Karaelmas Fen ve Mühendislik Dergisi / Karaelmas Science and Engineering Journal 2 (2), 1-12, 2012 Karaelmas Science and Engineering Journal
Journal home page: http://fbd.karaelmas.edu.tr Artificial Rearing of Entomophagous Insects, with Emphasis on Nutrition and Parasitoids - General Outlines from Personal ExperienceSimon Grenier Former INRA Research Director - 6 Rue des Mésanges, 69680 CHASSIEU, France The disposability of high numbers of entomophagous insects for their use in biological control strategies is an old objective carried on, between others, by the rearing in different kinds of artificial diets. The definition and the perfecting of these diets are at first based on nutritional studies. Food or carcass analyses, nutritional balance studies, and deletion/supplementation methods allow to evaluate the different nutritional needs. Nitrogen sources are the most critical needs especially with fast growing entomophagous insects. Lipids and carbohydrates mainly constitute energy sources with storage possibility. Other nutrients such as salts and vitamins are also needed, and sometimes some specific polyunsaturated fatty acids. There are other important physiological requirements, concerning the digestion process, the respiration, or the hormonal balances. Physico-chemical factors such as Osmotic Pressure and pH often show critical values for the normal development, mostly of endoparasitoid insects. For egg parasitoids and predators, the presentation of the food is of prime importance for a normal food intake, and finally for the success of the rearing. Sterilization of the diet or incorporation of preservative agents is often necessary for preventing bacterial or fungal contaminations. Many successes were obtained for artificial rearing of entomophagous insects, but ultimate efforts are still needed for crucial improvements and supports that may lead to the extension of the use of this biological control strategy.
Keywords: Artificial rearing, Entomophagous insect, Parasitoid, Predator, In vitro, Nutrition, Food, Diet, Medium, Nutriment,
Nutritional need considerations, the presence or absence of insect- The artificial rearing of parasitoid insects started a long derived components (hemolymph, tissue homogenates time ago, with the main goal to try obtaining a mean or extracts, egg juice) is a critical characteristic, leading to multiply and produce parasitoids to be released in to operate a simple distinction between food with or biological control strategies. But it is also a powerful tool without insect components. The type of diet does not to conduct studies on biology, physiology and behaviour prejudge of its performance for insect rearing, but may of entomophages, especially endoparasitoid species influence the accuracy of the experiments (Grenier 1986). For a complete success in rearing entomophagous insects in artificial conditions, all their physiological There are different appellations for the preparations requirements have to be fulfilled, but nutrition is one of used in artificial rearing. In this paper, "medium" will the most critical functions. Generally speaking, any non- be preferably employed for parasitoids, and "diet" natural food used to produce an insect for laboratory for predators. Food will represent the general term. studies, could be well known in its composition to draw Different kinds of foods have been tested, from very reliable conclusions of the achieved tests.
simple preparations (crushed lepidopteran pupae, piece of beef liver or meat…), to chemically defined media. This paper is mainly based on a 40 years' personal Several categories of food could be described, and experience on the rearing of entomophagous insects in different nomenclatures were proposed. One of the most artificial conditions for preimaginal development. Thus, known classifications is from Dougherty 1959, with the most of the bibliographic references are from the author. terms of holidic, meridic and oligidic, mainly based on For covering a subject, as far as possible, the most recent the presence or absence of complex components. The references, preferably review papers were given. For latter being not easy to typify, the distinction between other general data, the readers have to consult these key the 3 terms is not very relevant. In fact, only a complete references: Mellini 1975, Thompson 1999, Thompson and description of the composition would be able to Hagen 1999, Cohen 2004.
characterize an artificial food. Nevertheless for practical After a brief presentation of the various ways to Corresponding author: simon-grenier@orange.fr determine the nutritional requirements, these latter will Grenier / Artificial Rearing of Entomophagous Insects be described, as well as some other key physiological insect grown on control food, and to allow improving the requirements. Then, important parameters of the food, composition of this food (Grenier and De Clercq 2003, its presentation and preservation will be described, Zapata et al. 2005, Dindo et al. 2006, Sighinolfi et al. 2008).
before to conclude.
2.3 Nutritional balance sheet
There are different types of nutritional needs, and they The evaluations of food intake, weight gain, faeces and are variable according to the stage and the physiological wastes rejected during a given time, allow calculating state, usually higher for larvae than for adults, except some indexes (nutritional rating of digestibility, during reproduction. We can discriminate, general needs conversion efficiency . of the food). With this method, for basic metabolism, needs for development and needs specific compartments could be studied separately for reproduction. In this paper, only the preimaginal (nitrogen or lipid compartment). The determination development will be considered.
of the enzymatic activities of the insect to be reared in 2. Evaluation of nutritional needs
artificial food gives some information about its possibility of digestion and assimilation. Complementary studies Various analytical approaches were employed to try to could be conducted in vitro for digestion of nutriments determine the different requirements and define the food by enzymatic extracts of the insect concerned. Fine composition for entomophages.
experiments on digestion, metabolism processes and 2.1 Food analysis
inter-conversions could be conducted thanks to NMR spectroscopy or radiotracer methods (Thompson 1990b, For example, the biochemical analyses of host or prey Grenier et al. 2005).
could be conducted in their amino acid contents after total or partial hydrolysis. Fatty acids or carbohydrate 2.4 Classical dietary deletion/supplementation studies
analyses are also often achieved. The results have to be Many nutritional studies for free living insects are expressed in total amounts per weight or in percentages dealing with the omission/deletion or supplementation as relative values (patterns) useful for establish the of one component to verify if it is essential or not. But this quantity for each component of the food. Examples method is less powerful for parasitoids of which growth could be found for Tachinidae (lepidopteran larvae), is fast and because components balance, as well as pH Trichogrammatidae (lepidopteran eggs), predatory bugs and osmotic pressure stability, could be key parameters. and coccinellids (aphids, lepidopteran eggs, Artemia For predators the method gives some good results (Arijs and De Clercq 2002).
With parasitoids, the main difficulty lies in the necessity 3. The nutritional requirements
to know which exact part of the host is ingested in the course of the development (hemolymph, body It is generally admitted that the basic qualitative fluids, whole body or egg content.). To make fruitful nutritional requirements for parasitoids and predators comparison, host and non-host species could be studied are not different from those of free-living insects. as well (Barrett and Schmidt 1991, Yazlovetsky 1992).
Contrary to the species developing at the expense of growing stages (koinobionts), idiobiont parasitoids and 2.2 Carcass analysis of whole parasitoid/predator body
especially egg parasitoids develop in closed systems, Instead of host/prey, the same type of analysis could for a short time, without external nutritional supply be done with the entomophagous species itself. There (Mellini 1986). Consequently they need very rich and are many examples with Tachinidae, Trichogramma, concentrated food.
