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Chapter 3. Biological control of beetle pests of stored grain and field crops

V. O. Martynov, V. V. Brygadyrenko Oles Honchar Dnipro National University

Introduction 1

In natural conditions, the main regulating factor of the popula- tions of pests is their natural enemies. Also, natural control includes other biological factors – competition, accessibility of food, and also abiotic factors, among which temperature and moisture are critical. In the struggle against pests, biological control is orientated towards decreasing the pest population through the impact of predators, parasites and pathogens. Biological control can be considered as an element of natural control which involves manipulation of the popu- lation of natural enemies by man and can be used for any type of organism, regardless of whether it is a pest or not. There are differ- ent definitions of biological control. According to Alston (2011), it is “any activity of a species which reduces the non-favourable impact of another species”. Also, biocontrol can be defined as “study and use of predators, parasites and pathogens for regulating the density of pests” (De Bach, 1964). By contrast to biological control, natural control is not related to human manipulations. The history of biological control dates far back to antiquity. Around two thousand years B.C., the Ancient Egyptians used bio- logical control for the first time, when they began domesticating cats, for they feed on rodents which cause damage to the harvest. The first written records of biocontrol belong to the III century

1 Martynov V. O., & Brygadyrenko V. V. (2019). Biological control of beetle pests of stored grain and field crops. In: Current problems of agrarian industry in Ukraine. Accent Graphics Communications & Publishing, Vancouver, Canada. – P. 134–190. Doi:10.15421/511904 V. O. Martynov, V. V. Brygadyrenko 135

AD when in China, in the territory where the city Guangzhou is located today, a nest of weaver ants (Oecophylla smaragdina (Fabricius, 1775)) was sold for use against such pests as Tessarato- ma papillosa (Drury, 1770). By 1200, the significance of ladybirds (Coccinellidae (Latreille, 1807)) has been recognized as an agent of control against Aphids and Coccoidea. The first description of parasitism of insects was illustrated by van Leeuwenhoek in 1701. Cordyceps fungi which affect owlet moths (Noctuidae) were con- sidered to be the first pathogens of insects by Réaumur in 1726. In 1762, the British and the French successfully introduced the common myna (Acridotheres tristis (Linnaeus, 1766)) from India to Mauritius to use against the red locust (Nomadacris septemfas- ciata (Audinet-Serville, 1883)). In 1776, in Europe, a successful control of common bed bug (Cimex lectularius (Linnaeus, 1758)) was effected using Picromerus bidens (Linnaeus, 1758), a predatory shieldbug. In 1837, Koller for the first time described the concep- tion of “natural control”. In 1850–1887, the conception of biological control developed in the United States. In 1870, Charles Riley for the first time conducted a successful transportation of parasitoids from Kirkwood (Missouri) to other states for biological control of plum curculio (Conotrach- elus nenuphar (Herbst, 1797)). In 1883, the US Department of Agri- culture (USDA) imported Cotesia glomerata (Linnaeus, 1758) from England for the control of the small white (Pieris rapae (Linnaeus, 1758)) common in several states. It was the first intercontinental transportation of parasites. In Europe, projects developed for biological control were first implemented only in the 1800s. Intensification of horticulture dur- ing that period led to the search of new methods against insect pests in America as well. The first project on cottony cushion scale (Ic- erya purchasi (Maskell, 1878)), aimed at control of its number, was started in California in 1888, using the vedalia beetle Rodolia car- dinalis (Mulsant, 1850). Since that time, a number of projects have been started, including the project on gypsy moth (Lymantria dispar (Linnaeus, 1758)) in New England (1905–1911). Overall, more than 136 Chapter 3. Biological control of beetle pests of stored grain and field crops

6.000 introductions of over 2.000 insect species have been made for use as control agents against insect pests (Cock et al., 2016). The peak of activity in biological control with 57 different agents created in different places was observed from 1930 to 1940. During the World War II, a steep decrease in activity in biological control occurred, and after the war, it did not become popular due to pro- duction of relatively cheap synthetic pesticides. Biological control was revived as the main component of the conception of integrated pest management (IPM) only in the late 1960 s (Kwenti, 2017).

Biological control as a method against pests

Peculiarities of biological pest control The impact of biological control on the diversity of local species can be both positive and negative. The main problem of biocontrol is the impact of the agents on non-target species. Therefore, during the introduction of the control agent, the main requirement is speci- ficity to the host. A potential agent of biological control should un- dergo a variety of tests and quarantine before being released into the environment, for if an agent affects a broad range of species, it can be highly invasive, causing changes in biodiversity on a large scale. The hardy and prolificGambusia holbrooki (Girard, 1859) which lives in the South-East of the USA has been distributed all around the world for elimination of larvae of mosquitoes and the struggle against malaria. Unfortunately, it has caused great damage to en- demic species of fishes and amphibians, as it competes with them for food resources and eats their roe and fry. The short spawning period, high fertility and resistance to salinity have contributed to the wide distribution of Gambusia (Vila-Gispert et al., 2005; Alcaraz & Garcia-Berthou, 2007). Biological control of invasive pests can be conducted by natu- ral inhabitants of the territory of the pests’ distribution. Over time, they adapt to the presence of immigrants and have a negative effect on them through predation or competition, leading to a significant decrease in the number of pests. The birch leafminer (Profenusa V. O. Martynov, V. V. Brygadyrenko 137 thomsoni (Konow, 1886)), brought to North America from Europe, became a significant pest of birch in the 1970s. However, in the 1990s (MacQuarrie, 2008; Soper et al., 2015), its population steeply decreased under the impact of an American parasite Lathrolestes thomsoni (Reshchikov, 2010). Unfortunately, in most cases, local species are not able to control the population of pests sufficiently. For example, in Europe, the in- vasive horse-chestnut leaf miner (Cameraria ohridella (Deschka & Dimic, 1986)) is attacked by dozens of parasitoids, which causes no significant impact on the level of damage (Grabenweger et al., 2010). The dynamic of populations of invasive insects demonstrates increases and decreases, where their abundance and the damage they reach their peak soon after the invasion, following which their population begins to collapse. One of the reasons for collapse is the activity of local enemies. Kenis & Branco (2017) presume that local natural enemies will affect the invasive insects if they belong to a group of insects which is usually attacked by polyphages or is eco- logically and taxonomically closely related to the invader. Over time, local natural enemies start attacking invasive insects and can partly or completely control the pest, but the results are quite unpredict- able and in most cases are insufficient for providing a satisfactory level of control. In some cases, soon after the invasion of a pest, their exotic natural enemies occur, which perform a significant control. For ex- ample, parasites of invasive insect pests of Eucalyptus in Mediter- ranean regions, such as Avetianella longoi (Siscaro, 1992) – parasite of longhorn beetle Phoracantha semipunctata (Fabricius, 1775), Closterocerus chamaeleon (Girault, 1922) – parasite of Chalcid wasp (Ophelimus maskelli (Ashmead, 1900)) and Psyllaephagus bliteus (Riek, 1962) – parasite of plant lice (Glycaspis brimblecombei (Moore, 1964)) (Bush et al., 2016). Biological control is one of a few methods against pests which has a constant pattern and which requires no measures after the re- leasing and distribution of the agents. From a long-term perspec- tive, biological control has a number of advantages. However, the 138 Chapter 3. Biological control of beetle pests of stored grain and field crops assessment of benefits is complicated due to urgency of implemen- tation, complexity of the methods, absence of financial support and low priority given to post-release monitoring. Despite the dif- ficulties, Cock (2015) provide data which shows that the projects of biological control of cassava mealybug (Phenacoccus manihoti (Matile-Ferrero, 1977)) and mango mealybug (Drosicha mangiferae (Stebbins, 1903)) in Africa had the coefficients of costs and benefits of 1: 738 and 1: 808 respectively. Similar results were presented in the studies by Hill & Greathead (2000), Gutierrez et al. (1999), Dahlsten et al. (1998) and others, which demonstrates the obvious advantage of biological control from the perspective of economics. However, it should be mentioned that the development of technology of the control and the subsequent monitoring of the studied ecosystem re- quires a lot of time.

