How to escape from insect egg parasitoids: a review of potential factors explaining parasitoid absence across the Insecta.

The egg is the first life stage directly exposed to the environment in oviparous animals, including many vertebrates and most arthropods. Eggs are vulnerable and prone to mortality risks. In arthropods, one of the most common egg mortality factors is attack from parasitoids. Yet, parasitoids that attack the egg stage are absent in more than half of all insect (sub)orders. In this review, we explore possible causes explaining why eggs of some insect taxa are not parasitized. Many insect (sub)orders that are not attacked by egg parasitoids lack herbivorous species, with some notable exceptions. Factors we consider to have led to escape from egg parasitism are parental egg care, rapid egg development, small egg size, hiding eggs, by e.g. placing them into the soil, applying egg coatings or having thick chorions preventing egg penetration, eusociality, and egg cannibalism. A quantitative network analysis of host-parasitoid associations shows that the five most-speciose genera of egg parasitoids display patterns of specificity with respect to certain insect orders, especially Lepidoptera and Hemiptera, largely including herbivorous species that deposit their eggs on plants. Finally, we discuss the many counteradaptations that particularly herbivorous species have developed to lower the risk of attack by egg parasitoids.

Pest kill rate as aggregate evaluation criterion to rank biological control agents: a case study with Neotropical predators of Tuta absoluta on tomato.

Tuta absoluta (Meyrick), a key pest of tomato, is quickly spreading over the world and biological control is considered as one of the control options. Worldwide more than 160 species of natural enemies are associated with this pest, and an important challenge is to quickly find an effective biocontrol agent from this pool of candidate species. Evaluation criteria for control agents are presented, with the advantages they offer for separating potentially useful natural enemies from less promising ones. Next, an aggregate parameter for ranking agents is proposed: the pest kill rate km. We explain why the predator's intrinsic rate of increase cannot be used for comparing the control potential of predators or parasitoids, while km can be used to compare both types of natural enemies. As an example, kill rates for males, females and both sexes combined of three Neotropical mirid species (Campyloneuropsis infumatus (Carvalho), Engytatus varians (Distant) and Macrolophus basicornis (Stål)) were determined, taking all life-history data (developmental times, survival rates, total nymphal and adult predation, sex ratios and adult lifespan) into account. Based on the value for the intrinsic rate of increase (rm) for T. absoluta and for the kill rate km of the predators, we predict that all three predators are potentially able to control the pest, because their km values are all higher than the rm of the pest. Using only km values, we conclude that E. varians is the best candidate for control of T. absoluta on tomato, with C. infumatus ranking second and M. basicornis last.

Do nymphs and adults of three Neotropical zoophytophagous mirids damage leaves and fruits of tomato?

The predators Macrolophus basicornis (Stal), Engytatus varians (Distant) and Campyloneuropsis infumatus (Carvalho) consume large numbers of tomato pests such as Bemisia tabaci (Gennadius) and Tuta absoluta (Meyrick). However, they are zoophytophagous and feed on plant parts as well. We evaluated the type and effect of injury caused by nymphs and adults of these mirids on tomato seedlings and fruit in the absence of prey. For each mirid species, seedlings were exposed to groups of 20 nymphs or adults for 72 h, and fruits were exposed for 48 h to groups of four nymphs or adults. Type and the number of injury on stems, petioles and leaflets of tomato seedlings and fruits were recorded after removal of insects. Nymphs and adults of these mirids caused necrotic rings on the leaflets, but no injury was observed on stem and petioles. The necrotic rings on leaflets consisted of blemishes, characterized by feeding punctures surrounded by a yellowish, bleached area. The number of necrotic rings did not exceed one per individual mirid and seedlings developed normally. Nymphs also caused feeding punctures on tomato fruit, but in even lower numbers than on leaflets. Two weeks after the start of the experiment the tomato fruit still looked fresh and feeding punctures had disappeared. Adults did not cause any injury to tomato fruit. The results indicate that nymphs and adults of these zoophytophagous mirids cause little injury to tomato seedlings and fruit, even when present in high densities and in the absence of prey, making them interesting candidates for biological control.

