Journal of Plant Protection Research ISSN 1427-4345 REVIEW The stink bug, Andrallus spinidens (Hemiptera: Pentatomidae), a potential predator for effective biological control Arash Zibaee1*, Samar Ramzi2, Hassan Hoda3 1 Department of Plant Protection, Faculty of Agricultural Sciences, Plant Protection, University of Guilan, Guilan, Iran 2 Department of Plant Protection, Tea Research Institute of Iran, Lahijan, Iran 3 Department of Biological Control, Plant Protection Institute, Amol, Iran Vol. 60, No. 4: 336–344, 2020 Abstract The aim of this review is to describe ecological and physiological features of Andrallus DOI: 10.24425/jppr.2020.134913 spinidens Fabricius and to discuss various possibilities of using it as an appropriate bio- Received: February 17, 2020 control agent in different agroecosystems. This hemipteran is a cosmopolitan predator of Accepted: August 19, 2020 caterpillar pests of rice, wheat, soybean, moong, pigeon pea, maize, sugarcane and cowpea with special feeding on Chilo suppressalis Walker, Naranga aenescnes Moore, Helicoverpa *Corresponding address: armigera Hübner and Spodoptera litura Fabricius. Climate, spatial distribution of prey and [email protected] type of agricultural crop are among the factors influencing the biology and spatial-tempo- ral distribution of A. spinidens. Studies have shown random or aggregated distribution of the predatory bug with population peaks in April, July and October. The 1st instar nymphs have no feeding, the 2nd and 3rd (the first 2 days) instars are seedling feeders while they are voracious predators of caterpillars from the middle of 3rd instar to adulthood. The salivary gland consisted of two anterior-, two lateral- and two posterior lobes with major secretion of trypsin, chymotrypsin, amino- and carboxypeptidases. The alimentary canal has a four-sectioned midgut in which the third section seems to be the main place for digestive enzymes including α-amylase, trypsin, chymotrypsin, elastase cathepsins B, L and D as well as carboxy- and aminopetidases. Andrallus spinidens have shown compat- ibility with some insecticides and the entomopathogenic fungus, Beauveria bassiana. The predatory bug may be successfully reared in a laboratory using Galleria mellonella larvae as prey and both conservation and augmentation should be considered as biological control strategies against insect pests. Keywords: Andrallus spinidnes, biological control, distribution, mass rearing, physiology Introduction There are several constraints on rice production around and thrips (Zibaee 2013). Due to high insect diversity the world including improper transportation, lack of in paddy fields and the need to produce healthy rice, suitable warehouses, unfavorable weather, insect pests, it is recommended to design an efficient system of in- pathogens and weeds (Anonymous 2018). Insects and tegrated pest management to alleviate pest population pathogens cause an average loss of 37% to rice yield outbreaks. Some steps should be included in the system that can vary between 24 to 41% regarding the produc- like proper cleaning of agronomical equipment, using tion situation (Savary et al. 2000). Insects from differ- clean seeds and varieties resistant to environmental ex- ent orders cause significant damage to rice plantations tremes and insect damage, balanced use of fertilizers, some of which are rice hispa, case worm, leaf folders, conservation of natural biocontrol agents, use of ecof- planthoppers, stem borers, armyworms, gall midges riendly pesticides and efficient storage of harvested Arash Zibaee et al.: The stink bug, Andrallus spinidens (Hemiptera: Pentatomidae), a potential predator… 337 grains (Reissig et al. 1986). Due to the urgent need for strategies by providing proper habitat, using fewer an increased food supply which involves reducing rice toxic pesticides and providing seedlings in winter in- losses by pests, farmers neglect integrated pest man- crease its population which naturally suppresses out- agement and freely spray paddy fields with different breaks of rice caterpillars. Andrallus spinidens belongs classes of insecticides even higher than the recommend- to the Pentatomid family of Hemipterans which was ed doses (Parween and Nakagoshi 2001). Although identified by Fabricius while Distant in 1902 reported such action may be effective in short-term periods, it from India and described its current morphologi- it will definitely lead to extensive problems including cal characteristics (Distant 1902). In the current re- disruption of an ecological balance between pests and view, the biological and physiological characteristics of predators, environmental pollution, products contain- A. spinidens are discussed along with its potential com- ing pesticide residue and