Naturally occurring egg parasitoids of the genus Trichogramma (Hymenoptera: Trichogrammatidae) in a pomegranate orchard in Tunisia

Four Trichogramma species were found in a pomegranate orchard in Gabès, an arid region of Tunisia, from parasitized eggs of Ectomyelois ceratoniae Zeller (Lepidoptera: Pyralidae), an economically important insect pest. Identification based on assessment of male genitalia and internal transcribed spacer 2 ( ITS 2) sequences showed that they were T. bourarachae Pintureau and Babault, 1988, T. oleae Voegelé and Pointel, 1979, T. cacoeciae Marchal, 1927 and T. evanescens Westwood, 1833. Trichogramma evanescens is reported for the first time in Tunisia. Trichogramma cacoeciae was the largely dominant species in the analyzed samples, whereas T. bourarachae was present in a minor portion of 1.38%. The implications of these results for attempts at controlling E. ceratoniae are discussed.     

Molecular and morphological diagnoses of five species of Trichogramma: biological control agents of Chrysodeixis chalcites (Lepidoptera: Noctuidae) and Tuta absoluta (Lepidoptera: Gelechiidae) in the Canary Islands

Prospecting for potential natural enemies of the invasive lepidopteran tomato pest Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and the banana pest Chrysodeixis chalcites (Esper) (Lepidoptera: Noctuidae) on the Canary Islands archipelago, where no Trichogramma species were previously recorded, has led to the discovery of five distinct species. T. achaeae Nagaraja & Nagarkatti, T. bourarachae Pintureau & Babault, T. euproctidis (Girault) and T. evanescens Westwood are relatively widespread species. The fifth is close to T. brassicae Bezdenko, but differs sufficiently in the sequence of the ITS2 region of ribosomal RNA to warrant further investigation as a species probably new to science. Each species is treated in detail in order to facilitate identification in future using molecular and/or morphological characters, or a combination of both. All species are newly recorded for the Canary Islands, and the distribution of each within the islands and elsewhere is provided. Known host records are given within the Canary Islands and elsewhere. The most common species found, T. achaeae, is already being used in biological control programmes against T. absoluta in mainland Spain and field trials are ongoing to evaluate its effectiveness as a biological control agent of C. chalcites in banana crops.     

Host-foraging success of three species of Trichogramma (Hymenoptera: Trichogrammatidae) in a simulated retail environment

Three species of trichogrammatid egg parasitoids (Trichogramma deion Pinto & Oatman, Trichogramma ostriniae Pang & Chen, and Trichogramma pretiosum Riley) (Hymenoptera: Trichogrammatidae) were evaluated under laboratory conditions as potential biological control agents for the Indianmeal moth, Plodia interpunctella (Hübner) (Lepidoptera: Pyralidae), on retail shelves. A single shelving unit was used in each trial and a grid of sentinel egg disks was used to evaluate foraging success. The shelving consisted of pallet units with five shelves that were either bare or stocked with empty cereal boxes. In each replicate, approximately 500 female Trichogramma were released at the center of the shelving unit and allowed to forage for 48 h. Percentage of egg parasitism and percentage of host egg mortality were recorded after 7 d. Foraging success as well as the spatial pattern of parasitism differed significantly among the three Trichogramma species. Percentage of egg parasitism was approximately 4 times greater for T. deion than for T. ostriniae or T. pretiosum. The vertical distribution of parasitism by T. deion was also more uniform than for the other two species. In addition, the presence of packaging affected the foraging efficiency of T. ostriniae and T. pretiosum but not T. deion. Based on these findings, Trichogramma deion may be the best-suited candidate for augmentative biological control of P. interpunctella in retail stores, and a central release point of T. deion will likely provide adequate coverage of products on pallet-type shelving.     