Quantification of motility of carabid beetles in farmland.

Quantification of the movement of insects at field and landscape levels helps us to understand their ecology and ecological functions. We conducted a meta-analysis on movement of carabid beetles (Coleoptera: Carabidae), to identify key factors affecting movement and population redistribution. We characterize the rate of redistribution using motility µ (L2 T-1), which is a measure for diffusion of a population in space and time that is consistent with ecological diffusion theory and which can be used for upscaling short-term data to longer time frames. Formulas are provided to calculate motility from literature data on movement distances. A field experiment was conducted to measure the redistribution of mass-released carabid, Pterostichus melanarius in a crop field, and derive motility by fitting a Fokker-Planck diffusion model using inverse modelling. Bias in estimates of motility from literature data is elucidated using the data from the field experiment as a case study. The meta-analysis showed that motility is 5.6 times as high in farmland as in woody habitat. Species associated with forested habitats had greater motility than species associated with open field habitats, both in arable land and woody habitat. The meta-analysis did not identify consistent differences in motility at the species level, or between clusters of larger and smaller beetles. The results presented here provide a basis for calculating time-varying distribution patterns of carabids in farmland and woody habitat. The formulas for calculating motility can be used for other taxa.

Environmental risk assessment for plant pests: a procedure to evaluate their impacts on ecosystem services.

The current methods to assess the environmental impacts of plant pests differ in their approaches and there is a lack of the standardized procedures necessary to provide accurate and consistent results, demonstrating the complexity of developing a commonly accepted scheme for this purpose. By including both the structural and functional components of the environment threatened by invasive alien species (IAS), in particular plant pests, we propose an environmental risk assessment scheme that addresses this complexity. Structural components are investigated by evaluating the impacts of the plant pest on genetic, species and landscape diversity. Functional components are evaluated by estimating how plant pests modify ecosystem services in order to determine the extent to which an IAS changes the functional traits that influence ecosystem services. A scenario study at a defined spatial and temporal resolution is then used to explore how an IAS, as an exogenous driving force, may trigger modifications in the target environment. The method presented here provides a standardized approach to generate comparable and reproducible results for environmental risk assessment as a component of Pest Risk Analysis. The method enables the assessment of overall environmental risk which integrates the impacts on different components of the environment and their probabilities of occurrence. The application of the proposed scheme is illustrated by evaluating the environmental impacts of the invasive citrus long-horn beetle, Anoplophora chinensis.

Does Wolbachia infection affect Trichogramma atopovirilia behaviour?

Unisexual Trichogramma forms have attracted much attention due to their potential advantages as biocontrol agents. Fitness studies have been performed and understanding the cost that Wolbachia may inflict on their hosts will help in deciding if Wolbachia infected (unisexual) forms are indeed better than sexual forms when used in biological control programmes. The influence of Wolbachia on the foraging behaviour (including walking activity and speed) of T. atopovirilia is reported in this paper. Temperature strongly affected T. atopovirilia female walking activity, but Wolbachia infected and uninfected females differed in none of the behavioural components that were measured such as walking activity and walking speed. Walking activity was highest at 25 masculineC and differed significantly from that at 20 and 15 masculineC. Trichogramma wasps were highly affected at 15 masculineC. Behaviour analysis with females showed that female wasps spend most of the time on drilling + ovipositing on host eggs followed by host drumming and walking while drumming. The parasitism rate and number of offspring did not differ significantly between infected and cured Trichogramma females. Biological control implications of these findings are discussed.

Biological control and sustainable food production.

The use of biological control for the management of pest insects pre-dates the modern pesticide era. The first major successes in biological control occurred with exotic pests controlled by natural enemy species collected from the country or area of origin of the pest (classical control). Augmentative control has been successfully applied against a range of open-field and greenhouse pests, and conservation biological control schemes have been developed with indigenous predators and parasitoids. The cost-benefit ratio for classical biological control is highly favourable (1:250) and for augmentative control is similar to that of insecticides (1:2-1:5), with much lower development costs. Over the past 120 years, more than 5000 introductions of approximately 2000 non-native control agents have been made against arthropod pests in 196 countries or islands with remarkably few environmental problems. Biological control is a key component of a 'systems approach' to integrated pest management, to counteract insecticide-resistant pests, withdrawal of chemicals and minimize the usage of pesticides. Current studies indicate that genetically modified insect-resistant Bt crops may have no adverse effects on the activity or function of predators or parasitoids used in biological control. The introduction of rational approaches for the environmental risk assessment of non-native control agents is an essential step in the wider application of biological control, but future success is strongly dependent on a greater level of investment in research and development by governments and related organizations that are committed to a reduced reliance on chemical control.

Assessing risks of releasing exotic biological control agents of arthropod pests.

More than 5000 introductions of about 2000 species of exotic arthropod agents for control of arthropod pests in 196 countries or islands during the past 120 years rarely have resulted in negative environmental effects. Yet, risks of environmental effects caused by releases of exotics are of growing concern. Twenty countries have implemented regulations for release of biological control agents. Soon, the International Standard for Phytosanitary Measures (ISPM3) will become the standard for all biological control introductions worldwide, but this standard does not provide methods by which to assess environmental risks. This review summarizes documented nontarget effects and discusses the development and application of comprehensive and quick-scan environmental risk assessment methods.

Variation in plant volatiles and attraction of the parasitoid Diadegma semiclausum (Hellén).

Differences in allelochemistry of plants may influence their ability to attract parasitoids. We studied responses of Diadegma semiclausum (Hellén), a parasitoid of the diamondback moth (Plutella xylostella L.), to inter- and intraspecific variation in odor blends of crucifers and a non-crucifer species. Uninfested Brussels sprout (Brassica oleracea L. gemmifera), white mustard (Sinapis alba L.), a feral Brassica oleracea, and malting barley (Hordeum vulgare L.) were compared for their attractivity to D. semiclausum in a Y-tube bioassay. Odors from all plants were more attractive to the parasitoid than clean air. However, tested against each other, parasitoids preferred the volatile blend from the three cruciferous species over that of malting barley. Wasps also discriminated between uninfested crucifers: mustard was as attractive as feral B. oleracea, and both were more attractive than Brussels sprout. Attractivity of uninfested plants was compared with that of plants infested by larvae of the host P. xylostella. Host-infested mustard and Brussels sprout were more attractive than uninfested conspecifics. Interestingly, the volatile blends of uninfested white mustard and infested Brussels sprout were equally attractive. We also compared the volatile composition of different plant sources by collecting headspace samples and analysing them with GC-MS. Similarities of volatile profiles were determined by hierarchic clustering and non-metric scaling based on the Horn-index. Due to the absence of several compounds in its blend, the volatile profile of barley showed dissimilarities from blends of crucifers. The odor profile of white mustard was distinctly different from the two Brassicaceae. Feral Brassica oleracea odor profile was different from infested Brussels sprout, but showed overlap with uninfested Brussels sprout. Odor blends from infested and uninfested Brussels sprout were similar, and mainly quantitative differences were found. D. semiclausum appears to discriminate based on subtle differences in volatile composition of odor blends from infested and uninfested plants.

A two-component model of host-parasitoid interactions: determination of the size of inundative releases of parasitoids in biological pest control.

A two-component differential equation model is formulated for a host-parasitoid interaction. Transient dynamics and population crashes of this system are analysed using differential inequalities. Two different cases can be distinguished: either the intrinsic growth rate of the host population is smaller than the maximum growth rate of the parasitoid or vice versa. In the latter case, the initial ratio of parasitoids to hosts should exceed a given threshold, in order to (temporarily) halt the growth of the host population. When not only oviposition but also host-feeding occurs the dynamics do not change qualitatively. In the case that the maximum growth rate of the parasitoid population is smaller than the intrinsic growth rate of the host, a threshold still exists for the number of parasitoids in an inundative release in order to limit the growth of the host population. The size of an inundative release of parasitoids, which is necessary to keep the host population below a certain level, can be determined from the two-component model. When parameter values for hosts and parasitoids are known, an effective control of pests can be found. First it is determined whether the parasitoids are able to suppress their hosts fully. Moreover, using our simple rule of thumb it can be assessed whether suppression is also possible when the relative growth rate of the host population exceeds that of the parasitoid population. With a numerical investigation of our simple system the design of parasitoid release strategies for specific situations can be computed.