Risks of biological control In 1980s, concerns arose regarding the ecological safety of agents of biological control due to various side effects on the local biodiver- sity, which are still voiced today. This problematic was analyzed in the studies by Hajek et al. (2016) and Van Driesche & Hoddle (2017). The main risk related to the introduction of a foreign preda- tor, parasite or pathogen, is its potential effect on local non-target organisms, which leads to the changes in the populations and com- munities. One of the most known examples is the tachinid fly spe- cies (Compsilura concinnata (Meigen, 1824)) introduced to North America for the control of gypsy moth, causing decrease in the native species even today (Elkinton & Boettner, 2012). Side effects can occur as a result of competition with close relative species of predators, for example, competition of ladybugs Harmonia axyri- dis (Pallas, 1773) and Coccinella septempunctata (Linnaeus, 1758) with native species (Evans, 2004; Roy et al., 2016). The introduc- tion of agents of biological control can have a negative effect as a result of hybridization with related species. Yara et al. (2007) pres- ent data showing that Torymus sinensis (Kamijo, 1982) a parasite introduced to Japan as a control agent against the gall wasp (Dryo- V. O. Martynov, V. V. Brygadyrenko 139 cosmus kuriphilus (Jasumatsu, 1951)), caused reduction in the population of T. beneficus (Yasumatsu & Kamijo, 1979) as a result of hybridization. However, competition between these species is also possible. Despite this fact, currently, a relatively low number of introductions have directly affected particular non-target spe- cies at the level of population. Indirect impacts are possible, but they are mostly theoretical in character. The last 20 years have wit- nessed the development of international principles, rules and sci- entific methods of assessing the risks of biological control. Special attention should be paid to the specificity to the host. It is best to take into consideration the ratio of costs and benefits of biologi- cal control, which allows one to make a balanced decision on its implementation (Kenis et al., 2017).

Advantages and disadvantages of biological control Biological control has certain advantages in comparison with other strategies against pests, especially chemical methods. They in- clude safety for the environment, absence of residues, affordability, ease of use, duration of impact, and absence of development of re- sistance in the pests. The disadvantages of biological control include: – Low tempi of control. There is often a delay between the in- crease in the population of pests and that of the agent of biocontrol. If a population of pests is already at the level of economic damage or higher, the only alternatives are pesticides. – Biological agents cannot eliminate the host completely, be- cause this would cause their extinction. However, achieving com- plete elimination is possible through integration of biological con- trol with other strategies against pests. – There is a possibility that a biological agent may try to feed on beneficial insects and plants. This problem is minimized through ac- curate selection of biological control agent. – There are concerns about release of foreign agents of control for they can bring new parasites which would affect the local com- munity. 14 0 Chapter 3. Biological control of beetle pests of stored grain and field crops

– Methods of transport, maintenance and usage of a biological agent can be relatively difficult and in some cases expensive. – Biological control can be expansive compared chemical meth- ods, which is related to the methods of study prior to the introduc- tion of the strategy. – Badly prepared biological control can lead to rapid changes in the natural biodiversity (Kwenti, 2017).

General methods of using biological control Importation. The most broadly distributed classic method of bio- logical control. It is used for the species of pests exploring a new environment, immigrants or introduced species, which have no natural enemies in the area. The method includes determination of the pest’s origin and determination of its natural enemies, which are potential agents of biocontrol. They are imported to a new place in the pest’s range with the aim of strengthening the species in new conditions and regulating the number of the targeted pest. Higher efficiency against the pests requires a strong capacity of the control agent for colonization. Maximum control is achieved if the agent is temporarily stable and can maintain its numbers even during brief absence of the target pest species (Mahr & Ridgway, 1993). Augmentation. Mass cultivation and release of natural enemies of the pest. Practically, there are several types of augmentation. Inductive release is one-time release of a large number of natural enemies in areas of different sizes. At the same time, the natural ene- my does not have enough time to consolidate and does not reproduce. The method is used for one-time decrease in the numbers of the pest. Inoculating release is multi-time release of low numbers of the natural enemy over a certain period of time for its consolidation and distribution in the area of release. This method allows bio- logical control of the pest’s population to be conducted over a long period of time. Maintenance. Using methods orientated towards protection, strengthening and support of existing natural populations of agents of biological control. Such natural enemies are already adapted to V. O. Martynov, V. V. Brygadyrenko 141 the environment and target pest, and their maintenance can be simple and economical. Such practice can include diversification of habitat for providing additional shelter or food to the natural en- emy, using pesticides which are selective for target pests and cause minimum effect on natural enemies, provision of synthetic food ad- ditives, avoiding traditional agricultural methods which damage or eliminate natural enemies.

Agents of biological control

Predators Biological control of insects involves predators, parasites or pathogens such as viruses, bacteria and fungi. Predators are free liv- ing organisms, vertebrates or invertebrates which use pests as food and can consume them in large numbers. The efficiency of the con- trol of the pest population by predators can vary depending on con- ditions in particular habitats. For example, in open areas, predation is up to 8 times higher than in the territory of an agrarian complex. In the areas with high grass stand, the level of predation is lower than in places with low grass. Spiders and Acari. Spiders hunt a variety of insects. After creating favourable living conditions for spiders, for example by mulching soil, one can increase their population by 60% (Riechert & Bishop, 1990; Jackson & Pollard, 1996). Some species of Acari, for example from Phytoseiidae family, are predators of nematodes and are able to consume eggs of Ascarididae from the soil (Lysek, 1963; Riechert & Bishop, 1990; Jackson & Pol- lard, 1996). Several species of Acari, such as Macrocheles muscaedomesticae (Scopoli, 1772), actively consume eggs and larvae of different flies which develop in the faeces of cattle (Safaa, 2014). Natural enemies of insect pests include the following Acari: Py- emotes tritici (LaGrèze-Fossat & Montagné, 1851), Blattisocius tar- salis (Berlese, 1918), Acarophenax mahundai (Steinkraus & Cross) and A. lacunatus (Cross & Krantz) (Bruce & LeCato, 1979; Haines, 14 2 Chapter 3. Biological control of beetle pests of stored grain and field crops

1981; Steinkraus & Cross, 1993; Faroni et al., 2000, 2001). The most studied species is P. tritici, but using this is limited because of harm for humans. P. ventricosus (Newport, 1850) is another much studied species, but its commercial use is limited because it can also bite humans, as do other species of the Pyemotidae family (Moser, 1975). Acari of the Acarophenacidae family are parasites of eggs of dif- ferent pest insects. A. lacunatus affects Cryptolestes ferrugineus (Ste- phens, 1830), Rhyzopertha dominica (Fabricius, 1792) and Tribolium castaneum (Herbst, 1797), but cannot parasitize Oryzaephilus suri- namensis (Linnaeus, 1758). In the studies by Oliveira et al. (2003) Acari significantly decreased populations of R. dominica by 61% and populations of T. castaneum by 53%. A. lacunatus significantly re- duced the rapid tempi of growth of C. ferrugineus, R. dominica and T. castaneum populations. The range of hosts of A. lacunatus is not as broad as that of other parasitic Acari, agents of biological control of insects. For example, P. tritici attacks Plodia interpunctella (Hübner, 1813), Cadra cautella (Walker, 1863), Lasioderma serricorne (Fabricius, 1792) and even O. surinamensis (Bruce & LeCato, 1979). In the absence of the main host – С. cautella – B. tarsalis can parasitize T. castaneum. The ability to successfully parasitize several species is a good fea- ture for potential use of a species as an agent of biological control of pests of grain crops (Oliveira et al., 2003).

