的隐蔽性,是林业上的一类重要害虫,也是目前世界上最难防治的害虫类群之一.寄生蜂在与寄主长期的协同进化过程中,形成了搜索、发现和攻击寄主害虫的独特机制,能够有效地找到并寄生它们.总结了寄生性天敌寻找、发现并成功定位隐蔽性寄主害虫的行为学机制.寄生蜂可以利用来自嗅觉的化学信息物质(如寄主、寄主粪便、虫道共生菌的挥发性气味)、寄主成虫的化学通讯物质、来自视觉的植物表面色差信息、来自触觉的寄主保护物性状特征、来自寄主取食和运动所产生的介质振动信号以及来自寄主活动和代谢的红外辐射等多种途径有效地发现隐蔽性害虫的位置,从而完成寄生行为.有些寄生蜂还能综合利用来源不同的多种信息,从而提高寄主定位的可靠性和准确性.本文还对寄生蜂寻找寄主的这些线索在生物防治上可能的利用途径和前景进行了讨论.这对促进我国在该领域的研究,充分利用天敌昆虫,提高生物防治效率具有参考价值.     

The adaptiveness of searching and host selection behaviour in Pieris rapae (L.)

This study evaluates the adaptive significance of host preferences and searching behaviour in Vancouver and Canberra populations of the cabbage butterfly Pieris rapae (L.). As a result of a complex of responses to plant age, the butterflies concentrate their eggs on middle-aged plants. Young larvae develop faster and survive better on young plants than old ones, but larvae on smaller plants are more susceptible to crowding effects. Thus a preference for plants which are well-grown but not too old is selectively advantageous. By contrast, the butterflies’ host species preferences appear non-adaptive, and are unrelated to the quality of the host as larval food. Vancouver butterflies change their flight direction often and are very responsive to hosts, thereby generating a very aggregated distribution at a low cost in flight time. Canberra butterflies tend to fly in straight lines and are less responsive to hosts; their egg distribution is consequently more nearly random, but they fly further for each egg they lay. The relative costs of aggregation and increased flight time differ between the populations in a manner consistent with the observed behavioural differences.     

Behavioral mechanisms of parasitic wasps for searching concealed insect hosts

Wood borers are important forest insect pests and difficult to be controlled owing to their concealed behavior. However, parasitic wasps can effectively ascertain and parasitize wood borers as well as other concealed pests by using special searching, finding and attacking mechanisms, which have been developed during the course of long-term coevolution with their hosts. The present paper summarizes the behavioral mechanisms of parasitic wasps involved in searching and locating their concealed hosts. Parasitic wasps can accurately find the location of their hidden hosts and then parasitize them, usually by using olfactory semiochemicals from hosts (lavare and adults), host frass and symbiotic microorganisms in host galleries; visual signals from color contrast of plant surface; contact stimuli from characters of host physical defense; substrate vibrations produced by host feeding and movement; infrared radiation from host activities and metabolizability. Some parasitic wasps may integrate the information of several stimuli from different sources to enhance the reliability and accuracy of host locations. In addition, the potentials for utilizing the host location signals of parasitoids in biological control are discussed.     

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.     

Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction

Life history variation can be genetically based, or it may be due to environmental effects on the phenotype. In this paper we examine life history variation in relation to differences in habitat in the parasitoid Asobara tabida. Differences in the spatial distribution of host patches, the length of the season, host suitability, and competition between parasitoids all contribute to the selection for differences in life history between strains from northern and southern Europe. Strains were compared with respect to the allocation between reproduction and survival in experimental environments that varied with regard to the availability of food or to the number of hosts offered per day. Upon emergence parasitoids originating from southern Europe have higher egg loads and smaller fat reserves than parasitoids originating from northern Europe. Parasitoids from both southern and northern Europe show plasticity in allocation: food shortage causes a decrease in egg production, and rich breeding opportunities an increase in egg production. This plasticity is greater in the northern strain. Fat reserves play a central role in the physiology of this allocation. Fat can be used for both reproduction and survival. There is no oosorption, so once fat is allocated to reproduction it can no longer be used for survival. Differences in plasticity in allocation can therefore be considered as differences in the timing of egg production.     