Temperature and strain effects on reproduction and survival of Trichogramma oleae and Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae)

To assess differences in temperature sensitivity during development, life tables for two lines derived from the species Trichogramma oleae Voegelé and Pointel and a strain of Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae) were elaborated at 15, 20, 25, 30, 35, 36, and 37°C in the laboratory. Eggs of Ephestia kuehniella Zeller together with a fresh drop of honey were supplied every 2 days until the death of the test females, and the removed host egg batches were placed in the equivalent rearing cabinet. The line ‘2F’ of T. oleae was found to be the most efficient at any range of temperatures except at 20 and 37°C, in comparison to the other tested strains. For all species, no progeny emerged from eggs incubated at 36°C and none of the parasitized eggs turned black at 37°C. The better performance at a broader range of temperatures by T. oleae (line 2 F) might be caused by a shorter history in artificial rearing in comparison to the other strains. Fewer generations at laboratory conditions and frequent multiplication on eggs of its natural host (the olive moth Prays oleae) may have prevented a deterioration in the rearing population of this strain, maintaining its genetic diversity at a higher scale. Applying varying temperature regimes on the rearing stock at regular intervals during the mass production process may help to maintain the essential quality of the biological control agents for field performance at higher temperatures.     

Are indigenous strains of Trichogramma sp. (Hym., Trichogrammatidae) better candidates for biological control of lepidopterous pests of the olive tree?

Strains of the egg parasitoid, Trichogramma, indigenous in olive groves in the Mediterranean region (T. bourarachae Pintureau & Babault, T. cacoeciae Marchal, T. cordubensis Vargas & Cabello, T. euproctidis Girault, T. nerudai Pintureau & Gerding, T. oleae Voegelé & Pointel) as well as commercially available strains (T. brassicae Bezdenko, T. cacoeciae, T. evanescens Westwood), were assessed in laboratory and semi-field experiments for their attributes as biological control agents for use against lepidopterous olive pests like the olive moth (Prays oleae Bern.) and the jasmine moth (Palpita unionalis Hübn.). In a choice test, an Egyptian strain of T. cordubensis parasitized significantly more olive and jasmine moth eggs than those of the rearing host Sitotroga cerealella Olivier. This strain was also most efficient in finding eggs of the target pests on olive foliage and on potted olive trees. Survival and fecundity of a Tunisian strain of T. bourarachae was not affected when exposed to hot (35°C) and arid (< 40% relative humidity) conditions in comparison to the mild standard of 25°C and 70% relative humidity. It was concluded that indigenous strains collected from olive groves were more effective against the target pests and more tolerant to arid conditions than commercially available parasitoid species, indicating that biological control agents should preferably be isolated from the relevant pest/crop system.     

Comparative biology and life tables of Trichogramma evanescens and T. cacoeciae with Ephestia elutella as host at four constant temperatures

The age-specific fecundity of Trichogramma evanescens Westwood and T. cacoeciae Marchal (Hymenoptera: Trichogrammatidae) with Ephestia elutella (Hübner) (Lepidoptera: Pyralidae: Phycitinae) as host and the life span of the adults with and without hosts was determined at 20, 26, 30 and 35 °C and 75 ±5% r.h. in the laboratory. At 35 °C, no progeny emerged. The availability of hosts prolonged the longevity in both species. Longevity, percentage of parasitism, fecundity, and the intrinsic rate of natural increase were higher in T. evanescens than in T. cacoeciae. Trichogramma evanescens is expected to be more effective than T. cacoeciae for use in biological control of Ephestia spp., especially at low and high temperatures.     