A total system approach to sustainable pest management.

A fundamental shift to a total system approach for crop protection is urgently needed to resolve escalating economic and environmental consequences of combating agricultural pests. Pest management strategies have long been dominated by quests for "silver bullet" products to control pest outbreaks. However, managing undesired variables in ecosystems is similar to that for other systems, including the human body and social orders. Experience in these fields substantiates the fact that therapeutic interventions into any system are effective only for short term relief because these externalities are soon "neutralized" by countermoves within the system. Long term resolutions can be achieved only by restructuring and managing these systems in ways that maximize the array of "built-in" preventive strengths, with therapeutic tactics serving strictly as backups to these natural regulators. To date, we have failed to incorporate this basic principle into the mainstream of pest management science and continue to regress into a foot race with nature. In this report, we establish why a total system approach is essential as the guiding premise of pest management and provide arguments as to how earlier attempts for change and current mainstream initiatives generally fail to follow this principle. We then draw on emerging knowledge about multitrophic level interactions and other specific findings about management of ecosystems to propose a pivotal redirection of pest management strategies that would honor this principle and, thus, be sustainable. Finally, we discuss the potential immense benefits of such a central shift in pest management philosophy.

[Is chemical pest control coming to an end?]. / Heeft de chemische plaagbestrijding zijn langste tijd gehad?

Problems that arise when chemical control of pests is applied--risks for producer, applier, consumer and the environment as well as development of resistance against pesticides--have led to the conclusion that other forms of pest control have to be searched for to guarantee production of sufficient crops in the future. Out of the many available methods to prevent or reduce pests two methods seem to offer most possibilities for the near future: development of (partial) host-plant resistance against pests and the search for natural enemies of pests (the so called biological control). In this article the development of biological pest control is described and a comparison is made between working methods, efficiency and risks in application of chemical and biological control. Several examples are given of successful biological control projects as applied in greenhouses in the Netherlands.

Characterisation of the arrestment responses of Trichogramma evanescens.

Contact kairomones and oviposition in a host egg stimulated arrestment behaviour in Trichogramma evanescens, characterised by a reduction in walking speed and increased turning. Previous oviposition experience did not influence a parasitoid's response to contact kairomones, but successive encounters with kairomone patches resulted in parasitoids habituating to the contact chemical. Oviposition on a kairomone patch did not reverse this habituation effect. It was concluded that contact kairomones and host eggs will both contribute independently to the duration of a patch visit. The selection of patches by T. evanescens will depend on its response to kairomones. Results from this study indicate that the application of contact kairomones to field crops will not necessarily increase the probability of parasitoids finding hosts.

Kairomones for the egg parasiteTrichogramma evanescens Westwood : I. Effect of volatile substances released by two of its hosts,Pieris brassicae L. andMamestra brassicae, L.

In a four-armed airflow olfactometerTrichogramma evanescens Westwood females were attracted by a volatile substance(s) released by virgin females of the great cabbage white butterfly,Pieris brassicae L. Males or recently mated females did not cause attraction. Furthermore,T. evanescens was also attracted by volatiles released by calling virgin cabbage moths,Mamestra brassicae L. However, the parasites did not respond to (Z)-11-hex-adecenylacetate (the main component of the sex pheromone ofM. brassicae), a crude hexane extract of the sex pheromone gland, or to males or recently mated females.

Intensification and prolongation of host searching inLeptopilina heterotoma (Thomson) (Hymenoptera: Eucoilidae) through a kairomone produced byDrosophila melanogaster.

