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Zygogramma bicolorata (Coleoptera: Chrysomelidae): an exotic biocontrol agent of the noxious weed, Parthenium hysterophorus (Asteraceae)

Published online by Cambridge University Press:  15 February 2024

Uzma Afaq*
Affiliation:
Department of Biosciences, Faculty of Science, Integral University, Lucknow, Uttar Pradesh UP-226026, India
Gyanendra Kumar
Affiliation:
Department of Zoology, National P.G. College, Lucknow, Uttar Pradesh UP-226001, India
Arshi Siddiqui
Affiliation:
Department of Biosciences, Faculty of Science, Integral University, Lucknow, Uttar Pradesh UP-226026, India
Omkar
Affiliation:
Ladybird Research Laboratory, Department of Zoology, University of Lucknow, Uttar Pradesh UP-226007, India
*
Corresponding author: Uzma Afaq; Emails: [email protected]; [email protected]

Abstract

Parthenium hysterophorus Linnaeus (Asteraceae), commonly known as “congress grass,” is among the 10 worst weeds of India and is considered one of the world’s 100 most harmful invasive species. This species has been introduced accidentally into several countries, including India, and is a major agricultural and rangeland weed in more than 45 countries. It affects crop production, suppressing biodiversity, crop yields, the health of farm animals and human beings, and local and regional economies. Biological control has been found to be a cost-effective management strategy to control the weed, with the leaf beetle, Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae), considered an effective and safe biocontrol agent. Several studies have investigated the beetle’s biology, reproduction, and other life attributes. This review compiles the existing information about Z. bicolorata biology, growth, development, reproduction, food, and host specificity, and the effects of abiotic and biotic stressors on the insect’s life attributes. We anticipate that this review will helpful for improving strategies for this bioagent’s swift mass rearing and for developing classical biological control design for Parthenium weed.

Type
Review
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of Entomological Society of Canada

Introduction

Weeds have been ubiquitous since agriculture began around 10 000 years ago and are serious threats to the global production of food for human consumption. Worldwide, weeds alone are responsible for the loss of one-third of agricultural yield. Weed-driven losses in crop yield are shaped by numerous local characteristics such as climate, soil, weed density, crop type, and variety. Current overall global grain production is approximately 2.1 billion metric tonnes (Chauhan Reference Chauhan2020). Assuming the total loss in grain production by weeds globally is approximately 200 million metric tonnes (Chauhan Reference Chauhan2020). In India alone, weeds cost more than $USD 11 billion annually in agricultural losses (Gharde et al. Reference Gharde, Singh, Gupta and Gupta2018).

Weeds are classified based on their ontogeny (annuals, biennials, and perennials) and origin (indigenous or exotic; Maheswaran et al. Reference Maheswaran, Sathesh, Gayathri, Bhaarathei and Kavin2020). Parthenium hysterophorus Linnaeus (Asteraceae) is an annual herb that aggressively colonises disturbed sites. It is considered as one of the “100 most invasive species in the world” by the International Union for Conservation of Nature (Global Invasive Species Database 2018; http://www.iucngisd.org/gisd/) and is a weed of global significance (Navie et al. Reference Navie, McFadyen, Panetta and Adkins1996). It is considered an important agricultural weed in more than 45 countries (Bajwa et al. Reference Bajwa, Chauhan, Farooq, Shabbir and Adkins2016) and is listed as one of the world’s 100 most harmful invasive species (Indian Council of Forestry Research and Education 2020). In India, it is considered as one of the 10 most harmful weeds (Bhan et al. Reference Bhan, Kauraw and Chile1999) because of its invasiveness, ability to spread easily, and its economic and ecological impacts. Because of the harm it causes, efforts are made in India and other countries to control the plant. Mechanical and chemical controls for the weed have been found to be effective (Jasinskas et al. Reference Jasinskas, Steponavicius, Sniauka and Zinkevicius2015); however, most of the chemical herbicides are harmful and cannot be used over the long term (Fugere et al. Reference Fugere, Hebert, da Costa, Xu, Barrett and Beisner2020). Biocontrol is considered a green alternative weed management technique for Parthenium that is relatively less expensive and free of hazardous side effects (Mahadevappa Reference Mahadevappa2005; Abels Reference Abels2018). The first Parthenium biocontrol programme took place in Australia (Dhileepan and McFadyen Reference Dhileepan and McFadyen1997). Zygogramma bicolorata Pallister (Coleoptera: Chrysomelidae) is considered to be the most prominent biocontrol agent for Parthenium.