Insects Successfully used classic agents of biological control are wasps of the Scoliidae family, such as Colpa sexmaculata (Fabricius, 1781). They are large wasps, the larvae of which parasitize larvae of the Scarabaeidae and Curculionidae families, while the imagoes feed on nectar. Parasites of nymphs and imagoes of many species of lo- custs are flies of the Sarcophaga genus, though their range of host preferences of is much wider. For example, Sarcophaga fuscicau- da (Böttcher, 1912) attacks adults of Rhynchophorus ferrugineus (Olivier, 1790) (Murphy & Briscoe, 1999). V. O. Martynov, V. V. Brygadyrenko 14 3

Representatives of the Tachinidae family are highly specialized agents of biological control, the larvae of which parasitize different species of Lepidoptera and Coleoptera. An example is Paratheresia menezesi (Townsend), which according to research, parasitizes 50% of populations of R. palmarum (Moura et al., 1993). Some earwig species of the Forficulidae family are active preda- tors of insects. According to the data of Abraham et al. (1973), a single Chelisoches morio (Fabricius, 1775) consumes 5.3–8.5 of eggs and 4.2–6.7 larvae of R. ferrugineus daily. Predators broadly used against insect pests include the ware- house pirate bug Xylocoris flavipes (Reuter, 1884) and several other heteropterans of the Lyctocorinae subfamily (Reichmuth, 2000). These heteropterans are promising agents of control of Coleoptera and Lepidoptera in warehouses. They have strong ability to increase their number, even in conditions of prey shortage. However, X. flavi- pes is ineffective against Curculionidae species which hide in grains (Arbogast, 1975) and Teretriosoma nigrescens (Lewis) clown beetle (Richter et al., 1997). Another good example is Laelius pedatus (Say, 1836), a natural en- emy of the varied carpet beetle (Anthrenus verbasci (Linnaeus, 1767)) and several species of Trogoderma (Klein & Beckage, 1990; Al-Kir- shi, 1998). In Northern Europe, for control of the housefly (Musca do- mestica (Linnaeus, 1758)), the predatory fly Hydrotaea aenescens (Wiedemann, 1830) is used commercially (Pirali-Kheirabadi, 2012). Promising agents of biological control of tsetse fly Glossina sp. (Wiedemann, 1830) are the velvet ants Mutilla glossinae (Turner) (Oluwafemi, 2008). Around 27 species of ants from Aphaenogaster, Iridomyrmex, Monomorium, Pheidole and Solenopsis genera hunt Acari, Haema- tobia irritans (Linnaeus, 1758) horn flies and different agricultural pests. In Louisiana (USA), Solenopsis invicta (Buren, 1972) was suc- cessfully used against Ixodidae ticks. However, this programme was not implemented on a large scale due to the ants’ danger to humans (Jemal & Hugh-Jones, 1993). 14 4 Chapter 3. Biological control of beetle pests of stored grain and field crops

An important role in the struggle against flies is played by dung beetles of the family Scarabaeidae which breed in cow faeces. The beetles Onthophagus ganelle and Euniticellus intermedius brought from Africa to Australia are used for the control of the Austra- lian bush fly (Musca vetustissima (Walker, 1849)) and buffalo fly (Haematobia exigua (de Meijere, 1906)), due to the fact that they compete with the fly larvae for food. Also, their rapid burial of dung reduces the range of places for nesting of the flies (Bornemissza, 1970; Pirali-Kheirabadi, 2012). For the control of the Colorado po- tato beetle (Leptinotarsa decemlineata (Say, 1824)), the spotted lady beetle (Coleomegilla maculate (De Geer, 1775)) can be used, which feeds on its eggs and larvae. Larvae of Coccinellidae are active pred- ators which eat Aphids, Acari, small caterpillars and other insects (Acorn, 2007; Sing & Richard, 2008). For reducing the populations of C. cautella in warehouses, Bracon hebetor (Say, 1836) and Venturia canescens (Gravenhorst, 1829) parasitoids are used. Similarly, for reducing the population of O. surinamensis, the bethylid parasitoid wasp Cephalonmia tar- salis (Ashmead) is used. Other cosmopolite parasitoids of the wheat weevil are Lariophagus differendus (Forst) and Theocolax elegans (Westwood, 1874). Species used against P. interunctella are Tricho- gramma deion (Riley), which parasitizes eggs, and a larvae parasit- oid B. hebetor, which significantly reduce the population of adults (Grieshop et al., 2006). Schmale et al. (2001) assessed the potential of several species of parasitoids of the bean weevil (Acanthoscelides obtectus (Say, 1831)). The most promising parasitoid for the control of A. obtectus is Di- narmus basalis (Rond). which has a long duration of reproduction and high number of offspring. A. calandrae turned out to be inap- propriate to be used as a control agent against this host. Heterospilus prosopidis (Viereck, 1910) had a shorter period of laying eggs than D. basalis, which led to lower life expectancy of its progeny. Amphibolus venator (Klug) is a predator of a number of insect pests of grain stores. It hunts Trogoderma granarium (Everts, 1898), T. castaneum, Corcyra cephalonica (Stainton, 1866), Latheticus oryzae V. O. Martynov, V. V. Brygadyrenko 14 5

(Waterhouse, 1880) and Alphitobius diaperinus (Panzer, 1797) (Pingale, 1954; Haines, 1991). Pingale (1954) mentioned that A. venator is an ef- fective agent in the control of C. cautella and A. diaperinus. Nishi et al. (2004) in their study report that A. venator hunts larvae, pupae and adults of T. confusum, preferring the first. Predation is more significant- ly expressed at 30 °C than at 25 °C, because the optimum temperature for breeding and development of A. venator is 30.0–32.5 °C. Tempera- tures below 25 °C are unsuitable for the development of nymphs (Nishi & Takahashi, 2002). Females have a tendency towards consuming more prey compared to males because of the requirements of producing eggs. Another predator, Peregrinator biannulipes (Montrouzier & Signoret, 1861) is well known as a natural enemy of insect pests of grain stores. It hunts fungus moths such as Ephestia kuehni- ella (Zeller, 1879), P. interunctella, C. cephalonica, Pyralis farinalis (Linnaeus, 1758) and beetles, among which are T. castaneum, T. confusum, Stegobium paniceum (Linnaeus, 1758) and L. serricorne (Tawfik et al., 1983; Awadallah & Afifi, 1990). One of the most efficient parasitoids is a Pteromalidae wasp T. elegans, which attacks primary insect pests of grains, such as Si- tophilus spp., R. dominica, S. paniceum, Callosobruchus maculatus (Fabricius, 1775) and the Angoumois grain moth (Sitotroga cere- alella (Olivier, 1789)) (Cowan at al., 1881; Flinn et al., 1996; Flinn, 1998; Flinn & Hagstrum, 2001). However, T. elegans does not para- sitize secondary pests, including Tribolium spp. and C. ferrugineus, the immature stages of which develop outside the kernel of wheat. In the study by Flinn et al. (2006), processing with this parasit- oid led to significant decrease in the number of Sitophilus zeamais (Motschulsky, 1855), T. castaneum and C. ferrugineus by 78%, 94% and 70% respectively compared to the control group. Effective control of Indian meal moth (P. interpunctella) and oth- er pyraloid moths was achieved using B. hebetor (Press et al., 1982; Cline et al., 1984; Cline & Press, 1990). Wasps of the Trichogramma genus, which are parasites of eggs of many lepidopteran pests, were also assessed for the control of P. interpunctella (Brower, 1990; Schol- ler & Flinn, 2000; Grieshop, 2005). 14 6 Chapter 3. Biological control of beetle pests of stored grain and field crops

Menon et al. (2002) studied the impact of A. calandrae which parasitizes R. dominica in wheat at different temperature ranges and host densities. It was determined that the efficiency of the parasitoid increases as the temperature rises. The highest number of infested larvae was observed at 35 °C and equaled 15 individuals in 24 h. At 20 °C, this parameter decreased to two larvae. At 38 °C, the death rate of the parasites significantly increases. Adult females of A. calandrae can survive up to 75 days in the presence of hosts and presence of cellulose as an additional source of food (Chatterji, 1955). It was found that female parasitoids sur- vive up to 40 days if they have constant provision of hosts. Also, the parasitoid is a polyphage and is able to survive on different hosts such Sitophilus oryzae (Linnaeus, 1763) and S. zeamais (Williams & Floyd, 1971; Press et al., 1984). Therefore, the ability of A. calandrae to find and parasitize R. dominica in a wide range of temperatures makes it a good candidate for biological control of pests of grain storage in the areas with fre- quent fluctuations of temperature.

Pathogens

The conception of using pathogens The conception of using pathogens as agents of biological control appeared in the XIX century during the study of diseases of silkworm Bombyx mori (Linnaeus, 1758) (Tinsley, 1979). Already in 1880, Metchnikoff experimented with Metarhizium anisopliae ((Metch- nikoff) Sorokin, 1883), using it against pests of beet. As the role of pathogens in regulation of the insects was understood, the research focused on such biological problems as release of pathogens, their taxonomy, peculiarities of their life cycle, and further on comparative pathogenicity of different organisms (Mulligan et al., 1978; Baugher & Yendol, 1981), mechanisms of their transfer between hosts (An- dreadis & Hall, 1979) and on the ability of pathogens to maintain in the environment (Thompson & Scott, 1979). Also, researchers mentioned problems of development of methods of production, V. O. Martynov, V. V. Brygadyrenko 147 maintenance and transport of pathogens (Shapiro et al., 1981), their efficiency in field conditions (Ives & Cunningham, 1980) and prob- lems of safety for humans and animals connected with usage of the agents (Harrap, 1978). The main attributes of a pathogen used as an agent of biological control should be high pathogenicity, high efficiency of the transfer, ability to survive inside the host, ease of production and mainte- nance in the laboratory (Anderson, 1982).

Fungi Many insects and other species of arthropods are vulnerable to infestation with entomopathogenic fungi. Currently, 750 species of entomopathogenic fungi are distinguished, which belong mostly to the Ascomycota and Zygomycota types. A distinctive peculiarity of fungi, in contrast to other pathogens is entrance into the host’s organism through the cuticle, not food. On contact of an insect with spores in the soil, air and on different surfaces, in the condi- tions of sufficient moisture, the spores germinate, forming hyphae, through the cuticle, mainly on bends of limbs where it is thinnest (Fathy, 2012). The tempi of the host’s death depends on the type of fungus and number of spores and usually occurs after 4–10 days. Also, fungi can release toxins (mycotoxin). After the host dies, the fungus produces thousands of new spores which scatter and con- tinue their life cycle. Fungi are one of the most broadly used agents of biological pest control. The commonest species of entomopathogenic fungi are cos- mopolite hyphomycetes M. anisopliae and Beauveria bassiana ((Bals.-Criv.) Vuill., 1912). In favourable conditions, they often cause natural outbreaks, affecting a broad range of insects and arachnids. In research on the development of these fungi, significant attempts were made to use them as control agents in agriculture and forestry of climatically mild regions. Because of their long survival in the soil, these fungi provide long term control, eliminating larvae and pupae of insects. Also, they are effective against mosquitoes, infest- ing them on different stages of development and causing their death 14 8 Chapter 3. Biological control of beetle pests of stored grain and field crops after 3–14 days (Quesada-Moraga et al., 2006; Leger, 2008; Ebrahim, 2015). The number of conidia released per host depends on the species of fungus, and species and size of host. For example, B. bassiana produc- es 10–200 times more conidia on adult Curculio caryae (Horn, 1873) than on M. anisopliae (Gottwald & Tedders, 1982). The most impor- tant abiotic factors which affect entomopathogenic fungi are tempera- ture, moisture and ultraviolet radiation (Meikle et al., 2003). Other factors studied include moisture content and pH value (Lingg & Don- aldson, 1981), and soil structure (Groden & Lockwood, 1991). On the basis of B. bassiana, many products of Mycotrol ESO&WPO (BioWorks Inc.), Naturalis L (Troy BioSciences, Inc.) and Biosect® (KZ Chemicals) are available. As agents of biocontrol, oomycetes of Lagenidium giganteum (Schenk, 1859) are also used, which affect larvae of some species of mosquitoes. The fungus allows efficient control of the number of the mosquito Culex pipiens (Linnaeus, 1758) and as a result the spread of such diseases as filariasis and Rift Valley fever (Sur, 2001; Fathy, 2012). Another promising group of fungi which can cause natural out- breaks in insect populations is Entomophthora. Several genotypes of Entomophthora muscae ((Cohn) Fresen., 1856) were found, each be- ing highly specific to a particular host (Jensen, 2011). Meyling & Eilenberg (2007) studied pathogenic Entomoph- thorales such as Pandora neoaphidis ((Remaudiere & Hennebert) Humber, 1989) and Neozygites fresenii ((Nowak.) Remaud. & Keller, 1980) as agents of biological control of aphids in England and the USA (Shah & Pell, 2003; Ekesi et al., 2005; Steinkraus, 2006). For insect control, Hirsutella thompsonii (Fisher), Lecanicillium lecanii (Zare & Gams), Nomuraea rileyi (Farl.), Coelomomyces spp. and Leptolegnia spp. (Fathy, 2012) have also been used. Paecilomyces formosoroseus and N. rileyi fungi can cause sig- nificant decrease in egg laying and emergence of adult pests of the Bruchidius genus. For the control of P. interpunctella, four species of fungi are used: B. bassiana, L. lecanii, M. anisopliae and Paecilomy- V. O. Martynov, V. V. Brygadyrenko 14 9 ces farinosus (Būda & Pečiulytė, 2008). According to Cuthbertson et al. (2005), Lecanicillium muscarium (R. Zare & W. Gams) is the most efficient agent of biological control used against some pests in orangeries and against the silverleaf whitefly (Bemisia tabaci (Gen- nadius, 1889)) (Schreiter et al., 1994; Faria & Wraight, 2001). There are reports ofB. bassiana killing Blissus leucopterus (Say, 1832) and Chrysoperla carnea (Stephens, 1836) (Ramoska & Todd, 1985; Donegan & Lighthart, 1989). It was demonstrated that adding 50 mg of conidia/kg leads to 50% decrease in the off- spring, and 150 mg/kg – to 98% decrease, which is a maximum effect (Throne & Lord, 2004). Abd El-Aziz (2011) studied the impact of Bacillus thuringien- sis (Berliner, 1915) and B. bassiana and three botanical extracts on three storage insect pests: Р. interunctella, E. cautella and E. kuehni- ella. Botanical extracts tested in combination with B. thuringiensis caused significant strengthening of pathogens and increase in the death rate in almost all cases (Sabbour, 2003). Būda & Pečiulytė (2008) tested the impact of four species of fun- gi (B. bassiana, L. lecanii, M. anisopliae and P. farinosus) on adult Indian meal moths (P. interpunctella) and demonstrated that all iso- lates were pathogenic, despite different levels of effectiveness. Gindin et al. (2006) studied the sensitivity of the snout beetle R. ferrugineus to the entomopathogenic fungi, M. anisopliae and B. bassiana. It was determined that the strains of the former were more virulent than the latter, leading to death of 100% of larvae over 6–7 days. Total percentage of death of eggs and hatched lar- vae equaled 80–82% compared to 34% in the control. The prepara- tions were tested in the forms of powder and suspension. Using dry composition, 100% death of the adults was achieved after 2–3 weeks, and using suspension – after 4–5 weeks. The impact of the preparations reduced the life expectancy, the period of egg laying and caused a three-times decrease in the rate of hatching. Adane et al. (1996) studied the action of several isolates of B. bassiana against adult S. zeamais. The virulence of the studied iso- lates varied, the death rate of S. zeamais equaled 37–100%. Also, the 150 Chapter 3. Biological control of beetle pests of stored grain and field crops mean lethal time for different isolates was determined, the mini- mum value of which equaled 3 days. Lord (2001) studied the impact of B. bassiana on the snout beetle O. surinamensis and its control agent C. tarsalis. Processing the larvae of the snout beetle with fungi led to progeny of the wasp dying on all infested hosts two days after laying eggs and egg laying finishing on the fourth day after the processing. Decrease in egg laying is related to death of the host. It was determined that despite sensitivity to the fungus, the frequency of C. tarsalis visiting the storage site did not change, even when conidia were kept at 500 mg/kg of wheat, this be- ing determined visually. The wasps are unable to find infested hosts and avoid lethal concentration of conidia on the surface of grains. The impact of B. bassiana at concentration of 100 mg/kg of wheat on the female C. tarsalis led to death of 53% of them in 3 hours. Male C. tarsalis proved less sensitive to the fungus. Khashaveh et al. (2011) studied the pathogenicity of M. anisopliae for T. granarium. A series of 105 to 109 conidia/ml suspensions were used in the experiment. All isolates were pathogenic for the adults and larvae, the death rate increased following increase in conidia concentration and significantly varied depending on the isolate. The overall death rate after 10 days was 21% to 84%, though one of the isolates demonstrated 100% death rate at maximum concentration. The study demonstrated that M. anisopliae is an acceptable agent of biological control of T. granarium, though additional experiments are required for increasing its efficiency. Most studies devoted to the interaction of parasitoid insects and fungi included fungi which do not attack parasitoids (Powell et al., 1986; Brobyn et al., 1988). In such cases, the parasitoid-fungi in- teraction is competitive rather than pathogenic. An example is the refuse of Encarsia formosa (Gahan, 1924) from the larvae of green- house whitefly with hyphae of mycelium of Asherhersonia aleyro- dis (Webber) in their hemolymph (Fransen & Van Lenteren, 1993). Willers et al. (1982) reported on antifungal anal discharges of larvae of a Lepidoptera endoparasite, Pimpla turionellae (Linnaeus, 1758), which inhibit growth of B. bassiana. V. O. Martynov, V. V. Brygadyrenko 151

