BioControl (2009) 54:325–339 DOI 10.1007/s10526-008-9171-z
REVIEW
Benefits and limitations of factitious prey and artificial diets on life parameters of predatory beetles, bugs, and lacewings: a mini-review Eric W. Riddick
Received: 18 December 2007 / Accepted: 9 May 2008 / Published online: 26 May 2008 Ó International Organization for Biological Control (IOBC) 2008
Abstract The primary peer-reviewed literature pertaining to rearing of predatory beetles, true bugs, and lacewings was reviewed and synthesized. This study focused on the literature published from 1998 to 2007. Advances in rearing were revealed in relation to the influence of factitious prey and artificial diets on predator life parameters. Eggs of the Angoumois grain moth and Mediterranean flour moth were factitious prey that supported the development and reproduction of many species in lieu of natural prey. Artificial diets based on vertebrate protein were generally inferior to factitious prey for production of predators. A few exceptional cases demonstrated potential for continuous rearing of true bugs and lacewings on artificial diet, as a stand-alone food source. Factors that could ensure progressive rearing success might involve (1) exploiting the highly polyphagous nature of certain species, (2) exposing predators to artificial diet for multiple generations to incite adaptation, (3) formulating artificial diets to match the texture and chemical composition of preferred natural prey, and (4) encasing the diet within ParafilmÒ to resemble the shape of natural prey. Encasement may also reduce desiccation and
Handling editor: Patrick De Clercq. E. W. Riddick (&) Biological Control of Pests Research Unit, USDA-ARS, 59 Lee Road, Stoneville, MS 38776, USA e-mail:
[email protected]
retard spoilage of the diet. Identification of other factitious prey and development of artificial diets that ensure production of predators of high quality should be possible. This review was conducted, for the most part, in support of generalist insect predators used, or having the potential to be used, in augmentative biological control of pests on plants in semi-closed systems, such as greenhouses and interiorscapes. Keywords Augmentation Biological control Greenhouse Production Quality Rearing
Introduction In recent years, more interest in the use of biological control to manage crop pests has led to an increase in companies producing natural enemies, including predators and parasitoids. Approximately 85 companies, worldwide, produce 125 or more natural-enemy species mainly for the greenhouse industry (van Lenteren 2003). It is expected that the greenhouse industry in the USA will expand considerably in upcoming years; this should increase the market for biological control. Additionally, the increased popularity of interiorscapes (i.e., interior plantscapes) could provide unique opportunities for biological control (Goolsby et al. 2000; Smith and Krischik 2000).
123
326
Augmentative biological control is dependent upon the production of large numbers of natural enemies of high quality (Glenister and Hoffmann 1998; Nordlund 1998; Smith and Nordlund 1999, 2000). Cost-effective rearing techniques are needed so that augmentation can become a more competitive strategy for managing arthropod pests. One way of facilitating this is reducing the costs associated with rearing natural enemies. At present, biocontrol producers often culture natural enemies on their natural prey (or host), which are, in turn, maintained on their host plants. Maintaining three trophic levels leads to high labor costs and costs associated with operating and maintaining separate space and equipment (and even whole facilities, in some instances) to produce each trophic level. Reducing some of the rearing costs by eliminating the use of live plants for the prey (or hosts) could be an important first step (De Clercq 2004). For example, many lepidopterans can be reared effectively on diets that are devoid of any living plant material. Several species can be produced simply on relatively cheap foods, such as wheat flour or grains. The egg stage of a few species has been used as factitious prey by some commercial insectaries in recent years to produce generalist predators including predatory coleopterans (e.g., lady beetles), predatory heteropterans (e.g., anthocorids, mirids) and predatory neuropterans (e.g., lacewings). Besides predatory mites, these three groups represent a significant number of the predators reared and sold by commercial producers (Cranshaw et al. 1996; van Lenteren 2003). Research on the usefulness of other potential factitious prey that can be produced at low cost has been ongoing. An even further refinement of the costs associated with rearing predators could involve the use of artificial diets that support the development and reproduction of predators in the absence of any live prey (De Clercq 2004). Artificial diets must satisfy the nutritional requirements of predators and ensure the continuous production of progeny of high quality (Cohen 2004). In addition, predators produced on artificial diets (as well as factitious prey) must retain the capacity to search for, locate, and kill target prey (pests) under field conditions. In light of the urgent need to provide more cost-effective techniques to produce predators of high quality, this study endeavored to review the recent scientific literature pertaining to factitious prey and artificial diets of
123
E. W. Riddick
generalist predators. Most of the content of this review encompassed the years 1998–2007 and the primary research literature, in English language, was reviewed. This review was restricted to the past decade, because very fine reviews by Thompson (1999) and Thompson and Hagen (1999) have covered the literature prior to 1998. The abstract and the original text, when accessible, of literature published in the English language were compiled with the aid of the USDA, National Agricultural Library on-line databases and literature retrieval services. One or more of the following life parameters were used to gauge the impact (i.e., potential benefit) of factitious prey or an artificial diet on a predator. These included development time, survival rate, body size (weight or length), oviposition rate (i.e, fecundity), oogenesis rate, longevity, and predation potential. Most of these life parameters have been used to evaluate the quality of commercially-produced predators (Penn et al. 1998; Grenier and De Clercq 2003; van Lenteren et al. 2003a; Callebaut et al. 2004). The objective of this study was to highlight the potential benefits, if any, of various factitious prey and artificial diets on select predatory beetles, bugs, and lacewings. This review should help encourage continued research towards development and utilization of foods that generate predators of high quality for augmentative biological control.
Factitious prey Factitious prey may comprise live, frozen, irradiated, or lyophilized insects, mites, and crustaceans. The ability of a predator to adapt to factitious prey could depend on its feeding history, that is, whether the predator is polyphagous, oligophagous, or monophagous. In this study, polyphagous predators are capable of utilizing a broad range of prey species, often representing diverse arthropod orders; oligophagous predators utilize several prey species, and monophagous predators utilize a few related prey species. Consequently, highly polyphagous species could be more amenable to surviving and reproducing on factitious prey. Examples of studies that considered the impact of common and novel factitious prey on life parameters of select predatory beetles, bugs, and lacewings have been outlined in the following paragraphs.
