Chief EditorPradeep K. Sharma
Print ISSN 0253-1496
Online ISSN 0976-0741
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Biological Control Methods for Agricultural Mites: A Review
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First Online 27-10-2022|
Mites are a diverse group of insects that have been destroying and devastating the agricultural industry for many decades. They are categorized in the class Arachnida, subclass Acari and families Tenuipalpidae, Tarsonemidae, Tetranychidae and Eriophyidae (Baker and Wharton, 1958). They also occupy a wide range of habitats and a wide range of hosts including vegetable and ornamental crops (Al-Atawi, 2011; Boczek and Kropczynska, 1964). Mites cause damage by piercing plant cells with their mouthparts and sucking the plant juices (Bensoussan et al., 2016). Common symptoms of mite infection include yellow/ whitish spots on the leaf tissues and the formation of small webs (Jeppson et al., 1975).
Effects of these pests can be seen in industries such as soybean, which was devastated between 2005-2006 in the state Rio Grande do Sul, Brazil, by spider mites that attacked areas with and without chemical control and resulted in losses of 270 kg ha on average in soybean production (Arnemann et al., 2006). Symptoms of this infestation included white and yellow spots on the leaf surface while severe effects included premature leaflets, accelerated maturation and reduced grain yield (Dehghan et al., 2009). In 2009, the coconut industry in Brazil also suffered more than 70% losses in production due to the effects of the red palm mite (RPM) which were already dispersed in Martinique, Antilles islands and Trinidad (Rodrigues et al., 2020). Further studies on eggplant and tomato crops by Maina et al. (2014) on spider mites around the Lake Chad Shore Area of Nigeria showed that farmers experienced more than 50% yield losses href="#maina_2014">(Maina et al., 2014). Renkema et al., (2017) reported the grievances of strawberry growers due to the attack of Broad mites during the 2015-2016 growing season and its increase in 2016-2017. Symptoms of the mite infestation include stunted plants, curling of young leaves, darkening of leaf petioles, yellowing, etc. Plants showing such symptoms were recorded in five strawberry fields with <1% of each field area affected. Yong-Heon (2002) investigated the control of two-spotted spider mites (TSSM) destroying strawberry crops in Korea. The excessive use of pesticides to control these mites resulted in the death of untargeted species (e.g., pollinating bees) and the development of strains of TSSM that were highly resistant to all forms of pesticides. Furthermore, these studies found that the control of the pests was almost impossible because of their high fecundity rate, rapid development and rate of development of resistance to miticide (Yong-Heon, 2002).
Pest management is dominated by the use of pesticides which in the long term can cause severe environmental effects, public health concerns and insecticide resistance; hence the need for biological control (Tudi et al., 2021; Gangwar, 2017). These chemicals are detrimental to the environment as they pollute the air, water and soils, diminish biodiversity, reduce nitrogen fixation, etc. (Mahmood, 2016). Over 98% of sprayed insecticides and 95% of herbicides reach non-target species (Miller, 2004; Follet and Duan, 2000; Robinson et al., 1999). Toxic residues from these pesticides may remain in the environment for long periods; continued exposure is associated with immune system dysfunction, neurological dysfunction, reproductive system defects and blood disorders (Miraglia et al., 2009; Baker and Wilkinson, 1990). Bio-accumulation and bio-magnification may cause severe effects on human health as organisms at the top of the food chain are most affected (Ali et al., 2021; Lee et al., 2000).
Biological control is an environmentally friendly, sustainable and effective method of managing pests (Routray et al., 2016; Bale et al., 2008). This method is inexpensive, does not affect non-target species, environmentally friendly and involves a safe application and bio-control agents that can enhance root and plant growth by encouraging beneficial soil microflora (Sharma, 2013; Waage and Greathead, 1988). Bio-control agents include predators, parasitoids, pathogens and competitors (Kamal et al., 2015). It typically involves active human management. The history of biological control is divided into 3 periods; (1) preliminary efforts when living agents were released haphazardly with no scientific approach (2) the intermediate period (3) the modern period where there is now careful planning and evaluation of natural enemies (Polanczyk and Pratissoli, 2009; Van Driesche et al., 2008). In this paper, we analyze and synthesize results from previous studies on the biological control of mites in the agricultural field. We specifically examine different methods of biological control and their effectiveness in regulating agricultural mite populations.
