Plant structural complexity and host-finding by a parasitoid

Summary There are three major components to plant structure relevant to searching parasitoids: 1) plant size or surface area, 2) the variation among plant parts (structural heterogeneity), such as seed heads, flowers and nectaries, and heterogeneous surfaces (e.g. glabrous, hirsute), and 3) the connectivity of parts or plant form (structural complexity). We examined the effect of structural complexity, while controlling for size and structural heterogeneity, on searching behaviors of Trichogramma nubilale in controlled environments. Females were presented with a structurally simple surface and a structurally complex one. Parasitism rates were 2.9 times higher on simple surfaces than on complex ones. Unexpectedly, when no hosts were present, searching time on simple surfaces was 1.2 times higher than on complex surfaces. This implies that structural complexity per se can affect the giving-up-time of a searching parasitoid. Searching efficiency, however, was the dominant process, and females found hosts on simple surfaces 2.4 times faster than on complex surfaces. Structural complexity can have a dramatic effect on the success of parasitoid search.     

Influence of plant structural complexity on the foraging success of Trichogramma minutum: a comparison of search on artificial and foliage models

The influence of structural complexity on the foraging success for host eggs (Ephestia kuehniella Zeller) by Trichogramma minutum Riley was investigated in the laboratory. Naive females were released into arenas with structurally different paper models or foliage (simple: trembling aspen Populus tremuloides Michx., complex: balsam fir Abies balsamea L.). Observations of individual females were made every 15 min and searching success was measured by the number of host egg clusters found and the amount of time taken to find them, within a period of 196 min. Females found significantly more egg clusters and were quicker at finding them on the sample paper and foliage surfaces than on the most complex paper or foliage surfaces. Older females (2–3 days) were more successful and searched quicker than younger (<24 h) females on all paper surfaces. The timed observations suggested that wasps which spent more time walking had a significantly decreased probability of finding an egg mass and were significantly slower at finding them. Females that spent more time on paper surfaces had an increased probability of finding an egg mass. The significance of searching differences is discussed in relation to the potential effects of plant surfaces on Trichogramma movements and to the physiological readiness of the wasp.     

Egg laying rather than host quality or host feeding experience drives habitat estimation in the parasitic wasp Nasonia vitripennis

In variable environments, sampling information on habitat quality is essential for making adaptive foraging decisions. In insect parasitoids, females foraging for hosts have repeatedly been shown to employ behavioral strategies that are in line with predictions from optimal foraging models. Yet, which cues exactly are employed to sample information on habitat quality has rarely been investigated. Using the gregarious parasitoid Nasonia vitripennis (Walker; Hymenoptera: Pteromalidae), we provided females with different cues about hosts to elucidate, which of them would change a wasp's posterior behavior suggesting a change in information status. We employed posterior clutch size decisions on a host as proxy for a female's estimation of habitat quality. Taking into account changes in physiological state of the foraging parasitoid, we tested whether different host qualities encountered previously change the subsequent clutch size decision in females. Additionally, we investigated whether other kinds of positive experiences—such as ample time to investigate hosts, host feeding, or egg laying—would increase a wasp's estimated value of habitat quality. Contrary to our expectations, quality differences in previously encountered hosts did not affect clutch size decisions. However, we found that prior egg laying experience changes posterior egg allocation to a host, indicating a change in female information status. Host feeding and the time available for host inspection, though correlated with egg laying experience, did not seem to contribute to this change in information status.     

When parasitoids deal with the spatial distribution of their hosts: consequences for both partners

Insect parasitoids developing inside hosts face a true challenge: hosts are scattered in the field and their localization and selection require the use of complex and sometime confusing information. It was assumed for a long time that small-brained organisms like parasitoids have evolved simple and efficient behavioral mechanisms, leading them to be adapted to a given ecological situation, for example, the spatial distribution o f hosts in the habitat. However, hosts are not static and their distribution may also vary through generations and within the life of parasitoid individuals. We investigated if and how parasitoids deal with such a spatial com plexity in a m esocosm experiment. We used the Aphidius rhopalosiphi/Sitobion avenae parasitoid/host system to investigate if parasitoid females experiencing different host aggregation levels exhibit different foraging behaviors independently of the number of hosts in the environment. We showed that A. rhopalosiphi females exploited hosts more intensively both within and among patches at higher host aggregation levels. We discussed the adaptiveness of such behaviors in the light of evolution and biological control.     

