Evaluation and application of parasitoids for biological control of Aphis gossypii in glasshouse cucumber crops

IntroductionAphids are an important problem in glasshouse vegetables. Already at low aphid densities fruits can get contaminated with honeydew, which decreases the economical value of the fruits. When aphids feed on the growing tips of the plants, the new shoots can get heavily distorted and plant growth is reduced. At the time this project was started integrated aphid control in cucumber and sweet pepper crops consisted of introduction of the parasitoid Aphidius matricariae Haliday (Hymenoptera: Braconidae) and the predatory gall midge Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Integrated control of Myzus persicae Sulzer (Homoptera: Aphididae) in sweet pepper was effective, but A. gossypii was little affected by the introduced parasitoids. Additional control with the selective aphicide pirimicarb was also not possible since cotton aphid has developed resistance against this chemical. Aphid control with non-selective insecticides inhibits the use of biological control of other pests (like thrips and whitefly) in the glasshouse, which is applied on a large scale in the Netherlands. To be able to keep using biological control of other pests it is, therefore, necessary to develop an effective biological control programme for cotton aphid as well. In Chapter 1 the biology of cotton aphid and its most important natural enemies is described. This literature review showed that detailed data on the biology of A. gossypii were scarce. Therefore, the first experiments consisted of detailed research on the biology of cotton aphid.Research to develop biological control of A. gossypii can be divided into two main lines. First of all a selection of (a) potential candidate(s) for the control of A. gossypii has to be made. Many natural enemies of aphids are known, ranging from monophagous to polyphagous species. The natural enemies can be divided into three groups: pathogens (mainly parasitic fungi), predators (like ladybeetles, lacewings and hoverflies) and parasitoids. Based on several criteria, a literature survey indicated that parasitoids seemed most promising.Insect pathogens need very high humidities for successful germination and sporulation. These humidities are difficult to maintain in glasshouses for sufficiently long periods and can cause plant diseases.Predators have lower population growth rates than parasitoids and will, therefore, not be able to react to increasing aphid densities as quickly as parasitoids. Additionally, predator larvae need many aphids for successful development which might give problems during periods of low aphid density. Finally, predators are more expensive to culture (with the exception of A. aphidimyza ), because of the cannibalistic habits of the larvae. Parasitoid populations can multiply rapidly because of a short development time, and parasitoids need only one aphid for successful development. Based on the high reproductive capacity and the possibility of rearing parasitoids in large quantities, parasitoids seem to be the most promising group of aphid natural enemies.Secondly, an efficient method has to be developed for the introduction of natural enemies in a glasshouse. In glasshouses the interaction between aphids and natural enemies is wave-like. The natural enemies are efficient searchers and are able to destroy the aphid population almost completely. When few aphids are present, most of the natural enemies Will die and the aphid population can grow again once few aphids have entered the glasshouse from outside. A more stable situation can be created by introducing many parasitoids very frequently, but this would be very expensive. A second solution is the creation of a refuge for the parasitoids in the form of banker plants with aphids, which are harmless to the crop. On these refuges the parasitoidscan multiply independently of the presence of aphids in the crop. As a consequence a continuous presence of a large number of natural enemies is ensured during the entire cropping period.In the next section the life history of A. gossypii will be described. Thereafter the two lines of research ((a) what is the best parasitoid and (b) what is the best introduction method) will be dealt with.Life history of Aphis gossypiiIn Chapter 2 the influence of temperature, host plant cultivar and parasitism on the life history data of the cotton aphid are described. The potential population growth of a cotton aphid population is highest at 25 °C, because of a shorter development time and a higher daily reproduction at this temperature. There is a good agreement between life history data in the laboratory and in glasshouses. The development times on two cucumber cultivars differs markedly. Partial host plant resistance can be a useful tool for improving biological control of cotton aphid.Aphids, successfully parasitized by Aphidius colemani Viereck (Hymenoptera: Braconidae) only reproduce when they are parasitized in the fourth instar or as adult. These aphids produce nymphs for several days but, because of the short development time of the nymphs, they still have a large contribution to the growth of the aphid population.Evaluation of parasitoidsThe evaluation of several parasitoids is described in Chapter 3. For aphidiine parasitoids a small laboratory experiment gives a good indication on the usefulness of the parasitoids in glasshouses. Out of four parasitoid species A . colemani is the most promising control agent. This species finds more aphid colonies in glasshouses and higher parasitization rates are obtained than for A. matricariae , Ephedrus cerasicola Stary and Lysiphlebus testaceipes Cresson (Hymenoptera: Braconidae).Because of the different reproduction strategies, comparison of Aphelinus varipes Förster (Hymenoptera: Aphelinidae) with aphidiine parasitoids is not possible in the laboratory. Aphidiine parasitoids have a higher daily reproduction but a shorter reproduction period compared to aphelinids. Therefore, A. varipes was compared with A. colemani in small glasshouses. The combined effect of A. varipes and A. colemani results in better and more stable control than when A. colemani is introduced alone.Life history of parasitoidsFor several parasitoids life history data were collected in more detail (Chapter 4). Both A.colemani and L. testaceipes have a very high daily reproduction and a short development period. The population growth rates are slightly lower than for A. gossypii. The life span of the parasitoids is only a few days. This might create