Zygogramma bicolorata Pallister was first imported from Mexico to India for the management of P. hysterophorus in 1983 (Jayanth and Nagarkatti Reference Jayanth and Nagarkatti1987). Biological control trials using Z. bicolorata were initiated in India at Vindhyanagar, Madhya Pradesh, and within three years of its introduction, the insect became abundant in Bangalore and surrounding areas and reduced Parthenium weed density (Jayanth and Visalakshy Reference Jayanth and Visalakshy1996). The beetle spread as far as 35 km from its release points, mainly in north and east Bangalore, by August 1998. The beetle’s continuous field presence and action has led to an increasing decline in the weed’s density. Adults of Z. bicolorata were mass released in 1992 in Jammu and Kashmir, where the beetles spread over more than 9000 km2, resulting in Parthenium weed suppression in several regions of the state (Gupta et al. Reference Gupta, Bali and Khan2002, Reference Gupta, Bali, Khan, Monobrulla and Bhagat2004, Reference Gupta, Gupta, Balia and Srivastava2010). Dhileepan and Senaratne (Reference Dhileepan and Senaratne2009) used geographical information system-based map distribution to effectively verify the geographical distribution of the beetle in South Asia based on meta-analysis. They determined that Bangladesh, India, Nepal, and Sri Lanka have suitable climatic conditions for Z. bicolorata establishment (Fig. 1), and that large populations of the beetle could be found in the main regions of India and Nepal but not in Bangladesh, Pakistan, or Sri Lanka (Dhileepan and Strathie Reference Dhileepan and Strathie2009).

Figure 1. Distribution of Zygogramma bicolorata on world map (India and Mexico). (Source: https://www.cabi.org/isc/datasheet/57506).

A mass release of the insect in South Africa was unsuccessful (McConnachie Reference McConnachie2015; Cowie et al. Reference Cowie, Strathie, Goodall, Venter, Witkowski and Byrne2019). In Ethiopia, Mersie et al. (Reference Mersie, Alemayehu, Strathie, McConnachie, Terefe, Negeri and Zewdie2019) reported that field trials were awaiting authorisation for Z. bicolorata release into agroecosystems to manage P. hysterophorus.

Previous studies have documented information on many important aspects of this bioagent, including population dynamics, inter- and intraspecific interactions, prevalence, environmental tolerance, and so on (Table 1). This review compiles the most current available information and literature about Z. bicolorata. We expect that this review will facilitate classical biological control strategies using Z. bicolorata in areas with encroaching Parthenium.

Table 1. Previous studies on Zygogramma bicolorata

Morphological characteristics

Adults Z. bicolorata measure 5–6 mm long, with males usually being smaller in size (about 5 mm long) and females being larger in size (about 6 mm long; Singh et al. Reference Singh, Gill, Dhaliwal and Kumar2017). The beetles are oval, dorsally convex, and ventrally flat in structure. The body itself is off-white in colour, the appendages are dark brown, the pronotum has off-white patches at the anterior edges, and the elytra have undulating dark-brown longitudinal markings (Jayanth and Bali Reference Jayanth and Bali1993a; Siddhapara et al. Reference Siddhapara, Patel and Patel2012). The posterior edge of the last visible abdominal ventrite is complete in females, whereas the tip is somewhat serrated in males (Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020a). Males have a faint depression at the middle of their last abdominal sternite (Siddhapara et al. Reference Siddhapara, Patel and Patel2012) and larger antennomeres and more abundant sensilla basiconica than are found in the females (Qadir and Qamar Reference Qadir and Qamar2019).

Females oviposit singly or in clusters on stems, leaves, inflorescences, and axillary or terminal buds (Dhileepan et al. Reference Dhileepan, Setter and McFadyen2000a, Reference Dhileepan, Setter and McFadyen2000b; Dhileepan and McFadyen Reference Dhileepan and McFadyen2012). The eggs are yellowish–orange, oblong, 1 mm in size, finely reticulated, and usually hatch within 4–5 days after oviposition (Jayanth and Bali Reference Jayanth and Bali1993a, 1993b; Sushilkumar Reference Sushilkumar2005a; Afaq Reference Afaq2012). The newly emerged larvae eat inflorescences and new axillary buds (Dhileepan et al. Reference Dhileepan, Callander, Shi and Osunkoya2018). These instars are yellowish in colour and become creamy white as they grow.

Ontogenesis

The newly hatched grubs feed on young leaves and inflorescences and move over the leaf blades for successive feeding as they grow. The first- and second-instar larvae measure about 1.5 and 3.0 mm long, respectively. The third- and fourth-instar larvae can be as long as 5.5 and 7.0 mm, respectively. The instars moult three times to become full grown (Fig. 2). Fully grown larvae cease feeding before they bury themselves into the soil (as deep as 10 cm) to pupate. Singh et al. (Reference Singh, Gill, Dhaliwal and Kumar2017) report six stages of pupal development within the soil, whereas Dhileepan and McFadyen (Reference Dhileepan and McFadyen2012) report that, under in vitro conditions, pupation lasts for 8–14 days, being shortest (8.04 days) at 35 °C and longest (18.88 days) at 15 °C. Total larval developmental lasts from 27 to 29 days (Jayanth and Bali Reference Jayanth and Bali1992).

Figure 2. Life cycle of Zygogramma bicolorata on Parthenium weed.

However, increases in temperature can accelerate the larvae’s metabolism and feeding activities, leading to accelerated development (Hasan et al. Reference Hasan, Ansari, Dhillon, Muslim, Bhadauriya, Tanwar and Ahmad2018). The beetle’s life cycle is completed within 6–8 weeks, and, depending on temperature, humidity, and food availability, as many as four generations may occur in a year (Dhileepan et al. Reference Dhileepan, Setter and McFadyen2000a, Reference Dhileepan, Setter and McFadyen2000b; Ray Reference Ray2011; Hasan and Ansari Reference Hasan and Ansari2016a). The beetle’s adult life span can last as long as two years (Sushilkumar Reference Sushilkumar2005b), but Kour and Shenhmar (Reference Kour and Shenhmar2008) report that the male and female live for 74.33 and 64.93 days, respectively.

The beetle spends approximately six months in the soil for diapause and emerges at the start of the monsoon or spring rains to reproduce (Sushilkumar Reference Sushilkumar2005b). The female’s preoviposition period lasts 8–10 days, and oviposition continues for about 50–56 days, whereas the postoviposition period varies from 17 to 20 days (Rastogi Reference Rastogi2010). A female Z. bicolorata lays approximately 988–1054 eggs during her lifetime (Viraktamath et al. Reference Viraktamath, Bhumannavar and Patel2004; Siddhapara et al. Reference Siddhapara, Patel and Patel2012).

Diapause behaviour

Diapause is a widespread survival strategy used by insects to withstand unfavourable conditions. Zygogramma bicolorata adults diapause in soil during the summer to avoid heat and drought conditions and emerge when the rain begin (Jayanth and Bali Reference Jayanth and Bali1993b). On the other hand, Gautam et al. (Reference Gautam, Samyal and Khan2005) report that the beetle breeds throughout the year in northern India without undergoing diapauses. Numerous studies have been carried out to determine different factors’ effects on inducing and ending diapause in Z. bicolorata adults. Fazil et al. (Reference Fazil, Ansari, Mukesh, Muslim, Bhadauriya, Tanwar and Ahmad2018) showed that diapause initiation increases with the age of the beetle and from one generation to the next, resulting in increased fecundity of females. Temperature is known to have a determinant role in the beetle’s diapause behaviour, with a high percentage of diapause induced in adults at low temperature (Gupta et al. Reference Gupta, Gupta, Balia and Srivastava2010; Hasan et al. Reference Hasan, Ansari, Dhillon, Muslim, Bhadauriya, Tanwar and Ahmad2018). According to Sushilkumar and Ray (Reference Sushilkumar and Ray2010), diapause in Z. bicolorata reduces the insect’s effectiveness as a biological control agent of Parthenium because the plant typically finishes flowering and producing seeds by the time Z. bicolorata builds its population after diapause.

Natural enemies

The existence of natural enemies of Z. bicolorata in an agroecosystem significantly decreases its efficacy as a weed biocontrol. Several entomopathogenic fungi are reported to induce mortality in the beetle’s larvae: these fungi include Metarhizium anisopliae (Clavicipitaceae), green muscardine fungus, and Beauveria bassiana (Cordycipitaceae), white muscardine fungus (Jayanth and Bali Reference Jayanth and Bali1994; Sushilkumar Reference Sushilkumar2005a; Dubey et al. Reference Dubey, Ray and Pandey2010; Hasan and Ansari Reference Hasan and Ansari2016b). Some insects – including redbird, Rodolia cardinalis (Coleoptera: Coccinellidae), Harpector marginatus Fabricius (Heteroptera: Reduviidae), the two-spotted stink bug, Perillus bioculatus (Fabricius) (Hemiptera: Pentatomidae), the orange colour spot, Perillus splendidus (Uhler) (Hemiptera: Pentatomidae), and the reduviid bug, Sycanus pyrrhomelas Walker (Hemiptera: Reduviidae) – are also known to eat Z. bicolorata eggs and larvae (Dhiman and Bhargava Reference Dhiman and Bhargava2005b; Manjunath Reference Manjunath2010; Hasan Reference Hasan2015; Singh et al. Reference Singh, Gill, Dhaliwal and Kumar2017; Harshana Reference Harshana2021b). Gupta et al. (Reference Gupta, Bali, Khan, Monobrulla and Bhagat2004) identified predatory bugs such as Cantheoconidea furcellata Wolf (Pentatomidae: Hemiptera) (Hemiptera: Pentatomidae), Andrallus spinidens (Fabricius) (Hemiptera: Pentatomidae), and Sycanus pyrrhomelas Walker (Heteroptera: Reduviidae) as natural predators of the beetle. Palexorista sp. (Diptera: Tachinidae) and Erixestus zygogrammae Cave and Grissell (Hymenoptera: Pteromalidae) are known as egg and larval parasitoids of Z. bicolorata (Jayanth et al. Reference Jayanth, Visalakshy, Ghosh and Chaudhary1996; Singh et al. Reference Singh, Gill, Dhaliwal and Kumar2017), whereas Doryphorophagha hyalinipennis (Wulp) (Diptera: Tachinidae) attacks the pupal stage of the insect (Dhileepan and Strathie Reference Dhileepan and Strathie2009). Abels (Reference Abels2018) noted that ants might be a primary crawling predator of Z. bicolorata eggs. Harshana (Reference Harshana2021a) reported four species of insects – P. bioculatus, the yellow paper wasp, Polistes wattii Cameron (Hymenoptera: Vespidae), Eocanthecona furcellata (Wolff) (Hemiptera: Pentatomidae), and the assassin bug, Rhynocoris cf. fuscipes (Hemiptera: Reduviidae) – as natural enemies of Z. bicolorata. Based on this information, it is advisable that locations being considered for a Parthenium biological control programme be scrutinised thoroughly for natural enemies before the beetle is released to avoid constraining the Z. bicolorata populations and the biocontrol programme.

Host specificity

Studies on the host specificity of Z. bicolorata confirm that the beetle is specialised to feed on P. hysterophorus rather than on any other agricultural crop. However, a few earlier studies have reported the adult beetles eating cultivated crops – for example, Helianthus annuus, sunflower (Sridhar Reference Sridhar1991; Kumar Reference Kumar1992; Siddhapara et al. Reference Siddhapara, Patel and Patel2012). Several host-specificity studies were conducted using choice and no-choice experiments to scrutinise the beetle’s egg-laying and feeding response on other plants. Feeding and reproductive risk calculations revealed that damage to nontarget plants was almost insignificant (Bilashini et al. Reference Bilashini, Lokeshwari, Singh and Gautam2011). The nominal feeding of the beetle on H. annuus plant that Sridhar (Reference Sridhar1991), Kumar (Reference Kumar1992), and Siddhapara et al. (Reference Siddhapara, Patel and Patel2012) reported was due to Parthenium pollen deposition from nearby fields on sunflowers. In addition, Jayanth et al. (Reference Jayanth, Visalakshy, Ghosh and Chaudhary1997) report a steady diet of sunflower results in the ovarian degradation in Z. bicolorata adults. It can therefore be affirmed that Z. bicolorata’s largely host-specific preferences make the beetle a most promising biocontrol agent to exploit and detoxify the toxins and alkaloids found in Parthenium.