Effect of host switching on performance of mass‐reared Trichogramma minutum

The effect of host switching on parasitism by Trichogramma minutum Riley (Hymenoptera: Trichogrammatidae) (TM) was examined for parasitoids attacking a factitious host, the Mediterranean flour moth, Ephestia kuehniella Zell. (Lepidoptera: Pyralidae) (MFM), and a natural host, the eastern spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae) (SBW). Parasitoids that were switched from rearing on the natural host to rearing on the factitious host had lower realized fecundities on both MFM and SBW eggs than a control line that was maintained continuously on the natural rearing host, SBW eggs. Conversely, T. minutum reared on the factitious host and switched to rearing on the natural host showed greater realized fecundities. This increase in realized fecundity was lost in the first generation after switching parasitoids back to the factitious rearing host. T. minutum that were maintained on the natural rearing host (SBW eggs) showed more variation in realized fecundity and host acceptance of both MFM and SBW eggs, than parasitoids that were reared on MFM eggs.     

Host Preferences of Trichogramma pretiosum and the Influence of Prior Ovipositional Experience on the Parasitism of Plutella xylostella and Pseudoplusia includens Eggs

Trichogramma wasps are generalist egg parasitoids used in biological control efforts. In a multi host situation they may preferentially parasitize a non-target host species to the detriment of the control program. Plutella xylostella Linnaeus (Lepidoptera: Plutellidae) is a very serious pest of cabbage, but is only one in a number of species in the ‘cabbageworm’ complex. We investigated the host preferences of Trichogramma pretiosum Riley (Hymenoptera: Chalcidoidea) when offered the eggs of Plutella xylostella and the eggs of Pseudoplusia includens Hübner (Lepidoptera: Noctuidae), another species in the ‘cabbageworm’ complex. Trichogramma pretiosum reared on the eggs of the factitious host Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) parasitized both Plutella xylostella and Pseudoplusia includens eggs under laboratory conditions. For both choice and no-choice experiments, T. pretiosum parasitized significantly more P. xylostella eggs than P. includens eggs. Prior ovipositional experience with one or other of the two host species had no effect on the subsequent parasitism levels of the two host species. The preference for P. xylostella eggs was also not affected by this prior ovipositional experience.     

Host suitability and preference studies of Trichogramma cordubensis (Hymenoptera: Trichogrammatidae)

Studies of host suitability and preferences of Trichogramma cordubensis Vargas and Cabello (Hymenoptera: Trichogrammatidae) were performed with eggs of six Lepidoptera (Noctuidae) species: Thysanoplusia orichalcea Fabricius, Peridroma saucia (Hübner), Xestia c-nigrum L., Phlogophora meticulosa (L.), Noctua pronuba (L.), and N. atlantica (Warren). Host suitability was studied by analysing separately the effects of the attacked host species and the influence of the rearing host species on different biological parameters of T. cordubensis. Host preference was analysed by offering eggs of two host species simultaneously to a single female wasp without previous oviposition experience (dual-choice tests). Results show that P. saucia, followed by P. meticulosa were the least suitable hosts for T. cordubensis, since on these species the preimaginal development of the parasitoids was significantly longer and, the number of parasitized eggs as well the number of offspring per female were significantly lower. Contrarily, T. cordubensis parasitized at a higher rate the eggs of the endemic non-target species, N. atlantica. Dual choice tests showed that the option of the first host to be accepted by the wasp was random; however, the mean number of parasitized eggs differed significantly when two host species were offered simultaneously to T. cordubensis, always being the host species with heavier eggs the most parasitized.     

Biology and thermal requirements Trichogramma pratissolii Querino & Zucchi (Hymenoptera: Trichogrammatidae) on alternative hosts

The objective of this work was to study the biology and determine the thermal requirements of Trichogramma pratissolii Querino & Zucchi reared on Anagasta kuehniella Zeller (Lepidoptera: Pyralidae) and Corcyra cephalonica Stainton (Lepidoptera: Pyralidae) at 15, 18, 21, 24, 27, 30 and 33 masculineC. The highest percentage of emergence of T. pratissolii was obtained at 27 masculineC on A. kuehniella and from 24 masculineC to 30 masculineC on C. cephalonica. The lower threshold temperature (Tb) and the thermal requirement (K) of T. pratissolii were 12.59 masculineC (Tb) and 122.85 degree-days (K) when reared on A. kuehniella and 11.73 masculineC (Tb) and 139.80 degree-days (K) on C. cephalonica. These results indicate that both A. kuehniella and C. cephalonica are suitable hosts for T. pratissolii mass rearing. The optimal temperature for the immature development and emergence of T. pratissolii on A. kuehniella was 27 masculineC and 24 masculineC to 30 masculineC on C. cephalonica.     