problems when these parasitoids are used for preventive introductions in glasshouses, because the introduced parasitoids will be present for a short period only. Aphidius -species can parasitize many aphids during a reproduction period of a few days, whereas Aphelinus -parasitoids parasitize less aphids daily over a longer reproduction period. Development of A. varipes takes longer than the development of the aphidiine parasitoids at 20 °C, but at temperatures above 25 °C the development times and population growth rates are equal. The life span of A. varipes is considerably longer than for A. colemani.Aphefinus varipes parasitoids will survive periods of low aphid density for a longer period.Searching behaviour of Aphidius colemaniThe searching behaviour of A. colemani is described in Chapter 5. Few oviposition experiences increases the responsiveness of females to host plants. The parasitoids are able to detect the presence of aphids on a leaf from a short distance even if no directed air current is present. When the parasitoids can choose between a clean and an aphid infested leaf, most of the parasitoids fly to the aphid infested leaf. Oviposition experiences on the grain aphid Rhopalosiphum padi Linnaeus (Homoptera: Aphididae) do not change the in-flight host location by A. colemani. Therefore, the use of banker plants with R. padi will probably not influence the searching behaviour of A. colemani.Once in an aphid colony the functional response (the reaction of individual parasitoids to the number of aphids present) of A.colemani is sigmoid. The increase of the parasitization rates is clearest at densities of up to ten aphids per leaf disk. At higher aphid densities the parasitization rate decreases gradually. After re-entering a recently visited leaf disk the parasitoid stays for a much shorter time than the first visit. No evidence of patch marking is found, so the reduction of visiting times is probably caused by encounters with parasitized hosts.Also the time allocation of individual A.colemani female parasitoids foraging for A. gossypii nymphs on cucumber leaves has been investigated. The leaving tendency only decreases on leaves with a high host density (100 aphids), thus increasing the giving up time since the latest encounter. Rejection of aphids and the nearby presence of another aphid colony has no influence on the leaving tendency. The effect of the number of hosts encountered differs among aphid densities. When less than ten aphids are present the leaving tendency is much larger after 30 encounters than beforehand. At a density of 100 aphids the leaving tendency is lower than at the other aphid densities and increases only after 100 encounters. Repeated visits to leaves with ten unparasitized aphids results in an increase in the leaving tendency after approximately ten visits. These results can be explained by assuming that the parasitoids have some innate expectancy of the spatial distribution of hosts (which is likely to be clustered) and concentrate their searching time on high density patches.Application of Aphidius colemaniIn Chapter 6 application of A. colemani is studied. The effect of repeated introductions of parasitoids depends highly on the timing and size of the introductions. Natural enemies have to be present in large numbers to obtain sufficient and immediate control. With lower introduction rates not all aphids will be parasitized. As a consequence the aphid population keeps on growing. Sufficient control is only obtained when the parasitoid population has built up sufficiently, which might be too late to prevent damage to the crop. Especially in summer successful control will be difficult to obtain because at the higher temperatures the colonies which are not found by the parasitoids will grow much faster.An open rearing with wheat plants and grain aphids (R. padi) can be used to maintain a parasitoid population, independent of the occurrence of cotton aphid in the glasshouse. Compared to weekly introductions the open rearing method gives initially a much better aphid control, mainly because of the high number of parasitoids than can be reared on the open rearings. At the end of the cucumber cropping hyperparasitoids can occur on the open rearing of the parasitoids. At this point the number of parasitoids will decrease, followed by an increase in aphid numbers. If hyperparasitoids start to increase, other natural enemies (like the gall midge, A. aphidimyza ) can also be introduced with the open rearing method. In glasshouses with repeated introductions the influence of hyperparasitoids is much less, even though they do also occur in these glasshouses.Apart from A. gossypii several other aphid species frequently are a pest in glasshouses. The most important species are the tomato aphid, Macrosiphum euphorbiae Thomas (Homoptera: Aphididae) and the peach aphid M.persicae. A short test, as done for evaluation of parasitoids in Chapter 4 is used to test whether A. colemani , A. matricariae , E. cerasicola and L. testaceipes can be useful for control of these aphids too. None of the parasitoids produces mummies on M. euphorbiae. Only A. colemani parasitizes A. gossypii and M. persicae successfully and it is concluded that A.colemani seems to be the most suitable species for control of both cotton and green peach aphid.In the general discussion (Chapter 7) it is concluded that evaluation of parasitoids based on several individual criteria can give erroneous results. Life history data of A.colemani and L. testaceipes are not very different, whereas there is a large difference in the effectivity in glasshouses. Also it is made clear that evaluation of different types of parasitoids is difficult in the laboratory. Additionally, the importance of individual evaluation criteria will depend on the system that is studied and the type of control that has to be obtained. For aphid control in glasshouses it is important that a rather constant low aphid level is maintained. A good searching capacity (finding aphid colonies quickly) is a very important characteristic of a successful natural enemy. Aphid colonies have to be found quickly to prevent the colonies from becoming too large. Because aphid parasitoids are able to reduce the aphid population to very low levels (where also only a small amount of parasitoids will be present) the system is very sensitive to incoming aphids. The only way to obtain sufficient control is by ensuring a continuous presence of a sufficient amount of parasitoids. If this succeeds successful control of A. gossypii can be obtained by using the parasitoid A. colemani.