Feeding behaviour and food consumption efficiencies

Rastogi (Reference Rastogi2010) found that Z. bicolorata’s developmental period was shortest when the beetles fed on Parthenium leaves and longest when they fed on Parthenium stems. The beetle’s fourth-instar larvae and adults are voracious feeders of Parthenium leaves (Cowie et al. Reference Cowie, Witkowski, Byrne, Strathie, Goodall and Venter2018; Hasan et al. Reference Hasan, Ansari, Dhillon, Muslim, Bhadauriya, Tanwar and Ahmad2018; Patel et al. Reference Patel, Kumar and Kumar2018); however, the newly emerged larvae seem to prefer inflorescences over other parts of the plant. These larval stage-determined food preferences may be due to the presence in different parts of the plant of differing primary metabolites, nucleotides, amino acids, and lipids, which act as phagostimulants in the beetle (Kumar Reference Kumar2005). Sushilkumar and Bhan (Reference Sushilkumar and Bhan1997) found greater numbers of older larvae on mature leaves. This suggests that the older grubs require more polyphenols in their diet, which are found in larger amounts in mature Parthenium leaves.

The beetle’s feeding aspects differ according to their larval stage and nearby environment. Both quantity and quality of the food – that is, the height of the Parthenium plant, the number and area of its leaves, inflorescences, etc. – are known to influence the insect’s feeding preferences and developmental parameters. Larval stages that have been provided with superior-quality food are larger and develop faster, and subsequently, the emerged female adults lay greater numbers of eggs compared to females that were provided with average and lower-quality food as larvae (Cowie et al. Reference Cowie, Strathie, Goodall, Venter, Witkowski and Byrne2019). Both fourth-instar larvae and adult females are voracious feeders and proficient transformers of food into body biomass. However, growth and developmental rates were found to be greatest for first- and second-instar larvae, and amongst the adult beetles, food consumption attributes were greater for males than for females (Omkar and Afaq Reference Omkar and Afaq2011; Table 2). Voracious feeding by Z. bicolorata larvae and adults severely damages the host Parthenium plant, reducing the surface area of leaves, disrupting leaf functioning, and increasing the plant’s vulnerability to microorganisms (Venter et al. Reference Venter, Hill, Hutchinson and Ripley2013). When Z. bicolorata feeds on Parthenium, the plants can undergo skeletonisation, defoliation, and decreased flowering (Dhileepan et al. Reference Dhileepan, Setter and McFadyen2000a, Reference Dhileepan, Setter and McFadyen2000b; McConnachie Reference McConnachie2015).

Table 2. Ecological efficiencies of larvae of Zygogramma bicolorata fed on Parthenium leaves (Omkar and Afaq Reference Omkar and Afaq2011). Values are mean ± standard error; L1, first instar; L2, second instar; L3, third instar; L4, fourth instar; and E.C.I., efficiency of conversion of ingested food; * and **, F-values significant at P < 0.01 and P < 0.001, respectively; NS, F-values nonsignificant at P > 0.05.

Temperature and age are also known to constrain the insect’s feeding behaviour. When the influence of food quality and temperature has been studied together, Afaq (Reference Afaq2012) revealed that temperature can affect the beetle’s consumption rate of Parthenium. The beetles’ food consumption rate is greatest at 27 °C and decreases thereafter as the temperature increases and is least at 35 °C. Feeding by adult insects increases until 20 days after emergence and declines thereafter with beetle age. The increased rate of food consumption that takes place up to 20 days can be ascribed to the adults’ high energy requirements to fuel their ovarian and gonadal development. The decrease in feeding rate at the beetle’s later age may be an effect of age and senescence (Afaq Reference Afaq2012).

Omkar and Afaq (Reference Omkar and Afaq2011) report that the beetle’s sex influences the insect’s food consumption. Females were found to be more proficient than males at consuming and converting food into biomass. Among the larval stages, fourth-instar larvae are the most proficient and efficient feeders, possibly because of the increased energy demands of pupation.

However, there is some contradictory evidence on the effects of food quality on the beetle’s feeding preferences and characteristics. In Patel et al.’s (Reference Patel, Kumar and Kumar2018) study, fluctuations in food quality did not appear to significantly affect the beetle’s feeding behaviour or consumption efficiency.

