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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: [email protected] 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
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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.
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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.
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