Prey or host searching behavior that leads to a sigmoid functional response in invertebrate predators and parasitoids

Invertebrate predators and parasitoids have long been characterized as having a hyperbolic (Type 2) functional response. Modifications were made to Holling's sand paper disc experiment which consisted of limiting the initial period of search during which a host must be contacted. Failure to contact a host during this initial period causes the predator to emigrate from the search area. The modification generated a sigmoid (Type 3) functional response. This response resulted from the low probability of encountering a host during the initial period of search at low host densities in the time allotted. A limited period of search has been found in several insect parasitoids. Such a strategy would minimize the time (energy) spent per offspring produced by minimizing the time invested in searching microhabitats in which hosts are scarce or absent.     

Coevolution of Contrary Choices in Host-Parasitoid Systems

We investigate patch selection strategies of hosts and parasitoids in heterogeneous environments. Previous theoretical work showed that when host traits vary among patches, coevolved populations of hosts and parasitoids make congruent choices (i.e., hosts and parasitoids preferentially select the same patches) and exhibit direct density dependence in the distribution of percent parasitism. However, host-parasitoid systems in the field show a range of patterns in percent parasitism, while behavioral studies indicate that hosts and parasitoids can exhibit contrary choices (i.e., hosts avoid patches favored by the parasitoid). We extend previous theory by permitting life-history traits of the parasitoid as well as the host to vary among patches. Our analysis implies that in coevolutionarily stable populations, hosts preferentially select patches that intrinsically support higher host equilibrium numbers (i.e., the equilibrium number achieved by hosts when both populations are confined to a single patch) and that parasitoids preferentially select patches that intrinsically support higher parasitoid equilibrium numbers (i.e., the equilibrium number achieved by the parasitoids when both populations are confined to a patch). Using this result, we show how variation in life-history traits among patches leads to contrary or congruent choices or leads to direct density dependence, inverse density dependence, or density independence in the distribution of percent parasitism. In addition, we determine when populations playing the coevolutionarily stable strategies are ecologically stable. Our analysis shows that heterogeneous environments containing patches where the intrinsic rate of growth of the host and the survivorship rate of the parasitoid are low result in the coevolved populations exhibiting contrary choices and, as a result, promote ecological stability.     

Effects of asymmetric dispersal and environmental gradients on the stability of host–parasitoid systems

We consider host–parasitoid systems spatially distributed on a row of patches connected by dispersal. We analyze the effects of dispersal frequency, dispersal asymmetry, number of patches and environmental gradients on the stability of the host–parasitoid interactions. To take into account dispersal frequency, the hosts and parasitoids are allowed to move from one patch to a neighboring patch a certain number of times within a generation. When this number is high, aggregation methods can be used to simplify the proposed initial model into an aggregated model describing the dynamics of both the total host and parasitoid populations. We show that as the number of patches increases less asymmetric parasitoid dispersal rates are required for stability. We found that the 'CV²>1 rule' is a valid approximation for stability if host growth rate is low, otherwise the general condition of stability we establish should be preferred. Environmental variability along the row of patches is introduced as gradients on host growth rate and parasitoid searching efficiency. We show that stability is more likely when parasitoids move preferentially towards patches where they have high searching efficiency or when hosts go mainly to patches where they have a low growth rate.     

Host searching and oviposition behaviour of some parasitoids of aphidophagous Syrphidae

Abstract.

• 1 An analysis of host searching behaviour suggests that female parasitoids respond to aphid odours bringing them to the region of an aphid colony.
• 2 Syrphid hosts are located within the aphid colony by response to contact chemicals on the larval integument.
• 3 The behavioural mechanisms used by syrphid larvae to resist attacks and the subsequent responses made by parasitoids are described.
• 4 Oviposition behaviour and host size preferences of parasitoids are described.