Macrolophus, Dicyphus, Orius, and Harmonia. (Bonnot et The nutritional plasticity of some predator species is a al. 1976, Grenier et al. 1989, Bonnot et al. 1991, Grenier et positive characteristic regarding their possibility to be al. 1995, Specty et al. 2003, Vandekerkhove et al. 2009). reared on artificial food (Specty et al. 2003). Sometimes, a But, to establish the exact composition of the food, diet designed for a species can be appropriate for another it is necessary to take into account the intermediate species, possibly with small adaptations, as observed metabolism. Moreover, the existence of catabolism and with Harmonia axyridis diet used for Chrysoperla carnea inter-conversion metabolism impede from knowing the (El Arnaouty et al. 2006).
exact form (mono or polymers) of each component to incorporate into the food. One advantage of these carcass 3.1 Nitrogen sources
analyses is also to give an evaluation of the quality of The sources of nitrogen are a very important parameter an insect grown on artificial food by comparison with in the nutrition of entomophagous insects, because of the Grenier / Artificial Rearing of Entomophagous Insects very fast growth of many species (Grenier et al. 1974). P. caudata (Grenier et al. 1975), or Geocoris punctipes For example, the weights of newly hatched and mature (Cohen 1985, 1992). Fatty acids may be supplied as free larvae of the tachinid Lixophaga diatraeae are respectively fatty acids or triglycerides, and need the use of emulsify- 12 µg and 33 mg. The larval growth is completed in 8 ing agents to obtain their homogeneous dispersion in the days with a weight doubling time of about 17 hours aqueous phase. The most employed emulsifying agents (Grenier 1980). The supply in amino acids (aa) has are Tween 80 (polyoxyethylenesorbitan monooleate), to fit the needs, to avoid a lost of time and energy in lecithin (phosphatidyl-choline) or lauryl sulphate. Egg conversion between amino acids, and the production yolk frequently incorporated into artificial media for egg of toxic metabolites. Parasitoids and predators are parasitoids provides highly well emulsified concentra- carnivorous species needing a protein-rich diet, with tions in fatty acids, cholesterol, and lecithin. Free fatty some specific requirements in aromatic amino acids acids are toxic for the tachinid P. caudata (Grenier et al. especially in parasitoid diptera at the end of their larval 1974). The degree of toxicity may depend on the emulsi- development for cuticle tanning (Bonnot et al. 1976). fying agent used for E. roborator (Thompson 1977). Emul- Nevertheless some free aa like phenylalanine, may be sion process could have a detrimental effect on larval toxic at high concentration, or have a very low solubility like tyrosine, enforcing to deliver the aromatic aa as Eicosanoids (derived mainly from the arachidonic fatty tyrosine-rich peptides or proteins. The 10 "essential" aa acid) were recently recognised to mediate different are required, but some other ones are highly beneficial functions in insects, such as reproduction and immunity. for a normal growth (Grenier et al. 1994). Many species For example, the inhibition of eicosanoid biosynthesis need a complementary supply of several non-essential aa strongly reduced the production and hatchability of the because they fail to develop normally in diets containing eggs in the ectoparasitoid Bracon hebetor (Büyükgüzel only these 10 essential aa. The modification of the balance et al. 2011). These molecules also exert a role in between the different aa of a medium that only permits melanotic nodulation reactions to viral infection in the the larval survival of the tachinid fly Phryxe caudata, could endoparasitoid P. turionellae (Durmus et al. 2008). induce the start of its growth (Grenier et al. 1975). For the first time for a tachinid, the complete development from egg to adult was obtained with L. diatraeae, in a medium Carbohydrates are often considered as energy sources, containing 19 aa in well-balanced proportions (Grenier et as well as some lipids. It is usually admitted that there al. 1978). To maintain the osmotic pressure (OP) within are no specific needs for carbohydrates, but glucose acceptable values, part of the aa could be provided as promotes growth and lipogenesis, increasing the level of proteins, protein hydrolysates or peptides, but free unsaturated fatty acids in E. roborator (Thompson 1982). aa could be required for some species (Nettles 1987, Thompson 1980, 1986, Thompson et al. 1983). Casein, Trehalose, the most common non-reducing disaccha- lactalbumine, ovalbumine, serumalbumine, soybean ride in insects, plays an important role in metabolism extract and yeast are the most common used proteins and stress resistance (Qin et al. 2011). It could be used (Grenier 1994) (see § 4.1).
instead of sucrose or glucose, and also partly replaced hemolymph in media for Trichogramma (Lü et al. 2011) 3.2 Lipids
(see § 4.1). To reduce the OP in medium/diet it is recom- The similarity of the composition in total fatty acids mended to replace oligosaccharides by polysaccharides, of many parasitoids with that of their host, suggests like glycogen, but OP being not so critical for many they may copy to a certain extent the host composition predators, sucrose has been used in place of glycogen to (Thompson and Barlow 1972, Delobel and Pageaux reduce the cost of the diet (Cohen 1985, 1992). Moreover, 1981). It could be the same for predators (Sighinolfi 2008). sucrose may act as a feeding stimulant on parasitoid, as Itoplectis conquisitor (Yazgan 1972) can develop in a diet well as on predator insects.
without any fatty acids, but their addition improves the 3.4 Other needs
yield and the fecundity of the adults obtained, but con- versely Pimpla turionellae requires a mixture of fatty acids 3.4.1 Inorganic salts to produce normal adults (Yazgan, 1981). Polyunsatu- They are generally required for the normal development rated fatty acids may be required for normal growth of of insects, but their level and the balance between several entomophagous insects (Sighinolfi 2008). Dietary the different cations, especially K+/Na+ is of prime sterols are required by a great number of parasitoids and importance and varies according to the species. The predators, such as Exeristes roborator (Thompson 1990a), predator G. punctipes prefers to feed on diets containing Grenier / Artificial Rearing of Entomophagous Insects a K/Na ratio exceeding 2 than on diets with a ratio lower Extra-oral digestion could be observed in many than 1 (Cohen 1981). Many authors introduce in the predaceous species, and about 80% of predaceous medium/diet a classical list of salts, frequently, Wesson's terrestrial arthropods use this strange feature, according or Neissenheimer's salt mixture.
to Cohen (1995) (see § 6.2). 3.4.2 Vitamins Besides the composition of the medium/diet, protein digestion and utilization, are key processes that could The accurate determination of the needs in vitamins be investigated to assert a proper metabolization of the implies very delicate experiments, requiring vitamin- diet components (Gomes et al. 2000, Grenier et al. 2005). free components, and taking into account the egg stocks. This is also true for many other food ingredients. The Very few specific investigations were conducted for composition of the medium/diet nicely fitted with the entomophagous insects. It was usually admitted that needs, is necessary but not sufficient, it is also of prime their needs would be not different from those of other importance to make sure that digestion and assimilation insects. Habitually about 12 vitamins were added in the processes will correctly liberate the components required. diets, mainly hydrosoluble ones including B vitamins, as well as C vitamin, and 2 liposoluble ones (retinol-A, and tocopherol-E). Commercial preparations are available The good accomplishment of this crucial function is and often used by many authors, like Vanderzant vitamin closely related with the presentation of the food (see § 6). mixture for insects (Vanderzant 1969).