The broad survey of the literature indicates that biological control can be successful in eradicating agricultural mite populations. Over the years, there have been major developments in biological control as scientists work to find a balance between food production and conserving biodiversity within the environment for present and future generations (Ghosh, 2011). The excessive use of agrochemicals/ pesticides can have serious implications on human health and the environment (Mahmood, 2016; Baker and Wilkinson, 1990); hence most published articles emphasized the need for biological control as it is a step toward a ‘greener’ world (Sheppard et al., 2019; Bale et al., 2008). Successful bio-control programs require adequate knowledge of population dynamics of pest/predators, endemic species, seasonality of species, generation time and the ability to be mass-reared, among other areas of knowledge surrounding pest biology and ecology. Analysis of the publications identified the following key concepts: (i) predators, (ii) pathogens and (iii) parasitoids as biological control agents. Further, Hoy (1986) outlined the criteria for successful predator release as the potential of the agent to manifest after release, survive spray routines and manipulate target pest populations. Al-Atawi (2011) identified the four families of phytophagous mites that cause economic damage to crops: Tetranychidae Tenuipalpidae, Tarsonemidae and Eriophyidae as shown in Table 1.
In Mexico, the citrus rust mite, Phyllocoptruta oleivora Ashmead was a major pest of citrus fruits and caused decreased production in the industry (href="#canoye-eligio_2017">Vanoye-Eligio et al., 2017). href="#acosta-robles_2019">Acosta-Robles et al., (2019) evaluated the effect of concentrations of Beauveria bassiana, Metarhizium anisopliae and Isaria fumosorosea on mortality and growth rate of P. oleivora populations under greenhouse conditions. The results indicated that B. bassiana and M. anisopliae were efficient in controlling the citrus rust mite populations under greenhouse conditions as the growth rate of the mites under these pathogen treatments was lower than that of the control. In both treatments, the higher concentrations were inversely proportional to the mortality of the mites. However, it was evident that I. fumosorosea controlled the population at moderate levels as the growth rate of the citrus mites were still below that of the control but higher than that of B. bassiana and M. anisopliae. In other words, I. fumosorosea was not as effective as B. bassiana and M.anisopliae (href="#acosta-robles_2019">Acosta-Robles et al., 2019). Parveen et al., (2021) in an investigation to screen fungal isolates of B. bassiana, M. anisopliae and Lecanicillium lecanii against TSSM and broad mites found that both agricultural mites were susceptible to all fungal isolates tested. However, isolates of B. bassiana showed the highest mortality in TSSM and M. anisopliae showed the same in broad mites. Despite the varying degree of virulence, it was evident that with increased concentrations of fungal isolates there was an increase in the mortality rates of both mites href="#acosta-robles_2019">(Acosta-Robles et al., 2019). Table 2 further highlights various fungi reported to control agricultural mites.
Locusts and grasshoppers are the most dominant insect pest in dry grasslands and desert areas; often forming large swarms while feeding on crops resulting in massive economic losses and are therefore treated as a national priority (Lecoq and Cease, 2022; Lomer et al., 2001; Bullen, 1966). They attack plants such as cotton, corn, wheat and barley (Wright, 1986). Locust outbreaks were recorded in Ethiopia in 1958 amounting to £4 million in losses; later in 1962, Khuzistan also recorded £150,000 in losses and India and Pakistan suffered up to £600,000 in economic damage (Bullen, 1966). To rapidly eradicate these devastating pests chemical control techniques were implemented in areas prone to locusts and grasshopper infestation, as their control is critical to ensuring food security (Zhang et al., 2019; Lomer et al., 2001). However, with increasing awareness of public health and the negative environmental impacts caused by the excessive use of pesticides, there has been an active effort to implement bio-control techniques. Bio-pesticides from plants and micro-organisms proved to be an excellent alternative as it has high specificity, non-toxic to humans and animals and have little to no negative impact on the environment (Kooyman, 2003). Metarhizium flavoviride in water-based formulations was among the first pathogen to be tested against desert locusts in both laboratory and field conditions (Githae and Khuria, 2021). To improve its efficiency, treatments were made in oil formulations. Under laboratory conditions, daily food consumption and flight activity were reduced (Seyoum 1994; Moore 1992).
