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0OECD+WoS: 1.06+IY (Entomology) https://doi.org/10.31993/2308-6459-2023-106-2-15517
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EVALUATION OF DIETS FOR MASS REARING OF THE PREDATORY BUG NESIDIOCORIS TENUIS (HEMIPTERA, HETEROPTERA, MIRIDAE)
I.M. Pazyuk
All-Russian Institute of Plant Protection, St. Petersburg, Russia
e-mail: ipazyuk@gmail . com
Nesidiocoris tenuis (Hemiptera, Miridae) is a predatory bug which is widely used in biocontrol. This bug can consume both plant and animal matter. In the present paper, three alternative diets were evaluated in mass rearing of nymphs of N. tenuis maintained in cages on tobacco plants: eggs of the grain moth Sitotroga cerealella, cysts of Artemia salina, and bee-collected pollen. Adults of N. tenuis were fed a mixture of grain moth eggs and pollen during oviposition. The type of diet did not effect the survival of nymph. Output of adults was higher when nymphs were fed grain moth eggs than Artemia cysts while the body weight of adult bugs did not differ.
Keywords: biocontrol, entomophagous insect, grain moth, Artemia, pollen Submitted: 06.11.2022 Accepted: 27. 06.2023
Introduction
Nesidiocoris tenuis Reuter (Hemiptera, Miridae) is a predatory bug widely used in biocontrol alongside with the other representatives of the family, belonging to the genera of Macrolophus and Dicyphus. This bug can consume both plant and animal matter (Wheeler 2001). It feeds on whiteflies, aphids, thrips, spider mites, and young caterpillars and eggs of moths (Yano et al., 2020; Dhanapal et al., 2021; Nakano et al., 2021). However, plant-only diets are less nutrient-dense than carnivorous diets (Urbaneja et al., 2005; Sanchez 2008; Pazyuk, Vasiliev, 2013). This species was successfully used on tomato plants in greenhouses (Calvo et al., 2012) and in botanical gardens (Varfolomeeva, Pazyuk, 2017). Mass rearing of N. tenuis requires a nutrient-dense, advanced, and cost-effective feed. Eggs of moths such as Sitotroga cerealella Olivier (Lepidoptera, Gelehiidae) and Ephestia kuehniella Zeller (Lepidoptera, Pyralidae) have been used as an alternative feed for laboratory-reared entomophagous insects since the 20th century (van Lenteren, 2003). Since that time, Ephestia eggs have been tested in Europe as a feed for Orius, Macrolophus, and Nesidiocoris bugs. According to Fauvel et al. (1987) and Cocuzza et al. (1997), Macrolophus caliginosus Wagner (Hemiptera, Miridae) and Orius laevigatus Fieber (Hemiptera, Anthocoridae) reared on E kuehniella eggs possessed shorter nymph development time compared to the predators reared on whiteflies and thrips respectively. However, the high cost of these diets is a disadvantage. According to European researchers, the price of E kuehniella eggs ranged from 500 to 600 euros per kg (Vandekerkhove et al., 2009).
The first reports on using cysts of Artemia franciscana Kellogg (Branquiopoda, Artemiidae) for mass rearing of Orius species were published in Europe in the 2000s (Arijs, De Clercq, 2001). Belgian researchers discovered that decapsulated cysts soaked in water for two hours before feeding bugs, can be successfully used for their rearing. Similar studies were performed with Macrolophus spp. by Spanish researchers who demonstrated the ability of the bug M .
caliginosus to give 8 generations when fed on dry or hydrated Artemia cysts from two geographical populations (Castane et al., 2006). Later, researchers from Belgium and France emphasized the importance of Artemia cyst decapsulation before their use as a feed for the bug Macrolophus pygmaeus Rambur. They demonstrated that decapsulated Artemia cysts are a cost-effective alternative food source for mass rearing of this species (Vandekerkhove et al., 2009). Later, it was shown that decapsulated cysts are also suitable for feeding nymphs and adults of N. tenuis in laboratory (Owashi et al., 2020) and on tomato plants in greenhouses (Valiente, 2014). In Europe, one kilogram of Artemia cysts costs about 200 euros, which is much cheaper than one kilogram of E kuehniella eggs (Valiente, 2014).