Some lipids could hamper the respiration by alteration of the characteristics of the interface larval tegument / Ribonucleic acids (RNA) are sometimes incorporated in - Generally speaking, the gas exchanges in parasitoid medium/diet, but their dispensability is questionable. larvae occur through the tegument or by the spiracles. RNA could increase survival or promote growth. Early larval instars in hymenopterous and tachinid Supplementing an artificial diet devoid of insect species mainly respire by cutaneous diffusion from components with cells from an embryonic cell line host body fluids, allowing to use liquid media for their of Plodia interpunctella, enhanced oviposition rates in development. Nevertheless the volume of liquid has to the bug Orius insidiosus. Protein content or some other be adapted to insure an efficient gas exchange with the nutritional components of the cells might be responsible surrounding atmosphere (Grenier et al. 1975). Tachinid for this increase (Ferkovich and Shapiro 2004).
larvae present a special respiration structure resulting of interactions with host. The host immune response 4. Other physiological requirements
usually results in a partial encapsulation forming a For endoparasitoids, the medium is not only the food structure called respiratory funnel. This funnel allows source, but also the environment in which they are bathed the larva to be in relation with the tracheal system of its host. The larva could be attached to trachea or spiracle for all their larval life. Thus, besides the nutritional or sometimes directly on the integument, especially at needs, the medium must have acceptable physico- the end of the larval development (Mellini et al. 1996, chemical parameters, and provide for other requirements Herting 1960, Stireman et al. 2006). The last larval instar concerning essential physiological functions like respira- of most Tachinidae is amphipneustic and exhibits a high tion, excretion, and general protection (Grenier et al. respiratory rate of about 1 µl O2/mg wet weight /hour, in P. caudata (Bonnot et al. 1984). A gelled medium is 4.1 Digestion process - structure of the gut
recommended at that stage, also for some hymenopterous larvae, even those with hydrophobic tegument. The (temporarily) blind posterior gut of some hymenopterous species increases the efficiency of the - The problem of gas exchanges is critical with egg conversion of food and protects the remaining food parasitoids, because of their very high respiratory rate. from contamination by waste products, but implies The consumption of oxygen by Trichogramma dendrolimi, a high concentrated food. On the contrary, the open increases during larval development, reaching 7µl/h (for functional gut in several tachinid larvae has to be taken 100 larvae) at the prepupal stage and slightly decreases into consideration. The medium could be renewed along thereafter (Dai et al. 1988). To culture Trichogramma the larval development or supplied as an amount greatly species in vitro, it will be of prime importance to ensure exceeding the strict needs, in order to dilute the excretory a normal respiration of prepupae and pupae. Some products below a harmful level. species like Ooencyrtus pityocampae (Encyrtidae) have Grenier / Artificial Rearing of Entomophagous Insects a special anatomical adaptation, in a form of a stalk improves larval development in vitro (Greany 1986). It protruding from the host egg or plastic film, allowing is usually admitted that koinobiont parasitoids, either them to respire through the host tegument or through an alter the host endocrine system in order to promote their artificial membrane. But a high mortality was observed own growth (called "regulators"), or depend on host in artificial conditions when mature larvae leave their hormones to synchronize their development with that of respiratory stalk before pupation (Battisti et al. 1990, the host (called "conformers") (Lawrence 1986). Masutti et al 1992).
In presence of 20-OH ecdysone, lipophorin or lipophorin- 4.3 Hormones
transported lipids could act as a growth-promoting factor putatively involved in a pupal extract from Many egg parasitoids can develop in killed host their host Galleria mellonella for the development of the eggs revealing the low host-parasitoid interactions at endoparasitoid Venturia canescens (Nakahara et al. 1999).
hormonal level. In the absence of demonstration of the role of hormones, not any was added in artificial For predators, the role of hormones present in their prey, media for egg parasitoids, though insect hemolymph is not well documented. However, the development was frequently incorporated. In natural situation, the of many predators on artificial diets devoid of insect hormonal changes in parasitoids may be synchronized components (Cohen 1985, Arijs and De Clercq 2002) with those of their hosts, and are key factors for indicates that they are not dependent on exogenous parasitoid's development and species survival (Mellini hormones. Nevertheless, some juvenoids added in diets 1983, Beckage 1985, Lawrence 1986, Rhamadane et could prevent the reproductive diapause of the adults of al. 1987, 1988). The parasitoids allowing their host to coccinellids like Coccinella septempunctata L. (Chen et al. continue to feed and develop beyond parasitization are named "koinobionts" and those, which paralyze or kill The fenoxycarb, an insect growth regulator, mimetic of the host very soon after parasitization, usually before Juvenile Hormones, strongly disturbs the development their egg hatches, are named "idiobionts" (Askew and of the tachinid P. nigrolineata, by delaying or stopping Shaw 1986). Dipteran parasitoids, especially tachinids, the growth and reducing the yield in pupae (Grenier don't however fill well into this classification, as many and Plantevin 1990). Actually, the fenoxycarb shows a species show characteristics of both strategies (Dindo high JH activity and induces deleterious effects on many parasitoids and predators (Grenier and Grenier 1993).
Although the parasitoid's life cycle may be closely 4.4 Teratocytes
dependent upon host hormone titres in vivo, the dependence could be not so strict in vitro. Thus, Cells, called teratocytes, derived from the embryonic the tachinid P. caudata, whose cycle is accurately membrane of egg in some Scelionidae or Trichogramma- synchronized with its host cycle in nature, does not tidae species are released into host hemocele at hatching. need any hormone for the first and the second moults Their role in the successful in vitro culture of egg parasitoid in vitro (Grenier et al. 1975). Other tachinids, L. diatraeae, suggests a function on digestion and assimilation of host Eucelatoria bryani and Exorista larvarum can develop from components (Grenier 1994, Thompson and Hagen, 1999).
egg to adult in media devoid of hormones (Grenier et al. 1978, Nettles et al. 1980, Dindo et al. 1999). In the
5. Physico-chemical factors
same way, Thompson (1980) showed that the addition 5.1 Osmotic Pressure (OP)
of 20-OH ecdysone, neither stimulates the development, nor the pupation of the Hymenoptera Brachymeria The dietary osmolarity is an important parameter intermedia. The complete development of this parasitoid and must be adapted to each species, especially for has been obtained on an insect-material free artificial endoparasitoids for which the medium is not only the medium, devoid of host hormones (Dindo et al. 2001). food, but also the environment in which they are bathed But, for the tachinid Pseudoperichaeta nigrolineata, Grenier all their larval life. Ectoparasitoid Hymenoptera are (1988) showed that the presence of 20-OH ecdysone in usually more tolerant to high OP. Itoplectis conquisitor artificial media is necessary to trigger the first moult, and (Yazgan 1972) and E. roborator (Thompson 1976) can in Pseudogonia rufifrons the first instar larvae only moult to develop in medium reaching 1700 milliosmoles, but second instar when ecdysone is added into the medium for Brachymeria lasus and Pachycrepoideus vindemiae, the (Fanti 1990). In the hymenoptera Cotesia marginiventris, results were improved if the OP was lowered from 700 20-OH ecdysone can prevent egg hatching, but neither to 400 mOsM (Thompson et al. 1983). In tachinid larvae, ecdysone, 20-OH ecdysone, nor juvenile hormone, such as P. caudata and L. diatraeae, the optimal OP varies Grenier / Artificial Rearing of Entomophagous Insects between 350 and 400 mOsM, and no development was wax/paraffin mixture, polymerized paradixylylene or observed above 450 mOsM (Grenier et al. 1975, Grenier polyethylene/ polypropylene film, respectively (Grenier et al. 1978). Above the same threshold, for the oophagous and Bonnot 1988, Grenier 1994, 1997). Egg laying occurs species of Trichogramma, neither normal egg hatching, directly in these artificial host eggs, but the stimulation nor larval development occurs, the optimal OP being of the oviposition by the Trichogramma females is usually near 320 mOsM (Grenier and Bonnot 1988). The degree enhanced by smearing the surface of the artificial eggs of tolerance to OP seems in relation with the anatomical by some chemicals like moth scales extracts, or polyvinyl features of the larval integument. The thick hydrophobic alcohol solutions (Cônsoli and Grenier 2010, Grenier et cuticle of some ectoparasitoid Hymenoptera allows al. 1993, Grenier et al. 1998a, Han et al. 1994). In wax them to avoid a close contact with the medium. On the and paraxylylene eggs the development usually stops at contrary, endoparasitoid Hymenoptera and Diptera may pupation, probably because of gas exchange limitations. lack such integument and could undergo an osmotic The artificial egg shell has to be permeable to oxygen and carbon dioxide, but not to water vapour, in order to avoid desiccation. The development of Trichogramma from eggs to normal fecund adults was observed inside Usually hydrogen ion concentration in insect hemolymph small bags constituted by a heat sealed polypropylene/ varies from 6.0 to 8.2, but is more often observed between polyethylene film with a series of hemispherical cupules 6.4 and 6.8 (Mullins 1985). Most of the artificial media filled with the medium. This latter technique was greatly for parasitoids show a pH near these latter values in the developed in China and in France (Li 1986, Li et al. 1988, absence of studies concerning the effect of this factor on Grenier 1994, 1997).