Rearing predators
Hamasaki and Matsui (2006) tested the suitability of eggs of the Mediterranean flour moth (Ephestia kuehniella Zeller) as factitious prey for the lady beetle Propylea japonica (Thunberg). Interestingly, moth eggs supported satisfactory development of P. japonica larvae in lieu of its natural prey, pea aphids (Acyrthosiphum pisum (Harris)). Also, P. japonica larvae could be reared at high densities without concerns of cannibalism. Unfortunately, the fertility of adults that had been reared on E. kuehniella eggs was significantly reduced when compared to adults reared on natural prey. Michaud and Qureshi (2005) indicated that E. kuehniella eggs were an inferior food source for the convergent lady beetle, Hippodamia convergens Gue´rin-Me´neville. It took approximately four weeks for wild females to mature eggs when fed E. kuehniella eggs in the laboratory. Female cohorts fed natural prey, the greenbug, Schizaphis graminum (Rondani), produced mature eggs within one week. The multicolored Asian lady beetle, Harmonia axyridis (Pallas), was able to complete its development on E. kuehniella eggs (Specty et al. 2003). E. kuehniella eggs were richer in protein (amino acids) and lipids, whereas, natural prey (pea aphids, A. pisum) was slightly richer in carbohydrates (glycogen). Interestingly, mortality during the larval stage decreased, body weight of emerged adults increased, and fecundity increased when E. kuehniella eggs, rather than aphids, were used as prey. The authors concluded that H. axyridis has considerable plasticity to adapt to different food sources and compensate accordingly. In another study, H. axyridis was reared in the laboratory using fresh (live) versus previously-frozen (thawed) eggs of the Angoumois grain moth, Sitotroga cerealella (Olivier), as factitious prey (Abdel-Salam and Abdel-Baky 2001). In general, fresh rather than previously-frozen S. cerealella eggs were a more nutritional source of food for predator development and reproduction. Assuredly, the freezing and thawing processes could reduce the ‘‘quality’’ of the eggs. The eggs of E. kuehniella, with or without a bee pollen, were evaluated as factitious prey for larvae and adults of the two-spot ladybird, Adalia bipunctata (L.) (De Clercq et al. 2005a). They found that supplementing flour moth eggs with frozen, moist bee pollen provided a suitable diet, as compared to the preferred prey (live pea aphids), for larval development, survival and
327
hatchability of eggs laid by adult females fed this diet in the laboratory. This species can compensate for a suboptimal diet of factitious prey by supplemental feeding on plant products, such as flower pollen. Apparently, H. axyridis can utilize a broader range of prey species than P. japonica or A. bipunctata, since Ephestia eggs alone are sufficient for reproduction. In addition, Berkvens et al. (2008) suggest that H. axyridis has the ability to use pollen alone as an alternative food during periods of prey shortage and, therefore, has a competitive advantage over less capable species such as A. bipunctata. The development and reproduction of an anthocorid bug, Orius laevigatus (Fieber), on cysts (inactive embryos) of the brine shrimp (Artemia franciscana Kellogg; Branchiopoda) versus E. kuehniella eggs have been compared (Arijs and De Clercq 2001a; De Clercq et al. 2005b). Arijs and De Clercq (2001a) obtained O. laevigatus adults from a stock culture maintained on E. kuehniella eggs and bee pollen. Feeding this predator hydrated decapsulated cysts (which had been stored in dry form) resulted in nymphal development, fecundity and oviposition rates comparable to those of predators fed previously frozen Ephestia eggs. Brine shrimp cysts can be used as a supplementary food in the mass rearing of O. laevigatus (De Clercq et al. 2005b). These studies demonstrate the usefulness of a novel factitious food that can support the development and reproduction of an anthocorid. Research has shown that brine shrimp cysts are suitable food for other predators (Callebaut et al. 2004; Castan˜e´ et al. 2006). De Clercq et al. (1998) demonstrated that unnatural (factitious) prey supported the development and reproduction of a predaceous pentatomid, Podisus maculiventris (Say). Nymphal development was fastest on pupae of the yellow mealworm (Tenebrio molitor L., Tenebrionidae) than on larvae of this prey or on larvae of the greater wax moth (Galleria mellonella (L.), Pyralidae). Although male or female body weight was not affected by prey treatment, total egg production was greatest for females reared on G. mellonella larvae. Zanuncio et al. (2001) studied the nymphal development and reproductive potential of a predaceous pentatomid, Podisus nigrispinus (Dallas), fed with combinations of live, factitious prey. Experimental treatments included yellow mealworm (T. molitor) pupae, house fly (Musca domestica L.,
123
328
Muscidae) larvae, both prey presented together, and both prey presented on alternate days. The most notable result of this research was that female body weight was affected by treatments; heavier females were produced from a diet of T. molitor alone, or from a diet of both prey on alternate days, rather than both prey simultaneously, or M. domestica alone. Nevertheless, fecundity was greatest when predators developed on mixed prey (given simultaneously or on alternate days) than when given T. molitor alone. The authors indicated that female body weight did not correlate with fecundity. They concluded that P. nigrispinus should be reared on a mixed diet of T. molitor and M. domestica. Evans et al. (1999) and Michaud and Jyoti (2008) highlighted the benefits that feeding generalist predators a mixed diet (of arthropod prey) could have on reproduction. Zanuncio et al. (2000) determined that the combination of plant material (Eucalyptus spp. seedlings) and factitious prey (T. molitor pupae) improved the quality of nymphs and adults of a predaceous pentatomid, Brontocoris tabidus (Signoret). Apparently, plant-feeding provided essential nutrients (and water) that increased the longevity and reproductive output of B. tabidus adults. Uddin et al. (2005) discovered that chrysopids (i.e., lacewings) could be reared during the larval stages on prepupae of the alfalfa leafcutting bee (Megachile rotundata (F.), Megachilidae), a novel factitious prey. Survival rate from the egg to adult stage was 90% for Chrysoperla carnea (Stephens). Older larvae were reared individually to prevent cannibalism. Sex ratio of reared adults was 52% females for C. carnea larvae when reared on bee prepupae. Larvae of another chrysopid, Dichochrysa prasina (Burmeister), experienced high survival rates and shortened development times when fed E. kuehniella eggs (Pappas et al. 2007). Less favorable factitious prey for this species included larval stages of the stored product beetles, T. molitor and Tribolium confusum Duval. In summary, in comparison to natural prey, lepidopteran eggs (E. kuehniella, S. cerealella), decapsulated brine shrimp cysts, yellow mealworm pupae, house fly larvae, and Megachile bee prepupae generally had positive effects on development time or survival rate of predators. Fecundity (or fertility) was unaffected or even increased in most cases, with the exception of one study (Hamasaki and Matsui 2006).
123
E. W. Riddick
Body size actually increased for a few predators fed factitious prey (Zanuncio et al. 2001; Specty et al. 2003). These studies suggest that factitious prey, particularly the egg stage of several lepidopteran species, can be used for rearing predators in lieu of natural prey. Production of factitious prey should be more cost-effective than maintaining natural prey for representative species.
Artificial diets The next level of progression in cost-effective rearing of predators may involve the utilization of an artificial diet that obviates the use of prey. There are three classifications of artificial diets, based on the degree that the constituents are clearly defined. These include holidic diets, in which all constituents are known in chemical (i.e., molecular) structure, meridic diets, in which most of the constituents are known chemically, and oligidic diets, in which few of the constituents are known chemically (Dougherty 1959). However, the distinction between these three classifications has not always been clear. Another classification system has separated artificial diets based on whether they contained insect components (i.e., tissues, hemolymph, cells, protein, amino acids, etc.) or not (Grenier and De Clercq 2003). Artificial diets containing insect components are useful when predators require certain growth factors, feeding stimulants and other chemical cues that are typically found in arthropod prey (De Clercq 2004). Benefits and limitations of artificial diets containing insect components Artificial diets containing insect components were evaluated for Dastarcus helophoroides (Fairmaire), which is a colydiid beetle that attacks wood-boring insects, including cerambycid beetles and xylocopid bees (Ogura et al. 1999). Rearing newly-hatched larvae on diets composed of silkworm pupapowderTM (Maruqu Corp., Japan), dry yeasts, yeast extract, sucrose, peptone, squid liver oil, preservatives and distilled water, resulted in very low adult emergence rates (less than 10%). However, if larvae were fed with paralyzed cerambycid larvae until achieving a body length of approximately 8 mm, then reared on an artificial diet, adult emergence rates
Rearing predators