Acceptability and suitability of Tuta absoluta eggs from irradiated parents to parasitism by Trichogramma nerudai and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae)

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Genetic variability in the egg-laying behaviour ofTrichogramma maidis

SomeTrichogramma maidis females [Hymenoptera: Trichogrammatidae] aggregate their eggs in adjacent hosts whereas others scatter them amongst distant host eggs. The individual variability of aggregated-attack behaviour in matedTrichogramma maidis females was studied by isolating them with a uniform patch of about 500Ephestia kuehniella [Lepidoptera: Pyralidae] UV killed eggs. Genetic analysis demonstrated that similar behaviour exists between sisters and that the trait is transmissible and relatively stable over 2 successive generations. The ethological basis and the ecological significance of this variability are discussed.      

Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae)

The surface and structure of the chorion of eggs of Diatraea saccharalis (F.) (Lepidoptera: Crambidae), Anticarsia gemmatalis (Huebner), Heliothis virescens F., Spodoptera frugiperda (Smith) (Lepidoptera: Noctuidae), Sitotroga cerealella (Oliver) (Lepidoptera: Gelechiidae), Ephestia kuehniella Zeller and Corcyra cephalonica Stainton (Lepidoptera: Pyralidae), that are hosts of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) were studied on SEM and TEM. Other characteristics of these eggs, such as changes in their color during embryonic development, size and volume were also recorded. Sculpturing and texture of the surface of the chorion greatly varied among the species studied, as well as the number of layers of the chorion and their thickness. Eggs of the factitious hosts were among the smallest and their volume was very close to each other. All these characteristics would provide basic information for a better understanding of the host selection behavior and are useful for the development of a suitable artificial host egg for the in vitro rearing of these egg parasitoids.     

Environmental and maternal effects on host selection and parasitism success of Bracon hebetor

The biological control programs supporting the native species of natural enemies are far more sustainable than those which use exotic enemies of the target pest. Little is known about the effects of the surrounding environment on host selection behavior of Bracon hebetor Say (Hymenoptera: Braconidae). In the present study, the effects of the origin of the parasitoid populations, host species and parasitoid rearing history on host selection and parasitism success of B. hebetor were investigated. Several life-history parameters, including the frequency of parasitism, percentage parasitism, egg load, survival rate and the offspring sex ratio of the parasitoid were measured. In terms of both selection and parasitism success, B. hebetor preferred Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) over Apomyelois ceratoniae Zeller (Lepidoptera: Pyralidae) and Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), and A. ceratoniae over H. armigera. When different populations of B. hebetor were compared, the B. hebetor population originated from orchard was the most successful compared with the field and store populations. In addition, the rearing history was influential on the parasitism preference and success: a better performance of the parasitoid was obtained when it was reared on its original host compared with an intermediate host, E. kuehniella. The causes and consequences of these findings were further discussed in relation with mass rearing of this parasitoid for biological control programs.     