Biochemical assimilation of macronutrients

Many studies on other insects show that insects balance their ingestion of food and assimilation of nutrients, particularly macronutrients (Simpson and Raubenheimer Reference Simpson and Raubenheimer2000; Sterner and Elser Reference Sterner and Elser2002; Raubenheimer and Simpson Reference Raubenheimer and Simpson2003; Mayntz et al. Reference Mayntz, Raubenheimer, Salomon, Toft and Simpson2005); however, few such studies on Z. bicolorata have been undertaken. Biochemical assimilation of nutrients varies when Z. bicolorata inhabits Parthenium-dominant agroecosystems, according to local temperature and altitude. Adult females inhabiting high altitude–low temperature regions were large and assimilated greater concentrations of lipids than did females inhabiting low altitude–high temperature regions, but the small females assimilated higher concentrations of proteins from consumed Parthenium (Kumar et al. Reference Kumar, Choudhary and Kumar2021b). Another study reported that the assimilation of macronutrients is affected significantly by temperature: when temperature increases, nutrient assimilation decreases, and fourth-instar larvae were shown to assimilate the nutrient to the greatest degree, with third-instar larvae being the next most efficient at assimilation macronutrients (Bhusal et al. Reference Bhusal, Ghimire, Patel, Bishta, Upadhyaya and Kumar2020). Patel et al. (Reference Patel, Singh, Patel, Kumar and Kumar2020b) showed that larvae accumulated lower concentrations of glucose, proteins, and triacylglycerols and have reduced body biomass when semiochemical tracks are present; however, larvae reared in the presence of semiochemical tracks were shown to develop more quickly than those reared in the absence of semiochemical tracks.

Antimicrobial peptides

Considerable research has been conducted on antimicrobial peptides and proteins that are present in the haemolymph of insects. The protein composition of Z. bicolorata haemolymph is of diagnostic significance, but such studies regarding this beetle are rare. Jain et al. (Reference Jain, Mishra, Mishra and Parakash2021) illustrated the isolation, purification, identification, and bioinformatics analysis of antimicrobial peptides from the immunised haemolymph of Z. bicolorata: the researchers isolated three novel proteins in the family Chrysomelidae that have no homology in the database, representing novelty of these three isolated proteins and the expression of the rest of 36 well-known proteins.

Karyotypic and morphometric analysis

Morphology of chromosome, karyotype, and morphometric data of chromosomes was performed on Z. bicolorata, and the diploid number of the species was reported to be 24 (Bhatti et al. Reference Bhatti, Tripathi and Khajuria2017). In the same study, meiotic observations identified pachytene, diplotene, late diakinesis, and a metaphase I bivalent stage, and the sex chromosomes (XYp) were found to include the submetacentric X chromosome and a small acrocentric Y chromosome. The sex chromosomes in Z. bicolorata were a somewhat large X chromosome and a small Y chromosome displaying parachute-type morphology in the bivalent stage (Bhatti et al. Reference Bhatti, Tripathi and Khajuria2017).

Intra- and interspecific competition

Intra- and interspecific interactions are known to be associated with both costs and benefits. In predators, these interactions can result in both cannibalism and intraguild predation, whereas, in herbivores, they can result in reduced access to food as an immediate cost. Intra- and interspecific interactions result in many harmful and hazardous effects such as decreased feeding rates, wasting of resources, disease outbreaks, increased interference, decreased developmental rates or delayed development, and reduced adult body size and fitness.

In addition to Z. bicolorata, coccinellid predators (Coleoptera: Coccinellidae) have also been reported from P. hysterophorus (Kumar et al. Reference Kumar, Singh, Prasad, Tiwari and Kumar2017), and when this condition occurs, feeding stages of Z. bicolorata perceived the heterospecific chemicals of coccinellid predators on the leaves of Parthenium plant and reject to consume these leaves where semiochemical footprints were present. This confirms that interspecific interactions between Z. bicolorata and coccinellid predators hinder biocontrol of Parthenium by Z. bicolorata (Patel et al. Reference Patel, Bhusal, Kumar and Kumar2020a).