were much improved (greater than 50%). When D. helophoroides larvae were reared in groups (on shared prey) cannibalism was infrequent (Ogura et al. 1999). Although this colydiid could not be reared solely on the artificial diet, the strategy of providing natural prey during the critical period of development and artificial diet thereafter resulted in reasonable rearing success. Orius insidiosus (Say) can be reared on an artificial diet devoid of insect components, but oviposition rate and egg production of reared females have been poor (Ferkovich and Shapiro 2004a). In attempts to improve nutritional quality, this artificial diet (based on soy protein acid hydrolysate and chicken egg yolk) was supplemented with cells from an embryonic cell line, IPLB-PiE, of the Indian meal moth (Plodia interpunctella (Hu¨bner), Pyralidae). Results indicated that supplementation using this cell line led to increased egg production. Also, oviposition rate increased as concentration of cells added to the diet increased from 0.25 to 0.75 ml of PiE cells ml-1 of artificial diet. A follow-up investigation compared the effects of prey-derived and non-insect derived supplements, added to an artificial diet, on egg production and oviposition rate of O. insidiosus (Ferkovich and Shapiro 2004b). The artificial diet was also based on soy protein acid hydrolysate and chicken egg yolk. This study revealed that proteins derived from P. interpunctella eggs rather than from vertebrates (bovine serum albumin, chicken liver, beef liver, chicken egg albumin) provided superior nutritional value for O. insidiosus egg production and oviposition. The concentration of P. interpunctella egg proteins necessary for satisfactory oviposition rates of O. insidiosus was 80-fold less than the concentration of vertebrate-derived proteins needed for the same purpose. Ferkovich and Shapiro (2005) fractionated E. kuehniella eggs in an attempt to identify the most active fraction via feeding bioassays. Results indicated that O. insidiosus egg production increased only when a fraction with a pH of 5 was included. This result points to the presence of a specific nutritional factor in some lepidopteran eggs that enhances fecundity of predators. Ferkovich and Lynn (2005) supplemented an artificial diet, based on soy protein acid hydrolysate and chicken egg yolk, with cells from an embryonic cell line Ek-x4V, from E. kuehniella eggs. This procedure enhanced the
329
oviposition rate of O. insidiosus when compared against the rate achieved for adults fed the control (unmodified artificial diet). Unfortunately, oviposition was significantly reduced in females fed the supplemented artificial diet rather than E. kuehniella eggs. Similarly, O. insidiosus oviposition was enhanced when artificial diet (in 25 and 50 ll hemispherical capsules or domes) was supplemented with protein from E. kuehniella eggs in comparison to unmodified artificial diet (Ferkovich et al. 2007). Nevertheless, oviposition rate was greatest and mortality was least when females were fed whole E. kuehniella eggs. Lee and Lee (2004) reared Orius strigicollis (Poppius) on an artificial diet based on powdered Chinese oak silkworm (Antheraea pernyi (Gue´rinMe´neville), Saturniidae) pupae, beef liver, beef powder, and chicken egg yolk. When fed this diet, nymphal development time and survival rate were 14 days and 68.5%, respectively. Total fecundity averaged 82.5 eggs during an oviposition period of 18 days. Female longevity was 26.5 days. Unfortunately, no comparisons were made between individuals fed artificial diet versus a control, such as natural (live) prey. Lee and Lee (2005) reported that Chrysopa pallens (Rambur) larvae were reared on an artificial diet containing insect components (powdered A. pernyi pupae), beef liver, beef powder, and chicken egg yolk. C. pallens larvae required 27 days to complete development and mortality was 11%. No controls were mentioned in this study so comparisons as to the effectiveness of the larval diet cannot be made. Note that C. pallens adults were fed one of two artificial diets. One diet was based on powdered A. pernyi pupae, chicken egg yolk, and infant formula. The other diet contained no insect components, chicken egg yolk, infant formula (i.e., baby food), beef liver, and beef powder. Total fecundity, over the entire oviposition period, did not differ between females fed one or the other diet. Female longevity was unaffected by diet, whereas, males lived longer when fed the diet containing beef and no insect components (Lee and Lee 2005). Apparently, the incorporation of insect components into an artificial diet has some benefit to predators but development and reproduction might be reduced when compared with predators fed factitious or natural prey. Perhaps feeding predators with
123
330
reduced quantities of prey during critical periods of development, and artificial diet containing insect components at other times, might serve as a costeffective technique. Benefits and limitations of artificial diets devoid of insect components The most cost-effective means of rearing predators most likely involves the creation of artificial diets that eliminate the need to use any insect components; research leading in this direction is ongoing (Singh 1982; Thompson 1999; Thompson and Hagen 1999). Recent attempts at rearing predators with artificial diets devoid of insect components are chronicled in the following paragraphs. Using a deletion and addition approach, Arijs and De Clercq (2001b) found that egg yolk and beef liver were important components, whereas ground beef, ascorbic acid and sucrose were minor components in an artificial diet that supported the development of an anthocorid, O. laevigatus. Excessive amounts of any additive in the diet caused the production of undersized adults. Zaki and Gesraha (2001) tried to use an artificial diet based on a green algae, Chlorella vulgaris Beij, for larvae of the lacewing, C. carnea. Unfortunately, C. carnea larvae were not able to complete development when fed a water-based extract of the green algae. With the addition of other nutrients (molasses, dried yeast, yeast hydrolysate, and vitamin complex) to the algae extract development proceeded to the adult stage. The reproductive capacity and the longevity of females fed as larvae on this algae plus nutrient mix were similar to that of cohorts reared on aphids, Aphis gossypii Glover, Aphididae. Ulhaq et al. (2006) made comparisons between a standard diet (based on yeast extract, sugar, honey and casein) and three experimental diets containing hen’s egg yolk, milk and honey (diet A), hen’s egg white, milk, and honey (diet B), and hen’s egg yolk plus white, milk, and honey (diet C) on C. carnea oviposition and longevity. Lacewings oviposited significantly more eggs when fed diet A (containing the egg yolk) than diet B or diet C, but not the standard diet. Compared to those on diet B, females lived longer when fed diet A, but not the standard or diet C. The authors recommended the use of an egg yolk-based diet for mass production of C. carnea.
123
E. W. Riddick
In an attempt to compare the benefits of artificial diets based on vertebrate protein components to control diets (factitious or natural prey) on life parameters of predatory beetles, bugs, and lacewings, exemplary studies in the more recent literature, from 1998–2007, were reviewed. Table 1 outlines these studies by predator species, artificial diet (animal protein base components), results/outcome, and reference. The predatory beetles were represented by a carabid (Calosoma sycophanta (L.)), a clerid (Thanasimus dubius (F.)), a histerid (Carcinops pumilio (Erichson)), and a coccinellid (H. axyridis). The predatory bugs were represented by an anthocorid (O. laevigatus), lygaeid (Geocoris punctipes (Say)), mirids (Dicyphus tamaninii Wagner, Hyaliodes vitripennis (Say), Macrolophus caliginosus Wagner), and pentatomids (Perillus bioculatus (F.), Picromerus bidens (L.), P. maculiventris, P. nigrispinus). The lacewings were represented by one chrysopid species, Chrysoperla rufilabris Burmeister. Weseloh (1998) demonstrated that development time and survival of C. sycophanta larvae reared on an artificial diet were similar to that of cohorts reared on natural prey, gypsy moth (Lymantria dispar (L.), Lymantriidae) pupae. Unfortunately, diet-reared adults were smaller than adults reared on natural prey (Table 1). Reeve et al. (2003) showed that an artificial diet was beneficial to the survival and longevity of T. dubius. The composition of this diet closely resembled the chemical composition of the natural prey, the engraver beetle (Ips grandicollis (Eichhoff), Scolytidae). In addition, no difference was found between the ability of diet-reared and wild individuals to accept natural or factitious prey after larvae were reared on the artificial diet for five generations in the laboratory. This suggests that the artificial diet has potential for incorporation into a system for rearing T. dubius. The results of rearing C. pumilio, a histerid beetle that attacks dipteran larvae, such as the house fly, M. domestica, on artificial diet were not encouraging (Achiano and Giliomee 2006). Development time was prolonged, larval body weight was reduced, mortality rate was higher, and oviposition rate was lower for adults reared on artificial diet rather than natural prey. Dong et al. (2001) tested artificial diets versus factitious prey, Angoumois grain moth (S. cerealella) eggs, for the multicolored Asian lady beetle (H. axyridis). Survival rate (to the adult stage) of individuals reared
Rearing predators
331
Table 1 Exemplary studies that compared the influence of consuming artificial diets versus factitious or natural prey on life parameters of predatory beetles, true bugs, and a lacewing Predator
Artificial diet—animal protein base
Results/Outcome
Reference
Calosoma sycophanta larvae (Carabidae)
Beef liver, chicken meat
Development time (H), survival (H), size (;)
Weseloh (1998)
Survival (H), longevity (H), predation (H)
Reeve et al. (2003)
Thanasimus dubius larvae (Cleridae) Veal, veal gravy, chicken egg, potted meat, infant formula, casein hydrolysate—in ParafilmÒ capsules Carcinops pumilio larvae, adults (Histeridae)