Bacteria The most important entomopathogenic bacteria belong to the Bacillus genus. One of the most broadly used agents of biological insect control is B. thuringiensis. After the bacteria enter the host, they release enterotoxins, which leads to the death of insect. For the control, different subspecies of B. thuringiensis are used: B. t. var. israelensis infests larvae of mosquitoes, black flies and related Dip- tera, B. t. var. kurstaki and B. t. var. aizawai – larvae of lepidopter- ans, B. t. var. tenebrionis – imagoes and larvae of beetles, B. t. var. japonensis – beetles which live in the soil (Fathy, 2012). B. t. var. kurstaki is able to control Acari actively compared to other subspe- cies (Hassanain et al., 1997). Usually, B. thuringiensis does not have a negative effect on parasitoids. Accordingly, Venturia canescens (Gravenhorst, 1829) contributes to distribution of this agent among E. kuehniella. However, B. thuringiensis causes pathogenic effect on a carrier parasitoid of Bracon brevicornis (Wesmael) (Schöller, 1998). Such products based on B. thuringiensis as DiPel® 2X DF, VectoBac® WDG and HD703 are available. Over the recent years, in Ukraine, the following microbiological preparations were studied and brought into production: Fitosporin, Hetomik, Bitoksibatsylin, Lepidotsyd, Bakteredentsyn and others. An effective agent of control of larvae of Culex spp. and Anopheles spp. mosquitoes is B. sphaeri- cus (Robert et al., 1997). Streptomyces avermitilis bacteria produce avermectin toxins which are highly efficient against insects and oth- er invertebrates (Pirali-Kheirabadi, 2012). There are data on infestation of R. ferrugineus with Pseudomonas aeruginosa ((Schroeter) Migula, 1900), a pathogenic bacteria which causes death of the insect in 8 days (Banerjee & Dangar, 1995). Symondson & Liddell (1996) reports that Wolbachia bacteria can have a negative effect on agents of natural control. It was noted that small and thin cocoons occur on the parasitoid Microctonus ae- thiopoides (Loan, 1975) which parasitizes Hypera postica (Gyllen- hal, 1813) infested with the bacteria, which causes death of 90% of the pupae and prevents adults reproducing. Therefore, Wolbachia 152 Chapter 3. Biological control of beetle pests of stored grain and field crops change the physiological conditions of the snout beetle, making it unsuitable for the parasite and providing the snout beetle protection.

Viruses Several thousands of pathogenic viruses have been described, and the representatives of Entomopoxviridae, Reoviridae (Cypovi- ruses) and Baculoviridae have been successfully used as agents of biological control (Lacey & Kaya, 2007). The infection occurs after the virus enters into the organism with food, and the peculiarities of replication varies depending on family. The most commonly used group of viruses is Baculoviridae, due to their specificity and safety for vertebrates. The Baculoviridae family con- tains four genera: Alphabaculovirus (lepidopteran-specific nucleo poly- hedroviruses (NPVs)), Betabaculovirus (lepidopteran-specific GVs), Gammabaculovirus (hymenopteran-specific NPVs) and Deltabaculovi- rus (dipteran-specific NPVs) (Jehle et al., 2006; Szewczyk et al., 2011). Currently, 16 baculovirus-based biopesticides are available, mostly for the control of lepidopterans. For example, the baculovi- rus of the codling moth (Cydia pomonella Granulovirus) is effective against their caterpillars, Gemstar LC is a NPV of Heliothis/Helicov- erpa spp. such as corn earworm (H. zea (Boddie, 1850)) and cot- ton bollworm (H. armigera (Hübner, 1805)), Spod-X LC is a NPV of Spodoptera spp. such as small mottled willow moth (S. exigua (Hübner, 1808)), CYD-X and Virosoft CP4 – C. pomonella Granu- lovirus and CLVLC is a NPVof celery looper (Anagrapha falcipera (Kirby, 1837)) (Fathy, 2012). Gopinadhan et al. (1990) found a highly efficient cytoplasmic polyhedrovirus (CPV) which affects R. ferrugineus at all stages of development.

Protists Entomopathogenic protozoa are studied insufficiently. Such protozoa as Nosema, Theileria and Babesia are pathogenic for Acari and other anthropods. There are no examples of effective biological control using protists, though such protozoa as Onchocerca volvulus V. O. Martynov, V. V. Brygadyrenko 153

(Bickel, 1982) and Plasmodium spp. are able to indirectly control intermediary hosts. Theratromyxa weberi, predatory soil amoeba, swallowed by nematodes, eats the host in 24 hours as they travel through their body. Presumably, such amoebas have limited abili- ties for biocontrol, as they are significantly slower than nematodes. Other protists, such as Nosema locustae (Canning, 1953), are patho- genic for katydids and crickets, Nosema pyrausta – for the European corn borer (Ostrinia nubilalis (Hübner, 1796)), and Vairimorpha ne- catrix – for caterpillars of many lepidopterans (Olson et al., 2006). Assessment of Microsporidia as agents of biological control of Prostephanus truncatus (Horn, 1878) was conducted by Henning- Helbig (1994). Gregarines are an interesting object of studies. This group of parasitic protozoa is studied insufficiently and they presumably oc- cur in practically all species of insects. There are no data on usage of gregarines as agents of biological control. However, it was deter- mined that gregarines can significantly decrease the efficiency of biological control by parasitizing the agent. Accordingly, Yaman et al. (2012) found gregarines of the Mattesia (Naville, 1930) genus in Rhizophagus grandis (Gyllenhal, 1827), a predatory beetle of the Mo- notomidae family, an agent of the control of great spruce bark beetle (Dendroctonus micans (Kugelann, 1794)). This gregarine also para- sitizes victims which can be a source of invasion, though it causes no notable effect on its vital activity. At the same time, it was rather pathogenic for Rh. grandis. Mattesia parasitize the fat body of the host, in which merogony and sporogony occurs, leading to lysis of the tissues. This contributes to increase in life expectancy of the host and prolongation of the breeding period, leading to decrease in its potential of this agent for biological control. Lord (2003, 2006) studied the pathogenicity of Mattesia ory- zaephili neogregarines which infest some pests of grain stores, in- cluding O. surinamensis and C. ferrugineus, and also their parasit- oids such as C. tarsalis and C. waterstoni Gahan. Among wasps, the pathogen is distributed only among females during feeding on the host. Life expectancy of an infested female of C. tarsalis after contact 154 Chapter 3. Biological control of beetle pests of stored grain and field crops with highly infested O. surinamensis is 20 days, which is two times lower compared to a healthy individual. Infested C. waterstoni fe- males survive 36 days instead of 46. M. oryzaephili can be transmit- ted through corpses, faeces of wasps and egg laying.