Potential for controlling codling moth Cydia pomonella (Linnaeus) (Lepidoptera: Tortricidae) in Argentina using the sterile insect technique and egg parasitoids

Codling moth is the main pest affecting apples and pears worldwide. Most pest control strategies used against this insect have relied on the use of broad‐spectrum insecticides which have led to non‐desirable effects like pesticide resistance, residues in the environment, human health concerns and the reduction of access to international markets. Therefore, alternative pest control strategies that would result in sustainable fruit production systems while taking care of the environment are strongly promoted. The use of the sterile insect technique has proven to be a valuable pest control tactic within area‐wide integrated pest management strategies, and its synergistic effect for Lepidoptera pests when combined with other biological control tactics such as parasitoids has been documented. The purposes of this research were to evaluate the response of an Argentinean codling moth strain to a sub‐sterilizing radiation dose of 100 Gy and to assess the acceptability and suitability of sterile codling moth eggs by the egg parasitoids, Trichogramma cacoeciae (Marchal) and Trichogramma nerudai (Pintureau and Gerding). Irradiated female moths survived better than irradiated male moths and non‐irradiated male and female moths. Also, the fecundity of irradiated female moths was reduced by more than 30% as compared to non‐irradiated ones whereas their fertility was close to zero. The F₁ generation was male biased with a lower fertility (inherited sterility) than the parental generation. Trichogramma cacoeciae and T. nerudai parasitized both fertile and sterile eggs. However, there was a significant reduction in acceptability for sterile eggs. Trichogramma nerudai parasitized more eggs than T. cacoeciae, but egg acceptability for this species was proportionally lower than for T. cacoeciae especially on eggs oviposited by irradiated females. Development to adult of both parasitoids species was not substantially affected by the origin of the eggs and the wasps had acceptable levels of adult emergence, survival and fecundity. These results provided useful information on the potential for controlling the codling moth using egg parasitoids and the sterile insect technique in Argentina.     

Comparative study of entomopathogenic nematode isolation using Galleria mellonella (Pyralidae) and Spodoptera littoralis (Noctuidae) as baits

Entomopathogenic nematode (EPN) occurrence in soil from natural areas and crop field edges from La Rioja (northern Spain) was compared using two insects as baits: Galleria mellonella (Lepidoptera: Pyralidae) and Spodoptera littoralis (Lepidoptera: Noctuidae). Both insects trapped Steinernema feltiae, S. kraussei and S. carpocapsae, with G. mellonella being more efficient than S. littoralis recording 5.4 and 2.6% of positive soil samples, respectively. EPN recovery frequency and abundance obtained with G. mellonella were not statistically different between natural and crop field edges values; however, S. littoralis was more successful trapping EPNs from crop field edges. Statistical differences were observed for recovery frequency recorded by both hosts in natural areas. Significant differences in larval mortality between both insects were not observed. The use of S. littoralis in entomopathogenic nematode surveys is discussed.     

A molecular key to the common species of <Emphasis Type="Italic">Trichogramma</Emphasis> of the Mediterranean region

A molecular key for the identification of common Trichogramma (Hymenoptera: Trichogrammatidae) species found in agricultural settings around the Mediterranean is developed based on the sequence of the internal transcribed spacer 2 of the ribosomal cistron. Using the size of the ITS2 PCR product and restriction fragment length polymorphisms of the amplicon, ten Trichogramma species (T. bourarachae Pintureau and Babault, T. brassicae Bezdenko, T. cacoeciae Marchal/T. embryophagum Hartig, T. cordubensis Vargas and Cabello, T. dendrolimi Matsumura, T. euproctidis Girault, T. evanescens Westwood, T. nerudai Pintureau and Gerding, T. oleae Voegelé and Pointel, and T. pintoi Voegelé) can be distinguished.     

Trichogramma species (Hymenoptera: Trichogrammatidae) parasitoids of Lepidopteran eggs in Lara State, Venezuela