pesticide resistance (Parween patibility with other control methods. and Nakagoshi 2001; Zibaee et al. 2009; Zibaee 2019). The afore-mentioned concerns have forced producers and consumers toward using eco-friendly pest control Morphological identification methods, mainly biological control. Microbial bacteria like Bacillus thuringiensis and fungi like Beuaveria bas- siana and Metarhizium anisoplia, parasitoids of Braco- Eggs are oval-shaped with 1.149 mm length and nids and Trichogrammatids in addition to predators 0.84 mm diameter. The top of each egg is covered like Andrallus spinidens Fabricius (Hemiptera: Pen- with a disc-shaped valve and a dark brown ring. The tatomidae) are among the major biocontrol agents of eggs are white to pale yellow just after laying but turn rice pests around the world (Ramzi and Zibaee 2014; dark with embryonic growth (Rajendra and Patel Bhojendra et al. 2019). Their distribution, efficiency 1971; Javadi et al. 2005) (Fig. 1B). The newly hatched and adaptation to cultivation systems should be deter- nymphs are bright red and turn dark red in a matter mined for potential use in conservation or augmenta- of hours (Fig. 1B). In the second nymphal stage, there tion strategies against rice pests. are six black spots on the lateral sides of the abdomen Andrallus spinidens is a predatory bug of caterpil- and three black spots on the center of the abdomen lars that naturally resides in paddy fields. Apart from (Fig. 1C). The third nymphs are similar to second other biocontrol agents like parasitoids, conservation nymphs but they are dark red (Fig. 1D). In fourth and Fig. 1. Adults, eggs and nymphal instars of Andrallus spinidens. A – adult, B – eggs and 1st instar nymphs, C – 2nd instar nymph, D – 3rd instar nymph, E – 4th instar nymph, F – 5th instar nymph 338 Journal of Plant Protection Research 60 (4), 2020 fifth nymphal stages, imaginal discs and dorsal spines Walker (Lepidoptera: Noctuidae), Thermesia rubri- are distinct. There are four black spots in the center of cans Boiduval (Lepidoptera: Noctuidae), Mythimna the abdomen and seven black spots on the lateral sides unipuncta Walker (Lepidoptera: Noctuidae), Melanitis of the abdomen although some yellow spots are visible leda L. (Lepidoptera: Nymphalidae), Pelopida smathias on the abdominal segments (Rajendra and Patel 1971; Fabricius (Lepidoptera: Hesperiidae), Spilosoma ob- Javadi et al. 2005) (Fig. 1E). Adults (males 13.4 mm lique Walker in addition to a coleopteran, Zygogram- long, females 15.8 mm long) are pale brown with dis- ma bicolorata Pallister (Coleoptera: Chrysomelidae) tinct, dense black punctuation on the head, pronotum, (Lepidoptera: Erabidae) (Distant 1902; Maxwell-Le- scutellum and hemelytra which form a distinct pattern froy 1909; Cherian and Brahmachari 1941; Rajendra on the head and anterior part of the pronotum. Anten- and Patel 1971; Singh and Gangrade 1975; Pawar 1976; nae have dark brown segments with very fine setae; the Rao and Rao 1979; Singh and Singh 1989; Pandey et al. rostrum is robust and long-reaching to the posterior 2002; Mohaghegh and Amir-Maafi 2007; Claver and coxae (Ghate et al. 2012). The head is almost rectan- Jaiswal 2013; Shylesha and Sravika 2018; Bhojendra gular with the two compound eyes on both sides and et al. 2019). a pair of a simple red eyes near the compound eyes Several environmental factors may affect the biol- (Rajendra and Patel 1971). The pronotum is hexago- ogy and spatial-temporal distribution of A. spinidens nal and densely punctured. The scutellum is longer including climate, distribution of prey and type of than wide and densely punctured with a longitudi- host plant. Javadi et al. (2005) determined the spatial- nal smooth line in the middle (Ghate et al. 2012) temporal distribution of the adults and the nymphal (Fig. 1A). Corium of hemelytra is broad and extends stages of A. spinidnes in rice fields of northern Iran on to the lateral margin of the wing with two white two rice varieties. These authors reported a random to stripes on the outer sides of the curium wing (Javadi aggregated population index on the two rice varieties. et al. 2005). Moreover, they monitored population changes from March to October and reported the highest number of both adults and nymphs in July although two small Distribution and host range peaks were recorded in May and October for adults as well as in June and September for nymphs (Javadi et al. 2005) (Fig. 2) (Rezvani and Shahosseini 1976). Andrallus spinidens has been reported in different Shylesha and Sravika (2018) found active feeding of geographical areas of eastern Asia, Australia, North both adults and nymphs on the different larval stages Africa, some parts of Europe and North America [as of Spodoptera frugiperda Smith (Lepidoptera: