Challenges and Solutions for Managing Citrus Mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae) in Greenhouse Production Systems

Introduction

Citrus mealybug, Planococcus citri (Risso) (Hemiptera: Pseudococcidae), is an important insect pest of greenhouse-grown horticultural crops worldwide (Blumberg & Van Driesche, 2001; Cadée & Alphen, 1997; Copland et al., 1985; Cox, 1981; Dreistadt, 2001), including herbaceous annuals and perennials, herbs, foliage plants, orchids, and vegetables (Hennekam et al., 1987; Pillai, 2016). This review discusses the biology, behavior, movement, and damage associated with P. citri. In addition, it addresses the challenges of managing P. citri and provides solutions to help greenhouse producers maintain populations below plant-damaging levels.

Biology and Behavior

The P. citri life cycle includes the egg, nymphal instars (crawlers), and the adult stage. Egg-to-adult development can be completed in 30--60 days, depending on temperature and host plant (Meyers 1932; Mani and Shivaraju 2016a). Planococcus citri is elliptical with a distinct gray stripe extending along the top of the body. White, waxy protrusions project around the body periphery (Pritchard 1949; Mani and Shivaraju 2016a). Third- and fourth-instar nymphs, as well as adults possess a waxy, water-repellent covering (Dean, Hart, and Ingle 1971; Copland et al. 1985; Williams and Watson 1988). In general, P. citri populations consist of equal numbers of females and males (Copland et al. 1985; Mani and Shivaraju 2016a).

Planococcus citri adult females are 3--5 mm long (Pritchard 1949; Hajer and Hrubá 2007; Mani and Shivaraju 2016a), white, and wingless (Copland et al. 1985; Dreistadt 2001). Adult males are winged and smaller than females (Dreistadt 2001; Mani and Shivaraju 2016a). Adult females may lay up to 800 eggs beneath the body cavity in an egg sac (ovisac) (Meyers 1932; Copland et al. 1985; Moore 1988; Hajer and Hrubá 2007; Mani and Shivaraju 2016a), a white mass that protects the eggs from desiccation (Mani and Shivaraju 2016a; Venkatesan et al. 2016). Egg laying can occur over a 10-day period (Pritchard 1949). Newly emerged (eclosed) nymphs are initially yellow-orange, turn white after successive molts, and eventually develop a waxy covering. Nymphs search for feeding sites on plants (Copland et al. 1985). Once nymphs locate a suitable site, they begin feeding, with later instars becoming less mobile. Nymphs progress through several stages before becoming adults (Cloyd 2011).

Planococcus citri females have five developmental stages: egg, three nymphal instars (crawlers), and adult. Males undergo six developmental stages, including a prepupal stage. Planococcus citri males create a cottony cocoon and pupate (Mani and Shivaraju 2016a). Adult males are winged, mate with females, and then die shortly after. The female citrus mealybug lifespan is 40 days, which includes development and molting before dying. The eggs remain beneath the body of the dead female covered by a fluffy white mass (Cloyd 2011).

Planococcus citri nymphs and adults feed at leaf junctures where the petiole attaches to the stem, on leaf undersides, on terminal growth, and beneath the leaf sheaths of orchids and foliage plants (Mani and Shivaraju 2016a). Planococcus citri can undergo several generations per year, with egg-to-adult development taking 30 to 60 days, depending on temperature (Dreistadt 2001). Overlapping generations of different life stages (eggs, nymphs, and adults) may occur simultaneously (Pritchard 1949; Shrewsbury, Bejleri, and Lea-Cox 2002; Franco, Zada, and Mendel 2009)

Damage

Planococcus citri causes plant damage by feeding on leaves, stems, flowers, and fruits (McKenzie 1967; Franco, Zada, and Mendel 2009). Nymphs and adults feed on plant fluids in the phloem, mesophyll, or both (Franco, Zada, and Mendel 2009). During feeding, they inject toxic saliva, which results in stunted plant growth, leaf yellowing, wilting, chlorosis, leaf drop, premature fruit drop, and plant death (McKenzie 1967; Copland et al. 1985; Dreistadt 2001; Demirci et al. 2011; Mani and Shivaraju 2016b). During feeding, P. citri nymphs and adults excrete honeydew (Hajer and Hrubá 2007; Mani and Shivaraju 2016b) that serves as a substrate for black sooty mold (Copland et al. 1985; Dreistadt 2001), which can obstruct photosynthesis and reduce the aesthetic quality of plants (Pritchard 1949; Charles 1982; Copland et al. 1985; Pillai 2016).