A chemical cue (kairomone) of the host, larvae ofDrosophila, was found to influence patch-time allocation of the parasiteLeptopilina heterotoma. This kairomone is soluble in water and chloroform. The kairomone was purified using thin-layer chromatography. The concentration of the kairomone increases with an increasing number of hosts. The parasites may use presence and concentration of the kairomone as cues to determine patch-time allocation.

Chemical stimuli in host-habitat location byLeptopilina heterotoma (Thomson) (Hymenoptera: Eucoilidae), a parasite ofDrosophila.

Chemical stimuli play an important role in the process of searching for a host habitat by parasitic wasps. Volatile compounds originating from host habitats and/or hosts are the cues that enable such a location.Leptopilina heterotoma, a larval parasite ofDrosophila, is attracted to the food of its host, baker's yeast. Analysis of the fermentation products of baker's yeast, using a mass spectrometer, and olfactometer studies indicate that three fermentation products of this yeast, the main component of the host habitat in our laboratory, attractL. heterotoma: ethanol (5%), ethyl acetate (10(-2), 10(-3)%), and acetaldehyde (1%). A combination of these three compounds, however, cannot compete with baker's yeast in attracting the parasites. Thus other factors, such as different compounds, concentrations, and/or combinations, also, play a role and remain to be tested.Leptopilina heterotoma does not use host-related olfactory cues in long-distance habitat location as it cannot distinguish between host habitat and host habitat with hosts.

A "Border-Line detector" for recording locomotory activities of animals.

A T.V. Border-Line detector is described for making automatic long-term records of locomotory activity of animals.The apparatus is used in combination with a closed T.V. system. A video recorder is switched on for some seconds at the moment an animal passes a fictitious detection line corresponding with a scanning-line of a T.V.-picture.

Some models describing the distribution of eggs of the parasitePseudeucoila bochei (Hym., Cynip.) over its hosts, larvae ofDrosophila melanogaster.

Ovipositing females of the cynipid waspPseudeucoila bochei discriminate between parasitized and unparasitized hosts, which results in a far more uniform distribution of eggs over the hosts than would be obtained if oviposition were random (Fig. 1,a 0-f 0).For the description of the distributions a few models were worked out, which rest on the assumption that the hosts are probed at random. The total number of effective probes made in a larva during the experiment is a random variable with a Poisson distribution and an expectation λ. The chance that at a certain probe an egg will be laid (δ) is dependent on the number of eggs present (j); 1=δ0<δ1≧δ2≧δ3.... In model I it was assumed that the female had only the ability to distinguish parasitized from unparasitized hosts. The chance that an egg will be laid in an unparasitized host when it is probed, δ0, is considered to be equal to 1, while δ1=δ2=...=δ n <1 (Fig. 2, 1,a 1-f 1). When the mean number of eggs present in a host was larger than about 1.1, this model did not describe the distribution of eggs satisfactorily (Fig. 3).It seemed that the ovipositing female is not only able to distinguish parasitized from unparasitized hosts, but also to distinguish thenumber of eggs present in a host. In model II it was assumed that the wasp could distinguish between hosts with 0, 1, and 2 or more eggs: the chance that an egg would be laid in a host containing 2, 3, 4, ... eggs was, hence, the same in this model δ1<δ2=δ3=...=δ n (Fig. 2, 1,c 2,e 2,f 2). This model described the distributions of eggs much better (Figs. 4 and 5), but at mean numbers of eggs per host above 2 it was apparently inadequate.Two other models were then tried, in which the chance δ that an egg would be laid in a host decreased with the number of eggs already present (j). In model III (Fig. 2) the chance decreased according to the function δ j =δ/j (δ0=1, δ<1). Fig. 1,d 3,e 3,f 3, gives some examples. In model IV the chance δ j =δ j (δ0=1, δ<1) (see Fig. 1,d 4,e 4,f 4).From the comparison of Figs. 6 and 7 it is clear that model IV gives the best description of the distributions of eggs found.The value of these models is discussed, and plans for both an approach through experimental analysis and simulation models are given. In an Appendix the mathematical derivation of the models is presented.