Alongside animal food, the predatory mirids, including N tenuis, can feed on plant food such as: plant juices, nectar, and pollen (Wheeler, 2001). In this sense, pollen can be a good nutrient source for these bugs because it is rich in amino acids and proteins (Ioyrish 1976, Wackers et al., 2005). In nature, depending on the predators, pollen can be either primary or secondary food source for various entomophagous arthropods: Phytoseiidae, Carabidae, Caccinellidae, Chrysopidae, Syrphidae, Anthocoridae, Nabidae, Reduviidae, etc. (Zaher et al.,1969; Gilbert, 1981; Kiman, Yeargan, 1985; Larochelle, 1990; Villenave et al., 2005; Berkvens et al., 2007; Lundgran, 2009). As for mirids, the majority of M. pygmaemus nymphs when fed only on bee pollen or pollen and eggplant leaves, completed their development slightly later than those fed on animal diet (Perdikis, Lykouressis, 2000). In another study, the survival rate of M. pygmaemus nymphs fed on only pollen was 80 % less, and their oocyte weighted sum was 32 % lower as compared to nymphs fed on E kuehniella eggs. However, when given a small amount of E. kuehniella eggs (10 eggs for 3 days) together with pollen, 87 %> of adults emerged, and the number of oocytes in females was the same as when nymphs were fed only Ephestia eggs (Vandekerkhove, De Clercq,
© Pazyuk I.M., published by All-Russian Institute of Plant Protection (St. Petersburg).
This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0
(http://creatrvecommons.org/licenses/by/4.0/).
2010). N. tenuis is able to develop and reproduce feeding only on bee pollen (Pazyuk, Vasilyev, 2013) but the time of its development is longer, and fecundity is less than if it feeds on animal food (eggs of Sitotroga cerealella). When it comes to specific plants, two plant species, Verbena hybrida Voss (Lamiales: Verbenaceae) cv. Tapien and Scaevola aemula R. Br. (Asterales: Goodeniaceae) with flowers, are suitable for development, survival, and oviposition of N. tenuis (Kandori et al., 2022).
This predatory bug can be reared without plants (Puysseleyr et al., 2013) or using the following plant species: tomato Solanum lycopersicum L. (Solanaceae) (Urbaneja-Bernat
et al., 2013), tobacco Nicotiana tabacum L. (Solanaceae) (Pazyuk, 2010), Dittrichia viscosa L. (Asteraceae), Sesamum indicum (L.) (Pedaliaceae) (Biondi et al., 2016), and common bean Phaseolus vulgaris L. (Fabaceae) (Martinez-Garcia et al., 2016).
The goal of the present paper was to assess effect of diets on mass rearing of the predatory bug N. tenuis. Nymphs of N. tenuis, kept on tobacco plants, were fed three types of diet: 1) eggs of S. cerealella, 2) Artemia cysts, and 3) bee-collected pollen. We used dry, decapsulated cysts for the experiments because wet, hydrated cysts are shown to cause mold in rearing cages (Vandekerkhove et al., 2009).
Materials and Methods
Insect rearing
A stock culture of the bug Nesidiocoris tenuis, was obtained from Sesil Corporation (Nonsan, Republic of Korea) in the year 2010. Three types of diet were compared: 1) fresh eggs of S. cerealella, dry decapsulated cysts of Artemia salina, and ground pollen collected by bees from maple, coltsfoot, and willow (Oryol Region, Russia).
