Preference and performance of Anagrus nilaparvatae (Hymenoptera: Mymaridae): effect of infestation duration and density by Nilaparvata lugens (Homoptera: Delphacidae)

The effect of Nilaparvata lugens (St?l) infestation duration and density on the host preference and performance of Anagrus nilaparvatae Pang et Wang, an egg parasitoid of rice planthoppers, was determined. The results showed that the parasitoid preferred N. lugens eggs on the plants infested with 10 gravid N. lugens females for 1 d to those plants infested with 10 gravid females for 2 or 3 d. It was also found to prefer N. lugens eggs on plants infested with 10 or 20 adult females after 24 h of infestation to those plants infested with 5 or 80 females. The parasitoid's offsprings had lower survival rates, fecundities, female ratios, indexes of capacity for population increase, and longer developmental durations on plants when they were infested with high N. lugens density (80 adult females per plant). However, the performance of the parasitoid on plants infested with low N. lugens density (5 female adults per plant) was similar to those on plants with intermediate N. lugens density (10 or 20 adult females per plant). Low preference of the parasitoid for N. lugens eggs on plants with heavy or light infestation levels may be correlated with low host suitability and detectability, respectively. The result implies an important role of herbivore-induced rice volatiles in the host preference of the parasitoid A. nilaparvatae, by which the parasitoid perceives the host and its suitability.     

Prey Habitat Location by the Cassava Mealybug Predator Exochomus flaviventris: Olfactory Responses to Odor of Plant, Mealybug, Plant–Mealybug Complex, and Plant–Mealybug–Natural Enemy Complex

Exochomus flaviventris Mader is considered to be the most active predator of the cassava mealybug Phenacoccus manihoti Matile–Ferrero in Central Africa. The response of experienced gravid female coccinellids to the odor of cassava plant (var. Zanaga), unparasitized mealybugs, plant–mealybug complex with or without feeding prey (parasitized or not), and plant–mealybug complex with or without conspecific coccinellids was investigated in a Y-tube olfactometer. The odor of uninfested cassava plants was not more attractive than clean air. Dual-choice tests revealed that mealybug-infested plants were preferred to mealybugs alone and mealybug-damaged plants and were the major sources of volatiles that attract females coccinellids to the microhabitat of its prey. The emission of volatile chemicals did not appear to be limited to the infested parts of the plant but did occur systemically throughout the plant. The presence of conspecific coccinellid larvae or adult males did not modify the attractiveness of the mealybug-infested plants. However, when an infested plant with conspecific predator females (alone or with conspecific males) was compared to an infested plant or infested plant with conspecific males, E. flaviventris females showed a preference for the last two sources of odor. The uninfested plant with conspecific males was also preferred to the uninfested plant with conspecific females. In addition, the odor of conspecific males was preferred over that of conspecific females. Female predators preferred the plant infested with unparasitized mealybugs over the plant infested with mealybugs previously parasitized. These results showed that E. flaviventris females use herbivore-induced plant volatiles during foraging and can detect via olfaction the presence of conspecific gravid females and parasitized prey, thus assessing patch suitability from a distance.     

稻虱缨小蜂对褐飞虱和白背飞虱卵的识别机制

研究了室内条件下信息化合物及稻飞虱卵的形态特征在稻虱缨小蜂识别2种卵寄主褐飞虱和白背飞虱中的作用。结果表明,褐飞虱和白背飞虱雌成虫诱导的水稻挥发物对稻虱缨小蜂的引诱作用无显著差异,各自的引诱比例(头数)分别为57.50%(23头)和42.50%(17头)。稻虱缨小蜂对2种飞虱4组材料,完整卵、磨碎卵、带卵叶鞘和若虫为害叶鞘的行为反应,除了在褐飞虱完整卵上的搜索时间极显著地长于在白背飞虱完整卵上的以外,其余的均不存在差异。挥发物捕集结果表明,褐飞虱和白背飞虱雌成虫诱导的水稻挥发物组成相非常一致。上述结果表明水稻挥发物、稻飞虱利它素及飞虱卵的形态特征在稻虱缨小蜂识别褐飞虱和白背飞虱卵中的作用不明显。文中就稻虱缨小蜂识别2种寄主的机制进行了讨论。     

Role of volatile semiochemicals in host location by the egg parasitoid Anagrus breviphragma