On the other hand, in field experiments, Langewald et al., (1997) saw reduced numbers in swarms and mortality within 10-11 days in open fields and 6-10 days in cages. However, M. flavoviride in oil formulations displayed negative impacts on non-target organisms such as bees leading to the use of another entomopathogenic fungus, M. anisopliae (Ball et al., 1994; Zimmerman, 1993). This fungus kills approximately 70-90% of locusts in about 14-20 days with little to no effect on non-target organisms (Lomer et al., 2001). Mohamed et al., (2011) conducted a study to investigate the combined effects of Phenylacetonitrile (PAN) and Teflubenzuron with M. anisopliae on desert locusts. The results indicated that applying each component at half doses aided in speeding up the rate of fungal infection. This supports reports by Hassan and Charnley (1989) and Joshi et al., (1992) who demonstrated that a combination of Metarhizium and insect growth regulator e.g., Teflubenzuron can weaken the insect body wall increasing its susceptibility to fungal infection. Furthermore, PAN induces stress upon the insects also increasing their susceptibility to fungal infection (Lecoq, 2001). Therefore, implementing integrated management programs with the use of M. anisopliae can be ideal for effectively eradicating locust infection while protecting the environment and ensuring human safety.
Thuringiensin which is a bacterial pathogen was also proven to be successful in controlling agricultural mites (Vargas et al., 2001; Royalty et al., 1990). During vegetative growth, thuringiensin is secreted externally from Bacillus thuringiensis berliner cells into the culture medium (Farkas et al., 1969). It acts by hindering the ribosomal DNA-dependent RNA polymerase and competing with ATP for enzymatic binding sites href="#mohd-salleh_1980">(Mohd-Salleh et al., 1980). Toxicity is an expressed process that requires high rates of RNA synthesis i.e., high growth rates and physiological processes that occur in immature insects (Sebesta et al., 1981). Perring and Farrar (1986) investigated the use of thuringiens in the bio-control of TSSM on melons which resulted in no control of the pest population. Later, Royaltyet_al(1991, 1990) discovered low mortality after three days in the immature stages of TSSM and European red mite (ERM) which were more susceptible than adults. Vargas et al., (2001) conducted an experiment that involved the comparison of the direct and residual toxicity of thuringiensin on immature and adult stages of TSSM and ERM, also to determine the effects of the bacteria on the reproduction and population development of TSSM. The results indicated that direct toxicity was higher than residual toxicity to TSSM (Vargas et al., 2001). Also, the immature stages for both mites were more susceptible than adults. After adult females of TSSM were exposed to thuringiensin residues for varying periods, fecundity was significantly reduced. Tehri et al., (2014) stated that due to the high reproduction rates of TSSM, it is crucial to apply control measures as soon as mite infestation is detected.
There are several natural predators of agricultural mites including the green lacewings and mites such as the Amblyseius spp., Stethorus punctillum Weise and Phytoseilus persimilis Athias-Henriot.
Raoiella indica (Red Palm Mite)
Raoiella indica (RPM) was first discovered in Martinique in 2004 (Flechtmann and Etienne, 2004), after which it was rapidly dispersed in the Caribbean Regions: Saint Lucia (2005), Dominica (2005), Trinidad (2006) and Guyana (2013) (Van Lenteren, 2019; Kane et al., 2005). In almost all the affected countries, RPMs were prominent on palm trees of the family, Arecaceae, with the coconut palms being more severely affected (Pena et al., 2012). The leaves at the base of the coconut tree were the most targeted as they turned pale and yellow and some died completely after the attack of RPMs (Pena et al., 2012; Kane and Ochoa, 2006). The immature stages of lacewings of the genus Ceraeochrysa have actively shown to prey on RPMs on coconut palms, hence its potential as a biocontrol agent (Carrillo et al., 2012). Afzal and Khan (1978) discovered that one Chrysoperla carnea Stephens larvae can consume up to 487 aphids and 511 whitefly pupae before pupation and has excellent searching capacity. Viteri Jumbo et al., (2019) assessed the potential of Ceraeochrysa caligata Banks, as a biological control agent of RPMs by conducting functional response bioassays. Three stages of RPMs (eggs, immature stages and adult females) were provided to less than 24 hrs old C. caligata in coconut leaf arenas. The amount of prey consumed was recorded six hours after releasing the lacewings. They found that the ability of the lacewings to feed on the RPMs increased with larval development (Viteri Jumbo et al., 2019).
