Rainer Meyhöfer

Vibratory stimuli in host location by parasitic wasps

Parasitic wasps use a broad spectrum of different stimuli for host location and host acceptance. Here we review the published evidence for the use of mechanical stimuli, i.e. substrate born vibrations which are invariably regarded as vibrotaxis. We propose a set of criteria to class behavioural reactions as vibrotaxis or vibrokinesis and characterize 14 studies reporting the use of host-associated vibrations by parasitoids. The studies are compared concerning (i) experimental design; (ii) characterisation of vibrational signals; and (iii) progress of the parasitoid towards the host.The recent experimental development based on new measurement techniques shows the growing body of evidence that host-associated vibrations are exploited by parasitic wasps. Nevertheless a definite proof for vibrotaxis is still lacking. To assess the exact mechanisms by which parasitoids use vibrations bioassays comparing reactions to natural and artificially generated signals are needed. Vibrotaxis as well as vibrokinesis are both helpful host location strategies for parasitoids foraging in a multimodal environment. At the community level they may lead to niche differentiation.

Intraguild predation on the aphid parasitoid Lysiphlebus fabarum (Marshall) (Hymenoptera: Aphidiidae): mortality risks and behavioral decisions made under the threats of predation

Abstract Intraguild predation (IGP) is a primordial mortality factor that generates consequences for the coexistence of species in natural communities as well as for the implementation of antagonists in biological control programs. Among parasitoids and predators the most frequent form of IGP is asymmetric. Because it exerts a strong selection pressure on the inferior parasitoids it seems to be likely that these antagonists have evolved strategies to minimize IGP. Our study traced the behavior of the aphid parasitoid Lysiphlebus fabarum (Marshall) which is able to exploit the enemy free space in ant protected aphid colonies. In the agricultural landscape, L. fabarum frequently forages in aphid colonies without ant protection where it is exposed to situations with an extraordinary high risk of predation by aphidophagous predators. In the current study, we investigated predation risks for different developmental stages of L. fabarum and behavioral decisions made under the risk of predation by foraging females. All developmental stages of L. fabarum suffered from a high risk of predation in confrontations with most of the tested aphidophagous predators. Only aphid mummies turned out to be a less frequent IG-prey compared to unparasitized aphids when found simultaneously with adult Coccinella septempunctata L. and larvae of Episyrphus balteatus de Geer. Nevertheless, foraging females of L. fabarum did not avoid the presence of predators nor displayed an effective defense behavior in direct confrontations with any of the tested predator species. Coccinellids, syrphids as well as chrysopids proved capable of killing an adult parasitoid. The discrepancies between the observed predation risks and the lack of behavioral adaptations of adult L. fabarum are discussed in different contexts.

Vibration–mediated interactions in a host–parasitoid system

The aim of this paper was to obtain behavioral evidence of vibration mediated interactions between the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae) and its parasitoid Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae). The experimental set–up allowed the simultaneous recording on video film of both the parasitoids and the hosts behavior, thus enabling us to contrast their respective responses to the leaf vibrations produced by the other party. We analysed the one step transition probabilties from one behavioral state to the following. Active larval movements had a marked influence on the parasitoids behavior, while feeding and still had no detectable effect. We found no evidence for vibrotaxis on the part of the parasitoid. While parasitoid searching behavior on the leaf surface did not seem to alter the leafminers behavior, ovipositor insertions triggered a characteristic avoidance response. The described interactions are discussed in the context of the ‘princess and monster’ model developed in search and game theory.

Host location by a parasitoid using leafminer vibrations: characterizing the vibrational signals produced by the leafmining host

Abstract. The aim of this study was to characterize the vibrations produced by the apple tentiform leafminer Phyllonorycter malella (Ger.) (Lepidoptera, Gracillariidae). Host location using vibrations by one of its parasitoids Sympiesis sericeicornis Nees (Hymenoptera, Eulophidae) was postulated by Casas (1989) on the basis of detailed quantitative behavioural observations and has also been suggested by other authors on similar systems. Both host and parasitoid send and may receive vibratory signals; consequently we first attempted to characterize and classify the signals, one of the first steps required in the design of an adequate vibrational biotest. In this respect, our approach differs fundamentally from the familiar setting of host location via semiochemicals and is best framed within the context of vibratory communication.