Effects of plant diversity and structural complexity on parasitoid behaviour in a field experiment

1. In natural ecosystems, plants containing hosts for parasitoids are often embedded within heterogeneous plant communities. These plant communities surrounding host‐infested plants may influence the host‐finding ability of parasitoids. 2. A release‐recapture‐approach was used to examine whether the diversity and structural complexity of the community surrounding a host‐infested plant influences the aggregation behaviour of the leaf‐miner parasitoid Dacnusa sibirica Telenga and naturally occurring local leaf‐miner parasitoids. Released and locally present parasitoids were collected on potted Jacobaea vulgaris Gaertn.plants infested with the generalist leaf‐miner Chromatomyia syngenesiae Hardy. The plants were placed in experimentally established plant communities differing in plant diversity (1–9 species) and habitat complexity (bare ground, mown vegetation, and tall vegetation). Additionally, parasitoids were reared out from host mines on the trap plants. 3. Plant diversity did not influence the mean number of recaptured D. sibirica or captures of other locally present parasitoids but the number of recaptured parasitoids was influenced by habitat complexity. No D. sibirica parasitoids were recaptured in the bare ground plots or plots with mown vegetation. The mean number of recaptured D. sibirica generally increased with increasing complexity of the plant community, whereas locally present parasitoids were captured more frequently in communities with more bare ground. There was a unimodal relationship between the number of reared out parasitoids and diversity of the surrounding vegetation with the highest density of emerged parasitoids at intermediate diversity levels. 4. The present study adds to the thus far limited body of literature examining the aggregation behaviour of parasitoids in the field and suggests that the preference of parasitoids to aggregate in complex versus simple vegetation is association specific and thus depends on the parasitoid species as well as the identity of the plant community.     

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.     

The relationship between host selection behaviour and offspring fitness in a koinobiont parasitoid

1. When host quality varies, optimal foraging theory assumes that parasitic wasps select hosts in a manner that increases their individual fitness. In koinobiont parasitoids, where the hosts continue developing for a certain period of time after parasitisation, host selection may not reflect current host quality but may be based on an assessment of future growth rates and resources available for the developing larvae. 2. When presented with hosts of uniform quality, the koinobiont parasitoid Leptomastix dactylopii exhibits a characteristic host‐selection behaviour: some hosts are accepted for oviposition on first encounter, while others are rejected several times before an egg is laid in them, a behaviour that is commonly associated with a changing host acceptance threshold during the course of a foraging bout. 3. The fitness of the offspring that emerged from hosts accepted immediately upon encounter was compared with the fitness of offspring emerged from hosts rejected several times before being accepted for oviposition. 4. The pattern of host acceptance and rejection was not related to any of the measured fitness parameters of the offspring emerging from these hosts (development time, size at emergence, sex ratio at emergence, and female offspring egg load). 5. While complex post facto adaptive explanations can be devised to explain the nature of such a time and energy consuming host selection process, it is suggested that physiological constraints on egg production or oviposition may provide an alternative, purely mechanistic, explanation for the results obtained.     

寄生蜂成虫在寄主搜索过程中的学习行为

综述了寄生蜂寄主搜索过程中的学习行为的概念、过程、适应性意义及影响因子。学习是寄生蜂的一种普遍特征,但学习基本上只发生在成虫期,其中联系性学习是一个主要特征。学习可产生启动和嗜好性学习二种效应,在寄生蜂搜索寄主的各个步骤中发挥重要作用,使其在复杂多变的生存环境中可高效地识别和利用各种有用信息,提高搜索效率。学习的潜力及效应可依寄生蜂和寄主的食性专化程度、寄主的发育阶段、寄生蜂自身的生理状态及环境中刺激的性质等因子而变化。对寄生蜂学习行为的了解有助于发展对其行为调控的技术,提高寄生蜂对害虫控制的效能。     

Early experience influences several steps of the host selection process differentially in Aphidius ervi (Hymenoptera,Braconidae)

Experience of host-associated olfactory stimuli during development affects subsequent foraging decisions in many parasitoids, leading to host fidelity. We have recently shown that odours emitted by an alien host-plant complex (HPC) may affect this learning process. However, the consequences of this olfactory experience on parasitoid host foraging decisions is unknown. Here, we investigated if olfactory preferences induced by experience might drive parasitoid HPC choice and oviposition decisions. We presented two HPCs in dual choice experiments to Aphidius ervi females that had been reared on each HPC, either in a simple (one HPC) or complex (two HPCs) olfactory environment. HPC choice, time before landing on a HPC and number of aphid attacks were recorded. Early experience had contrasting effects on each of these parameters. Regardless of their origin, parasitoids did not land preferentially on any HPC, but they more frequently attacked one of the two hosts (Acyrthosiphon pisum) once they had landed on its HPC. Females emerging from the A. pisum/faba bean HPC attacked more aphids, regardless of the host species. Finally, the olfactory complexity of the environment had inconsistent effects on foraging decisions. These observations, contrasting with previous results obtained in olfactometer assays, indicate that olfactory preferences induced in early stages are not sufficient to predict parasitoid oviposition decisions. Moreover, the integration of multiple signals at several scales might generate different foraging patterns at each step of the host selection process.     

拟寄生蜂搜索产卵过程中对寄主的竞争

综述拟寄生蜂搜索产卵过程中对寄主竞争的最新研究进展.这类竞争具有四种方式,即标记寄主、杀卵和杀幼、守护寄主和捕食寄主.（1）标记寄主常涉及寄主标记信息素,这是由雌蜂在产卵前、产卵时或产卵后分泌的化学物质.寄主标记信息素常介导拟寄生蜂对已寄生和健康寄主的辨别、减少过寄生和多寄生、减轻种内和种间竞争压力.（2）雌蜂遇到已寄生寄主时,很多种类杀死前一雌蜂遗留的卵和幼虫,再产下自己的卵.雌蜂使用三种方法杀卵和杀幼,即产卵器穿刺、取食和使用有毒物质.通过杀卵和杀幼,产卵雌蜂清除了前一雌蜂遗留的后代,主动改善了寄主品质,从而有利于自身后代的生存.（3）守护寄主在肿腿蜂科、缘腹细蜂科、金小蜂科、缨小蜂科和茧蜂科中均有报道,守护者驱逐入侵者以保护后代及健康寄主.（4）捕食寄主不仅减少了健康寄主数量,且直接导致已寄生寄主中拟寄生蜂卵和幼虫的死亡.雌蜂一般在体内成熟卵量较少时捕食寄主.讨论了研究拟寄生蜂搜索产卵过程中竞争寄主的理论意义和实际应用价值.     

Habitat complexity modifies ant–parasitoid interactions: implications for community dynamics and the role of disturbance

Species must balance effective competition with avoidance of mortality imposed by predators or parasites to coexist within a local ecological community. Attributes of the habitat in which species interact, such as structural complexity, have the potential to affect how species balance competition and mortality by providing refuge from predators or parasites. Disturbance events such as fire can drastically alter habitat complexity and may be important modifiers of species interactions in communities. This study investigates whether the presence of habitat complexity in the form of leaf litter can alter interactions between the behaviorally dominant host ants Pheidole diversipilosa and Pheidole bicarinata, their respective specialist dipteran parasitoids (Phoridae: Apocephalus sp. 8 and Apocephalus sp. 25) and a single species of ant competitor (Dorymyrmex insanus). We used a factorial design to manipulate competition (presence/absence of competitors), mortality risk (presence/absence of parasitoids) and habitat complexity (presence/absence of leaf litter). Parasitoid presence reduced soldier caste foraging, but refuge from habitat complexity allowed increased soldier foraging in comparison to treatments in which no refuge was available. Variation in soldier foraging behavior correlated strongly with foraging success, a proxy for colony fitness. Habitat complexity allowed both host species to balance competitive success with mortality avoidance. The effect of fire on habitat complexity was also studied, and demonstrated that the immediate negative impact of fire on habitat complexity can persist for multiple years. Our findings indicate that habitat complexity can increase dominant host competitive success even in the presence of parasitoids, which may have consequences for coexistence of subordinate competitors and community diversity in general.     