Nematodes Entomopathogenic nematodes are another variant of biologi- cal control, which can be used in combination with parasitoids and other strategies of biological control. They have been successfully used for regulating a large number of pests, including ground pests and wood-destroying pests (Canhilal & Carner, 2006; Mwaitulo et al., 2011; Kega et al., 2013). For distribution of the nematodes, there are used pulverizing devices and solutions of the agents which contain adjuvants and humidifiers – surface-active substances, oils and gels, which signifi- cantly increase the efficiency of the pest control, because nematodes survive only few hours on leaves due to their quick drying out and sensitivity to ultraviolet radiation (Arthurs et al., 2016). This indi- cates that entomopathogenic nematodes can be efficient against a broader range of insect pests, when combined with chemical ad- ditives prolonging their survival above ground (Baur et al., 1997; Schroer et al., 2005; Ditoet al., 2016; Noosidum et al., 2016). Nematodes of the Steinernema and Heterorhabditis genera are effective agents of control of a broad range of insect pests, in- cluding drain flies, the German cockroach (Blattella germanica (Linnaeus, 1767)), the cat flea (Ctenocephalides felis (Bouché, 1835)), Pennisetia marginata (Harris, 1839), leaf miners, mole crickets, flea beetles, plume moths, dark-winged fungus gnats, pyralid moths, owlet moths and others (Smart, 1995; Lacey & Kaya, 2007). Nematodes enter into the host organism with food, through the cuticle and spiracles. They contain specific symbiotic bacteria which cause death of the host and contribute to its decomposition, providing food to nematodes. Young nematodes consume a mix- ture of bacteria and liquefied tissue of insects, develop and breed inside the host. When the resources of nutrients are exhausted, V. O. Martynov, V. V. Brygadyrenko 155 the new generation emerges outside in search of new hosts (Grewal et al., 2005). For Steinernema, the presence of Xenorhab- dus spp. bacteria is typical, for Heterorhabditis – Photorhabdus spp. (Fathy, 2012). Entomopathogenic nematodes usually cause a high level of mortality of experimental insects. According to Caroli et al. (1996), Steinernema sp. caused death of 100% of Galleria mellonella (Linnaeus, 1758), Spodoptera exigua (Hübner, 1808) and Agrotis ip- silon (Hufnagel, 1766). For Heterorhabditis sp., lower mortality has been observed. Less sensitive to nematodes were Ostrinia nubilalis (Hübner, 1796) and Tenebrio molitor (Linnaeus, 1758), mortality of which equaled 73–100% for O. nubilalis and 20–100% for T. molitor. Also, the tempi of nematodes’ entry into the organism of T. molitor significantly varied depending on the species. The highest value was observed for S. glaseri and S. feltiae, the lowest for Heterorhabditis sp. (Caroli et al., 1996). An efficient agent of control is S. carpocapsae, an entomopatho- genic nematode which parasitizes and sterilizes Musca autumnalis (De Geer, 1776). Portman et al. (2016) studied the virulence of several species of entomopathogenic nematodes for Cephus cinctus (Norton, 1872), a wheat pest. It was determined that the most effective species is H. indi- ca (Poinar et al., 1992), because the mortality of the pest equaled 100% after two days. High concentrations of S. feltiae (200 and 500 IJ/larva) also caused 100% mortality after three days. The least harmful species studied was S. kraussei; the maximum mortality it caused was 60%. The obtained results indicate that H. indica and S. feltiae can be ef- ficient agents of biological control of C. cinctus. Entomopathogenic nematodes are in widespread commercial use against insects. Currently, S. carpocapsae, S. riobraus, S. feltiae, S. glaseri, H. bacteriophora, H. megidis and H. marelatus are avail- able, and also some nematodic products, Spear® and Saf T-Shield® (Kaya & Koppenhöfer, 1996). S. carpocapsae and S. glaseri are ef- fective against mosquitoes, fleas and Acari, and also nematodes of Teladorsagia spp. and Trichostrongylus spp. (Henderson et al., 1995; Zhioua et al., 1995; Samish et al., 1996; Kocan et al., 1998). 156 Chapter 3. Biological control of beetle pests of stored grain and field crops

Nematodes of the Aphelenchida order have a broad range of rela- tions with many species of Coleoptera (Hunt, 1993). They can range from simple commensalism to strictly parasitic relations. A well known example is the relationship between Bursaphelenchus cocophilus ((Cobb) Goodey) and Rhynchophorus palmarum (Linnaeus, 1758) in Central and South America. Rhynchophorus sp. were also observed to have two species of nematodes of Praecocilenchus. P. rhaphidiophorus (Poinar) parasitizes R. bilineatus (Montrouzier, 1857), and P. ferruginophorus (Rao & Reddy) parasitizes R. ferrugineus. Nematodes of both species occur in the trachea, intestines and the fat body of infested larvae, and also the womb and haemocoel of infested adults. The distribution of the nematodes occurs through oviposition or the intestines. It was deter- mined that nematodes reduce the sizes of ovaries and egg production, and decrease life expectancy of snout beetles (Murphy & Briscoe, 1999). Ramos-Rodriguez et al. (2007) studied the efficiency of S. riobrave, an entomopathogenic nematode, against the storage pests T. castane- um and P. interunctella. Usage of the pathogen reduced the survivabil- ity of T. castaneum at all stages of its development from 78% to 27%. The temperature (25 and 30 °C) and relative moisture (40–100%) caused no significant effect on the efficiency ofS. riobrave in that ex- periment. During the usage of the agent in field conditions onT. cas- taneum and P. interunctella, the total survivability of the first equalled 42% and the total survivability of the second was 27% compared to the control. The larval stages of both species of insects were most sensitive to S. riobrave, the death rate equaling 99% and 80% for P. interunctella and T. castaneum respectively. S. riobrave is a promising agent of bio- logical control for insect pests of grain warehouses. As biocontrol agents, entomopathogenic nematodes are safe, cause no harm to humans, vertebrates and plants.

Biological control of the main pests of wheat

Curculionidae The studies of biological control of S. oryzae were conducted by Riudavets & Lucas (2000). The natural enemies of these pests are V. O. Martynov, V. V. Brygadyrenko 157 parasitic wasps of Anisopteromalus calandrae (Howard, 1881) and Lariophagus distinguendus (Förster, 1841), which infest the snout beetle. Their potential against S. zeamais and S. oryzae was demon- strated in a number of studies (Arbogast & Mullen, 1990; Wen et al., 1994; Ryoo et al., 1996). Biological control with usage of these parasites leads to de- crease in the number of progeny of S. oryzae by 57%. The efficiency of the control can be increased up to 90% by grain polishing. The development period of L. differentendus on S. oryzae is 20 days at 25 °C (Ryo et al., 1991), and of A. calandrae on S. zeamais – 17 days (Smith, 1992). The success of the control depends on several fac- tors: grain polishing, which contributes to reducing the density of the pests; grain type which can inhibit the development of the stout beetle; integrity of laid eggs, which helps the parasite to identify its host. Also, the parasites exhibit great preference for larval stages of the fourth age, which indirectly affects the identification of the host as well (Smith, 1993; Ryoo et al., 1996). Smith (1994) studied and modeled the biological control of S. zeamais using A. calandrae, a parasitoid. It was determined that the long period of life and long period of laying eggs of S. zeamais hinders the control of its population by the parasitoid, though it is able to reduce the tempi of the snout beetle’s population growth. The imitation of the effect of releasing different numbers of A. calandrae demonstrated that there is no need to release over 10 times more parasitoids than the target species, and that the proportion 1: 1 is really efficient. The period between the first and the second genera- tions of parasitoids allows the populations of snout beetle larvae to avoid parasitism, which causes the subsequent surge in the number of the pest after two weeks. Therefore, effective control requires min- imum breaks in the continuity of parasitism. For the high efficiency, the optimum temporal interval between the successive releases of the parasitoid should not exceed 9 days at 25 °C. Throne & Lord (2004) provide data on the biological control of sawtoothed grain beetle (O. surinamensis) using an entomopatho- genic fungus. The usage of the fungus at 300 mg conidia/kg of wheat 158 Chapter 3. Biological control of beetle pests of stored grain and field crops