their development. The tachinid larvae of E. bryani seem 6.2 Predators
highly tolerant to pH because Nettles (1986) observed that there is no significant difference in pupal and adult For predators, the presentation of the diet is a key yields between diets with pH varying from 5.5 to 8.0, parameter although the respiration is not mainly although higher absolute yields (egg to adult) were involved. Liquid diets that were fully- or semi-defined obtained between 6.75 and 7.5.
were presented within wax capsules for the neuropteran With media containing holotissue of Antheraea pernyi C. carnea and the hemipteran predator G. punctipes. pupae, egg yolk, milk and water, the optimal pH Diets for different lacewing species (chrysopids) were for parasitization, pupation and adult production of encapsulated, presented on cellulose sponge or in the Trichogramma confusum varies between 6.7 and 6.95 form of a free hygroscopic powder.
(Zhong and Zhang 1989). Usually, high percentages Diets for predaceous coccinellids could be presented of adults of Trichogramma spp. were obtained for pH in gelled cubes or as powder, or dry pellets. Stretched between 6.6 and 7.0 by many authors. Parafilm was used to package diets with a paste-like consistency for several hemipterous predators, as well 6. Presentation of the food
as for some species of coccinellids. Parafilm enclosing The medium consistency could be a limiting factor for synthetic foam cubes soaked with diet devoid of insect the larval and pupal parasitoids, mainly in relation with components was successfully used to rear Macrolophus respiration (see § 4.2), but the presentation of the food is caliginosus (Grenier et al. 1989). For other bibliographic more crucial for egg parasitoids and predators. references, see Grenier et al. 1994, Thompson and Hagen 6.1 Egg parasitoids
1999, Cohen 2004.
Especially for non-gregarious species, larvae need a For the rearing of the stinkbugs Podisus spp., cylindrically limited quantity of food because they cannot regulate shaped "artificial larvae", 2-4 cm long and 0.3 cm their food intake, otherwise the development will diameter, were produced by bringing thawed or fresh terminate mainly at pupation, or will produce adults diet onto a stretched Parafilm M sheet and wrapping showing abnormalities (Grenier and Bonnot 1988). a single layer of the Parafilm around the meat-based Thus, for egg parasitoids the medium is presented in diet paste (De Clercq and Degheele 1992). For Orius various ways to create an artificial host egg. The hanging laevigatus, the diets were encapsulated in Parafilm M drop technique consists in the deposition of droplets of using an encapsulation device (ARS, Gainesville, USA) medium on a flat surface in which the Trichogramma eggs forming small hemispherical domes (35µl) sealed with are deposited for development. In wax eggs, paraxylylene transparent tape. The Parafilm was stretched before eggs or plastic egg cards, the artificial eggshell is made of encapsulation to facilitate stylet penetration by early Grenier / Artificial Rearing of Entomophagous Insects instars of the predator (Bonte and De Clercq 2008, the protein content of the pupae of the parasitoid P. 2010). The same presentation with 2 artificial diets was turionellae while this content was decreased by nystatin successfully used for the development and reproduction of M. caliginosus (Vandekerkhove et al. 2006). Glycerol Various effects, some positive ones, were observed for and starch are texture and consistency agents used in bacterial DNA gyrase inhibitors (novobiocin, nalidixic diets for predators such as coccinellids or chrysopids.
and oxolinic acids) on survival and development of The presentation has to take into consideration the quite the ichneumonid parasitoid P. turionellae reared on common habit of many predators to exhibit an extra- chemically defined synthetic medium (Büyükgüzel oral digestion, allowing them to attack relatively large 2001).
prey compared to their own size. Thanks to the injection 8. Discussion and Conclusion
of specific hydrolytic enzymes in the prey and the At final, during several decades, many successes were absorption of the resulting fluids, these predators greatly obtained in different countries around the world, mainly increase the nutritional efficiency of a prey (Cohen 1995). with idiobiontic parasitoids and polyphagous predators. A bulk of food included in a same membrane could be Approximately 130 entomophagous species have been preferable to scattered small pieces.
partly or completely reared in artificial diets, among 7. Sterilization and Preservatives
them more than 20 species of Trichogrammatidae. Nevertheless from the years 2000, it appeared a slow The artificial diets are rich in all the nutrients allowing down of the works concerning artificial diets, even if the growth of bacteria and fungi. Fungi are especially some teams are still working hard (Cônsoli and Grenier detrimental because they can spread in the entire rearing 2010). Besides it was observed, at the same time, that the system from a unique contamination spot thanks to motivation of the researchers in artificial rearing moves mycelia and spores. The sterilization of the medium/diet from academic objectives to more applied orientated by filtration or heating is not always possible because of works, sometimes not steadily published or even size particles or coagulation. Gamma irradiation could patented, as in the USA for example (Grenier 2011).
also modify the consistency of the diet and the structure of some components. Some classical bactericides The development and especially the continuous rearing (penicillin, streptomycin, gentamycine) are efficient of parasitoid and predator insects are currently limited. to control bacteria and non-toxic for entomophagous Yet, except for laboratory tests, it is not recommended to maintain entomophagous insects on artificial diet, and insects (Dindo et al. 2003, Grenier 1994, Cônsoli and even on factitious hosts or prey. In the tachinid Lixophaga Grenier 2010). Nevertheless it is necessary to pay a diatraeae, a long rearing in the laboratory on Galleria special attention with insects harbouring symbionts, mellonella induced some modifications of capability to because some antibiotics, such as tetracycline used with develop in artificial medium (Grenier and Pintureau 1991). Trichogramma, could remove these symbionts and deeply The nutrition is one of the main constraints to reach these modify the reproductive status of the hosts (Grenier et objectives, but generally speaking more knowledges are al. 2002). The fungicides incorporated into the food for required about the physiology, behaviour and genetics phytophagous insects (nipagine, merthiolate, sorbic acid) of the insects to be reared. are often detrimental for entomophages (Grenier 1977). Specific fungicides used in cell cultures (amphotericine, There are special lacks of basic research in functional nystatin) are better tolerated than more generalist morphology and host-parasitoid relationships for products (Grenier and Liu 1990).
