Elisabeth Tabone

Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control.

The tomato leafminer Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a devastating pest of tomato originating from South America. After its initial detection in eastern Spain in 2006, it rapidly invaded various other European countries and spread throughout the Mediterranean basin. If no control measures are taken, then the pest can cause up to 80–100% yield losses in tomato crops in recently invaded areas and may pose a threat to both greenhouse and open-field tomato production. The exceptional speed and extent of T. absoluta invasion have called for studies documenting its biology and ecology, while indicating an urgent need for efficient and sustainable management methods. The development of approaches to manage T. absoluta would be facilitated through a detailed revision of information on this pest in its area of origin. This review combines information on the invasion by T. absoluta, its ecology, and potential management strategies, including data that may help the implementation of efficient biological control programs. These programs, together with a variety of other management tactics, may allow efficient integrated pest management of T. absoluta in Europe and Mediterranean Basin countries.

Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta.

The South American tomato pinworm (Tuta absoluta) has recently invaded Europe and is rapidly spreading in the Afro-Eurasian continent where it is becoming a major pest on tomato crops. Laboratory tests were undertaken to evaluate the potential of 29 European strains of Trichogramma parasitoids to control T. absoluta. In addition to the host itself, the host plant (tomato) was used during the laboratory tests in order to increase the chance of selecting the best parasitoid strains. Trichogramma females were placed with T. absoluta eggs on a tomato leaflet in tubes. We compared the parasitism of T. absoluta by the various Trichogramma species tested to the Trichogramma species currently commercially available for the pest control in Europe, i.e. Trichogramma achaeae. Thereafter, the more promising strains were tested on a larger scale, in mesocosm (i.e. cages in greenhouses) and in greenhouse compartments to evaluate efficiency of laboratory selected strains under cropping conditions. The most efficient strain from the laboratory screening trials did not perform as efficiently under the greenhouse conditions. We discuss differences in parasitism levels among species and strains and among the different scales tested in the experiments, as well as implications of these results for further screening for biocontrol agents.

Suitability of the Pest—Plant System Tuta absoluta (Lepidoptera: Gelechiidae)—Tomato for Trichogramma (Hymenoptera: Trichogrammatidae) Parasitoids and Insights for Biological Control

ABSTRACT The South American tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), is a major pest that has recently invaded Afro-Eurasia. Biological control, especially by Trichogramma parasitoids, is considered to be promising as a management tool for this pest. However, further development of Trichogramma-based biocontrol strategies would benefit from assessing the impact of released parasitoid offspring on the pest. Under laboratory conditions, we 1) compared the parasitism of five Trichogramma species-strains on the pest-plant system T. absoluta-tomato, and 2) assessed various biological traits of parasitoids, mass-reared on a factitious host (Ephestia kuehniella Zeller), when developing on T. absoluta. In addition, we evaluated the overall efficiency of two specific Trichogramma species when released under greenhouse conditions in combination with a common natural enemy in tomato crop, the predator Macrolophus pygmaeus Rambur. Parasitoids emerging from T. absoluta on tomato showed lower parasitism rates and poor biological traits, for example, wing deformations, reduced longevity, when compared with the control reared on the factitious host. Under greenhouse conditions, the parasitoids that developed on T. absoluta after initial releases contributed little to biological control of T. absoluta, and parasitism tended to be lower when the predator was present. However, a slightly higher T. absoluta control level was achieved by combining the predator and release of the parasitoid Trichogramma achaeae Nagaraja and Nagarkatti. This study shows that Trichogramma parasitoids may not build up populations on the T. absoluta-tomato system, but that Trichogramma parasitoids can be used in combination with M. pygmaeus to enhance biological control of the pest in tomato crops.

A comparative analysis of patch-leaving decision rules in a parasitoid family

The proximate behavioural rules adopted by parasitoid females to manage their foraging time on patches of hosts were studied, under standardized laboratory conditions, in different species (and populations) of the Trichogrammatidae (Hymenoptera) family. Seventeen species/populations were compared and the behavioural mechanisms adopted by the females were identified by means of a Coxs proportional hazards model. On average, females increased their patch-leaving tendency each time a healthy host was attacked and each time a parasitized host was rejected. Strong variation was observed in these patch-leaving mechanisms among the different species. Moreover, the interspecific variation in these two behavioural mechanisms showed a significant positive correlation, and this correlation remained significant when the phylogenetic relationship between the strains was controlled with the use of phylogenetic comparative methods. The adaptive and evolutionary meanings of these results are probably related to the ecological features and distribution patterns of the hosts attacked by the species/populations compared.