(ppm) caused death to 72% of the adult individuals (Lord, 2001). The processing in 317 ppm led to death of 91% of larvae and pupae (Searle & Doberski, 1984). It was demonstrated that B. bassiana effi- ciently controls other pests, including S. zeamais (Adane et al., 1996, Hidalgo et al., 1998), S. oryzae (DalBello et al., 2001, Padin et al., 2002), P. truncates (Bourassa et al., 2001; Meikle et al., 2001), A. ob- tectus (Ferron, 1977), R. dominica, C. ferrugineus and T. castaneum (Rice & Cogburn, 1999; Lord, 2001). The experiments were conducted in the conditions favourable for O. surinamensis at 30 ± 1 °C and 76% relative moisture. Searle and Doberski obtained 91% decrease in larvae and pupae in the con- ditions of the culture at 20 °C and 100 relative moisture. Optimum temperature range for the growth of the most isolates of B. bassiana is 25–28 °C (Fargues et al., 1997). Sheeba et al. (2001) tested B. bassiana against the rice weevil (S. oryzae). It was determined that the strain used in study in the dosage of 7,6 log conidia/ml exhibits high efficiency at 28 ± 2 °C and relative moisture 70 ± 5%, leading to 76% mortality after 25 days, and reduction in the production of offspring by 86%. These results support the results obtained by Searle & Doberski (1984), where 100% mortality was recorded 20 days after the inoculation at 100% relative moisture and 25 °C. Trdan et al. (2005) studied the efficiency of four species of ento- mopathogenic nematodes (S. feltiae, S. carpocapsae, H. bacteriopho- ra, H. megidis) for the control of S. granarius. A suspension of nema- todes in 5,000, 10,000 and 20,000 IJs/ml concentrations was used at temperatures of 15, 20 and 25 °C over a week. It was determined that the least effective was H. megidis, whereas the remaining species had no significant differences in mortality rate they caused. Mortality of the beetles was statistically significantly higher at 20 and 25 °C. It has been proven that the impact of the suspension concentration was less important for the biological activity of the studied agents. Suspension in 20,000 IJs/ml proportion was most effective for the control of S. granarius (63%). No statistically significant differ- ences between the other concentrations were found, though they V. O. Martynov, V. V. Brygadyrenko 159 were efficient in comparison with the control processing. Usage of the highest concentration (20.000 IJs/ml) of suspension was not jus- tified, because higher costs for purchasing biological agents do not provide significantly higher efficiency compared to the two other concentrations. S. feltiae, S. carpocapsae and H. bacteriophora were the most efficient against the pests, accordingly, all three species can be recommended as agents of biological control. Laznik et al. (2010) studied the effectiveness of several strains of S. feltiae against S. oryzae. The results demonstrated that the studied strains were most pathogenic at 25 °C and at highest concentration of nematode suspension (2,000 IJ/imagoes), mortality equalled 42– 72%. Minimum pathogenicity from 6% to 11% was observed at low concentrations of suspension and temperature of 30 °C. The lowest value of LC50 (1,165 IJs/imagoes) was obtained after 8 day exposure at 25 °C, whereas the highest (2,533 IJs/imagoes) – at 30 °C. Low efficiency of suspensions of all nematode strains at 30 °C, not ex- ceeding 20%, can be explained by the inappropriateness of the tem- perature intervals for most species of entomopathogenic nematodes, which equals 20–26 °C. S. oryzae reproduces more actively at high temperatures from 25 to 35 °C. According to the results obtained, the efficiency of S. feltiae depends on the temperature and level of concentration. There is a number of studies on the efficiency of S. feltiae against other storage pests, such as S. granarius (Trdan et al., 2006), T. con- fusum (Athanassiou et al., 2007), T. molitor, T. castaneum, T. varia- bile, S. oryzae (Ramos-Rodriguez et al., 2006) and O. surinamensis (Svendsen & Steenberg, 2000; Schöller et al., 2006; Tóth, 2006).

Tenebrionidae Rahman et al. (2009) studied the influence of X. flavipes on several species of pest insects. X. flavipes is a cosmopolite predator which affects such storage pests as T. castaneum, T. confusum, Cryp- tolestes pusillus (Schönherr, 1817), R. dominica and T. granarium (Ahmed, 1991). Arbogast (1976) reports that the victims include 13 species of insects from other orders. 160 Chapter 3. Biological control of beetle pests of stored grain and field crops

It was determined that the efficiency of X. flavipes depends on the sizes and density of the victims. In an empty medium, the predator killed a low number of large larvae of T. confusum and T. castaneum, compared to the other species of prey and living forms. This is related to the fact that the larvae can actively avoid the predator’s attacks, thus resisting their suppression and elimination. However, in wheat, this advantage disappeared, significantly increasing the effectiveness of the control. Also, it was found that X. flavipes prefers to prey on C. pusil- lus, compared to T. confusum and T. castaneum. Also, the efficiency of the control depends on the sex of the predator, for the females kill far more victims than the males. It should be mentioned that using X. flavipes in programmes of biological pest control in grain warehouses requires operational studies and surveys in field conditions. Wakefield (2006) studied the adhesion and germination of the conidia of B. bassiana on O. surinamensis and T. confusum. Con- centrations of 1х108 conidia/ml were used in the study. It was deter- mined that the attachment of entomopathogenic fungi to the cuticle of insects is passive and non-specific (Boucias et al., 1988). Adhesion of the spores occurs through hydrophobic interactions (Jeffs et al., 1999). The highest mortality was recorded for O. surinamensis. For T. confusum, this indicator was significantly lower. Mortality of the control group equaled less than 5%. A high death rate was recorded for O. surinamensis, but for S. granarius, significantly lower death rates were observed, and even lower death rates for T. confusum. The death rate in the control equaled less than 5% for all three spe- cies. Few differences between the efficiency of two different isolates of B. bassiana were observed for each particular species. It was de- termined that the number of conidia and their germination on O. surinamensis are at significantly higher level than onT. confusum. This is related to the fact that O. surinamensis have much more se- tae and have a higher level of moisture on the surface of the cuticle, providing favourable conditions for germination of conidia. It was demonstrated that cuticular hydrocarbon can contribute to the ger- mination of conidia or inhibit it. Also, Tribolium species produce protective quinones which, perhaps, can inhibit the germination. V. O. Martynov, V. V. Brygadyrenko 161

The potential of B. bassiana as an agent of biological control was studied by Khashaveh et al. (2011). They performed an experiment on adult individuals of T. castaneum, S. granarius and O. surinamen- sis, using 0, 250, 500, 750 and 1000 mg/kg concentrations over 5, 10 and 15 days at 24 ± 2 °C and 50 ± 5% moisture. In all experi- ments, the death rate increased as the dose and duration of exposure were increased. The highest values were observed after exposure to 1000 mg/kg concentration over 15 days and equalled 88%, 78% and 65% for S. granarius, O. surinamensis and T. castaneum respectively. Also, as the concentration increased, the production of offspring de- creased. Michalaki et al. (2016) studied the effectiveness of M. anisopliae for biological control of T. confusum. Three dosages were tested – 8 · 106, 8 · 108 and 8 · 1010 conidia/kg of wheat or flour respectively. It was determined that at maximum concentration, the effectiveness of this form of control equaled 75%. Arthur (2000) studied the impact of diatomaceous earth on T. castaneum and T. confusum. The death rate of both species after the initial impact was minimum at 22 °C, but increased as the tem- perature and the interval of exposure increased, and decreased as the relative humidity increased. The highest mortality (100%) for both species was observed at 32 °C and 40% relative humidity. White & Loschiavo (1989) placed T. confusum in diatomaceous earth (0.72 mg/cm2) for 6 h, at 25 °C and 50% relative humidity, which led to absolute mortality after 3 days. McLaughllin (1994) placed S. granarius and S. oryzae, for 30 h at 25 °C and 56% RH in alumin- ium pots processed with diamaceous earth in the amount of 2 g/m2 and assessed the mortality during 6 days. In general, Tribolium spp. seem less sensitive to the inert dust and diatomaceous earth than other species of beetle pests of the stored grain (Korunic, 1998).