用替代寄主繁殖的川硬皮肿腿蜂的学习行为

采用Y型嗅觉仪进行双向选择实验,研究了用替代寄主黄粉虫蛹繁殖的川硬皮肿腿蜂寄主搜索过程中的学习行为。结果表明,川硬皮肿腿蜂羽化期和成虫初期经历松枝皮、松针、松节油、杉枝皮等的挥发物后,雌蜂对这些挥发物的选择性明显提高,但对杉叶挥发物无明显的学习行为。羽化期和成虫初期是否投放新鲜寄主,对雌蜂的气味选择性没有明显的影响。成蜂取食黄粉虫蛹和蜂蜜时均可联系性学习松枝和杉枝气味。取食并经历杉枝和松枝挥发物4天和8天的寄生蜂之间对相应气味的选择性无显著差异。     

寄生蜂取食寄主特性及其在害虫生物防治中的作用

许多寄生性天敌昆虫的雌虫不仅寄生寄主, 而且还能取食寄主。在卵育型（synovigenic）寄生蜂类群中, 取食寄主行为是较为普遍的现象。本文综合近20年相关研究进展, 从寄生蜂类群、取食类型、生态学意义及影响因子等方面对寄生蜂的取食寄主行为进行了归纳总结。寄生蜂通过取食不仅可以杀死寄主, 直接起到控制害虫种群数量的作用, 还能通过取食策略为卵的成熟和再生提供营养来源, 对延长雌虫的寿命也有一定的帮助。对取食寄主行为的了解可为筛选优势寄生性天敌种类、评估寄生蜂在害虫生物防治中的作用提供重要信息。     

Importance of host feeding for parasitoids that attack honeydew-producing hosts

Insect parasitoids lay their eggs in arthropods. Some parasitoid species not only use their arthropod host for oviposition but also for feeding. Host feeding provides nutrients to the adult female parasitoid. However, in many species, host feeding destroys an opportunity to oviposit. For parasitoids that attack Homoptera, honeydew is a nutrient‐rich alternative that can be directly imbibed from the host anus without injuring the host. A recent study showed that feeding on host‐derived honeydew can be an advantageous alternative in terms of egg quantity and longevity. Here we explore the conditions under which destructive host feeding can provide an advantage over feeding on honeydew. For 5 days, Encarsia formosa Gahan (Hymenoptera: Aphelinidae) parasitoids were allowed daily up to 3 h to oviposit until host feeding was attempted. Host feedings were either prevented or allowed and parasitoids had ad libitum access to honeydew between foraging bouts. Even in the presence of honeydew, parasitoids allowed to host feed laid more eggs per hour of foraging per host‐feeding attempt than parasitoids that were prevented from host feeding. The higher egg‐laying rate was not compromised by survival or by change in egg volume over time. In conclusion, host feeding can provide an advantage over feeding on honeydew. This applies most likely under conditions of high host density or low extrinsic mortality of adult parasitoids, when alternative food sources cannot supply enough nutrients to prevent egg limitation. We discuss how to integrate ecological and physiological studies on host‐feeding behavior     

Odour-mediated long-range avoidance of interspecific competition by a solitary endoparasitoid: a time-saving foraging strategy