Intraspecific interactions among Z. bicolorata have been shown to dramatically reduce the growth, development, and survival of the insect’s developmental stages. Crowding due to increased larval density decreases area available for the larvae to move and increases competition among larvae for food (Omkar and Afaq Reference Omkar and Afaq2009; Afaq Reference Afaq2012). As a result, the food use efficiency and survival rates of immature stages decline, and the total larval developmental period increases. Afaq (Reference Afaq2012) also reported that overall mortality was greatest at a larval density of 24 and least at a larval density of four.

Demographic attributes under different biotic and abiotic stressors

Growth and development are key considerations in the identification of optima in living organisms. Abiotic and biotic stressors are recognised to affect growth and development of phytophagous insects (Bernays and Chapman Reference Bernays and Chapman1994). Omkar et al. (2008) confirmed that temperature is a major influence on the growth, development, and survival of Z. bicolorata. According to Saha et al. (Reference Saha, Bangadkar and Raja2015), the optimal thermal range for larval development in Z. bicolorata is 20–30 °C. Rastogi (Reference Rastogi2010) reports that temperatures below 18.5 °C pause larval development and that a temperature above this value hastens the rate of development in Z. bicolorata. However, the beetle’s ability to forebear high or low temperatures relies on the availability of food, the beetle’s age, and its thermal regime (Chidawanyika et al. Reference Chidawanyika, Nyamukondiwa, Strathie and Fisher2017). Zygogramma bicolorata males tend to be smaller in size than females and develop faster, which indicates the occurrence of protandry in the beetle (Pandey Reference Pandey2010). Existence of developmental-rate polymorphism within a group was found during the development of Z. bicolorata; few larvae complete their development sooner and more rapidly acquire the critical biomass for pupation than other larvae. The larvae with slower developmental rates are called slow developers, whereas the larvae that develop more quickly are called fast developers (Afaq et al. Reference Afaq and Kumar2021). The influence of temperature on developmental-rate polymorphism, with slower-developing individuals, found at lower thermal regimes, and these individuals have higher reproductive potential than the fast developers (Afaq et al. Reference Afaq and Kumar2021).

Omkar et al. (2013b) reported the effect of photoperiod in all levels of biological organisation in Z. bicolorata: the insect was found to have the lowest amount of mortality and greatest generation survival rate during times of the year with long days, followed by equinox, short days, and continuous light, whereas greatest mortality and lowest generation survival rate were recorded for periods of the year with continuous darkness (Omkar et al. 2013b). First-, second-, and third-instar larvae were more susceptible to the different photoperiodic conditions than fourth-instar larvae (Rastogi Reference Rastogi2010). King (Reference King2008) reported that the eggs and pupae of the beetle are susceptible to dehydration. However, desiccation of eggs can be decreased by the increased humidity on the under surface of leaves. In addition, the late-stage larvae that undergo pupation make compartments within the soil that restrict transpiration and protect the pupae from desiccation (Dhileepan et al. Reference Dhileepan, Setter and McFadyen2000a, Reference Dhileepan, Setter and McFadyen2000b). In consequence, Z. bicolorata establishment might be restricted in locations where thermal regimes are too high or humidity falls below levels that are lethal to the beetle.

Rastogi (Reference Rastogi2010) reported that Z. bicolorata development and immature survival are influenced by different wavelengths of light. White light was found to be the most suitable wavelength of light for Z. bicolorata and suitability declined from white to yellow to blue to red. This confirms the findings of previous studies that factors like temperature (Omkar et al. Reference Omkar, Rastogi and Pandey2008), food (Omkar and Afaq Reference Omkar and Afaq2011), wavelength (Rastogi Reference Rastogi2010), photoperiod (Rastogi Reference Rastogi2010), and crowding (Omkar and Afaq Reference Omkar and Afaq2009) vitally affect the efficacy, survival, and field establishment of the beetle. It would be essential to monitor Z. bicolorata seasonally after field releases to verify its continued existence and activity – particularly after unfavourable conditions such as extreme heat, cold, rain, and fluctuating food availability occur. If a surviving population of the beetle in the field is insufficient to provide effective Parthenium biocontrol, additional releases can be undertaken to increase the local population (Chidawanyika et al. Reference Chidawanyika, Nyamukondiwa, Strathie and Fisher2017).