This work was conducted to determine the occurrence of Trichogramma wasp species in Lara State, Venezuela. Lepidopteran egg samples collected from various crop leaves were observed daily under laboratory conditions for emergence of Trichogramma species adult wasps. Trichogramma were also obtained from traps containing eggs from the hosts Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae) and Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae). In the laboratory, specimens of Trichogramma species were mounted on microscope slides to show male genitalia and other morphological characters used for its identification. Trichogramma atopovirilia Oatman y Platner emerged from S. frugiperda eggs collected in a cornfield at La Palomera, Humocaro Alto and at El Parchal, Humocaro Bajo, Municipio Morán. T. atopovirilia also emerged from S. frugiperda eggs collected in a cornfield at Sabana Grande and from S. cerealella eggs used as traps in a pepper culture at Tintinal, Municipio Andrés Eloy Blanco. T. exiguum Pinto y Platner emerged from S. frugiperda eggs used as traps or collected in cornfield at Totumito and at La Palomera, Humocaro Alto. T. pretiosum Riley emerged from Phthorimaea operculella Zeller eggs collected on stored potatoes at Monte Carmelo, Sanare. The identification of Trichogramma species in Lara State would be useful in the development of biological control programs for lepidopteran pests.     

Effect of fertilized,unfertilized, and UV‐irradiated hosts on parasitism and suitability for Trichogramma parasitoids

Trichogramma spp. (Hymenoptera: Trichogrammatidae) parasitoids have been commonly used as biological control agents in insect pest management. Host quality is believed to influence parasitism, host preference, and suitability for parasitoids. To date, limited studies have compared the parasitism of Trichogramma parasitoids on fertilized, unfertilized, and sterilized host eggs. Hence, we studied the performance of three Trichogramma egg parasitoids, Trichogramma japonicum Ashmead, Trichogramma chilonis Ishii, and Trichogramma leucaniae Pang & Chen, on fertilized, unfertilized, and ultraviolet (UV)‐irradiated fertilized (UVF) eggs of rice moth, Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). In a no‐choice test, T. japonicum and T. leucaniae parasitized significantly more fertilized or UVF than unfertilized hosts, and T. chilonis parasitized significantly more UVF than either fertilized or unfertilized hosts. In a choice test, all three Trichogramma parasitoids parasitized UVF hosts the most, and unfertilized hosts the least. There were similar percentages of adult emergence and female progeny among fertilized, unfertilized, and UVF hosts for all three Trichogramma parasitoids, except that T. japonicum had significantly lower adult emergence on fertilized hosts. We also found that all three Trichogramma parasitoids developed slower on unfertilized hosts. Regardless of host treatments, T. leucaniae had the longest developmental time and T. chilonis had the shortest. We conclude that Trichogramma parasitoids prefer parasitizing UVF eggs of C. cephalonica without negative effects on their emergence and sex allocation.     

Selectivity of neem to Trichogramma pretiosum Riley and Trichogrammatoidea annulata De Santis (Hymenoptera: Trichogrammatidae)

Trichogramma pretiosum Riley and Trichogrammatoidea annulata De Santis are commonly found in avocado and persimmon orchards in northern Parana state. However, their abundance depends on whether insecticides are used or not to control the key lepidopteran pests Stenoma catenifer (Wals.) (Lepidoptera: Elachistidae) and Hypocala andremona (Stoll) (Lepidoptera: Noctuidae), respectively. The aim of this work was to evaluate the effects of an aqueous neem seed extract (ANSE) at 15, 3 and 1.5%, and of an emulsifiable concentrate neem oil (ECNO) at 2.5, 0.5 and 0.25% on lifetime parameters of these trichogrammatids as a way of testing the feasibility of integrating the biological and chemical control methods. Chemicals were applied on Anagasta kuehniella (Zeller) (Lepidoptera: Pyralidae) eggs before or after parasitization (one, three or five days). ANSE was more deleterious to both parasitoid species than ECNO, regardless of the concentration and the time of application. The chemicals acted on a concentration and time dependent manner. Treating the host with neem before parasitism was less deleterious to wasp emergence, especially for T. annulata. Pre-treatments (24h) of the host eggs with ECNO at concentrations varying from 0.5% to 0.25% did not affect T. pretiosum longevity, but 2.5% reduced T. annulata survival. Feeding wasps with honey mixed with 0.25% ECNO negatively affected T. annulata survival.