PRO-PLEXTM protein additive Development time (:), size (;), oviposition (;)
Achiano and Giliomee (2006)
Harmonia axyridis larvae, adults (Coccinellidae)
Chicken egg yolk, chicken liver, casein hydrolysate
Development time (:), survival (H), size (;), oviposition (;)
Dong et al. (2001)
H. axyridis larvae, adults
Chicken whole egg, chicken liver, casein hydrolysate
Development time (:), survival (H), oviposition (;)
Dong et al. (2001)
Orius laevigatus nymphs, adults (Anthocoridae)
Beef liver, ground beef—in ParafilmÒ packets
Development time (:), survival (;), size (H), oviposition (H)
Arijs and De Clercq (2004)
Geocoris punctipes adults (Lygaeidae)
Beef liver, ground beef—in ParafilmÒ
Size (;), predation (H)
Cohen (2000)
Dicyphus tamaninii nymphs, adults (Miridae)
Beef liver, fatty ground beef, Development time (:), survival Iriarte and Castan˜e´ (2001) hen’s egg yolk—in ParafilmÒ (H) by 4th–5th generation, size (;), oviposition (H) Beef liver, fatty ground beef, Predation (H) Castan˜e´ et al. (2002) hen’s egg yolk—in ParafilmÒ
D. tamaninii nymphs, adults D. tamaninii nymphs, adults
Beef liver, fatty ground beef, hen’s egg yolk, casein— Reformulated diet
Development time (:), survival (:), size (H), oviposition (H)
Zapata et al. (2005)
Hyaliodes vitripennis nymphs, adults Pork liver, whey powder—in (Miridae) ParafilmÒ
Survival (:), longevity (:), oviposition (:)
Firlej et al. (2006)
H. vitripennis nymphs, adults
Beef liver, ground beef, whole hen’s egg—in ParafilmÒ
Survival (:), longevity (:)
Firlej et al. (2006)
Macrolophus caliginosus nymphs, adults (Miridae)
Beef liver, fatty ground beef, hen’s egg yolk, casein—in ParafilmÒ Hen’s egg yolk—in ParafilmÒ domes
Development time (:), survival (;), size (;), predation (H)
Castan˜e´ and Zapata (2005)
Development time (:), survival (H), size (;), oviposition (;), oogenesis (;)
Vandekerkhove et al. (2006)
M. caliginosus nymphs, adults
Perillus bioculatus adults (Pentatomidae)
Pork liver, fatty ground beef— Oogenesis (;) in ParafilmÒ domes
Adams (2000a)
P. bioculatus adults P. bioculatus nymphs, adults
Pork liver—in ParafilmÒ domes Oviposition (;), longevity (H) Beef, whole hen’s egg—in Development time (:), survival Mylar-ParafilmÒ (;), total oviposition (;), longevity (;)
Adams (2000b) Coudron and Kim (2004)
P. bioculatus nymphs, adults
Chicken liver, tuna fish—in ParafilmÒ capsules
Development time (:), survival (;), oviposition (;)
Rojas et al. (2000)
Picromerus bidens nymphs, adults (Pentatomidae)
Beef liver, fatty ground beef, Development time (:), survival hen’s egg yolk—in ParafilmÒ (;), size (;)
Mahdian et al. (2006)
Podisus maculiventris nymphs, adults (Pentatomidae)
Beef liver, fatty ground beef, Development time (:), survival hen’s egg yolk—in ParafilmÒ (H), size (;), oviposition (;), longevity (H)
Mahdian et al. (2006)
P. maculiventris adults
Size (;), predation (H) Beef liver, fatty ground beef, hen’s egg yolk—in ParafilmÒ
Chocorosqui and De Clercq (1999)
123
332
E. W. Riddick
Table 1 continued Predator
Artificial diet—animal protein base
Results/Outcome
Reference
P. maculiventris nymphs, adults
Beef liver, whole hen’s egg—in Mylar-ParafilmÒ
Development time (:), size (;), oviposition (;)
Wittmeyer and Coudron (2001)
P. maculiventris nymphs, adults
Beef liver, whole hen’s egg—in Mylar-ParafilmÒ
Body size (;), oviposition (;), Wittmeyer et al. (2001) oogenesis (;), vitellogenesis (;)
P. maculiventris nymphs, adults
Beef liver, whole hen’s egg—in Mylar-ParafilmÒ
Development time (:), size (;), survival (H), oviposition (;)
Coudron et al. (2002)
Podisus nigrispinus nymphs, adults (Pentatomidae)
Beef liver, ground beef
Development time (:), size (;), ovarian weight (;)
Lemos et al. (2003)
P. nigrispinus adults
Beef liver, ground beef
Ovarian development (;), oogenesis (;)
Lemos et al. (2005)
Chrysoperla rufilabris larvae (Chrysopidae)
Beef liver, fatty ground beef, whole hen’s eggs—in ParafilmÒ
Development time (:), survival (H), size (:), predation (H)
Cohen and Smith (1998)
Symbols indicate decrease (;), increase (:), or no significant effect (H) on a given life parameter, in comparison to a control, for designated predator
on the artificial diets was the only parameter that was similar to that of cohorts reared on S. cerealella eggs (Table 1). To summarize the effects of artificial diets on life parameters of predatory beetles (presented in Table 1), the animal protein base components were variable from one species to the next. Chicken products were a component in the artificial diet fed to C. sycophanta, T. dubius and H. axyridis. None of the artificial diets (in Table 1) could maintain oviposition rates comparable to those of cohorts fed factitious or natural (control) prey. Nevertheless, the artificial diet that consisted of multiple sources of vertebrate protein (veal, hen’s egg, potted meat, infant formula, casein) was shown to be most promising for rearing of the clerid, T. dubius (Reeve et al. 2003). Potential benefits of artificial diets on life parameters of several predatory bugs were assessed and outlined in Table 1. The effect of rearing an anthocorid bug, O. laevigatus, on artificial diets versus factitious prey (E. kuehniella eggs) was assessed by Arijs and De Clercq (2004). Adult body size (weight) and oviposition rate were similar amongst females fed all treatment foods. Predation potential of the bigeyed bug, G. punctipes, was compared between domesticated (i.e., laboratory-reared on an artificial diet for 60 continuous generations) versus F1 progeny of feral (wild) females (Cohen 2000). The artificial diet was enclosed within stretched Parafilm feeding
123
units (Cohen 1985), perhaps to reduce rate of desiccation as well as spoilage of diet. Cohen (1985) suggests that the Parafilm may have the added benefit of providing a barrier against microbial attack. The Parafilm coating may provide a firm surface that facilitates the penetration and stabilization of the piercing-sucking mouthparts of predatory bugs (Cohen 1990; De Clercq et al. 1998). Progeny of wild females were fed tobacco budworm (Heliothis virescens (F.), Noctuidae) eggs and heat-killed beet armyworm (Spodoptera exigua Hu¨bner, Noctuidae) larvae in the laboratory. In experiments, females in both treatments were provided with H. virescens larvae or aphids (A. pisum) as prey. Although domesticated females were smaller than wild females, consumption rates were approximately the same between the two treatment groups, regardless of the prey species (Cohen 2000). Demonstrating that a predator (or parasitoid) has the capacity to capture, kill, and consume live (target) prey, despite continuous culturing on an artificial diet, may be one of the most relevant measures of predator quality (Grenier and De Clercq 2003). Iriarte and Castan˜e´ (2001), Castan˜e´ et al. (2002), and Zapata et al. (2005) conducted diet-related research on a mirid, D. tamaninii, which is a zoophytophagous predator found in the Mediterranean area. It has been considered as an effective natural enemy of some whiteflies and thrips. Iriarte and Castan˜e´ (2001) demonstrated that D. tamaninii
Rearing predators
was amenable to rearing, during nymphal and adult stages, on an artificial diet devoid of plant material. Despite an initial reduction of survival of individuals in the first generation, an incremental increase in survival occurred with succeeding generations reared on the artificial diet. Castan˜e´ et al. (2002) proved that D. tamaninii cohorts on a meat diet (see Table 1) were just as effective as cohorts reared on E. kuehniella eggs at killing two important prey, the greenhouse whitefly (Trialeurodes vaporariorum (Westwood), Aleyrodidae) and the cotton aphid (A. gossypii). In an attempt to increase the suitability of a meat-based artificial diet for rearing D. tamaninii, Zapata et al. (2005) conducted a biochemical analysis of the carcass of diet-reared adults. Nutritional deficiencies in the original diet formulation were detected via comparison of the total, free amino acid and lipid profiles of meat-reared vs. controlreared females. Control females were reared on factitious prey (E. kuehniella eggs) and had access to a tobacco plant. To ameliorate the nutritional deficiencies, new sources of protein (aspartate, casein) and fatty acids (soybean oil) were added to the original diet, and more water was added to lower the concentration of all components and improve diet acceptability. This reformulated artificial diet was more beneficial to predators as evidenced by an increase in nymphal body size (i.e., fresh weight) and survival rates. Also, adults fed the reformulated diet had hind tibia of similar lengths as cohorts reared on Ephestia eggs. Oviposition rate was similar between all food treatments. Promising effects of artificial diets on another mirid, H. vitripennis, was witnessed by Firlej et al. (2006). H. vitripennis is an indigenous generalist predator that attacks a range of arthropod pests, including mites, in apple orchards in North America. Predator longevity and survival rate were improved when H. vitripennis 5th instar nymphs and adults were reared on two meat-based diets (originally designed for a coccinellid, C. maculata, and a chrysopid, C. rufilabris) rather than natural prey, Tetranychus urticae Koch (spider mites). In fact, adults reared on the coccinellid diet had greater fecundity (oviposition rate) than those reared on the chrysopid diet or on natural prey, T. urticae. The addition of a possible phagostimulant, b-sistosterol, to the coccinellid diet led to a decrease in nymphal mortality and a slight increase in weight gain in
333