immature parasitoids (Cônsoli and Parra 1999). An analytical approach with biochemical analyses of the food Sometimes, high levels of antimicrobial agents, and of the carcass of the insects produced is a powerful especially antibiotics, could modify the diet consistency method to define and test artificial diets (Grenier 2002). or cause the formation of some aggregations destroying A new research direction recently open concerns the the homogeneity of the diet. These modifications may nutrigenomics with some new tools, such as micro-arrays, interfere with the nutritional value of the diet and with allowing to improve a diet by comparing gene expression the food intake of the larvae (Büyükgüzel 2002).
patterns under different nutrition conditions (Coudron Some antimicrobial agents (penicillin, streptomycin, et al. 2006). More studies on host/symbiont relationships rifampicin, tetracycline hydrochloride, lincomycin would probably be profitable for better knowledge hydrochloride, methyl p-hydroxybenzoate, cyclohexi- on nutrition and reproduction as well as for enhanced mide and sodium benzoate) could significantly increase definition of quality criteria, possibly by transfer of Grenier / Artificial Rearing of Entomophagous Insects symbionts between species (Grenier et al. 1998b). Many Askew, RR., Shaw, MR. 1986. Parasitoid communities: Their
parameters control the different physiological functions, size, structure and development. In: Waage J., Greathead D. [eds], Insect Parasitoids, London Academic Press, pp. including nutrition and may interact with each other simultaneously. It is recommended to use multivariate/ multifactorial analyses to take into account efficiently Barrett, M., Schmidt, JM. 1991. A comparison between the
amino acid composition of an egg parasitoid wasp and these multiple interactions (Grenier et al. 1986). some of its hosts. Entomol. Exp. Appl., 59: 29-41.
A lot of constraints limit the development in the Battisti, A., Ianne, P., Milani, N., Zanata, M. 1990. Preliminary
rearing of entomophagous insects, mainly technical accounts on the rearing of Ooencyrtus pityocampae (Mercet) and economical ones. Thus, new directions and future (Hym., Encyrtidae). J. Appl. Entomol., 110: 121-127.
trends for this field may also concern the structures of Beckage, NE. 1985. Endocrine interactions between
the research, the choice of the most promising species, endoparasitic insects and their hosts. Ann. Rev. Entomol., 30: and the development of specific production means such as automation and quality assurance (Grenier 2009). Bonnot, G., Delobel, B., Grenier, S. 1976. Composition
For better chances of success, it is also recommended corporelle en acides aminés du parasitoïde Phryxe caudata to constitute teams with different specialists such as Rond. (Diptera) au cours de sa croissance larvaire. J. Insect entomologists, engineers, and economists. (Cohen et al. Physiol., 22: 505-514.
Bonnot, G., Delobel, B., Grenier, S. 1984. Elevage, croissance
et développement de Phryxe caudata Rond. (Diptera, The quality of the insects produced is of prime importance Tachinidae), sur son hôte de substitution Galleria mellonella to ensure success in the biological control strategies and L. (Lepidoptera) et sur milieux artificiels. Bull. Soc. Linn. therefore to retain the confidence of the end users. The Lyon, 53: 313-320.
required characteristics of the insects vary in relation Bonnot, G., Grenier, S., Delobel, B., Guillaud, J. 1991.
with the purposes of their production. For example, Comparison of body composition of 3 Tachinids (Phryxe the criteria retained are not the same for inoculative or caudata, Lixophaga diatraeae and Pseudoperichaeta nigrolineata) inundative releases. Morphological characters, immature growing on the same host, Galleria mellonella : comparative development parameters, sex ratio, symbiont association, study of nutritional needs. Redia, 74: 453-455.
fecundity, longevity as well as biochemical parameters Bonte, M., De Clercq, P. 2008. Developmental and Reproductive
are important cues to be considered for quality control Fitness of Orius laevigatus (Hemiptera: Anthocoridae) and in addition, these latter could indicate the deficiency Reared on Factitious and Artificial Diets. J. Econ. Entomol., or excess in a particular nutritional component. In fine 101: 1127-1133.
the predation efficiency or the parasitization rate have to Bonte M., De Clercq, P. 2010. Influence of predator density,
be evaluated (Grenier and De Clercq 2003).
diet and living substrate on developmental fitness of Orius The current public opinion highly suspicious to the laevigatus. J. Appl. Entomol., 135: 343–350. immoderate use of chemicals and more and more Büyükgüzel, K., 2001. Positive Effects of Some Gyrase
disposed towards organic products may encourage the Inhibitors on Survival and Development of Pimpla practice of biological control strategies and consequently turionellae (Hymenoptera: Ichneumonidae) Larvae Reared on an Artificial Diet. J. Econ. Entomol., 94: 21-26.
stimulate the development of artificial rearing, one of the way to reach economically acceptable mass production Büyükgüzel K., 2002. Effects of some Antimicrobial Agents
on the Total Protein Content of the Endoparasitoid Pimpla of entomophagous insects. Further efforts have to turionellae L. (Hymenoptera: Ichneumonidae). Turk. J. Zool., be accomplished to burst the last locks impeding the 26: 101-109.
development of these approaches.
Büyükgüzel, E., Tunaz, H., Stanley, DW., Büyükgüzel, K.
9. In Memoriam
2011. The influence of chronic eicosanoid biosynthesis
inhibition on life history of the Greater waxmoth, Galleria This paper is dedicated to the memory of Guy Bonnot, mellonella and its ectoparasitoid, Bracon hebetor. J. Insect Bernard Delobel, and Pierre Laviolette.
Physiol., 57: 501-507.
10. References
Chen, ZH., Qin, JD., Fan, XM., Li, XL. 1984. Effects of adding
lipids and juvenoid into the artificial diet on feeding and Arijs, Y., De Clercq, P. 2002. Artificial diets for the production of
reproduction of Coccinella septempunctata L. Acta Entomol. natural enemies (predators and parasitoids) of greenhouse Sinica, 27: 136-146.
pest insects. Final consolidated report, FAIR 6-project no. Cohen, AC. 1981. An artificial diet for Geocoris punctipes.
Southwestern Entomology, 6: 109-113.
Grenier / Artificial Rearing of Entomophagous Insects Cohen, AC. 1985. Simple method for rearing the insect predator
and in vivo-reared Exorista larvarum. Entomol. Exp. Appl., Geocoris punctipes (Heteroptera: Lygaeidae) on a meat diet. 120: 167-174.
J. Econ. Entomol., 78: 1173-1175.
Dougherty, EC. 1959. Introduction to axenic culture of
Cohen, AC. 1992. Using a systematic approach to develop
invertebrate metazoa : a goal. Ann. N. Y. Acad. Sci., 77: 27-54.
artificial diets for predators. In: Anderson T., Leppla NC. Durmus, Y., Büyükgüzel, E., Terzi, B., Tunaz, H., Stanley
[eds], Advances in insect Rearing for research and Pest D., Büyükgüzel, K. 2008. Eicosanoids mediate melanotic
management, pp 77-92.
nodulation reactions to viral infection in larvae of the Cohen, AC. 1995. Extra-oral digestion in predaceous terrestrial
parasitic wasp, Pimpla turionellae. J. Insect Physiol., 54: 17-24.
arthropoda. Ann. Rev. Entomol., 40: 85-103.