Competition in biological control Competition is an important element of biological control, which covers both target species of pests and the agents of control. Intraspecies and interspecies interactions include competition for 162 Chapter 3. Biological control of beetle pests of stored grain and field crops general resources such as food and space, and also predation and cannibalism (Park, 1962; Park et al., 1965, Stevens & Mertz, 1985). Introduction of agents of biological control significantly affects the competition of target species, causing changes in the structure of the community. A classic example of change in the outcome of com- petition between two species as a result of pathogenic invasion is the experimental study conducted by Park (1948) and Anderson et al. (1986). The study analyzed the competition between two species of flour beetle (T. confusum and T. castaneum) under the impact of Adelina tribolii (Bhatia, 1937), a species of Apicomplexa. In the ab- sence of the parasite in a mixed population, the stable domination of T. confusum was observed, but after the pathogen was introduced, the domination disappeared. This is related to the fact that the para- site was pathogenic for the dominating competitor. Accordingly, the pathogen reduces the competitiveness of T. confusum, allowing a weak competitor to remain (Hudson, 1998). The impact of the rat tapeworm (Hymenolepis diminuta (Rudol- phi, 1819)) on the competition between two species of Tribolium was studied by Yan et al., (1998). Cestode parasitism causes a nega- tive impact on the host`s reproductive success which affects the co- efficient of the host’s competition (Yan 1997). T. castaneum is usually a dominating competitor of T. confusum, for it is usually the most active among the species (Park, 1948, 1957; Leslie et al., 1968). Ac- cording to Craig (1986), while living together, adult species of T. cas- taneum mostly feed on eggs of T. confusum, because they are large. Prediction of the results of competition between the two species is complicated due to the impact of demographic stochastic processes (fluctuations in birth and death rates) and genetic stochastic pro- cesses (genetic drift with low number of founders) (Park, 1948; Park et al., 1964; Dawson & Lerner, 1966; Dawson, 1970; Mertz et al., 1976; Goodnight & Craig, 1996). T. castaneum is more vulnerable than T. confusum to infesta- tion with H. diminuta (Yan & Norman, 1995). Therefore, the prob- ability and extent of the invasion for T. castaneum is much high- er. Parasitic invasion leads to decrease in the fertility of females, V. O. Martynov, V. V. Brygadyrenko 163 predominance of male and increase in cannibalism of eggs by the adults (Yan & Stevens, 1995). Accordingly, T. castaneum should be at a disadvantage in competition with T. confusum in the presence of the parasite. The results of the research demonstrate that the invasion of the cestode affected the competition between the two species of Tribo- lium, affecting the average time of death and population density. The presence of the parasite significantly increased the competitive- ness of T. castaneum, especially in the case of high initial density of T. confusum. Mortality of T. confusum was increased by the parasite, therefore the species loses the competition with higher probability. The parasitism significantly reduced the average size of the popula- tion of T. confusum in the culture of the two species. This indicates that the invasion of the tapeworm gave T. castaneum an advantage in the competition with T. confusum. In this parasite-host-competitor system, T. castaneum is more sensitive to cestodes and has more clearly manifested pathogenesis than T. confusum, therefore having an advantage in competition. However, changes in the behavior, which were induced by the para- site, can give T. castaneum an advantage. Alabi et al. (2008) studied cannibalism and predation among seven species of Tribolium. The most usual type of cannibalism is consumption of passive forms (eggs and pupae) by the active forms (imagoes and larvae). Cannibalism of eggs is the most probable, for the eggs are least mobile, do not have highly developed protection, and at the same time contain a full set of nutrients in a form conve- nient for metabolism. One of highly developed forms of cannibalism is the production of trophic eggs, the aim of which is to be food for progeny, which is one of the forms of parental care (Crespi, 1992; Perry & Roitberg, 2006). Though pupae are also relatively immobile, they are more developed, sclerotized and can protect themselves (Eisner & Eisner, 1992). The highest tempi of egg cannibalsim was demonstrated by the larvae – they consumed 10 times more eggs than the imagoes of T. confusum and T. destructor. Among the adults of T. confusum 164 Chapter 3. Biological control of beetle pests of stored grain and field crops and T. brevicornis, they in total consumed 40, while by contrast T. freemani, consumed only a single egg. Imagoes of T. brevicornis, T. confusum and T. destructor demonstrate a greater tendency towards cannibalism than their larvae stages, whereas one can say exact the opposite, regarding T. anaphe, T. freemani and T. madens. Pupa can- nibalism among the larvae is relatively low, with a maximum of 9 for T. anaphe. Among the imagoes, T. castaneum, T. confusum and T. destructor consumed 20 or more pupae, which is 4–5 times more than their larval stages, which was not manifested in other species. Regarding predation on T. castaneum, T. anaphe and T. brevicornis consumed 20 or 30 eggs respectively, which is 2 and 3 times more than the larvae of other species. The most voracious among the spe- cies were T. confusum and T. destructor, which consumed 54 and 28 eggs respectively. Pupae of T. castaneum were attacked mostly by the imagoes, the biggest consumer of which was T. destructor, con- suming 34 pupae on average, whereas other species consumed less than ten. Research on predation on T. confusum showed that larvae of T. anaphe consumed 47 eggs on average, which is over double the consumption by T. brevicornis and T. madens. Among the imagoes, T. castaneum was the greatest predator both on eggs and pupae of T. confusum. When pupae of T. brevicornis were offered as victims, they were not consumed by any species, and predation was not high- er than 5% for the larvae and 10% for the imagoes. According to results of the research, three groups of cannibals and predator species were distinguished in relation to the extent of cannibalism and predation. The first group was represented by T. castaneum, T. confusum and T. destructor, the adults of which are more voracious in cannibalism and predation than the larvae. The second group, where the larvae tended to be more active than the imagoes, consisted of T. anaphe, T. freemani and T. madens. The last group included only T. brevicornis, which is explained by variability in voracity for different types of prey among the larvae and adults of this species. Interspecies competition between natural enemies of a particular host can be an important factor in using biological control, because V. O. Martynov, V. V. Brygadyrenko 165 it influences the size, structure and stability of the agents’ communi- ties (Ehler, 1978; Morris et al., 1988; Hagvar, 1989; van Alebeek et al., 1993; Chow & Mackauer, 1986). Interspecies competition between parasitoids can reduce the level of total parasitism and regulate the populations of pests (Turnbull & Chant, 1961; Watt, 1965; Pschorn- Walcher, 1977; Ehler & Hall, 1982). However, a minimization of the competition between the parasitoids may occur as a result of differ- entiation of the niche and interspecies specificity to the host, which leads to a significant inhibiting effect (DeBach, 1966; Huffaker et al., 1976; Keller, 1984). Parasitoids of the Pteromalidae family, A. calandrae and T. el- egans attack immature stages of several insect pests of storages. The potential for inhibiting the rice weevil (S. oryzae) in wheat by the wasps A. calandrae and T. elegans was demonstrated in a number of works (Press et al., 1984; Cline et al., 1985; Press, 1992). Competition between A. calandrae and T. elegans was studied by Wen & Brower (1995). On combined release of the parasitoids, the domination of A. calandrae was observed, which was found three times more often than T. elegans, which coincides with the re- ports of Wen et al. (1994). However, the frequency of occurrence of both T. elegans and A. calandrae was significantly reduced when both were present compared to when they were released separately. The inhibition of the populations by competition can be a result of negative interactions between immature stages or caused by some activities of adult groups which affect the survivability of the larvae (Chow & Mackauer, 1986). The results of the experiment demonstrate the presence of a sig- nificant direct competition between the two parasitoids, which leads to significant decrease of both species. It should be mentioned that suppression of the populations of the rice weevil using a combina- tion of the two species has the same effect as using only A. calandrae.

Conclusion Currently, biological control is one of the most promising and safe methods against pests. A large number of effective control agents 166 Chapter 3. Biological control of beetle pests of stored grain and field crops has been found, including predators, parasites and pathogens. Bio- logical control is one of the few methods against pests which has a stable pattern and which requires no activities after the release and distribution of the agents. In long term perspective, biological control has many advantages, such as safety for the environment, economic feasibility, ease in use, duration of the effect, absence of development of resistance in the pest. The main problem of biocontrol is the impact of agents on non- target species. On introduction of the control agent, the main task of the control is determination of the specificity of the agent to the host, because the main problem is the impact of agents on non-target species, which leads to changes in the communities. Before released into the environment, a potential agent of biological control should undergo a broad range of tests and quarantine. In selection of agents of biological control of a certain pest, one should take into account a number of factors such as popula- tion index, threshold effect, pest’s localization, species composition and stages of development (Burkholder & Faustini, 1991). However, there is a number of problems in the implementation of biological control including their potential effect on the natural diversity and unwillingness of farmers to give up using chemical methods (Heong & Escalada, 1998; Sun & Peng, 2007). Nevertheless, the methods of biological control continue to develop, adopting new technolo- gies, enlarging the usage of natural enemies, finding new agents of control and modifying old agents, for more efficient control of pests (Goswami et al., 2010; Ma et al., 2015). V. O. Martynov, V. V. Brygadyrenko 167

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