Higher feeding levels were recorded for the first and second instars of C. caligata when preying upon the eggs and immature stages of R. indica. Viteri Jumbo et al., (2019) stated that C. caligata of different stages exhibited differential functional responses, for example, C. caligata second instar individuals exhibited an increase in consumption rate with increasing prey availability (type III functional response) when preying upon immature stages of R. indica. However, when preying on the adult females, C. caligata second instar individuals exhibited a type II functional response (i.e., an increase in consumption rate with increasing prey availability, before reaching a plateau). Predator individuals of the first and third instar stages exhibited a type II functional response for all prey types. As the prey density increased, predatory consumption also increased eventually leading to a decline in the prey population. Therefore, green lacewings can be considered excellent predators/natural enemies of RPM. Hassanpour et al. (2009) also evaluated green lacewings as a potential predator against the two-spotted spider mites and found similar results. As the prey density increased, predatory consumption also increased leading to a decline in the prey population. The first and second instar showed a type II functional response i.e., as prey density increases, predator consumption increases. However, the third larval instar showed type III functional response i.e., responding to high levels of prey density in a density-dependent manner (Hassanpour et al., 2009). According to these studies, we can conclude that green lacewings are excellent predators/ natural enemies of RPMs and TSSM.
The phytophagous mites of the Amblyseius species were the most effective predators against Red Palm mites, Broad mites, European red mites and Two Spotted Spider Mites. They occupy a wide range of habitats and are generalists feeding on several prey, pollen and plant exudates (McMurtry et al., 2015; Carillo et al., 2014). Numerous overlapping observations of Amblyseius spp. attribute these characteristics to its successes.
Carillo et al., (2014) assessed the effects of Amblyseius largoensis Muma on R. indica using exclusion and release strategies to obtain coconut palms with varying levels of the natural enemy. Four treatments consisting of four rates of release of A. largoensis females (0= control, 1:10, 1:20 and 1:30 A. largoensis: R. indica) were tested. The results showed that the highest reduction of R. indica (92%) was observed at the highest predator release rate (1:10 A. largoensis: R. indica). Meanwhile, the other release rates (1:20 and 1:30 A. largoensis: R. indica) caused 55% and 43% reductions, respectively in the pest populations. In another study, Carillo and Pena (2011) assessed the potential of A. largoensis to control R. indica populations by evaluating the predator preferences among R. indica developmental stages and estimating predator functional and numerical responses to varying densities of its most preferred prey stage. The results indicated that A. largoensis consumed significantly more eggs than in other stages, therefore it was the most preferred stage. Moreover, A. largoensis displayed a type II functional response which demonstrated that with increased prey population density there was increased mortality. Hence, the results of these assessments support the hypothesis that A. largoensis is an important biological control agent of R. indica and should be implemented in Integrated Pest Management programs (Carillo et al., 2014).
Furthermore, Van Maanen et al. (2010) analyzed the ability of Amblyseius swirskii Athias-Henriot to control broad mites on pepper plants in a greenhouse by measuring oviposition and predation. Plants infested with adult female broad mites were used in the experiment. Pollen was used as food by A. swirskii, hence, young plants without flowers (without food) and pollen-producing plants were used as a control. The oviposition rate of A. swirskii, on a diet of broad mites, was lower than the oviposition rate on a diet of pollen, but higher than oviposition in the absence of food. On average, the predators consumed 8.6 and 10.2 adult female broad mites during the first and second day respectively (Van Maanen et al., 2010).