comparison to cohorts reared on the coccinellid diet alone. Firlej et al. (2006) suggest that further diet development is needed to increase egg hatch and fecundity of females that had been reared on either one of the meat diets from the 1st nymphal instar. Castan˜e´ and Zapata (2005) assessed the advantages, if any, of a meat-based artificial diet on life parameters of a mirid, M. caliginosus. Unfortunately, insects reared on the meat diet were smaller in hind tibia length and body weight and required more time to complete development than counterparts reared on Ephestia eggs on tobacco leaves (Castan˜e´ and Zapata 2005). Despite the shortcomings, M. caliginosus adults of the 7th generation, on the artificial diet, were as adept at killing the greenhouse whitefly (T. vaporariorum), the sweet potato whitefly (Bemisia tabaci (Gennadius)), and the two-spotted spider mite (T. urticae), as adults reared on E. kuehniella eggs. Similarly, Vandekerkhove et al. (2006) confirmed that Ephestia eggs, rather than an artificial diet based on hen’s egg yolk, provided adequate nutrition for development and reproduction of M. caliginosus. Development of the ovaries was influenced by diet; females fed Ephestia eggs had more developing eggs (oocytes) in their ovaries than females fed artificial diet. Callebaut et al. (2004) also indicated that Ephestia eggs were more suitable than artificial diets for M. caliginosus reproduction via an examination of egg load. Egg load correlated significantly with oviposition rate in this mirid. The search for suitable artificial diets for predatory pentatomids (asopine stink bugs) has been ongoing. The potential benefits of artificial diets on the life history of the two-spotted stink bug, P. bioculatus, were explored by Adams (2000a, b), Rojas et al. (2000), and Coudron and Kim (2004). Adams (2000a) found that females fed artificial diet rather than a control diet of freeze-killed H. virescens larvae had fewer developing follicles. Interestingly, 10-dayold females that were fed the artificial diet contained chorionated (mature) follicles in just 40% of their ovarioles, whereas 9-day-old females fed the control diet contained chorionated follicles in 100% of their ovarioles. Adams (2000b) indicated that an average of 42 and 138 eggs were oviposited by mated females fed the artificial diet and frozen H. virescens larvae, respectively. Apparently, the artificial diets did not provide an adequate supply of nutrients essential for egg development in P. bioculatus.
123
334
In another study on P. bioculatus, two meridic diets were formulated to resemble the nutritional composition of eggs of the Colorado potato beetle, L. decemlineata, a major prey of this predator (Rojas et al. 2000). The first diet (diet 1) was simplified by the substitution of chemically defined components to produce the second diet (diet 2). In comparison to a control of Leptinotarsa decemlineata (Say) (Chrysomelidae) eggs, both artificial diets were not satisfactory for timely development and survival of P. bioculatus immatures or oviposition and longevity of adults. After 11 generations, females fed diet 2 weighed more than cohorts fed the control. The observation that larger predators result after feeding on diet for many generations suggest that some adaptation has occurred such that predators readily consume and then metabolize sufficient quantities of the diet. Nevertheless, the artificial diet was inferior to natural prey in terms of nutritional quality. Although Coudron and Kim (2004) were able to culture P. bioculatus on an artificial diet based on animal protein and undisclosed plant protein for 11 generations, this diet was substandard to natural prey (cabbage looper, Trichoplusia ni (Hu¨bner) larvae, Noctuidae). A cost analysis suggested that the expense associated with rearing P. bioculatus on artificial diet or natural prey was about the same. In comparison to natural and factitious prey, an artificial diet was deemed inferior for culturing another pentatomid, P. bidens (Mahdian et al. 2006). For example, survival was best when nymphs were fed E. kuehniella eggs rather than artificial diet. Female body size (weight) was greatest when lepidopteran larvae (such as the cotton leaf worm, Spodoptera littoralis (Boisduval) (Pyralidae), and the greater wax moth, G. mellonella, were used as prey rather than the artificial diet. Total fecundity (or oviposition) of P. bidens was greatest on S. littoralis larvae than on G. mellonella; P. bidens did not produce eggs when fed the meat-based artificial diet. Mahdian et al. (2006) also indicated that the spined soldier bug, P. maculiventris, benefited little when reared on the same artificial diet tested on P. bidens. Although nymphal survival and longevity were acceptable, female body weight and oviposition rate were hindered when using the artificial diet rather than live prey, such as S. littoralis or G. mellonella larvae. Chocorosqui and De Clercq (1999) reared P. maculiventris on an artificial diet, enclosed in
123
E. W. Riddick
stretched ParafilmÒ to resemble the shape of a larva, for three consecutive generations. Despite the smaller size of nymphs and adults reared on artificial diet rather than factitious prey (G. mellonella larvae), predation rate was not affected. Diet-reared predators killed as many or slightly more beet armyworm (S. exigua) larvae than cohorts on factitious prey. Wittmeyer and Coudron (2001) tested the usefulness and cost-effectiveness of an artificial diet enclosed in a Mylar-Parafilm dome on life parameters of P. maculiventris. This diet was inferior to using coddled (heat-killed) cabbage looper (T. ni) larvae. The actual cost required to double the size of the P. maculiventris population, in culture, was two times greater when predators were fed solely artificial diet, rather than T. ni larvae, during predator nymphal and adult stages. Feeding T. ni larvae to adults and artificial diet to nymphs tended to improve oviposition, reproductive rate and intrinsic rate of increase, but not enough to offset the loss in egg production. In a companion study, Wittmeyer et al. (2001) provided further evidence that an artificial diet, enclosed in a Mylar-Parafilm dome, was ineffective, in comparison to T. ni larvae, as a sole food source for maximizing egg production in P. maculiventris females. They highlighted the impact that nymphal and adult food sources can have on oogenesis (egg maturation) and vitellogenesis (yolk deposition) in this predator. In a follow-up study, Coudron et al. (2002) evaluated the effect of a blended, buffered mixture of a meat and plant-based diet, enclosed in a MylarParafilm dome, on P. maculiventris. Although nymphal survival was suitable, other parameters (see Table 1) were negatively impacted when predators were fed the zoophytogenous artificial diet for 1 or 11 generations compared to cohorts fed natural prey, T. ni larvae, for 1 generation. Nevertheless, a somewhat gradual improvement in these parameters occurred from the 1st to the 11th generation on the artificial diet, possibly as a consequence of adaptation. The authors stated that after 11 generations the cost of rearing P. maculiventris on the artificial diet was 1.2 times more expensive than rearing conspecifics on natural prey. Podisus nigrispinus, the final pentatomid listed in Table 1, was found to have benefited least when fed an artificial diet rather than natural or factitious prey (Lemos et al. 2003). For example, nymphs reared on this artificial diet weighed significantly less than
Rearing predators
cohorts fed cotton leafworm (Alabama argillacea Hu¨bner, Noctuidae) larvae. Also, fresh weight of ovaries of newly-emerged P. nigrispinus females was least for individuals reared on artificial diet than on yellow mealworm (T. molitor), house fly (M. domestica), or cotton leafworm larvae. In a subsequent study, Lemos et al. (2005) discovered that food source can have a profound impact on ovarian development. Newly-emerged P. nigrispinus females had ovaries containing oocytes in an advanced, intermediate, or early stage of development when fed A. argillacea larvae, T. molitor or M. domestica larvae, or an artificial diet, respectively. In summary, artificial diets tested for culturing predatory bugs (given in Table 1) were variable in composition, but usually consisted of vertebrate protein from cattle and chicken and, infrequently, from pig. One study tested a novel combination of chicken liver and tuna fish base components (Rojas et al. 2000). However, beef liver was a component in the artificial diet of 8 of 9 species, and hen’s egg (whole or yolk only) was a component in the diet of 6 out of 9 species. In most cases, artificial diets were not suitable as a stand-alone food source of comparable effectiveness as factitious or natural prey for predatory bugs. In several cases, however, artificial diets have proven to be nearly as suitable (Zapata et al. 2005) or perhaps even more suitable (Firlej et al. 2006) than factitious or natural prey. Potential benefits of artificial diets on life parameters of a lacewing species were assessed and indicated in Table 1. Cohen and Smith (1998) studied the impact of an artificial diet on life parameters of the green lacewing, C. rufilabris. Note that the artificial diet was cooked to a semisolid, paste-like consistency, which gave it a texture and composition similar to that of the insides of insect prey (eggs and larvae of H. virescens). The diet was then encased inside stretched Parafilm membranes and presented to C. rufilabris larvae. Larvae were reared on this diet and adults were fed a yeast, sucrose and water mixture, for 15 consecutive generations. Effects of the artificial diet on biological parameters of C. rufilabris were determined from the 6th through 10th generations and compared to cohorts reared on a control (E. kuehniella eggs). As stated previously for rearing of predatory bugs, a gradual improvement in certain life parameters, such as survival and body size, could arise from adaptation to an artificial diet.