Combining plant- and soil-dwelling predatory mites to optimise biological control of thrips

The efficiency of a natural enemy combination compared to a single species release for the control of western flower thrips (WFT) Frankliniella occidentalis (Pergande) on cucumber plants was investigated. Since a large part of F. occidentalis seems to enter the soil passage, a joint release of the plant-inhabiting predatory mite Amblyseius cucumeris (Oudemans) that feeds on thrips first-instar larvae and the soil-dwelling predatory mite Hypoaspis aculeifer (Canestrini) that preys on thrips pupae in the ground might offer a promising approach for a holistic control strategy. Therefore, two sets of experiments were conducted in cooperation with a commercial vegetable grower where the plants in plots were infested with a defined number of larval and adult F. occidentalis. Two species of natural enemies were released either synchronously or solely, and their efficacy was compared to control plots devoid of antagonists. In both experiments, the predatory mites were released twice with a density of 46 A. cucumeris/m2, and 207 H. aculeifer/m2 (low-density) in the first experiment and 528 H. aculeifer/m2 (high-density) in the second one. Population growth of all arthropod species on the plants and in the soil was quantified at regular intervals and included all soil-dwelling mites and alternative preys present in the substrate. The results showed that H. aculeifer alone had a significant impact on thrips population development only when released at high-densities, but competence was lower compared to the other antagonist treatments. The impact of A. cucumeris alone and A. cucumeris and H. aculeifer combined was similar. Thus, the pooled exploitation of natural enemies did not boost thrips control compared to the single species application of A. cucumeris (non-additive effect), which could be explained by resource competition between both predatory mite species. Species number and population size in the soil of the experimental plots both showed a high variability, a possible consequence of their interaction with released soil-dwelling predatory H. aculeifer mites. The impact of resource competition and presence of alternative preys on thrips biological control is exhaustively discussed. From our study, we can extract the subsequent conclusions: (1) the combined use of H. aculeifer and A. cucumeris cannot increase thrips control on cucumber compared to the release of A. cucumeris alone, but the overall reliability of thrips biological control might be enhanced, (2) the availability of alternative preys seemed to affect the thrips predation rate of H. aculeifer, and (3) the impact of naturally occurring soil predatory mites on the control of WFT seemed to be partial.

Predation capacity of two predatory laelapid mites on soil‐dwelling thrips stages

The life cycle of the Western Flower Thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae), one of the most important glasshouse pests, includes a soil passage composed of three instars that deserve more attention in terms of biocontrol strategies. It has been repeatedly reported that two polyphagous predatory mites, Stratiolaelaps miles (Berlese) and Hypoaspis (Geolaelaps) aculeifer (Canestrini) (Acari: Laelapidae), also prey on these thrips stages, in addition to several other soil inhabiting prey species. However, the potential thrips consumption rates have never been quantified for these predatory mites. Therefore, an arena experiment was carried out to investigate the potential predation rates of the two mites on second instar larvae, prepupae, and pupae of F. occidentalis. In addition, the fecundity on the thrips diet was assessed and compared to oviposition rate on a nematode prey. All thrips instars were accepted as prey by each mite species. Females of H. aculeifer preyed on 3.5 (± 0.5) thrips instars and laid 2.5 (± 0.87) eggs per day, whereas females of S. miles preyed on 1.64 (± 0.3) thrips and laid 0.8 (± 0.53) eggs. Males of both species killed 0.6 (± 0.3) thrips per day. The fitness of the two predatory mites on F. occidentalis as prey and their suitability as biocontrol agents are elucidated. Reasons for reduced thrips control in the soil environment, in contrast to the results obtained in arena assays are discussed.

Geometrical Games between a Host and a Parasitoid

Avoiding detection by parasitoids is nearly impossible for most leafminers in their visually striking mines, and they often suffer from a high mortality rate by a great variety of parasitoid species. The leafminer‐parasitoid interaction bears a strong resemblance to the princess‐monster game developed in game theory, in which a “monster” (parasitoid) selects an optimal search strategy to capture the “princess” (leafminer), while the princess selects an optimal strategy to hide from the monster. This article attempts to illustrate and to quantify the additional complexity that occurs when the princess can modify the arena in which the monster searches. Feeding activity of the leafminer Phyllonorycter malella creates feeding windows, which are spots on the mine. Its main parasitoid Sympiesis sericeicornis is able to insert its ovipositor only through these feeding windows. Parasitism risk depends both on the leafminer‐feeding pattern, which determines the structure of the arena in which the parasitoid searches, and on the position of the leafminer within the mine. The adaptive value of observed patterns of mine development and leafminer behavior is evaluated by comparing them to predictions from a simulation model of random patterns and leafminer positions. The leafminer creates a heterogeneous environment by leaving a central area of uneaten tissue. This area acts as a protecting shield and greatly diminishes the risk of parasitism. Hence, by controlling the structure of the arena in which the princess‐monster game is played, the leafminer defines some of the rules of the game.