Recent investigations conducted on several tritrophic systems have demonstrated that egg parasitoids, when searching for host eggs, may exploit plant synomones that have been induced as a consequence of host oviposition. In this article we show that, in a system characterized by host eggs embedded in the plant tissue, naïve females of the egg parasitoid Anagrus breviphragma Soyka (Hymenoptera: Mymaridae) responded in a Y‐tube olfactometer to volatiles from leaves of Carex riparia Curtis (Cyperaceae) containing eggs of one of its hosts, Cicadella viridis (L.) (Hemiptera: Cicadellidae). The wasp did not respond to host eggs or to clean leaves from non‐infested plants compared with clean air, whereas it showed a strong preference for the olfactometer arm containing volatiles of leaves with embedded host eggs, compared with the arm containing volatiles of leaves from a non‐infested plant or host eggs extracted from the plant. When the eggs were removed from an infested leaf, the parasitoid preference was observed only if eggs were added aside, suggesting a synergistic effect of a local plant synomone and an egg kairomone. The parasitoid also responded to clean leaves from an egg‐infested plant when compared with leaves from a non‐infested plant, indicating a systemic effect of volatile induction.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Density‐mediated indirect interactions alter host foraging behaviour of parasitoids without altering foraging efficiency

1. Foraging decisions of parasitoids are influenced by host density via density‐mediated indirect interactions. However, in the parasitoid's environment, non‐suitable herbivores are also present. These non‐hosts also occur in different densities, which can affect a parasitoid's foraging behaviour. 2. The influence of non‐host densities can be expressed during the first phase of the foraging process, when parasitoids use plant volatiles to locate plants infested by their host. They may also play a role during the second phase, when parasitoids use infochemicals from the host and plant to locate, recognise and accept the host. 3. By using laboratory and field setups, it was studied whether the density of non‐host herbivores influences these two phases of the foraging behaviour of the parasitoid Cotesia glomerata as well as the parasitoid's efficiency to find its host, Pieris brassicae caterpillars. 4. The findings show that a high non‐host density, regardless of the species used, negatively affected parasitoid preference for host‐infested plants, but that the behaviour on the plant and the total host‐finding efficiency of the parasitoids were not influenced by non‐host density. 5. These results are discussed in the context of density‐mediated indirect interactions.     

Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera: Chrysomelidae)

Eggs of the elm leaf beetle Xanthogaleruca luteola are often heavily attacked by the chalcidoid wasp Oomyzus gallerucae. We studied the chemical signals mediating interactions between the egg parasitoid, its host, and the plant Ulmus campestris. Olfactometer bioassays with O. gallerucae showed that volatiles of the host-plant complex attract the parasitoid. In order to determine the source of attractive volatiles within this host-plant-complex, we tested separately the effect of odours of eggs, gravid elm leaf beetle females, faeces of the beetles and elm twigs (with undamaged leaves and leaves damaged either mechanically or by feeding of the beetles). Odours of faeces of the elm leaf beetle were attractive, whereas neither volatiles from eggs nor from gravid females acted as attractants. Volatiles from undamaged or damaged plants did not elicit a positive reaction in O. gallerucae, whereas volatiles from feeding-damaged plants onto which host eggs had been deposited were attractive. This latter result suggests that it is not feeding but deposition of host eggs onto elm leaves that induces the production of plant volatiles attractive to the egg parasitoid. Investigations of the search patterns of O. gallerucae within the habitat by laboratory bioassays revealed that the egg parasitoid encounters host eggs by chance. Contact kairomones from faeces were demonstrated to be important in microhabitat acceptance, while contact kairomones isolated from the host eggs are relevant for host recognition. Received: 12 February 1997 / Accepted: 29 April 1997     

Male and female Trybliographa rapae (Hymenoptera: Figitidae) behavioural responses to food plant, infested host plant and combined volatiles

Many parasitoids use volatiles produced by plants as important cues during their food and host search process. We investigated the attraction of the parasitic wasp Trybliographa rapae Westwood (Hymenoptera: Figitidae) to volatiles emitted from plants infested by the cabbage root fly Delia radicum L. (Diptera: Anthomyiidae), as well as to volatiles from a nectar food plant. Behavioural choice tests showed that male parasitoids were not attracted to any volatiles from plants infested by D. radicum or from nectar plants, while females showed clear attraction to both volatile sources. Young females were more attracted to combined volatiles of host and food plants over those from only the host plant, whereas older females showed no differences in attraction to the two odour sources. This suggests that intercropping attractive flowers with host plants could potentially be used to recruit newly emerged parasitoids from surrounding fields while older parasitoids invest more energy in host location than in additional food search. Volatiles from a whole infested plant were chosen over those emitted from separated above- and below-ground parts from infested plants. It is important to consider the availability of both energy and host resources for parasitoids when designing an eco-compatible management of a vegetable crop system.     