Parasitism of different Trichogramma species and strains on Plutella xylostella L. on greenhouse cauliflower

The diamondback moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae), is the most important pest of cultivated Brassica worldwide, including those grown in greenhouses like cauliflower. In this article, we evaluate the potential of various species (and various strains of some species) of Trichogrammatidae (Hymenoptera: Chalcidoidea) to control this pest on cauliflower in greenhouse in France. We assessed the parasitism levels on P. xylostella of 17 Trichogrammatidae strains, belonging to 12 different species (2 indigenous strains from France), under greenhouse conditions. Parasitism levels for each of the Trichogrammatidae species and strains were determined on cauliflower leaves (Brassica oleraceabotrytis L., Brassicaceae) infested with P. xylostella eggs. Nine strains parasitized 60% (or more) of the P. xylostella eggs. Compared to previous results in laboratory conditions, climatic conditions of the greenhouse did not influence parasitism levels. The presence of the cauliflower plants may have a positive effect on eight strains, a negative effect on four strains and no effect on five strains. Our study points out the importance of including the host plant of P. xylostella when conducting studies aiming to select the most efficient parasitoid against this pest.

Functional response of #Trichogramma chilonis# to #Galleria mellonella# and #Chilo sacchariphagus# eggs

A biological control programme using inundative releases of Trichogramma chilonis Ischii (Hymenoptera: Trichogrammatidae) reared on Galleria mellonella L. (Lepidoptera: Pyralidae) is currently underway to reduce infestations of Chilo sacchariphagus Bojer (Lepidoptera: Crambidae) in sugarcane, Saccharum spp., on Réunion Island. To assess the potential of the parasitoid as an inundative biocontrol agent, the functional response of three T. chilonis strains was tested with G. mellonella and one strain with C. sacchariphagus host eggs in glass tubes in the laboratory. The shape of the functional response (type II or III) was determined using logistic regression, and attack coefficients and handling times (Th) were determined using non‐linear least‐square regression. The behaviour of all three strains with G. mellonella host eggs corresponded to a type III response. The St Benoît T. chilonis strain had a significantly shorter estimate of Th than the St Pierre strain (P<0.05) and may, therefore, be more appropriate as a biocontrol agent. The functional response with C. sacchariphagus host eggs was a type II with the St Benoît T. chilonis strain. More T. chilonis wasps developed per host egg from the larger C. sacchariphagus host eggs (2.9) relative to G. mellonella (1.1). Superparasitism at low host egg densities was, therefore, likely to have been less frequent with C. sacchariphagus. Black eggs were chosen as an estimate of number of eggs parasitized, although they represent the number of eggs where parasitism led to complete pupal development. The low rate of detected parasitism at low host densities with G. mellonella eggs may be due to incomplete pupal development due to superparasitism rather than lack of parasitism, thus explaining the type III functional response.

Importance of host oviposition pattern and plant size for the selection of Trichogramma strains to control the diamondback moth

The aim of this work was to select a candidate strain of Trichogrammatidae (Hymenoptera: Chalcidoidea) to control the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), an important pest of cabbage in Europe. The parasitic efficiency of Trichogramma chilonis Ishii from Japan and Réunion Island, Trichogramma evanescens Westwood from Egypt, Trichogramma ostriniae Pang & Chen from Japan, and Trichogramma semblidis (Aurivillius) from France was studied with sentinel eggs in greenhouse‐grown cauliflower. The percentage of parasitized eggs was measured 1 m from the release point and 3 days after release. Two factors were studied: host‐egg density (three eggs per stem vs. 50 eggs per stem) and plant size (50–100 cm high plants vs. 100–150 cm high plants). Trichogramma evanescens from Egypt achieved the best parasitism. Parasitism efficiency of T. ostriniae from Japan and T. chilonis from Réunion Island was not influenced by egg density. In contrast, parasitism efficiencies of the three other strains were higher at the lower egg density than at the higher egg density. Parasitism efficiency was lower when the plants were bigger, with the exception of T. chilonis from Réunion Island, for which the level of parasitism was not affected by plant size. Thus, T. chilonis from Réunion Island appeared to be the most suitable Trichogramma strain for use in controlling P. xylostella, regardless of the growth stage of the crop. However, T. ostriniae from Japan may also be more suitable for use on cauliflower crops at the early stage of crop development. If potential problems related to the introduction of exotic species are taken into consideration, it is possible to consider the native T. evanescens.