Experimental design
Bugs were reared at 24±0.2 °C in organza-covered cages measuring 60*40*40 cm, as previously described (Pazyuk, 2010): Eight tobacco plants with 6-8 leaves (tobacco seeds were obtained from the All-Russian Scientific Research Institute of Tobacco, Makhorka and Tobacco Products, Krasnodar, Russia) and 250 mature adults of N. tenuis were placed in each cage and kept there for a week. During oviposition, adult insects were supplied with the same diet: a mixture of grain moth eggs and pollen, three times per week. The diet was applied on top of the leaves. During this week, females laid eggs in tobacco plant tissues. The tobacco plants with eggs of N. tenuis were removed from the cages and transferred to new cages for hatching and further development of nymphs.
Results and
The obtained results showed that the three types of diet (grain moth eggs, Artemia cysts and bee pollen) did not affect number of nymphs, but number of adults was higher in the case of Sitotroga eggs while the percentage of emerged adults was less in the case of Artemia cysts.
One-way ANOVA showed that the number of nymphs per cage did not significantly differ in all three experimental groups (p=0.124) (see Table). The Tukey's test revealed that the number of adults (offspring) in the case of grain moth eggs was significantly higher than in the case of Artemia cysts (Tukey's test, p<0.05) with the case of pollen in between.
After nymphs hatched from eggs, they were fed one of three diets: 1) grain moth eggs, 2) Artemia cysts, and 3) ground pollen. The amount of food was 2.5 g per cage for all diets. Nymphs were counted on the 23rd day after oviposition started. By that time, nymphs of the first, second, and third instar were present. The emerged adults were collected with electric exhauster and counted on the 40th day. Ten females and ten males were taken from each cage and individually weighed on a balance Vibra HT Shinko Denshi, Japan. There were eight replications for each treatment. Overall, 1300 adults of maternal generation were tested in this study.
Statistical analysis
One-way analysis of variance (ANOVA) was used to access the effect of 3 diets (1) Sitotroga eggs; (2) Artemia cysts and (3) pollen, on the mean values of the following variables: (1) the number of nymphs of offspring (F1); the number of adults successfully developed from these nymphs;(3) the adult to nymph ratio, (4) the weight of F1 males and females.
Tukey's parametric test was used to assess differences between experimental treatments. All calculations were made with SYSTAT 12.00.08.
Discussion
Comparison of the three diets based on the percentage of emerged adults showed no differences between grain moth eggs and honeybee pollen while significantly fewer adults emerged in the case of the Artemia cysts diet (Tukey's test, p<0.05). Feeding on Artemia cysts and pollen yielded 27 % and 17 % less adults of N. tenuis, respectively, compared to feeding on grain moth eggs (taken as 100 %).
At the same time, the weight of females and males did not statistically differ between experimental groups (see Table 1) probably due to cannibalism.
Table 1. Effect of diets on F1 generation of Nesidiocoris tenuis in mass rearing
Feed type Number of offspring nymphs per cage (instars 1-3, offspring generation) (mean±SE) Number of adults per cage (offspring generation) (mean±SE) Share of emerged adults (% of nymphs) (mean±SE) Weight of females, (mean±SE), mg Weight of males, (mean±SE), mg
Sitotroga cerealella eggs Artemia cysts Bee pollen 2,705.5±144.1a 2,504.5±208.7a 2,141.4±204.3a 1,909.1±80.2a 1,394.9±150.9b 1,589±181.2ab 71±4a 56±4b 74±3a 1.1±0.07a 1.03±0.06a 1.02±0.11a 0.82±0.06a 0.73±0.06a 0.82±0.12a
Different letters (a, b) indicate values which are significantly different at p<0.05 (Tukey's test).