El Arnaouty, SA., Galal, H., Bessat-Arnaouty, V., Ferran, A.,
Cohen, AC. 2004. Insect diets: Science and technology. Cohen
Grenier, S. 2006. Influence of artificial diet supplements
AC (ed), CRC Press, Boca Raton, FL. 324p.
on developmental features of Chrysoperla carnea Stephens. Egypt. J. Biol. Pest Co., 16: 29-32. Cohen, AC., Nordlund, DA., Smith, RA. 1999. Mass rearing
of entomophagous insects and predaceous mites: are the Fanti, P. 1990. Fattori ormonali inducenti la prima muta larvale
bottlenecks biological, engineering, economic, or cultural?. del parassitoids Pseudogonia rufifrons Wied. (Diptera: Biocont. News Inform., 20: 85 -90.
Tachinidae) in substrati di crescita in vivo e in vitro. Boll. Ist. entomol. Univ. Bologna, 45: 47-59.
Cônsoli, F.L., Grenier, S. 2010. In vitro rearing of egg parasitoids,
Ferkovich, SM., Shapiro, JP. 2004. Increased egg-laying in
in "Progress in Biological Control- Egg parasitoids, In: Orius insidiosus (Hemiptera: Anthocoridae) fed artificial Cônsoli FL., Parra JRP., Zucchi RA. [eds], Agroecosystems diet supplemented with an embryonic cell line. Biol. Control, with emphasis on Trichogramma", Springer Dordrecht, Chap. 11, pp. 293-313.
Gomes, SM., Grenier, S., Febvay, G., Guillaud, J., Parra,
Cônsoli, FL., Parra JRP. 1999. In vitro rearing of parasitoids:
JRP. 2000. Development of Trichogramma pretiosum
constraints and perspectives. Trends Entomol., 2:19-32.
(Hymenoptera: Trichogrammatidae) in artificial diet, Coudron TA., Yocum GD., Brandt, SL. 2006. Nutrigenomics:
focusing on protein utilization. Proceedings XXI- Intern. a case study in the measurement of insect response to Congress Entomol. Iguaçu, Brazil, pp. 387.
nutritional quality. Entomol. Exp. Appl., 121:1-14.
Greany, P. 1986. In vitro culture of hymenopterous larval
Dai, KJ., Zhang, LW., Ma, ZJ., Zhong, LS., Zhan, QX.,
endoparasitoids. J. Insect Physiol., 32: 409-419.
Cao, AH., Xu, KJ., Li, Q., Gao, YG. 1988. Research and
Grenier, S. 1977. Effets nocifs de la nipagine M sur le parasitoïde
utilization of artificial host egg for propagation of parasitoid Phryxe caudata [Dipt.: Tachinidae]. Entomophaga, 22: 23-26.
Trichogramma, In: Voegelé J., Waage JC., Van Lenteren J. [eds], Trichogramma and other egg parasites, Les colloques Grenier, S. 1980. Développement endoparasitaire et croissance
de l'INRA, pp. 311-318.
pondérale larvaire du parasitoïde Lixophaga diatraeae (Dip. : Tachinidae) dans un hôte de substitution Galleria mellonella De Clercq, P., Degheele, D. 1992. A meat-based diet for rearing
L. (Lep. : Pyralidae). Entomophaga, 25 : 17-26.
the predatory stinkbugs Podisus maculiventris and Podisus Grenier, S. 1986. Biologie et physiologie des relations hôtes-
sagitta (Het.: Pentatomidae). Entomophaga, 37: 149-157.
parasitoïdes chez 3 Tachinaires (Diptera, Tachinidae) Delobel, B., Pageaux, JF. 1981. Influence de l'alimentation sur la
d'intérêt agronomique. Développement en milieux composition en acides gras totaux des Diptères Tachinaires. artificiels. Lutte biologique. Thèse de Doctorat d'Etat ès Entomol. Exp. Appl., 29: 281-288.
Sciences, Lyon, n° IDE 8604, pp. 156 + 61p d'illustrations. Dindo, ML., 2011. Tachinid parasitoids: are they to be Grenier, S. 1988. Developmental relationships between the
considered as koinobionts? BioControl, 56: 249-255.
tachinid parasitoid Pseudoperichaeta nigrolineata and two Dindo, ML., Farneti, R., Scapolatempo, M., Gardenghi, G.
host species - Hormonal implications, In: Boulétreau M., 1999. In vitro rearing of the parasitoid Exorista larvarum (L.)
Bonnot G. [eds], Parasitoid Insects, European Workshop, (Diptera: Tachinidae) on meat homogenate-based diets. Lyon.,1987, Les Colloques de l'INRA, 48, pp. 87-89.
Biol. Control , 16: 258-266.
Grenier, S. 1994. Rearing of Trichogramma and other egg
Dindo, ML., Farneti, R., Baronio P., 2001. Rearing of the pupal
parasitoids on artificial diet, In: Wajnberg E., Hassan SA. parasitoid Brachymeria intermedia on veal homogenate-based [eds], Biological control with egg parasitoids, CAB Intern. artificial diets: evaluation of factors affecting effectiveness. Pub., Chap. 4, pp. 73-92.
Entomol. Exp. Appl., 100: 53-61.
Grenier, S. 1997. Desenvolvimento e produção in vitro de
Dindo, ML., Marchetti, E., Galvagni, G., Baronio, P. 2003.
Trichogramma, In: Parra JRP., Zucchi RA. [eds], Trichogramma Rearing of Exorista larvarum (Diptera: Tachinidae): e o controle Biologico Aplicado, FEALQ - FAPESP, pp. 235-258.
simplification of the in vitro technique. Bull. Insectology, 56: Grenier, S. 2000. Rearing in artificial conditions as a tool for
physiological or behavioural studies of egg parasitoid Dindo, ML., Grenier, S., Sighinolfi, L., Baronio, P. 2006.
insects. Proceedings XXI International Congress of Entomology, Biological and biochemical differences between in vitro- Iguaçu, Brazil: 389 (1541).
Grenier / Artificial Rearing of Entomophagous Insects Grenier, S. 2002. Artificial diets for the production of natural
Grenier, S., Delobel, B. Bonnot, G. 1986. Physiological
enemies (predators and parasitoids) of greenhouse pest interactions between endoparasitic Insects and their hosts: insects. Final consolidated report, FAIR 6-project no. CT 98 Physiological considerations of importance to the success of in vitro culture: an overview. J. Insect. Physiol., 32: 403-408.
Grenier, S. 2009. In vitro rearing of entomophagous insects -
Grenier, S., Guillaud, J., Delobel, B., Bonnot, G. 1989.
Past and future trends: a minireview. Bull. Insectology, 62: Nutrition et élevage du prédateur polyphage Macrolophus caliginosus (Heteroptera, Miridae) sur milieux artificiels. Entomophaga, 34: 77- 86.
Grenier,S. 2011. Artificial rearing of entomophagous insects,
General outlines. Proceedings of Inter. Sympo. Mass Grenier, S., Veith, V., Renou, M. 1993. Some factors stimulating
Production and Commercialization of Arthropod Biological the oviposition by the oophagous parasitoid Trichogramma Control Agents (ISMC), Beijing, China, p.4-5.
brassicae Bezd. (Hym., Trichogrammatidae) in artificial host eggs. J. Appl. Entomol., 115: 66-76.