Density-dependent dispersal in biological control agents: a reflexion on the side-effects of mass-rearing conditions

High-density rearing conditions for the mass-production of biological control agents are known to affect individual quality and performance. However, complex phenotypic traits like dispersal behaviour and their response to rearing conditions are rarely investigated, although they are likely to affect directly biocontrol efficiency in the field. In this study, we develop an original experimental design to evaluate two complementary components of dispersal behaviour in Trichogramma. Then, we investigate how these components respond to variations in rearing density, and their correlation with traits related to parasitoid fitness. We find that under high-density conditions, a large proportion of individuals display reduced mobility and fecundity, indicative of a lower-quality phenotype. These interactive effects between dispersal performance and individual fitness highlight the need to develop integrative experimental designs to easily quantify complex phenotypic traits related to the field performance of biological control agents.

A new substitute host and its effects on some biological properties of Ooencyrtus kuvanae

Lymantia dispar (L.) (Lepidoptera: Lymantriidae), commonly known as the gypsy moth, is a serious forest pest, and beneficial insects are particularly important for reducing its population numbers. Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) is an arrhenotokous, solitary egg parasitoid of L. dispar. In this study, we evaluated a new substitute host, Philosamia ricini (Danovan) (Lepidoptera: Saturniidae) for O. kuvanae. We investigated some of the biological effects of O. kuvanae on P. ricini eggs. In this context, the importance of the age of the female parasitoid (1, 3 or 5 days old), host age (1-2 and 3-4 days old) and host number (40, 60 and 80 host eggs) were examined under laboratory conditions (25 ± 1 °C, 65 ± 5% relative humidity and a 16 : 8 h photoperiod [light : dark]). The highest rate of offspring production (89.90%) occurred with 40 (1-2-day-old) host eggs and 5-day-old females. The mean developmental period ranged from 16.5 ± 0.08 days to 18.7 ± 0.08 days. The mean lifespan of the parasitoid was 51.10 ± 1.1 (n = 60) days with bio-honey and 3.92 ± 0.14 (n = 60) days without food. The mean fecundity was 68.88 ± 3.22 offspring/female. Peak adult emergence occurred between 2 and 9 days. The mean oviposition and mean post-oviposition periods of the female parasitoid were 22.76 ± 1.37 days and 13.64 ± 1.40 days, respectively. O. kuvanae was reared for more than ten generations on the eggs of P. ricini. Based on our findings, P. ricini can be used to rear O. kuvanae for the biological control of L. dispar.

Incidence of superparasitism in the egg parasitoid, Ooencyrtus kuvanae Howard (Hymenoptera: Encyrtidae)

ABSTRACT The encyrtid Ooencyrtus kuvanae is a solitary parasitoid of the gypsy moth, Lymantria dispar L. (Lepidoptera-Lymantridae) that is used in biological control programmes and whose mass rearing is influenced by superparasitism. The purpose of this study was to investigate the effect of the self-superparasitism of O. kuvanae at different host densities (5, 10, 15 and 20), female ages (3 and 5 days) and durations of exposure (1 and 5 days) under various laboratory conditions (25°C ± 1°C, RH 60 ± 5% and a 16:8 h light:dark photoperiod) as well as in a new laboratory host, Philosamia ricini (Danovan) (Lepidoptera: Saturniidae) of O. kuvanae. In this study, we determined the rate of egg superparasitism and adult emergence and recorded development time, longevity and body weight. Superparasitism increased with female age and the duration of exposure to parasitoids when females had access to five host eggs. Superparasitism increased the number of parasitoid offspring, but it resulted in male-biased (56.90%) progeny. Furthermore, superparasitism caused deleterious effects to the fitness of the progeny by prolonging the developmental process, and decreasing longevity. For example, we found that when four adults can emerge from one superparasitised host egg, the body size of the parasitoid offspring decreases significantly. Hence, superparasitism should be avoided when mass rearing O. kuvanae.