Intraguild predation by aphidophagous predators on parasitised aphids: the use of multiple video cameras

A video technique that allows simultaneous behavioural observations of several experimental replicates under field and laboratory conditions is described. The technique was used to analyse predation risk of parasitised aphids in a sugar beet field. The images of 16 black and white video cameras were recorded by a video multiplexer in combination with a time‐lapse video recorder. Each camera was weather protected and equipped with a single infrared diode to allow observations during night times. Single leaves carrying aphid mummies only or mummies and unparasitised aphids were monitored. All colonies were exposed to predation and parasitation by the community of natural enemies in the field. Colonies with mummies and unparasitised aphids were visited significantly more often by predators than those without additional aphids. Predators also stayed significantly longer in patches with unparasitised aphids. Although an equal proportion of aphid mummies were destroyed in both treatments, the video analysis showed differences in predator species spectrum between treatments. In patches with aphids, coccinellid and hemipteran predators preyed on mummies, while in patches with only mummies, chrysopids accounted for most of the damage. The decrease in parasitoid survival could be attributed to the increasing number of predator visits in aphid patches and to a lesser extent to the decreasing number of unparasitised aphids (alternative prey). Parasitoid survival in colonies without alternative prey was correlated with the number of predator visits and the time predators spent on a leaf.

Effect of intercrops on thrips species composition and population abundance on French beans in Kenya

The study aimed at determining thrips species composition and thrips population density on French bean planted as a sole crop and as an intercrop with either sunflower, Irish potato, or baby corn, in various combinations. Field experiments were conducted in two seasons to examine: (1) thrips population development and thrips species composition over time, (2) effect of intercrops on thrips population density and natural enemies, and (3) effect of intercrops on French bean yield. The experiments were conducted at the Kenya Agricultural Research Institute, Embu, Kenya in a randomized complete block design with four replicates. The thrips population on French beans increased with time. It showed a peak at the flowering stage then started declining when the crops were nearing senescence. French beans hosted four thrips species, Megalurothrips sjostedti (Trybom), Frankliniella schultzei (Trybom), Frankliniella occidentalis (Pergande), and Hydatothrips aldolfifriderici (Karny) (all Thysanoptera: Thripidae) in order of decreasing abundance. The main thrips species on Irish potato and sunflower was F. schultzei. Baby corn hosted only Frankliniella williamsi (Hood) and Thrips pusillus (Bagnall). A monocrop of French bean hosted more thrips than a French bean intercrop mix. Thrips natural enemies such as Orius spp. and Ceranisus spp. were recorded in all crop plants but in especially high numbers on French bean and baby corn, respectively. Plots with French bean alone had about 1.4 times higher yields compared to intercropped plots of French bean with sunflower and French bean with baby corn. However, the percentage of pods that could get rejected on the market due to thrips damage was highest on plots with French bean alone (68 and 63%) and lowest on plots with French bean and baby corn (35 and 37%) in the first and second seasons, respectively. This study showed that a complex of thrips is found in the field and its composition varies with crop stage and species. Intercropping French bean with other crops compromises on French bean yield but reduces damage to the French bean pods, thereby enhancing marketable yield.

Are Gastropods, Rather than Ants, Important Dispersers of Seeds of Myrmecochorous Forest Herbs?

Seed dispersal by ants (myrmecochory) is widespread, and seed adaptations to myrmecochory are common, especially in the form of fatty appendices (elaiosomes). In a recent study, slugs were identified as seed dispersers of myrmecochores in a central European beech forest. Here we used 105 beech forest sites to test whether myrmecochore presence and abundance is related to ant or gastropod abundance and whether experimentally exposed seeds are removed by gastropods. Myrmecochorous plant cover was positively related to gastropod abundance but was negatively related to ant abundance. Gastropods were responsible for most seed removal and elaiosome damage, whereas insects (and rodents) played minor roles. These gastropod effects on seeds were independent of region or forest management. We suggest that terrestrial gastropods can generally act as seed dispersers of myrmecochorous plants and even substitute myrmecochory, especially where ants are absent or uncommon.