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.     

Intimate Rendezvous in a Tritrophic Context? Nothing but the Girls for Male Lysiphlebus testaceipes

In insects, mating often occurs after natal dispersal, and hence relies on a coevolved combination of sexual communication and movement allowing mate encounter. Volatile sex pheromones are widespread, generally emitted by females and triggering in‐flight orientation of conspecific males. In parasitoid wasps, unmated females can start laying unfertilized eggs via parthenogenesis so that host patches could serve as sites of rendezvous for mating. Males could therefore use cues associated with host patches to focus their search on females that have successfully found oviposition sites. We hypothesized that in parasitoids exploiting herbivorous hosts, sex pheromones, and herbivore‐induced plant volatiles (HIPV) should act in synergy, triggering male orientation toward ovipositing females. We tested this hypothesis with the aphid parasitoid Lysiphlebus testaceipes. Results from both field and laboratory experiments show that males are strongly attracted to virgin females, but that volatiles from aphid‐infested plants have no effect on male orientation, neither has a cue, nor in interaction with the female sex pheromone. The absence of synergy between sex pheromones and HIPV contrasts with results on other species and raises interesting questions on mating systems and sexual selection in parasitoid wasps.     

Behavioral responses of the parasitoid Psyllaephagus pistaciae (Hymenoptera: Encyrtidae) to host plant volatiles and honeydew

The behavioral responses of the parasitoid Psyllaephagus pistaciae, the major biocontrol agent of the common pistachio psylla, Agonoscena pistaciae, to volatiles emanating from its host plant and host honeydew, were examined using a four‐arm airflow olfactometer. In addition, the arrestment behavior of this parasitoid on clean and honeydew‐treated leaves of the pistachio, Pistacia vera, was monitored. The infested pistachio leaves were the most favored source of the volatile attracting the parasitoids. The parasitoid clearly distinguished and responded to infochemicals emitted by psyllid honeydew but at a lower level than to the volatiles from infested host plants. However, the searching time, locomotory behavior, antennal drumming and ovipositor probing were all affected when they encountered honeydew‐contaminated zones on pistachio leaves. These findings suggest that the psyllid honeydew releases kairomones that stimulate the parasitoids to greater searching activity, as well as providing a directional cue. The intensive searching activities in the presence of the volatiles tested were very similar to responses by the parasitoid females when encountering patches treated with psyllid honeydew. Such behavior could retain the parasitoid in a favorable area, thereby increasing the probability of additional host encounters.     

The role of herbivore‐ and plant‐related experiences in intraspecific host preference of a relatively specialized parasitoid

Parasitoids use odor cues from infested plants and herbivore hosts to locate their hosts. Specialist parasitoids of generalist herbivores are predicted to rely more on herbivorederived cues than plant-derived cues. Microplitis croceipes (Cresson)(Hymenoptera: Braconidae) is a relatively specialized larval endoparasitoid of Heliothis virescens (F.)(Lepidoptera: Noctuidae), which is a generalist herbivore on several crops including cotton and soybean. Using M. croceipes/H. virescens as a model system, we tested the following predictions about specialist parasitoids of generalist herbivores:(i) naive parasitoids will show innate responses to herbivore-emitted kairomones, regardless of host plant identity and (ii) herbivore-related experience will have a greater influence on intraspecific oviposition preference than plant-related experience. Inexperienced (naive) female M. croceipes did not discriminate between cotton-fed and soybean-fed H. virescens in oviposition choice tests, supporting our first prediction. Oviposition experience alone with either host group influenced subsequent oviposition preference while experience with infested plants alone did not elicit preference in M. croceipes, supporting our second prediction. Furthermore, associative learning of oviposition with host-damaged plants facilitated host location. I terestingly, naive parasitoids attacked more soybeathan cotton-fed host larvae in two-choice tests when a background of host-infested cotton odor was supplied, and vice versa. This suggests that plant volatiles may have created an olfactory contrast effect. We discussed ecological significance of the results and concluded that both plant- and herbivore-related experiences play important role in parasitoid host foraging.     

Differential induction of volatiles in rice plants by two stink bug species influence behaviour of conspecifics and their natural enemy Telenomus podisi

Tritrophic interactions mediated by semiochemicals have been intensively studied from the viewpoint of ecological relationships with Nearctic tritrophic organisms. However, there are few studies involving interactions with different herbivores on the same host plant in Neotropical systems. The objective of the current study was to investigate the effects of herbivory by two species of stink bugs (Heteroptera: Pentatomidae) with the same feeding habit – Tibraca limbativentris Stål and Glyphepomis spinosa Campos & Grazia – on indirect and direct defence strategies of rice plants. The responses of each stink bug species (virgin and mated females) and of their main natural enemy, the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Platygastridae; mated females), to volatiles from undamaged and herbivore-damaged rice plants were evaluated using a Y-tube olfactometer. The results showed that rice plants responded differently to T. limbativentris or G. spinosa herbivory, enhancing the production of a different blend of volatile compounds, which reduced the attraction for conspecific stink bugs and elicited the foraging behaviour of T. podisi.     

Superparasitism as an ESS: to reject or not to reject, that is the question

A stochastic model is formulated to determine the optimal strategy for a solitary parasitoid which has discovered an already parasitized host. The model assumes that the parasitoid can count both the number of eggs already present in a host and the number of conspecifics searching in the same patch. The survival probability of an egg is assumed to depend on the total number of eggs in a host. The decision to (super)parasitize depends both on the degree to which the discovered host already is parasitized and on the number of conspecific females searching in the same patch. We consider both the case that egg laying does not involve any costs for the parasitoid and the case that it involves some marginal costs. Uniform behaviour of all the conspecific parasitoids in a patch, i.e. laying one additional egg in all encountered larvae containing a particular number of eggs, appears to be a pure evolutionary stable strategy (ESS). If either the probability that a parasitoid emerges from a host decreases with an increasing degree of parasitism, at least from a particular number of eggs onwards, or if parasitism involves marginal costs, the maximum number of eggs for which it is still profitable to superparasitize a host once more is limited. This number increases with the number of conspecifics searching in the patch. Large marginal costs (i.e. the expected gain of not parasitizing now) decrease the profit of superparasitism. For newly emerged parasitoids the rejection of an already parasitized host is not advantageous as long as the marginal costs of parasitism are small, because the host can never contain an egg of its own.     

The Role of Chemical Cues in Host and Mate Location in the Pear Psylla Cacopsylla bidens (Homoptera: Psyllidae)

Chemical communication was shown to play a role in the pear psylla, Cacopsylla bidens. Electrophysiological (EAG) and behavioral responses were investigated in males and females pear psylla . Males were found to be attracted to females, and especially to those on host plants, but not to males, uninfested host plants, or plants infested with conspecific larvae. On the other hand, females were not attracted to males or females but displayed some attraction to host plants. Furthermore, females showed a preference for uninfested pear versus plants infested with conspecific larvae. The antennae of males gave highest electroantenographic response to volatiles from pears infested with females but not males, while females, responded also toward the volatiles of pear alone. These results indicate that females of C. bidens emit sex pheromones that are attractive to the males and suggest that, host volatiles may play a role in host selection by pear psylla females.     

Aboveground herbivory affects indirect defences of brassicaceous plants against the root feeder Delia radicum Linnaeus: laboratory and field evidence

1. Belowground herbivory has recently been shown to disrupt the host location behaviour of aboveground parasitoids and thereby impact plants indirect defences. Reverse interactions, on the other hand, have received little attention so far. 2. Lab and field studies were conducted to examine whether the presence of the leaf herbivore Pieris brassicae Linnaeus on brassicaceous plants influences the response of Trybliographa rapae Westwood, a specialist parasitoid of the root feeder Delia radicum Linnaeus. 3. The present results show that the attraction of the parasitoid towards host‐infested plants disappeared when these plants were also infested by P. brassicae. This absence of attraction was observed both when the complete odour blend or only undamaged leaves from damaged plants were offered, emphasising the role of systemically induced volatiles for host location in T. rapae. 4. Furthermore, the field study revealed that parasitism levels dropped from 30% on root‐infested plants to 4% on double‐infested plants. 5. The present study is the first to confirm that reduced attraction to host‐infested plants as a result of simultaneous attack by below‐ and aboveground herbivores translates into lower levels of parasitism in the field.     

Discrimination of the age of conspecific eggs by an ovipositing ectoparasitic wasp

The recognition and avoidance of already parasitized hosts is a major issue in parasitoid behavioural ecology. A key factor affecting the fitness reward expected from superparasitism is the probability that the second or subsequent egg laid on a host will win the contest with the first-laid egg. The present study investigated the ability of females of the solitary ecto parasitoid Anisopteromalus calandrae Howard (Hymenoptera: Pteromalidae) to (i) discriminate between unparasitized Callosobruchus maculatus (Fabricius) (Coleoptera: Bruchidae) hosts and those parasitized by a conspecific, and (ii) discriminate between a host parasitized by an egg just laid (2 h) and one parasitized by an egg about to hatch (28 h). However, they did not adjust their offspring sex ratio on already parasitized hosts compared to unparasitized ones. Our results show that A. calandrae females can discriminate between parasitized and unparasitized hosts, as they lay more eggs on the latter. The probability of the second or subsequent egg laid on a host (superparasitism) winning the contest with a conspecific increases as the time between the two ovipositions decreases. Consequently, parasitoid females should lay more eggs on recently parasitized hosts than on those that have been parasitized for a long time (i.e., when the first eggs are about to hatch), and that is indeed what they were found to do. To increase their fitness in spite of the presence of already parasitized hosts, A. calandrae females have developed highly discriminative capacities regarding the parasitism status of hosts.     

Experimental field studies on predation and egg parasitism of rice brown planthopper in Indonesia

• 1 Egg parasitism and general predation are known to be important mortality factors in the population dynamics of rice brown planthopper (BPH) Nilaparvata lugens in tropical Asia, but previous studies have not attempted to quantify and compare them.
• 2 Field experiments in Java, Indonesia, are reported for 1993 and 1994. Plants previously infested with BPH eggs were put out in field cage‐enclosures, which, by means of different size mesh gauze covering, allowed either: (1) free access to all natural enemies, (2) access only to egg parasitoids, or (3) no access to any natural enemies.
• 3 After one BPH generation (30 days), numbers of adults and gravid females were counted for each treatment. In addition, plants were dissected to determine the numbers of eggs laid.
• 4 An additional treatment in which all natural enemies were excluded, but lycosid spiders were added, was used in 1994 experiments in an attempt to assess the effects of predators in the absence of egg parasitoids.
• 5 Numbers of BPH adults and eggs laid were highest when natural enemies were excluded and lowest when they had free access. Mortality due to egg parasitoids in the absence of predators was intermediate and significantly different to the two other treatments.
• 6 The effects of added predators in the absence of egg parasitoids gave variable results, but again clearly demonstrated the significance of egg parasitism in overall BPH mortality.
• 7 The conservation of BPH egg parasitoids should form an important element of any rice pest management programme in tropical Asia.

     

Hyperparasitoids Use Herbivore-Induced Plant Volatiles to Locate Their Parasitoid Host

Plants respond to herbivory with the emission of induced plant volatiles. These volatiles may attract parasitic wasps (parasitoids) that attack the herbivores. Although in this sense the emission of volatiles has been hypothesized to be beneficial to the plant, it is still debated whether this is also the case under natural conditions because other organisms such as herbivores also respond to the emitted volatiles. One important group of organisms, the enemies of parasitoids, hyperparasitoids, has not been included in this debate because little is known about their foraging behaviour. Here, we address whether hyperparasitoids use herbivore-induced plant volatiles to locate their host. We show that hyperparasitoids find their victims through herbivore-induced plant volatiles emitted in response to attack by caterpillars that in turn had been parasitized by primary parasitoids. Moreover, only one of two species of parasitoids affected herbivore-induced plant volatiles resulting in the attraction of more hyperparasitoids than volatiles from plants damaged by healthy caterpillars. This resulted in higher levels of hyperparasitism of the parasitoid that indirectly gave away its presence through its effect on plant odours induced by its caterpillar host. Here, we provide evidence for a role of compounds in the oral secretion of parasitized caterpillars that induce these changes in plant volatile emission. Our results demonstrate that the effects of herbivore-induced plant volatiles should be placed in a community-wide perspective that includes species in the fourth trophic level to improve our understanding of the ecological functions of volatile release by plants. Furthermore, these findings suggest that the impact of species in the fourth trophic level should also be considered when developing Integrated Pest Management strategies aimed at optimizing the control of insect pests using parasitoids.