Movement

Planococcus citri nymphs can move within a greenhouse via air currents from horizontal airflow fans (Beardsley 1960) and workers handling infested plants that inadvertently transfer individuals to noninfested plants (Cloyd 2011). In addition, nymphs can disperse among greenhouse plants when spaced close together with leaves touching (Williams and Granara de Willink 1992; Tanwar, Jeyakumar, and Monga 2007). Planococcus citri populations may also be introduced into new greenhouses or locations through movement of infested plant material (Copland et al. 1985; Parrella 1999; Mani and Shivaraju 2016c).

Management

Management of P. citri populations in greenhouses involves inspecting incoming plant material for infestations before introduction into greenhouse production systems, scouting crops regularly twice per week, implementing proper cultural practices, applying insecticides, and releasing biological control agents (Cloyd 2011). Once P. citri establish on plants, it is too late to implement management strategies (Cloyd 2011).

A. Scouting

Greenhouse producers must ensure that incoming plant material is inspected for populations of P. citri before introduction into greenhouse production systems (Dreistadt 2001) because low populations early in production can increase to damaging levels later (Parrella 1999). The primary method for early detection is visual inspection of plants (Cloyd 2011; Pillai 2016). However, visual inspection is labor intensive, impractical, and nymphs are difficult to detect during the early stages of an infestation (Moore 1988) because the first- and second-instar nymphs are only 2--3 mm in length. In addition, P. citri populations tend to reside in concealed areas on plants, such as leaf undersides and base of leaf petioles (Moore 1988).

Planococcus citri populations typically are clumped, meaning nymphs and adults are aggregated on specific areas of plants (Mani and Shivaraju 2016d). Consequently, scouting efforts should focus on these areas, as well as plant species susceptible to infestation (Cloyd 2011). A designated number of plants should be flagged and inspected twice per week for early detection of P. citri nymphs during the growing season (Cloyd 2011).

B. Cultural Practices

Cultural practices include removing weeds, properly fertilizing plants, and disposing of infested plants and old plant material. Planococcus citri feeds on plants in more than 27 plant families (Gill, Goyal, and Gillett-Kaufman 2019). Consequently, weeds should be removed from within and around the greenhouse perimeter because they may harbor P. citri, including common mallow (Malva sylvestris), redroot pigweed (Amaranthus retroflexus), black nightshade (Solanum nigrum), and common purslane (Portulaca oleracea) (Mani and Shivaraju 2016d; Celepci et al. 2017), which can move onto the main crop. Plant nutrition can influence the reproduction of P. citri females (Franco, Zada, and Mendel 2009). For example, females feeding on coleus (Solenostemon scutellarioides) receiving 200 and 400 ppm nitrogen from a water-soluble fertilizer laid 265--312 eggs, significantly more than females feeding on coleus plants receiving 25, 50, and 100 ppm (Hogendorp, Cloyd, and Swiader 2006). Therefore, greenhouse producers should only provide the amount of fertilizer required based on information from plant suppliers. Plants infested with P. citri should be disposed of immediately to avoid infesting other plants in the greenhouse (Dreistadt 2001; Mani and Shivaraju 2016d). Infested plants should be placed into refuse containers or dumpsters located outside the greenhouse (Cloyd 2016).

C. Insecticides

Insecticides are commonly used in greenhouse production systems to manage P. citri (Parrella 1999). However, systemic insecticides are not effective in maintaining P. citri populations below plant-damaging levels on greenhouse-grown horticultural crops. This reduced efficacy may be due to insufficient ingestion of lethal concentrations of the active ingredient, since P. citri feeds within the mesophyll tissues and on plant stems (Moore 1988; Pillai 2016; Herrick and Cloyd 2023, 2017; Herrick, Cloyd, and Raudenbush 2019). Consequently, greenhouse producers must rely primarily on foliar applications of contact insecticides to maintain populations below plant-damaging levels.

Contact insecticides also have limited effectiveness against P. citri because 1) eggs are not susceptible to insecticide sprays as they are protected by the ovisac; 2) populations are often not exposed to insecticide spray applications when feeding in concealed areas of plants (Charles 1982; Copland et al. 1985; Franco, Zada, and Mendel 2009; Mani and Shivaraju 2016d; Herrick and Cloyd 2017); and 3) third- and fourth-instar nymphs, as well as adults, possess a water-repellent waxy covering, which protects them from insecticide spray applications (Copland et al. 1985; Greathead 1986; Dreistadt 2001; Franco, Zada, and Mendel 2009; Walton, Daane, and Pringle 2004; Mani and Shivaraju 2016d; Pillai 2016; Venkatesan et al. 2016). The addition of a surfactant to spray solutions may not increase the effectiveness of insecticides (Herrick and Cloyd 2023). However, first- and second-instar nymphs are susceptible to insecticide applications because they do not have a water-repellent waxy covering (Charles 1982; Dreistadt 2001; Franco, Zada, and Mendel 2009; Ahmed and Abd-Rabou 2010; Venkatesan et al. 2016)

Factors influencing the efficacy of contact insecticides against P. citri include spray coverage and application frequency. Thorough insecticide applications are important for maintaining populations below plant-damaging levels (Venkatesan et al. 2016). For example, Radosevich and Cloyd (2021) demonstrated that a total spray volume of 75 ml per coleus plant resulted in mortality >60% of P. citri, which was higher than spray volumes of 25 or 50 ml. In addition to spray coverage and application frequency, insecticides must be applied when nymphs are present to maximize mortality before they develop into adults (Radosevich and Cloyd 2021). Repeated applications are required to target nymphs that were in the egg stage during previous applications (Dreistadt 2001). Once adult females begin laying eggs, insecticides are minimally effective at maintaining populations below plant-damaging levels. Furthermore, insecticides with different modes of action should be rotated during the growing season to mitigate the risk of insecticide resistance development in P. citri populations (Flaherty et al. 1982; Mendel et al. 1999; Franco, Zada, and Mendel 2009). Cloyd (2021) provides information on how to rotate insecticides with different modes of action, including a list of products suitable for rotation programs against P. citri.

D. Biological Control Agents

Biological control agents, including parasitoids and predators, have been used to manage P. citri populations in greenhouse production systems (Doutt 1952; Moore 1988). However, the commercial availability of biological control agents for use against P. citri is currently limited. Available biological control agents include the predatory ladybird beetle Cryptolaemus montrouzieri Mulsant (Coleoptera: Coccinellidae), commonly known as the "mealybug destroyer" (Whitcomb 1940; Copland et al. 1985; Moore 1988; Afifi et al. 2010); the green lacewings, Chrysopa carnea (Stephens) (Neuroptera: Chrysopidae) and Chrysoperla rufilabris (Burmeister) (Neuroptera: Chrysopidae) (Afifi et al. 2010); and the parasitoid, Leptomastix dactylopii (Howard) (Hymenoptera: Encyrtidae) (Doutt 1952; Jong and Alphen 1989; Mani, Krishnamoorthy, and Shivaraju 2011).

Leptomastix dactylopii is no longer commercially available. The parasitoid, Anagyrus vladimiri Triapitsyn (Hymenoptera: Encyrtidae) is commercially available from biological control suppliers, and P. citri is one of its primary hosts (Andreason, Triapitsyn, and Perring 2019). Increased availability of commercial biological control agents would provide greenhouse producers with additional management options.

However, the water-repellent covering and waxy protrusions surrounding the body can protect P. citri from biological control agents (Franco, Zada, and Mendel 2009). Moreover, biological control agents generally do not maintain P. citri populations below plant-damaging levels, which may be related to greenhouse temperatures that are either above or below the optimal activity range of biological control agents (Doutt 1951).

Discussion

Planococcus citri is an insect pest that is difficult for greenhouse producers to manage due to its biological and behavioral attributes, including 1) eggs not being susceptible to insecticide sprays because they are protected by an ovisac; 2) third- and fourth-instar nymphs, as well as adults having a water-repellent covering that reduces exposure to insecticide spray applications; and 3) populations are often protected from exposure to insecticide spray applications when feeding in concealed areas of plants (Charles 1982; Copland et al. 1985; Greathead 1986; Dreistadt 2001; Franco, Zada, and Mendel 2009; Mani and Shivaraju 2016d; Pillai 2016; Venkatesan et al. 2016; Herrick and Cloyd 2017).

Another challenge is that the presence of P. citri can disrupt biological control programs. For example, biological control programs have been developed for poinsettia (Euphorbia pulcherrima) using the parasitoid, Eretmocerus eremicus Rose & Zolnerowich (Hymenoptera: Aphelinidae) to maintain sweetpotato whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), populations below plant-damaging levels. However, the presence of P. citri populations on poinsettia may require insecticide applications that disrupt biological control programs for sweetpotato whitefly (R. A. Cloyd, personal observation).

Despite these challenges, greenhouse producers can overcome them by implementing the following practices: 1) inspecting incoming plant material to prevent P. citri introduction into greenhouse production systems; 2) scouting plants regularly twice per week during the growing season to detect infestations; 3) disposing of infested plants; and 4) applying contact insecticides when nymphs are detected -- ensuring thorough spray coverage of all plant parts with spray solutions and frequent applications to maintain populations below plant-damaging levels (Radosevich and Cloyd 2021); and 5) continuing to evaluate additional integrated pest management strategies that are effective for greenhouse production systems.

References