1. In studies on optimal foraging strategies, long-range decisions in the pursuit of resource are rarely considered. This is also the case for sympatric parasitoids, which may be confronted with the decision to accept or reject host larvae that are already parasitized by a competing species. They can be expected to reject already parasitized hosts if it is likely that they will lose the resulting intrinsic competition. However, examples of such interspecific host discrimination are rare. 2. We propose that parasitoids that are not egg-limited should reject inferior hosts only if it saves them time, and that this will be achieved mainly when the parasitoids are able to detect competitors from a distance. We tested this hypothesis using the sympatric parasitoids Cotesia marginiventris (Cresson) and Campoletis sonorensis (Cameron). 3. C. sonorensis was found to be the superior intrinsic competitor but, upon contact with a host larva, both wasps readily accepted hosts that had already been parasitized by the other species. However, in an olfactometer experiment, C. marginiventris females were found to strongly avoid the odour of their superior competitor. 4. These results are in accordance with a time optimization scenario, whereby the inferior competitor accepts competition if it costs only an egg, but avoids competition if it may save time that can be allocated to the search for more profitable hosts. 5. Models on host discrimination strategies in parasitoids had not yet considered discrimination from a distance. Long-range foraging decisions can also be expected for other organisms that have to choose between resources of varying suitability and profitability.     

Body size affects host defensive behavior and progeny fitness in a parasitoid wasp,Lysiphlebus fabarum

This study tested effects of maternal body size on foraging behavior and progeny development in a thelytokous population of Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). Small and large wasps were reared from first and second instar hosts [black bean aphid, Aphis fabae Scopoli (Hemiptera: Aphididae)], respectively, and each was provided with a patch (bean leaf disk) containing either 15 small (second instar) or 15 large (fourth instar) hosts for a 30‐min foraging period. Neither body size nor host size affected time allocation to various behaviors within a patch, but second instar aphids produced significantly more mummies than fourth instars. The preferred attack orientation was from the side of the aphid, suggesting wasps were sensitive to the risk of smearing with cornicle secretions. Few wasps developed in fourth instar hosts, suggesting later host instars were somewhat resistant to parasitism. Second instar hosts, the most suitable stage for L. fabarum development, relied more on defensive behavior, specifically kicking and secreting cornicle droplets. Large wasps were more likely to elicit a double cornicle secretion, indicating that aphids graded their response to the size of the attacker. Larger wasps were also more likely to be smeared with cornicle secretion, suggesting they were more vulnerable than small wasps. Although small wasps had smaller eggs than large wasps, there was no effect of maternal egg size on the size of progeny. However, daughters of small females emerged with larger egg loads than daughters of large mothers, and their eggs tended to be slightly smaller, although not significantly. Regression analysis revealed a positive correlation between maternal egg size and progeny developmental time for small and large wasps, and between maternal egg size and progeny egg load for small wasps. These results confirm maternal effects of body size in an aphid parasitoid, and reveal that vulnerability to host behavioral defenses is also body size dependent.     

Foraging Behavior of the Parasitoid Encarsia formosa on Gerbera jamesonii Leaves

Insight into the foraging behavior of the parasitoid Encarsia formosa Gahan for whitefly hosts was gained by continuous observation of individual parasitoids on leaves of the ornamental plant Gerbera jamesonii, until females left the leaf. Comparison of the parasitoid behavior on three cultivars gave similar results. Mean searching time on uninfested G. jamesonii leaves of three cultivars was 1 h 30 min and the mean percentage of walking activity of the total observation time on those cultivars was 61%. Both parameters were not influenced by different leaf structures of Gerbera cultivars. Encounters with hosts arrested the parasitoids on the leaves. The walking activity and the percentage of host encounters that resulted in an oviposition decreased with decreasing egg load of the parasitoid. In comparison with tomato, where biological control of whiteflies is successful, only minor differences in the foraging behavior occur, except for the residence time of females, which was about three to four times longer on G. jamesonii leaves, but these leaves are about seven times larger than tomato leaves. The facts that (1) the foraging behavior of E. formosa on G. jamesonii is independant of the cultivar and (2) the foraging behavior is, in many aspects, similar to that on tomato suggest that biological control of whitefly on this ornamental plant is a potential option.     

Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field

We used field observations of freely foraging Aphytis aonidiae parasitoids in conjunction with results of laboratory studies of A. aonidiae and other Aphytis species to simulate lifetime patterns of behavior and reproduction. Field observations provided estimates of encounter rates with three classes of hosts, the mortality rate from predation on adult parasitoids, and host-handling times for oviposition and host feeding by adult wasps. A series of physiological parameters, including the egg maturation rate and the value of host-feeding meals, were estimated from previously published studies. Plasticity in parasitoid behavior was incorporated in two ways. For one set of simulations we used a behavioral rule derived empirically from observations of parasitoids made in the field, and for another we used a dynamic state-variable model to generate a set of behavioral rules that maximize lifetime reproductive success. As was expected, the empirically derived rule led to better matches with field observations than did simulations using the output of the dynamic model. Projections of lifetime reproductive success in the field ranged between three and 37 eggs within the 95% confidence intervals of the mortality rate and host encounter rate and depending on which behavioral rule was used. Lifetime reproductive success from the simulation with central estimates of the mortality and host encounter rates that incorporated the empirical rule was 6.25 eggs. Using the empirical versus the theoretical rule in the simulations led to a 10%-30% decline in projections of lifetime reproductive success, depending on mortality and host encounter rates. Regardless of the behavioral rule, the simulations underscored the observation that the host encounter rate was greater than the egg maturation rate. The overall oviposition rate was sufficiently high to lead to daily episodes of temporary egg limitation during which parasitoids must mature an egg before being able to oviposit.     

Effect of host quality of Callosobruchus maculatus (Coleoptera: Bruchidae) on performance of the egg parasitoid Uscana lariophaga (Hymenoptera: Trichogrammatidae)

Development and reproductive success of the solitary egg parasitoid Uscana lariophaga Steffan were examined after development in eggs of the bruchid storage pest Callosobruchus maculatus Fabricius reared at either low or high densities on cowpea seeds and laid at day 1 and 4 of maternal life. Both bruchid larval competition and maternal age negatively affected egg size, but the latter more than the former. Uscana lariophaga reared in small hosts developed slower, were smaller and produced fewer eggs compared to parasitoids reared in large hosts. Fecundity of the parasitoid was heavily influenced by host egg size. This was reflected in the values for the intrinsic rate of increase of U. lariophaga, which differed for wasps that developed in host eggs laid by bruchid females of different age. Wasps allocated marginally more female offspring to larger hosts.     

Ratio dependence in the functional response of insect parasitoids: evidence from Trichogramma minutum foraging for eggs in small host patches

Abstract.  1. Despite considerable recent debate on the suitability of ratio dependence as a more general form for the functional response in consumer–victim relationships, there have been few detailed studies to experimentally determine the response of insect parasitoids to host and parasitoid density at a local scale.
2. The experimental host, Ephestia kuehniella , was used to test for host dependence and ratio dependence in the functional response of the egg parasitoid, Trichogramma minutum , a species widely used in inundative biological control. The functional response was examined through four series of experiments in which either host density, parasitoid density, or the ratio of previously parasitised to healthy hosts was manipulated.
3. The response to host density was type I for both single and simultaneously foraging parasitoids, indicating a lack of host dependence in the functional response. The upper limit to the response was estimated as 39 hosts attacked in a 24-h period, with an estimated per capita search rate of 1.32 for individual females and 0.37 for three simultaneously searching females.
4. The response to parasitoid density provided an interference constant of unity, indicating an equal sharing of hosts and thus ratio dependence in the functional response. Female parasitoids responded to the presence of conspecifically parasitised eggs with a significant increase in search rate (1.75), but with no change to the form or upper limit of the response.
5. It is suggested that ratio dependence may be more common among insect parasitoids than previously supposed, and that a type I functional response, or the absence of host dependence, may be an emergent property of phylogenetic constraint within the monophyletic grouping of Cales , Eretmocerus , and Trichogramma .