     

Cuckoo females preferentially use specific habitats when searching for host nests

Egg mimicry is an important adaptation of common cuckoos, Cuculus canorus, against rejection of eggs by their respective hosts. A precondition for the maintenance of egg mimicry is that female cuckoos find hosts with a matching egg type. Experimental evidence indicated that habitat imprinting may be important for host selection. We tested whether the spacing and laying patterns of female cuckoos in the field are compatible with the supposed habitat-imprinting mechanism. We observed 16 females, with the help of radiotelemetry; of seven females, we observed directly 26 egg layings and 27 nest visits without laying. As expected if females were imprinted on different vegetation types, (1) the distribution of vegetation types differed between female home ranges, (2) female habitat use differed from average habitat availability within the egg-laying area (habitat preference), (3) females visited nests and deposited their eggs in the habitat they preferred, and (4) females laid their eggs consistently in a particular habitat type, irrespective of the host species. These results indicate that cuckoo females show habitat preference when searching for suitable host nests. Hence our data are compatible with the habitat-imprinting hypothesis, but owing to the habitat specificity of hosts the data cannot disprove a potential role of host specificity in cuckoo females.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Parasitism rate, parasitoid community composition and host specificity on exposed and semi-concealed caterpillars from a tropical rainforest

The processes maintaining the enormous diversity of herbivore—parasitoid food webs depend on parasitism rate and parasitoid host specificity. The two parameters have to be evaluated in concert to make conclusions about the importance of parasitoids as natural enemies and guide biological control. We document parasitism rate and host specificity in a highly diverse caterpillar-parasitoid food web encompassing 266 species of lepidopteran hosts and 172 species of hymenopteran or dipteran parasitoids from a lowland tropical forest in Papua New Guinea. We found that semi-concealed hosts (leaf rollers and leaf tiers) represented 84 % of all caterpillars, suffered a higher parasitism rate than exposed caterpillars (12 vs. 5 %) and their parasitoids were also more host specific. Semi-concealed hosts may therefore be generally more amenable to biological control by parasitoids than exposed ones. Parasitoid host specificity was highest in Braconidae, lower in Diptera: Tachinidae, and, unexpectedly, the lowest in Ichneumonidae. This result challenges the long-standing view of low host specificity in caterpillar-attacking Tachinidae and suggests higher suitability of Braconidae and lower suitability of Ichneumonidae for biological control of caterpillars. Semi-concealed hosts and their parasitoids are the largest, yet understudied component of caterpillar—parasitoid food webs. However, they still remain much closer in parasitism patterns to exposed hosts than to what literature reports on fully concealed leaf miners. Specifically, semi-concealed hosts keep an equally low share of idiobionts (2 %) as exposed caterpillars.     

Optimal use of patches by parasitoids with a limited fecundity

1. a mathematical model is presented which predicts the expected optimal-patch-use strategy for solitary parasitoids with a limited fecundity.
2. The model predicts that the quality of the patches is determined by the proportion of unparasitized hosts and not by the density of those hosts, and that throughout the searching period the parasitoids should maintain the level of parasitism equal in all the patches irrespective of the host density per patch.
3. The spatial pattern of parasitism among field patches by a parasitoid with a low fecundity, Praestochrysis shanghaiensis, was in agreement with the prediction of the model, i.e., a similar level of parasitism in different patches was observed when the ratio of female parasitoids to hosts in the whole study area exceeded 0.07. When the ratio was less than 0.05, however, the level of parasitism per patch showed an inverse relation to the host density, and was positively correlated with the female parasitoid-host ratio.
4. The model assumes that the parasitoids move between patches without cost and have perfect information about patch quality. Consideration of the cost of moving and sampling bridges the gap between the observed and predicted rates of parasitism found when the female parasitoid-host ratio in the whole study area was low

     

The combined effect of host and food availability on optimized parasitoid life‐history traits based on a three‐dimensional trade‐off surface

The reproductive success of many insects is considered to be limited by two main factors: the availability of mature eggs to lay (termed egg limitation) and the time to locate suitable hosts (termed time limitation). High host density in the environment is likely to enhance oviposition opportunities, thereby selecting for higher investment in egg supply. In contrast, a shortage of food (e.g. sugar sources) is likely to increase the risk of time limitation, thereby selecting for higher allocation to initial energy reserves. To our knowledge, the combined effect of host and food availability on these optimal life‐history allocations has never been investigated. We thus modelled their simultaneous effects on a three‐dimensional trade‐off between initial investment in energy reserves, egg number and egg size, while focusing on insect parasitoids. The model was based on Monte Carlo simulations coupled with genetic algorithms, in order to identify the optimal life‐history traits of a single simulated parasitoid female in an environment in which both hosts and food are present in varying densities. Our results reproduced the simple predictions described above. However, some novel predictions were also obtained, especially when specific interactions between the different factors were examined and their effects on the three‐dimensional life‐history surface were considered. The work sheds light on long‐lasting debates regarding the relative importance of time versus egg limitation in determining insect life‐history traits and highlights the complexity of life‐history evolution, where several environmental factors act simultaneously on multiple traits.     

