H.J.W. van Roermund

Life-history parameters of different biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to temperature and host plant: a selective review

Life-history parameters of different biotypes of the whitefly Bemisia tabaci (Gennadius) species complex were reviewed. This included the B-biotype of B. tabaci , identified as B. argentifolii (Bellows & Perring). Comparisons were made among different biotypes on cotton, among host plants for biotype B and among the whitefly species B. tabaci and Trialeurodes vaporariorum (Westwood), the greenhouse whitefly. The biotype identification of different populations of B. tabaci was summarized in a table. Biotypes discussed were A, B, Indian and biotypes of the Old World group. Temperature dependent relationships were estimated for egg development rate, development rate from egg to adult, immature mortality, adult longevity, sex-ratio, pre-oviposition period and fecundity. The fitted curves will be used as input for a simulation model of the population dynamics of B. tabaci in a greenhouse when parasitoids are released. The model makes it possible to evaluate the integrated effect of different life-history parameters and behavioural parameters of parasitoids on whitefly population levels in a greenhouse.

Aphelinid parasitoids as sustainable biological control agents in greenhouses

Aphelinid parasitoids have been used for control of pests in greenhouses since the 1920s, but large scale application started only some 25 years ago. Today, several aphelinid parasitoids are commercially used for the biological control of scale, aphid and whitefly pests in greenhouses. A success story is the biological control of greenhouse whitefly, Trialeurodes vaporariorum, with the aphelinid Encarsia formosa. Encarsia is applied on 5000 ha of vegetable crops worldwide. Weekly, more than 20 million individuals of E. formosa are mass reared and shipped to growers in 20 countries. About 10 years ago, another whitefly species, Bemisia sp., developed to pest status and a search for control of scales and aphids in greenhouses is summarized, as well as the status of commercial biological control with aphelinid parasitoids. Further, the questions whether effective natural enemies can be identified before introduction and if autoparasitoids should be imported and released are addressed. Finally, the usefulness of parasitoid biotype studies to recognize suitable candidates for biological is considered.

Influence of intrapatch experiences and temperature on the time allocation of the whitefly parasitoidEncarsia formosa (Hymenoptera: Aphelinidae)

The effect of experiences, such as contact with honeydew, rejections of hosts, and ovipositions in hosts, and of temperature on the time allocation of individualEncarsia formosa female parasitoids on tomato leaflets have been studied. Behavioral records were analyzed by means of the proportional hazards model. Analyses were carried out at two levels: (1) the tendency of leaving and (2) the tendency of changing from one leaf side to another. The patch-leaving behavior ofE. formosa can be described by a stochastic threshold mechanism, which is characterized by a certain tendency (probability per time) to leave. The median time from being placed on the leaflet or, if it occurred, from the latest encounter with a host until leaving was 18.6 min. The median time for changing from one leaf side to the other was initially 11.6 min and dropped to 5.7 min after both leaf sides had been visited. The effect of temperature, ranging from 20 to 30°C, was negligible. The presence of honeydew as well as the first oviposition in an unparasitized host decreased the tendency to leave, thus increasing the giving up time (GUT) since the latest encounter with a host. Encounters with parasitized hosts did not affect the GUT since latest encounter; as a result, the total residence time increased. After the first oviposition in an unparasitized host the tendency of changing from the lower leaf side on which hosts were present to the upper side was decreased. The presence of honeydew did not affect the tendency of changing leaf sides.

Foraging behaviour of the whitefly parasitoid Encarsia formosa on tomato leaflets

Individual Encarsia formosa parasitoids were observed continuously until the parasitoids flew away, either on clean tomato leaflets, on leaflets with honeydew, or on leaflets with unparasitized and parasitized whitefly larvae. Encounters with unparasitized and parasitized whitefly larvae, and contact with honeydew arrested the parasitoids on the leaflet. The walking speed increased linearly from 0.179 to 0.529 mm/s between 15 and 25–30 °C. The walking activity showed another relationship with temperature: it was below 10% at 15 and 18 °C, and increased to about 75% at 20, 25 and 30 °C. It was not affected by host encounters or by 1 to 4 ovipositions. The total handling time of hosts was between 1.8–21.8% of the total time on the leaflet. Self‐superparasitism was not observed. Conspecific‐superparasitism did occur in 14% of the encounters with hosts containing a parasitoid egg, but was not observed anymore when the parasitoid egg had hatched. Experienced parasitoids superparasitized as often as naive females. The foraging behaviour of E. formosa from landing on a leaf until departure has now been quantified and is discussed.