335
Although C. rufilabris larvae took slightly longer to complete development when reared on the artificial diet than on E. kuehniella eggs, survival rate was 87 and 89% for insects developing on artificial diet and factitious prey, respectively, and fresh weight was greater for pupae reared on artificial diet rather than the control. Development of larvae on artificial diet did not significantly affect reproduction of adults. Daily fecundity per female, over a 5-day time period, averaged 21.5 and 19 eggs for those reared on artificial diet and control food, respectively, during the larval stage. Rearing of C. rufilabris on artificial diet for consecutive generations did not reduce the predation capacity of larvae. For instance, larvae readily attacked and consumed cotton aphids, A. gossypii Glover, in the laboratory. The authors indicated that the artificial diet was much less expensive. The costs associated with producing the artificial diet and E. kuehniella eggs were approximately $6 and $500 (USD) per kilogram, respectively. This study demonstrates the potential of a cost-effective artificial diet for rearing lacewing larvae for consecutive generations.
Concluding remarks Advancements in rearing of predators might entail one or more of the following: (1)
(2)
A rigorous experimental approach in the evaluation of factitious prey and artificial diets is needed. To date, many studies are difficult to compare because of the lack of controls, differences in prey condition (well-fed, starved, freshly-killed, frozen, irradiated, etc.), and the use/disuse of certain antimicrobials in diets. Eggs of the Angoumois grain moth and Mediterranean flour moth support the development and reproduction of many species in lieu of natural prey. Vertebrate protein-based diets appear inadequate as a stand-alone food source for continuous production of most predatory insects of the highest quality. However, a few exceptional diets can support the continuous rearing of true bugs and lacewings. The ability of generalist predators to undergo adaptation to specific prey after several generations of exposure has been documented (Rana et al. 2002).
123
336
(3)
(4)
(5)
(6)
E. W. Riddick
More research is needed to determine which generalist predators have the plasticity to develop a preference for a given artificial diet rather than factitious or live prey after several generations of exposure. Incorporating feeding stimulants into artificial diets could increase the pace of adaptation. More of a concerted effort is needed to identify novel sources of animal protein as constituents in insect-free artificial diets. Vertebrate protein from beef or chicken appears to be the mainstay in most diets. The large-scale utilization of invertebrate protein from crustaceans as artificial diets for predatory insects should be explored. Further explore the value of plant products as constituents in artificial diets—even for species that are decidedly carnivorous. Various plant products (pollen, nectar) could enhance the nutrition of predators that are subjected to feeding on suboptimal artificial diets (Gillespie and Mc Gregor 2000; Patt et al. 2003). Some generalist predators are capable of regulating their intake of protein and lipids to compensate for nutritional imbalances, after feeding on prey deficient in these molecules (Mayntz et al. 2005). Develop some consensus of what methods or techniques best measure ‘‘quality’’. At present, several measures such as predator size, weight, fecundity, fertility, and progeny sex ratio are often used. An assessment of the development of the ovaries of adults reared on experimental diets is probably one of most useful measures. Predation capacity is also very useful. Predation potential of predators, after rearing on an artificial diet for multiple generations, is probably one of the most important life parameters for evaluating artificial diet success (Grenier and De Clercq 2003). There is a widely held belief that predators loose their ability to capture and kill live prey after many generations on an artificial diet. On the contrary, little if any published research has shown that diet-reared predators loose this capacity. The influence of symbionts on predator performance on artificial diets is not well understood. Bacterial, fungal, or protozoan symbionts may alter the consumption rate of some predators
123
(7)
(8)
and may affect their ability to extract specific molecules from the diet. The indiscriminate use of antibiotics in artificial diets could have beneficial, neutral, or detrimental effects on symbionts and their hosts. Further research on the presentation or compartmentalization of artificial diets in a form that is acceptable to the predator is necessary. Gains have been made in this area. However, the effect of membrane (e.g., Parafilm) chemicals on predator development is not well understood. Encasement may reduce desiccation and retard spoilage of the diet. Parafilm membranes around artificial diets might serve as a barrier against microbial attack (Cohen 1985). Potential of using other forms of encapsulation (e.g., hydrocapsulesÒ, ARS, Inc., Gainesville, FL, USA) should be explored. More effort in facilitating the transfer of dietrelated technology to the commercial industry is necessary. Several diets are currently patented (e.g., Greany and Carpenter 1998; Cohen 1999, 2003; White et al. 2001) but others, and more effective ones, are needed to meet the demands of the burgeoning biological control industry.
The chances of developing an effective artificial diet and automated system for mass rearing are probably much greater for a generalist than a specialist predator (Cohen et al. 1999). Unfortunately, generalist (polyphagous) predators have come under tremendous scrutiny because of concerns of the potential adverse effects they might pose to the environment (Strong and Pemberton 2001; van Lenteren et al. 2003b; Stiling 2004; Snyder and Evans 2006). Accumulating evidence suggests that certain generalist, exotic species have the potential to out-compete native species, leading to localized extirpation of some populations (De Clercq 2002). This concern should not diminish the commercial production and use of generalist predators in augmentation biological control. Continuing to focus on using generalists in managing pests on greenhousegrown crops rather than on crops in open-field situations should alleviate some of these concerns. Presumably, safeguards will be in place to limit the escape of generalist predators from greenhouses. Also, expansion of the market for growing ornamentals in enclosed spaces (interiorscapes) could provide
Rearing predators
increased opportunities for commercial-scale rearing and application of generalist predators (Smith and Krischik 2000). Acknowledgments J. P. Shapiro and C. S. Glenister reviewed and commented on an earlier version of this manuscript. P. De Clercq and T. Coudron shared reprints of their work on predatory stink bugs. P. De Clercq and two anonymous reviewers provided useful comments that improved the text. The United States Government has the right to retain a non-exclusive, royalty-free license in and to any copyright of this article. This article reports the results of research only. Mention of a commercial or proprietary product does not constitute an endorsement of the product by the United States Department of Agriculture.