Grenier, S., Bonnot, G. 1988. Development of Trichogramma
dendrolimi and T. maidis (Hymenoptera, Trichogrammatidae) Grenier, S., Greany , P., Cohen, AC. 1994. Potential for
in artificial media and artificial host eggs, In: Voegelé J., mass release of insect parasitoids and predators through Waage J., Van Lenteren JC. (eds), Trichogramma and other development of artificial culture techniques, In: Rosen egg parasites, Les colloques de l'INRA, pp. 319-326.
D., Bennett FD., Capinera JL. [eds], Pest management in the subtropics: Biological control - a Florida perspective, Grenier, S. De Clercq, P. 2003. Comparison of Artificially vs.
Intercept. Pub., Chap.10, pp. 181- 205.
Naturally Reared Natural Enemies and Their Potential for Use in Biological Control, In: van Lenteren JC. [ed.], Grenier, S., Yang, H., Guillaud, J., Chapelle, L. 1995.
Quality Control and Production of Biological Control Comparative development and biochemical analyses of Agents –Theory and Testing Procedures, CABI Publishing, Trichogramma (Hymenoptera: Trichogrammatidae) grown Cambridge, pp. 115-131.
in artificial media with hemolymph or devoid of insect components. Comp. Biochem. Physiol., 111B: 83-90.
Grenier, S., Grenier, A.M. 1993. Fenoxycarb, a fairly new
Insect Growth Regulator: a review of its effects on Insects. Grenier, S., Han, SC., Chapelle, L., Liu, WH., Guillaud, J. 1998a.
In vitro development of Trichogramma spp. (Hymenoptera: Ann. appl. Biol. 122: 369-403.
Trichogrammatidae) in long-term stored, freeze-dried Grenier, S., Liu, WH. 1990. Antifungals: Mold control and safe
artificial media. Biocontrol Sci. Techn., 8: 589-596.
levels in artificial media for Trichogramma (Hymenoptera, Grenier, S., Pintureau, B., Heddi, A., Lassablière, F., Jager, C.,
Trichogrammatidae). Entomophaga, 35: 283-291.
Louis, C., Khatchadourian, C. 1998b. Successful horizontal
Grenier, S., Pintureau, B. 1991. Essai d'élevage en milieux
transfer of Wolbachia symbionts between Trichogramma artificiels de Lixophaga diatraeae (Dipt. Tachinidae), wasps. Proc. R. Soc. Lond. B 265(1404): 1441-1445.
parasitoïde des Lépidoptères foreurs de la canne à sucre. Grenier, S., Gomes, SM., Pintureau, B., Lassablière, F.,
Importance de la souche, In: Pavis, C. and Kermarrec, Bolland, P. 2002. Use of tetracycline in larval diet to
A. [eds], Rencontres Caraïbes en Lutte Biologique, Les study the effect of Wolbachia on host fecundity and clarify Colloques de l'INRA, pp. 451-458.
taxonomic status of Trichogramma species in cured bisexual Grenier, S., Plantevin, G. 1990. Development modifications
lines. J. Invert. Pathol., 80: 13-21.
of the parasitoid Pseudoperichaeta nigrolineata (Dipt, Grenier, S., Gomes S., Febvay, G., Bolland, P., Parra, JRP.
Tachinidae) by fenoxycarb, an insect growth regulator, 2005. Artificial diet for rearing Trichogramma wasps
applied onto its host Ostrinia nubilalis (Lep., Pyralidae). J. (Hymenoptera: Trichogrammatidae) with emphasis on appl. Entomol. 110: 462-470.
protein utilisation. Proceedings of International Symposium Grenier, S., Delobel, B., Bonnot, G. 1974. Développement et
on Biological Control of Arthropods, Davos, Switzerland, M.S. croissance pondérale de Phryxe caudata Rond. (Diptera, Hoddle Compiler, 481-487.
Tachinidae) sur Galleria mellonella L. (Lepidoptera). Han, SC., Chen, QX., Li, LY. 1994. A study of the oviposition
Influence de l'âge de l'hôte. Ann. Zool. Ecol. Anim., 6: 61-79.
synergists for in vitro rearing Trichogramma spp. Entomol. Grenier, S., Bonnot, G., Delobel, B. 1975. Définition et mise au
Sinica, 1: 333-338.
point de milieux artificiels pour l'élevage in vitro de Phryxe Herting, B. 1960. Biologie der westpalaärktischen Raupen fliegen
caudata Rond. (Diptera, Tachinidae). II - Croissance et mues Dipt., Tachinidae, Paul Parey, pp.188.
larvaires du parasitoïde en milieux définis. Ann. Zool. Ecol. Anim., 7: 13-25.
Lawrence, PO. 1986. Host parasite hormonal interactions : an
overview. J. Insect Physiol., 32: 295-298.
Grenier, S., Bonnot, G., Delobel, B. Laviolette, P. 1978.
Développement en milieu artificiel du parasitoïde Lixophaga Li, LY. 1986. Mass production of natural enemies (parasites and
predators) of insect pests. Natural Enemies of Insects, 8: 52-62.
diatraeae (Towns.) (Diptera, Tachinidae). Obtention de l'imago à partir de l'oeuf. C.R. Acad. Sci. Paris, série D, 387: Li, LY., Liu, WH., Chen, CS., Han, SC., Shin, JC., Du, HS.,
Feng, SY. 1988. In vitro rearing of Trichogramma spp. and
Grenier / Artificial Rearing of Entomophagous Insects Anastatus sp. in artificial "eggs" and the methods of mass Ramadhane, A., Grenier, S., Plantevin, G. 1987. Physiological
production, In: Voegelé J., Waage J., Van Lenteren JC. interactions and development synchronisations between [eds], Trichogramma and other egg parasites, Les colloques de non-diapausing, Ostrinia nubilalis larvae and the tachinid l'INRA, pp. 339-352.
parasitoid Pseudoperichaeta nigrolineata. Entomol. Exp. Appl., 45: 157-165.
Lü, X., Han, SC., Li, LY., Dai, JQ., Ye, JW. 2011. Rearing
Trichogramma dendrolimi in vitro with artificial diets Ramadhane, A., Grenier, S., Plantevin, G. 1988. Photoperiod,
containing trehalose. Proceedings of Inter. Sympo. Mass temperature and ecdysteroid influences on physiological interactions between diapausing Ostrinia nubilalis larvae Production and Commercialization of Arthropod Biological and the Tachinid parasitoid Pseudoperichaeta nigrolineata. Control Agents (ISMC), Beijing, China, p.9.
Ent. Exp. Appl., 48: 275 - 282.
Masutti, L., Battisti, A., Milani, N., Zanata, M. 1992. First
Sighinolfi, L., Febvay, G., Dindo, ML., Rey, M., Pageaux, JF.,
success in the in vitro rearing of Ooencyrtus pityocampae Baronio, P., Grenier, S., 2008. Biological and biochemical
(Mercet) (Hym. Encyrtidae). Preliminary note. Redia, 75:
characteristics for quality control of Harmonia axyridis (Pallas) (Coleoptera, Coccinellidae) reared on liver-based Mellini, E. 1975. Possibilità di allevamento di Insetti entomofagi
diet. Archiv. Insect Biochem. Physiol., 68: 26-39. parassiti su diete artificiali. Boll. Ist. entomol. Univ. Bologna, Specty, O., Febvay, G., Grenier, S., Delobel, B., Piotte, C.,
32: 257-290.