Residence times of the whitefly parasitoid Encarsia formosa Gahan (Hym., Aphelinidae) on tomato leaflets

Individual Encarsia formosa parasitoids were observed continuously on either clean, honeydew‐contaminated or whitefly‐infested tomato leaflets until the parasitoids flew away. The residence time on clean leaflets was about 20 min at 20, 25 and 30°C, and was the same on infested leaflets when no hosts were encountered. Encounters with unparasitized and parasitized whitefly larvae, and contact with honeydew prolonged the residence time of the parasitoid on the leaflet. Even when many parasitized black whitefly pupae (unsuitable hosts) were encountered and rejected, the parasitoid was still arrested on that leaflet. Encarsia formosas walking pattern seemed to be random, and parasitoids showed no preference for searching on the upper or lower leaf side when no hosts were encountered. There is also no preference for the edge or for the middle of a leaf. Walking and flight activity of the parasitoids was hardly observed at 15 and 18°C. Many parasitoids became inactive during periods when the barometric pressure decreased but did not when it was stable or increasing.

Analysis of Foraging Behaviour of the Whitefly Parasitoid Encarsia formosa on a plant: A Simulation Study

The foraging behaviour of Encarsia formosa was analyzed using a stochastic simulation model of the parasitoids behaviour. Parasitoids were allowed to search during a day on a tomato plant infested with immatures of the greenhouse whitefly, Trialeurodes vaporariorum. The model simulates searching, host selection, host handling and patch leaving behaviour, and the physiological state of the parasitoid. The outputs of the model are the number of visited leaflets and the number of hosts encountered, parasitized or killed by host feeding. The simulation results agreed well with observations of parasitoids foraging on tomato plants. The number of encounters and ovipositions on the plant increased with host density according to a type II functional response. At a clustered host distribution over leaflets and low host densities, the most important parameters affecting the number of ovipositions were the leaf area, the parasitoids walking speed and walking activity, the probability of oviposition after encounter...

Analysis of foraging behavior of the whitefly parasitoid Encarsia formosa (Hymenoptera: Aphelinidae) in an experimental arena: a simulation study.

Foraging ofEncarsia formosa was analyzed using a stochastic simulation model of the parasitoids behavior. Parasitoids were allowed to search during a fixed time in an experimental arena with immatures of the greenhouse whitefly,Trialeurodes vaporariorum. The model simulates host searching, selection, and handling behavior and the physiological state (egg load) of the parasitoid. The simulated number of hosts encountered, parasitized, or killed by host feeding agreed well with observations on leaf disks. The hypothesis of random host encounter seems to be correct. The number of ovipositions on the leaf at low host densities was strongly affected by the parasitoids walking speed and walking activity, the probability of oviposition after encountering a host, and the initial egg load. At high densities, the initial and maximum egg load were most important. A strong temperature effect was found at 18°C or below. The number of encounters, ovipositions, and host feedings increased with host density to a maximum of 25, 6.5, and 1.5, respectively, during 2 h at 25°C. The shape of the curves resembled a Holling Type II, which may be the result of the “experimental” procedure, where a parasitoid was confined to a patch during a fixed time.

Better biological control by a combination of experimentation and modelling

Greenhouse whitefly (Trialeurodes vaporariorum) and sweet potato whitefly (Bemisia tabaci) are very common, highly polyphagous pest insects worldwide. Biological control of greenhouse whitefly with the parasitoid Encarsia formosa has been applied with great commercial success during the past twenty years, while natural enemies for the sweet potato whitefly are now evaluated. Modelling has played a role in the process of selecting and improving the efficacy of releases of natural enemies, but often biologically unrealistic simplifications were part of these models which strongly limited their predictive value. We have developed a model which is unique in that it is individual-based and simulates the local searching and parasitization behaviour of individual parasitoids in a whitefly-infested crop. The model includes stochasticity and spatial structure based on location coordinates of plants and leaves. This model comprises several submodels for the parasitoid’s foraging behaviour, the whitefly and parasitoid population development, the spatial distribution of whitefly and parasitoid within and between plants in the crop, and for leaf production. With the model we can simulate temporal and spatial dynamics of pest and natural enemy. The model will allow us to explain why the parasitoid can control whiteflies on some crops and not on others in large commercial greenhouses, to improve introduction schemes of parasitoids for crops where control was difficult, to predict effects of changes in cropping practices (e.g. greenhouse climate, choice of cultivars) on the reliability of biological control and, finally, to develop criteria for the selection of natural enemies.

Temporal and spatial analysis of greenhouse whitefly and its parasitoid Encarsia formosa in two types of greenhouse ecosystems

Temporal and spatial relationships between greenhouse whitefly and its parasitoid Encarsia formosa were analysed at different levels by using Rook’s neighbourhood model, and for two types of greenhouses: a small greenhouse in China (15.1u2003m2) and a large greenhouse in the Netherlands (6480u2003m2). For whitefly eggs and larvae, there was no difference in their spatial relationship occurring within‐ and between‐plot in the two types of greenhouses. Eggs and larvae occurrence aggregated with no special directional distributions. Whitefly adults exhibited nonlinear spatial density dependence within‐plot, and moved randomly between‐plot. Whitefly adults preferred to fly away in a N–S directions and to settle down at a NW–SE directions with an increase in the number of their neighbouring infected plants within‐plot. The parasitoid E. formosa showed a strong relationship with the temporal and spatial distribution of the host, but influenced the spatial distribution of whitefly.