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.     

Costs of reproduction and geographic variation in the reproductive tactics of the mosquito Aedes triseriatus

Intraspecific host discrimination is widespread in solitary parasitoids whose adult females forage for and evaluate host suitability, whereas interspecific discrimination is less common. In some parasitoid species, mostly Diptera and Coleoptera, the larva performs the last step of host searching. It has been suggested that host discrimination will rarely occur in such host-seeking larvae because their low mobility results in a low host encounter rate. We determined the extent to which the larvae of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae), a solitary parasitoid of aggregated Diptera pupae: (1) discriminated between unparasitized hosts and hosts parasitized by conspecifics; (2) used semiochemical cues to discriminate; (3) were influenced by life expectancy, presence of conspecifics and host availability in their host acceptance decision; and the extent to which (4) A. bilineata and A. bipustulata L., a species exploiting the same hosts and occurring sympatrically, showed interspecific host discrimination. A. bilineata larvae were able to discriminate between unparasitized hosts and hosts parasitized by conspecifics in a choice experiment. Such behavior has never previously been described for a coleopteran parasitoid or for a parasitoid species whose larvae perform host searching. Host discrimination in this species was not based on the presence of visual or tactile cues (e.g., entrance holes) but rather on chemical cues. The life expectancy of A. bilineata larvae was significantly shorter in the presence than in absence of hosts, and older larvae had lower parasitism success than young larvae in a 24-h experiment. However, the host acceptance decision of A. bilineata larvae was not influenced by larval age or the presence of conspecifics when the ratio of hosts per larva was greater than or equal to 1. When hosts were scarce, the degree of superparasitism increased significantly with the number of foraging conspecifics and the age of the larvae. Both species of Aleochara showed intra- and interspecific host discrimination in a choice experiment. In contrast to A. bipustulata, A. bilineata larvae more frequently parasitized hosts parasitized by A. bipustulata than those parasitized by conspecifics. We suggest that host discrimination will be frequent in solitary parasitoids with host-seeking larvae when hosts are aggregated. Received: 4 June 1998 / Accepted: 1 September 1998     

Searching for Food or Hosts: The Influence of Parasitoids Behavior on Host–Parasitoid Dynamics

A host–parasitoid system with overlapping generations is considered. The dynamics of the system is described by differential equations with a control parameter describing the behavior of the parasitoids. The control parameter models how the parasitoids split their time between searching for hosts and searching for non-host food. The choice of the control parameter is based on the assumption that each parasitoid maximizes the instantaneous growth rate of the number of copies of its genotype. It is shown that optimal individual behavior of parasitoids, with respect to time sharing between hosts and food searching, may have a stabilizing effect on the host–parasitoid dynamics.     

Nectar provisioning close to host patches increases parasitoid recruitment,retention and host parasitism

In the adult stage, many parasitoids require hosts for their offspring growth and plant-derived food for their survival and metabolic needs. In agricultural fields, nectar provisioning can enhance biological control by increasing the longevity and fecundity of many species of parasitoids. Provided in a host patch, nectar can also increase patch quality for parasitoids and affect their foraging decisions, patch time residence, patch preference or offspring allocation. The aim of this study was to investigate the impact of extrafloral nectar (EFN) provisioning close to hosts on parasitoid aggregation in patches. The aphid parasitoid Diaeretiella rapae (M’Intosh) was released inside or outside patches containing Brassica napus L. infested by Brevicoryne brassicae L. aphids and Vicia faba L. with or without EFN. When parasitoids were released outside patches, more parasitoids were observed in patches with EFN than in patches deprived of EFN. This higher recruitment could be linked to a higher attraction of a combination of host and food stimuli or a learning process. A release–recapture experiment of labeled parasitoids released within patches showed the higher retention of parasitoids in patches providing EFN and hosts, suggesting that food close to the host patch affects patch residence time. Both attractiveness and patch retention could be involved in the higher number of parasitoids foraging in host patches surrounded by nectar and for the higher parasitism recorded. Nectar provisioning in host patches also affected female offspring allocation inside the patch.