Таблица 1. Влияние корма на F1 поколение Nesidiocoris tenuis при массовом разведении
Тип пищи Число нимф на садок (1-3 возрастов) (потомство) Число взрослых особей на садок (потомство) Доля вышедших имаго (% от нимф) Вес самок, мг Вес самцов, мг
яйца Sitotroga cerealella цисты Artemia Пчелиная пыльца 2,705.5±144.1a 2,504.5±208.7a 2,141.4±204.3a 1,909.1±80.2a 1,394.9±150.9b 1,589±181.2ab 71±4a 56±4b 74±3a 1.1±0.07a 1.03±0.06a 1.02±0.11a 0.82±0.06a 0.73±0.06a 0.82±0.12a
Различными буквами (a, b) в столбцах отмечены различия
Thus, the experimental data showed significant differences in the three tested diets used for rearing of the predatory bug N. tenuis at the nymphal stage. Cannibalism appeared to occur during the mass rearing of N tenuis in all experimental groups but was more prevalent with unfavorable diets. Cannibalism was also observed in all diets of the predatory bug M. pygmaeus but decreased when the bug was fed a more favorable diet (E. kuehniella eggs) (Hamdi et al., 2013). In similar experiments with the predatory bug M pygmaeus, the authors demonstrated that two foods, Artemia cysts and pollen, were worse in nutritional value than grain moth eggs (Kozlova, Khodzhash, 2019), the share of emerging adults dropped to 33.6 % and 43.7 %, respectively, comparing to grain moth eggs (taken as 100 %). More significant fall in the percentage of emerged adults in the case of M pygmaeus than in N tenuis suggests that the latter species has less cannibalism.
When the diet is marginally worse in nutritional value but is much cheaper it may be the best option, since prices
между вариантами при p<0.05 (тест Тьюки).
for natural enemies have to compete with chemicals and production of entomophagous insects must be economically efficient and still managing their optimal quality (Arjis, De Clercq, 2001, De Clercq et al., 2005). In Russia, the average market prices for 100 grams of grain moth eggs, Artemia cysts, and pollen are around 10,000 rubles, 1,150 rubles, and 260 rubles, respectively. Therefore, less nutritious but more affordable diet can be used for mass rearing of N tenuis nymphs. Lu et al. (2011) came to the same conclusion, showing that the predatory bug Orius strigicollis Poppius (Hemiptera, Anthocoridae) is rationally maintained at the nymphal stage when feeding on cysts, and at the adult stage when feeding on eggs of the moth Cadra cautella Walker (Lepidoptera, Pyralidae). Our investigation suggests that the tested diets (Artemia cysts and pollen) can be used for mass rearing of N. tenuis at nymphal stage. But whether it is possible to use these diets on the constant basis and commercially produce predatory bugs of high quality, requires additional research.
Acknowledgements
The author wishes to thank N.V. Binitskaya for her assistance with the experiment. This study was supported by Russian Science Foundation Project No. 20-66-47010.
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Вестник защиты растений, 2023, 106(2), с. 100-104
OECD+WoS: 1.06+IY (Entomology) https://doi.org/10.31993/2308-6459-2023-106-2-15517
Краткое сообщение
ОЦЕНКА КОРМОВ ДЛЯ МАССОВОГО РАЗВЕДЕНИЯ ХИЩНОГО КЛОПА NESIDIOCORIS TENUIS (HEMIPTERA, HETEROPTERA, MIRIDAE)
ИМ. Пазюк
Всероссийский научно-исследовательский институт защиты растений, Санкт-Петербург
e-mail: ipazyuk@gmail . com
Nesidiocoris tenuis (Hemiptera, Miridae) - хищный клоп, широко используемый в защите растений. Он способен употреблять в пищу материалы как растительного, так и животного происхождения. В настоящей работе была проведена оценка различных вариантов корма для массового содержания нимф N. tenuis в садках на растениях табака. При откладке яиц имаго N. tenuis питались смесью яиц зерновой моли и пчелиной пыльцы. Варианты корма для нимф включали яйца зерновой моли Sitotroga cerealella, цисты Artemia salina и пчелиную пыльцу. Состав корма не влиял на выживаемость нимф. Выход имаго был выше, когда нимфы питались яйцами зерновой моли, чем при питании цистами артемии, хотя вес имаго не различался.
Ключевые слова: биометод, энтомофаги, зерновая моль, артемия, пыльца Поступила в редакцию: 06.11.2022 Принята к печати: 27. 06.2023
© Пазюк И.М. Статья открытого доступа, публикуемая Всероссийским институтом защиты растений (Санкт-Петербург) и распространяемая на условиях Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