References Abdel-Salam AH, Abdel-Baky NF (2001) Life table and biological studies of Harmonia axyridis Pallas (Col.: Coccinellidae) reared on the grain moth eggs of Sitotroga cerealella Olivier (Lep.: Gelechiidae). J Appl Entomol 125:455–462 Achiano KA, Giliomee JH (2006) Rearing the house fly predator Carcinops pumilio (Erichson) (Coleoptera: Histeridae) on an artificial diet. Afr J Biotechnol 5:1161–1166 Adams TS (2000a) Effect of diet and mating status on ovarian development in a predaceous stink bug Perillus bioculatus (Hemiptera: Pentatomidae). Ann Entomol Soc Am 93:529–535 Adams TS (2000b) Effect of diet and mating on oviposition in the twospotted stink bug Perillus bioculatus (F.) (Heteroptera: Pentatomidae). Ann Entomol Soc Am 93: 1288–1293 Arijs Y, De Clercq P (2001a) Rearing Orius laevigatus on cysts of the brine shrimp Artemia franciscana. Biol Control 21:79–83 Arijs Y, De Clercq P (2001b) Development of an oligidic diet for Orius laevigatus nymphs using a deletion-addition approach. Meded Fac Landbouwwet Univ Gent 66:315–320 Arijs Y, De Clercq P (2004) Liver-based artificial diets for the production of Orius laevigatus. BioControl 49:505–516 Berkvens N, Bonte J, Berkvens D, Deforce K, Tirry L, De Clercq P (2008) Pollen as an alternative food for Harmonia axyridis. BioControl 53:201–214 Callebaut B, Van Baal E, Vandekerkhove B, Bolckmans K, De Clercq P (2004) A fecundity test for assessing the quality of Macrolophus caliginosus reared on artificial diets. Parasitica 60:9–14 Castan˜e´ C, Zapata R (2005) Rearing the predatory bug Macrolophus caliginosus on a meat-based diet. Biol Control 34:66–72 Castan˜e´ C, Iriarte J, Lucas E (2002) Comparison of prey consumption by Dicyphus tamaninii reared conventionally, and on a meat-based diet. BioControl 47:657–666 Castan˜e´ C, Quero R, Riudavets J (2006) The brine shrimp Artemia sp. as alternative prey for rearing the predatory bug Macrolophus caliginosus. Biol Control 38:405–412
337 Chocorosqui VR, De Clercq P (1999) Developmental and predatory performance of Podisus maculiventris (Say) (Heteroptera: Pentatomidae) reared on a meat-based artificial diet. Meded Fac Landbouwwet Univ Gent 64: 229–234 Cohen AC (1985) Simple method for rearing the insect predator Geocoris punctipes on a meat diet. J Econ Entomol 78:1173–1175 Cohen AC (1990) Feeding adaptations of some predaceous Hemiptera. Ann Entomol Soc Am 83:1215–1223 Cohen AC (1999) Artificial media for rearing entomophages comprising sticky, cooked whole egg. US Patent 5945271 Cohen AC (2000) Feeding fitness and quality of domesticated and feral predators: effects of long-term rearing on artificial diet. Biol Control 17:50–54 Cohen AC (2003) Artificial diets for arthropods. US Patent 6506597 Cohen AC (2004) Insect diets: science and technology. CRC Press LLC, Boca Raton, FL Cohen AC, Smith LK (1998) A new concept in artificial diets for Chrysoperla rufilabris: the efficacy of solid diets. Biol Control 13:49–54 Cohen AC, Nordlund DA, Smith RA (1999) Mass rearing of entomophagous insects and predaceous mites: are the bottlenecks biological, engineering, economic, or cultural? Biocontrol News Info 20:85N–90N Coudron TA, Kim Y (2004) Life history and cost analysis for continuous rearing of Perillus bioculatus (Heteroptera: Pentatomidae) on a zoophytogenous artificial diet. J Econ Entomol 97:807–812 Coudron TA, Wittmeyer J, Kim Y (2002) Life history and cost analysis for continuous rearing of Podisus maculiventris (Say) (Heteroptera: Pentatomidae) on a zoophytophagous artificial diet. J Econ Entomol 95:1159–1168 Cranshaw W, Sclar DC, Cooper D (1996) A review of 1994 pricing and marketing by suppliers of organisms for biological control of arthropods in the United States. Biol Control 6:291–296 De Clercq P (2002) Dark clouds and their silver linings: exotic generalist predators in augmentative biological control. Neotrop Entomol 31:169–176 De Clercq P (2004) Culture of natural enemies on factitious foods and artificial diets. In: Capinera JL (ed) Encyclopedia of entomology, vol 1. Kluwer Acad Publ, Dordrecht, The Netherlands, pp 650–652 De Clercq P, Merlevede F, Tirry L (1998) Unnatural prey and artificial diets for rearing Podisus maculiventris (Heteroptera: Pentatomidae). Biol Control 12:137–142 De Clercq P, Bonte M, Van Speybroeck K, Bolckmans K (2005a) Development and reproduction of Adalia bipunctata (Coleoptera: Coccinellidae) on eggs of Ephestia kuehniella (Lepidoptera: Phycitidae) and pollen. Pest Manage Sci 61:1129–1132 De Clercq P, Arijs Y, Van Meir T, Van Stappen G, Sorgeloos P, Dewettinck K, Rey M, Grenier S, Febvay G (2005b) Nutritional value of brine shrimp cysts as a factitioud food for Orius laevigatus (Heteroptera: Anthocoridae). Biocontrol Sci Technol 15:467–479 Dong H, Ellington JJ, Remmenga MD (2001) An artificial diet for the lady beetle Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Southwest Entomol 26:205–213
123
338 Dougherty EC (1959) Introduction to axenic culture of invertebrate metazoan: a goal. Ann NY Acad Sci 77:27–54 Evans EW, Stevenson AT, Richards DR (1999) Essential versus alternative foods of insect predators: benefits of a mixed diet. Oecologia 121:107–112 Ferkovich SM, Lynn DE (2005) Enhanced egg laying in adult predators fed artificial diet supplemented with an embryonic cell line derived from eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Fla Entomol 88:329–331 Ferkovich SM, Shapiro JP (2004a) Increased egg-laying in Orius insidiosus (Hemiptera: Anthocoridae) fed artificial diet supplemented with an embryonic cell line. Biol Control 31:11–15 Ferkovich SM, Shapiro JP (2004b) Comparison of preyderived and non-insect supplements on egg-laying of Orius insidiosus maintained on artificial diet as adults. Biol Control 31:57–64 Ferkovich SM, Shapiro JP (2005) Enhanced oviposition in the insidious flower bug, Orius insidiosus (Hemiptera: Anthocoridae) with a partially purified nutritional factor from prey eggs. Fla Entomol 88:253–257 Ferkovich SM, Venkatesan T, Shapiro JP, Carpenter JE (2007) Presentation of artificial diet: effects of composition and size of prey and diet domes on egg production by Orius insidiosus (Heteroptera: Anthocoridae). Fla Entomol 90:502–508 Firlej A, Chouinard G, Coderre D (2006) A meridic diet for the rearing of Hyaliodes vitripennis (Hemiptera: Miridae), a predator of mites in apple orchards. Biocontrol Sci Technol 16:743–751 Gillespie DR, McGregor RR (2000) The functions of plant feeding in the omnivorous predator Dicyphus hesperus: water places limits on predation. Ecol Entomol 25: 380–386 Glenister CS, Hoffmann MP (1998) Mass-reared natural enemies: scientific, technological, and informational needs and considerations. In: Ridgway RL, Hoffmann MP, Inscoe MN, Glenister CS (eds) Mass-reared natural enemies: application, regulation, and needs. Entomological Society of America, Thomas Say Publ, Lanham, MD, pp 242–267 Goolsby JA, Rose M, Morrison RK, Woolley JB (2000) Augmentative biological control of longtailed mealybug by Chrysoperla rufilabris (Burmeister) in the interior plantscape. Southwest Entomol 25:15–19 Greany PD, Carpenter JE (1998) Culture medium for parasitic and predaceous insects. US Patent 5799607 Grenier S, De Clercq P (2003) Comparison of artificially vs. naturally reared natural enemies and their potential for use in biological control. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI Publ, Wallingford, UK, pp 115–131 Hamasaki K, Matsui M (2006) Development and reproduction of an aphidophagous coccinellid, Propylea japonica (Thunberg) (Coleoptera: Coccinellidae), reared on an alternative diet, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) eggs. Appl Entomol Zool 41:233–237 Iriarte J, Castan˜e´ C (2001) Artificial rearing of Dicyphus tamaninii (Heteroptera: Miridae) on a meat-based diet. Biol Control 22:98–102
123