To control ERM and TSSM at peach orchards in Ontario in 1995, Lester et al., (1999) released a pyrethroid-resistant strain phytoseiid mite known as Amblyseius fallacis Garman. The predator was mass-produced on kidney bean plants and approximately three bean leaves were wrapped in a ‘twist tie’ around one peach leaf which was infected with two-spotted spider mites. Overall, approximately 1000-2000 predatory mites were released per tree. Throughout 1995, the peach orchard received deltamethrin on seven occasions and additional fungicides as part of a spray program. The initial release of 2,000 A. fallacis per tree in June and July 1995 showed an increased density of the predator species than those observed in control trees where no predatory mite was released. However, the release of 1,000 A. fallacis per tree in August, did not result in increased abundance. The following year displayed low densities of A. fallacis throughout the growing season with increased densities of TSSM (Lester et al., 1999). In 1995, A. fallacis was established and its abundance increased, however, in 1996 the organisms overwintered and arrived too late to be used as a biological control agent in peach orchards (Lester et al., 1999). This study involved spray programs that may have affected the re-emergence of the predatory mite. Hence, the importance of gathering substantial information before conducting such research. Penman et al. (1979) recognized a similar trend where A. fallacis was introduced in Australia and significantly controlled TSSM and ERM populations affecting apple orchards. Unfortunately, in the following season, Penman et al., (1979) observed a decline in predator populations. A. fallacis typically overwinters at the base of plants or beneath the ground; after winter they recolonize their way up to the canopy, feeding on prey species present (Johnson and Croft, 1976). This shows that the nourishment of ground cover is important for the survival and renewal of predators (Croft and McGroarty, 1978). Climatic elements, spray routines, low humidity, the presence of other species acting together in a complex food web, etc. are all factors that may influence the ability of A. fallacis to establish, survive and accomplish biological control (Janssen et al., 1998; Berry et al., 1991; Boyn and Hain, 1983). The success of Amblyseius spp. as a biological control agent is due to varying characteristics as shown in Fig 1.
Stethorus spp., Weise, commonly known as the lady beetles and belonging to the family Coccinellidae; are well known for being natural predators (Biddinger et al., 2009). Chazeau (1985) reported Stethorus beetles present in various regions and ecosystems (tropical rainforests to dry savannahs) with differing climates. The adults and larvae of S. punctillum were identified as a potential biological control agent of spider mites in various crops (Roy et al., 1999; Hull 1977; Hull et al., 1976). Parvin and Haque (2008) investigated the ability of three predators (Scolothrips sexmaculatus Pergande, P. persimilis, S. punctillum) to control TSSM affecting bean plants in Bangladesh (Takafuzi et al., 2000; Herron et al., 1993; Helle and Sabelis 1985). The experiment was carried out during three different periods. The bean plants were cultivated in pots and infected with TSSM eight weeks after cultivation. The predators were later released on the plants of group B after one week of mite infestation and on the plants of group C after three weeks of mite infestation; hence plants of group A were considered the control and went untreated (Parvin and Haque, 2008). The results indicated that TSSM populations increased exponentially up to the sixth week on plants of group A. However, in plants of Group B and C, where the predators were released, the mite population was reduced significantly due to predation. Parvin and Haque (2008) concluded that the early release of the predators reduced the TSSM population earlier in all the cases. Table 3 shows predators of agricultural mites and crops that are mostly affected by the infestation of these mites.
Despite several studies on parasitoids’ ecology and evolution, (Calatayud, 2020; Colmenarez, 2018) no study documented parasitoids’ potential to minimize agricultural mite populations. Key gaps lie in the availability of adequate data to understand and resolve challenges for current and future potential biological control programs. Further field investigations will enable more precise attempts at developing control plans since several environmental elements cannot manifest under laboratory conditions. Information on population dynamics throughout a season, dispersion levels and patterns can aid in unpredicted setbacks such as predator species affecting untargeted organisms. In addition, for parasitoids to successfully develop and infect insect hosts, they must be adapted to the physiology, life cycle and defenses of the host (Stoner, 1998). Consequently, increased accuracy of informed control plans leads to less application of chemicals which overall achieves environmental sustenance and improved health and wellness.
Conflict of interest
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