Pageaux, JF., Ferran, A., Guillaud, J. 2003. Nutritional
Mellini, E. 1983. L'ipotesi della dominazione ormonale,
plasticity of the predatory ladybeetle Harmonia axyridis esercitata dagli ospiti sui parassitoidi, alla luce delle recenti (Coleoptera : Coccinellidae): Comparison between natural scoperte nella endocrinologia degli insetti. Boll. Ist. entomol. and substitution prey. Arch. Insect Biochem. Physiol., 52: Univ. Bologna, 38: 135-166.
Mellini, E. 1986. Importanza dell'età dell'uovo, al momento
Stireman, JO., O'Hara, JE., Wood, DM., 2006. Tachinidae:
della parassitizzazione, per la biologia degli Imenotteri Evolution, Behavior, and Ecology. Ann. Rev. Entomol., 51: oofagi. Boll. Ist. entomol. Univ. Bologna, 41: 1-21.
Thompson, SN. 1976. The amino acid requirements for larval
Mellini, E., Campadelli, G., Dindo, ML. 1996. Actual
development of the hymenopterous parasitoid Exeristes possibilities of mass production of the parasitoid Exorista roborator Fabricius (Hymenoptera: Ichneumonidae). Comp. larvarum (L.) (Diptera: Tachinidae) on ologidic diets. Boll. Biochem. Physiol. A, 53: 211-213.
Ist. entomol. Univ. Bologna, 50: 233-241.
Thompson, SN. 1977. Lipid nutrition during larval development
Mullins, DE. 1985. Chemistry and physiology of the
of the parasitic wasp, Exeristes. J. Insect Physiol., 23: 279-283.
hemolymph, In: Kerkut GA., Gilbert LI. [eds], Comprehensive Thompson, SN. 1980. Artificial culture techniques for rearing
Insect Physiology, Biochemistry and Pharmacology. Vol. 3, larvae of the chalcidoid parasite, Brachymeria intermedia. Integument, respiration and circulation., Pergamon Press, pp. Entomol. Exp. Appl., 27, 133-143.
Thompson, SN. 1982. Characterization of the phospholipids
Nakahara Y., Hiraoka T., Iwabuchi K. 1999. Effects of lipo-
in the insect parasite, Exeristes roborator (Fabricius) and phorin and 20-hydroxyecdysone on in vitro development of the effects of dietary glucose on their distribution. Comp. the larval endoparasitoid Venturia canescens (Hymenoptera: Biochem. Physiol. 71: 127-131.
Ichneumonidae). J. Insect Physiol., 45: 453-460.
Thompson, SN. 1986. The metabolism of insect parasites
Nettles, WC.Jr., 1986. Effects of Soy Flour, Bovine Serum
(parasitoids): an overview. J. Insect Physiol., 32: 421-423.
Albumin, and Three Amino Acid Mixtures on Growth and Thompson, SN. 1990a. Nutritional considerations in
Development of Eucelatoria bryani (Diptera: Tachinidae) propagation of entomophagous species, In: Baker R., Dunn Reared on Artificial Diets. Environ. Entomol., 15: 1111-1115.
P. [eds], New directions in Biological Control. UCLA Nettles, WC. 1987. Amino acid requirements for growth and
symposium on molecular and cellular biology, NewYork, development of the Tachinid Eucelatoria bryani. Comp. Alan R. Liss. 112, pp. 389-404.
Biochem. Physiol., 86A: 349-354.
Thompson, SN. 1990b. NMR spectroscopy: its basis, biological
Nettles, WC., Wilson, CM., Ziser, SW. 1980. A diet and
application and use in studies of insect metabolism. Mini- methods for the in vitro rearing of the tachinid, Eucelatoria review. Insect Biochem., 20: 223-237.
sp. Ann. entomol. Soc. Am., 73: 180-184.
Thompson, SN. 1999. Nutrition and culture of entomophagous
insects. Ann. Rev. Entomol., 44: 561-592.
Qin, Z., Zhang, F., Wang, S., Xu, HX., Tang, B. 2011. A trehalose
6-phosphate synthase gene of the ladybird Harmonia Thompson, SN., Barlow, JS. 1972. Influence of host fatty
axyridis: cloning, the expression and its function under acid composition on that of ichneumonoid and chalcidoid various stress conditions. Proceedings of Inter. Sympo. wasps. J. Parasitology, 58: 836-839.
Mass Production and Commercialization of Arthropod Thompson, SN., Hagen KS. 1999. Nutrition of entomophagous
Biological Control Agents, Beijing, China, p.36.
insects and other arthropods, In: Bellows TS., Fisher TW. Grenier / Artificial Rearing of Entomophagous Insects [eds], Handbook of biological control: Principles and Yazgan, S. 1981. A meridic diet and quantitative effects of
applications. Academic Press, New York, pp. 594-652.
Tween 80, fatty acid mixtures and inorganic salts on development and survival of the endoparasitoid Pimpla Thompson, SN., Bednar, L., Nadel, H. 1983. Artificial culture
of the insect parasite, Pachycrepoideus vindemiae. Entomol. turionellae L. Z. Angew. Entomol., 91: 433-441.
Exp. Appl., 33: 121-122.
Yazlovetsky, IG. 1992. Development of artificial diets for
Vanderzant, ES. 1969. An artificial diet for larvae and adults
entomophagous insects by understanding their nutrition of Chrysopa carnea, an insect predator of crop pests. J. Econ. and digestion, In: Anderson TE., Leppla NC. [eds], Advances Entomol., 62: 256-257.
in Insect Rearing for Research & Pest Management, Westview Press, pp. 41-62.
Vandekerkhove, B., Van Baal, E., Bolckmans, K., De Clercq,
P. 2006. Effect of diet and mating status on ovarian Zapata, R., Specty, O., Grenier, S., Febvay, G., Pageaux, J.F.,
development and oviposition in the polyphagous predator Delobel, B., Castane, C. 2005. Carcass analysis allowing
Macrolophus caliginosus (Heteroptera: Miridae). Biol. to improve a meat-based diet for the artificial rearing of Control, 39: 532–538 the predatory mirid bug Dicyphus tamaninii. Archiv. Insect Biochem. Physiol., 60: 84-92.
Vandekerkhove, B., Parmentier, L., Van Stappen, G., Grenier,
S., Febvay, G., Rey, M., De Clercq, P. 2009. Artemia cysts
Zhong, LS., Zhang, JL. 1989. Influence of diet pH to the
as an alternative food for the predatory bug Macrolophus development and the efficacy of reproduction of pygmaeus. J. Appl. Entomol., 133: 133-142.
Trichogramma confusum (Hym.: Trichogrammatidae) in artificial rearing. Chinese J. Biol. Control, 5: 101-103.
Yazgan, S. 1972. A chemically defined synthetic diet and larval
nutritional requirements of the endoparasitoid Itoplectis conquisitor (Hymenoptera). J. Insect Physiol., 18: 2123-2141.

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