E. W. Riddick Lee K-S, Lee J-H (2004) Rearing of Orius strigicollis (Heteroptera: Anthocoridae) on artificial diet. Entomol Res 34:299–303 Lee K-S, Lee J-H (2005) Rearing of Chrysopa pallens (Rambur) (Neuroptera: Chrysopidae) on artificial diet. Entomol Res 35:183–188 Lemos WP, Ramalho FS, Serra˜o JE, Zanuncio JC (2003) Effects of diet on development of Podisus nigrispinus (Dallas) (Het., Pentatomidae), a predator of the cotton leafworm. J Appl Entomol 127:389–395 Lemos WP, Ramalho FS, Serra˜o JE, Zanuncio JC (2005) Morphology of female reproductive tract of the predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) fed on different diets. Braz Arch Biol Technol 48: 129–138 Mahdian K, Kerckhove J, Tirry L, De Clercq P (2006) Effects of diet on development and reproduction of the predatory pentatomids Picromerus bidens and Podisus maculiventris. BioControl 51:725–739 Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113 Michaud JP, Jyoti JL (2008) Dietary complementation across life stages in the polyphagous lady beetle Coleomegilla maculata. Entomol Exp Appl 126:40–45 Michaud JP, Qureshi JA (2005) Induction of reproductive diapause in Hippodamia convergens (Coleoptera: Coccinellidae) hinges on prey quality and availability. Eur J Entomol 102:483–487 Nordlund DA (1998) Capacity and quality: keys to success in the mass rearing of biological control agents. Nat Enemies Ins 20:169–179 Ogura N, Tabata K, Wang W (1999) Rearing of the colydiid beetle predator, Dastarcus helophoroides, on artificial diet. BioControl 44:291–299 Pappas ML, Broufas GD, Koveos DS (2007) Effects of various prey species on development, survival and reproduction of the predatory lacewing Dichochrysa prasina (Neuroptera: Chrysopidae). Biol Control 43:163–170 Patt JM, Wainright SC, Hamilton GC, Whittinghill D, Bosley K, Dietrick J, Lashomb JH (2003) Assimilation of carbon and nitrogen from pollen and nectar by a predaceous larva and its effects on growth and development. Ecol Entomol 28:717–728 Penn SL, Ridgway RL, Scriven GT, Inscoe MN (1998) Quality assurance by the commercial producer of arthropod natural enemies. In: Ridgway RL, Hoffmann MP, Inscoe MN, Glenister CS (eds) Mass-reared natural enemies: application, regulation, and needs. Entomological Society of America, Thomas Say Publ, Lanham, MD, pp 202–230 Rana JS, Dixon AFG, Jarosˇ´ık V (2002) Costs and benefits of prey specialization in a generalist insect predator. J Anim Ecol 71:15–22 Reeve JD, Rojas MG, Morales-Ramos JA (2003) Artificial diet and rearing methods for Thanasimus dubius (Coleoptera: Cleridae), a predator of bark beetles (Coleoptera: Scolytidae). Biol Control 27:315–322 Rojas MG, Morales-Ramos JA, King EG (2000) Two meridic diets for Perillus bioculatus (Heteroptera: Pentatomidae), a predator of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Biol Control 17:92–99
Rearing predators Singh P (1982) The rearing of beneficial insects. N Z Entomol 7:304–310 Smith RA, Nordlund DA (1999) Automation of insect rearing – a key to the development of competitive augmentative biological control. Nat Enemies Ins 21:70–81 Smith RA, Nordlund DA (2000) Mass rearing technology for biological control agents of Lygus spp. Southwest Entomol (Suppl 23):121–127 Smith SF, Krischik VA (2000) Effects of biorational pesticides on four coccinellid species (Coleoptera: Coccinellidae) having potential as biological control agents in interiorscapes. J Econ Entomol 93:732–736 Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122 Specty O, Febvay G, Grenier S, Delobel B, Piotte C, Pageaux J-F, Ferran A, Guillaud J (2003) Nutritional plasticity of the predatory ladybeetle Harmonia axyridis (Coleoptera: Coccinellidae): comparison between natural and substitution prey. Arch Insect Biochem Physiol 52:81–91 Stiling P (2004) Biological control not on target. Biol Invas 6:151–159 Strong DR, Pemberton RW (2001) Food webs, risks of alien enemies and reform of biological control. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating Indirect Ecological Effects of Biological Control. CABI Publ, Oxon, UK, pp 57–79 Thompson SN (1999) Nutrition and culture of entomophagous insects. Annu Rev Entomol 44:561–592 Thompson SN, Hagen KS (1999) Nutrition of entomophagous insects and other arthropods. In: Bellows TS, Fisher TW (eds) Handbook of biological control: principles and applications of biological control. Academic Press, San Diego, CA, pp 594–652 Uddin J, Holliday NJ, MacKay PA (2005) Rearing lacewings, Chrysoperla carnea and Chrysopa oculata (Neuroptera: Chrysopidae), on prepupae of alfalfa leafcutting bee, Megachile rotundata (Hymenoptera: Megachilidae). Proc Entomol Soc Manitoba 61:11–19 Ulhaq MM, Sattar A, Salihah Z, Farid A, Usman A, Khattak SUK (2006) Effect of different artificial diets on the biology of adult green lacewing (Chrysoperla carnea Stephens). Songklanakarin J Sci Technol 28:1–8 Vandekerkhove B, Van Baal E, Bolckmans K, De Clercq P (2006) Effect of diet and mating status on ovarian development and oviposition in the polyphagous predator Macrolophus caliginosus (Heteroptera: Miridae). Biol Control 39:532–538 van Lenteren JC (2003) Commercial availability of biological control agents. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI Publ, Wallingford, UK, pp 167–178 van Lenteren JC, Hale A, Klapwijk JN, Van Schelt J, Steinberg S (2003a) Guidelines for quality control of commercially produced natural enemies. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI Publ, Wallingford, UK, pp 265–303
339 van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen GMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, Van Rijn PCJ, Thomas MB, Tommasini MG, Zeng Q-Q (2003b) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38 Weseloh RM (1998) An artificial diet for larvae of Calosoma sycophanta (Coleoptera: Carabidae), a gypsy moth (Lepidoptera: Lymantriidae) predator. J Entomol Sci 33: 233–240 White JH, Stauffer LA, Gallagher KA (2001) Materials for rearing insects, mites, and other beneficial organisms. US Patent 6291007 Wittmeyer JL, Coudron TA (2001) Life table parameters, reproductive rate, intrinsic rate of increase and realized cost of rearing Podisus maculiventris (Say) (Heteroptera: Pentatomidae) on an artificial diet. J Econ Entomol 94:1344–1352 Wittmeyer JL, Coudron TA, Adams TS (2001) Ovarian development, fertility and fecundity in Podisus maculiventris Say (Heteroptera: Pentatomidae): an analysis of the impact of nymphal, adult, male and female nutritional source on reproduction. Invertebr Reprod Dev 39:9–20 Zaki FN, Gesraha MA (2001) Production of the green lacewing Chrysoperla carnea (Steph.) (Neuropt., Chrysopidae) reared on semi-artificial diet based on the algae, Chlorella vulgaris. J Appl Entomol 125:97–98 Zanuncio JC, Zanuncio TV, Guedes RNC, Ramalho FS (2000) Effect of feeding on three Eucalyptus species on the development of Brontocoris tabidus (Het.: Pentatomidae) fed with Tenebrio molitor (Col.: Tenebrionidae). Biocontrol Sci Technol 10:443–450 Zanuncio JC, Molina-Rugama AJ, Serra˜o JE, Pratissoli D (2001) Nymphal development and reproduction of Podisus nigrispinus (Heteroptera: Pentatomidae) fed with combinations of Tenebrio molitor (Coleoptera: Tenebrionidae) pupae and Musca domestica (Diptera: Muscidae) larvae. Biocontrol Sci Technol 11:331–337 Zapata R, Specty O, Grenier S, Febvay G, Pageaux JF, Delobel B, Castan˜e´ C (2005) Carcass analysis to improve a meatbased diet for the artificial rearing of the predatory mirid bug Dicyphus tamaninii. Arch Insect Biochem Physiol 60:84–92
Author Biography Dr. Eric W. Riddick is a researcher concerned with the behavioral and chemical ecology of natural enemies. He is currently developing techniques for efficient rearing and cold storage of predatory mites and beetles in support of augmentative biological control. He is also interested in the overwintering biology of ladybird beetles and the biotrophic parasites (Laboulbeniales fungi, podapolipid mites) that attack them. This review was completed as part of the official duties of Dr. Riddick as an employee of the United States Department of Agriculture, Agricultural Research Service, in Stoneville, Mississippi, USA.
123