Oviposition: Cues and orientations

The selection of sites for egg laying by females is one of the critical events in the life cycle of phytophagous insects. Oviposition site selection depends not only on food availability and the presence of conspecific semiochemical tracks but also on the texture, colour, and curve of the surface, the physical structure, and the chemical composition of the oviposition site (Hodek and Honek Reference Hodek and Honek1996; Hrabar et al. Reference Hrabar, Hattas and Du Toit2009; Mattingly and Flory Reference Mattingly and Flory2011). Oviposition site selection has a major effect on spatial allocation of a species and can influence the population dynamics (Hassell Reference Hassell1978; Pearman and Wilbur Reference Pearman and Wilbur1990) and structure of communities (reviewed by Morris Reference Morris2003).

To the best of our knowledge, only one study (Afaq et al. Reference Afaq and Kumar2022) to date reports on the orientation of Z. bicolorata’s oviposition sites and this insect’s preference for colour and texture as substrates for oviposition. According to that study, Z. bicolorata females oviposit the greatest amount of eggs on negatively geotactic substrata that are 100% parallel to base; however, females oviposited on both negatively phototactic (PN) and positively phototactic (PP) substrata. The females preferred the substrata that had negatively geotactic orientation, regardless of their phototaxis. This may be because of the negatively geotactic foraging behaviour of Z. bicolorata larvae (Afaq Reference Afaq2012). Greatest oviposition was found to occur on green-coloured substrata, least oviposition was observed on white-coloured substratum, and no egg laying was observed on black-coloured substrata. The beetle’s preference for green may be explained by the insect’s preferred food being green. Other studies have shown that Z. bicolorata females oviposited more eggs on plastic than on substrata of other textures – for example, glass, leaves, filter paper, cardboard, or muslin: this may indicate a preference for smooth substrata, which may protect the eggs from abrasion that could occur on rougher substrata. The beetle, however, may find very smooth surfaces, such as glass, problematically slippery. The selection of best oviposition site, in terms of colour and texture, may increase Z. bicolorata’s oviposition rates and offspring survival under laboratory conditions (Afaq Reference Afaq2012).

Chronobiology

The day–night cycle is an important and regular environmental change that all living organism are exposed to. An ability to adjust physiology and behaviour appropriately at specific times during this cycle is necessary for survival. The light- and dark-phase periods are known to influence insects’ physiology, behaviour, and populations. Photoperiod controls the circadian rhythm of an organism and is responsible for the time–activity allocation that characterises a species as diurnal, nocturnal, or crepuscular (Beck Reference Beck1980). According to Afaq and Omkar (Reference Afaq2016), various life history traits of Z. bicolorata – hatching, moulting, eclosion, mating, oviposition, etc. – are controlled by circadian rhythms. Although these rhythms are produced endogenously, they are entrained by the surrounding environment. The majority of mating incidences, oviposition, and pupation were obtained during photophase, but higher incidences of hatching, moulting, and eclosion were observed during the scotophase (Afaq and Omkar Reference Afaq2016). In addition, the progenies of mating pair from late photophase were found to have higher survival rates and develop faster (Afaq and Omkar Reference Afaq2016). These outcomes suggest that offspring derived from late-photophase Z. bicolorata mating pairs may be preferable in augmentative biocontrol of Parthenium because these beetles may have intrinsic capabilities for longer survival and faster development.

Mate selection and mating behaviour

Mate choice can be explained as an organism’s attempt to produce genetically superior offsprings, obtaining direct phenotypic benefits convertible into reproductive ability, or both. Heisler et al. (Reference Heisler, Andersson, Arnold, Boake, Borgia and Hausfater1987) explained it as a route that leads to the propensity of an individual of one sex to mate nonrandomly with respect to one or more varying characters in individuals of the opposite sex. Darwin (Reference Darwin1874) assumed that males typically compete to access females and that females pick among the males. However, the adaptive importance of female choice has been the centre of controversy (e.g., Lande Reference Lande1981; Kirkpatrick Reference Kirkpatrick1982; Halliday Reference Halliday1983; Maynard Smith Reference Maynard Smith1987).

Mate selection in relation to body size

Body size has usually been regarded as a main constraint on an individual’s ecological and physiological characteristics (Honek Reference Honek1993). Omkar and Afaq (Reference Afaq2012) report that Z. bicolorata exhibits size-based mate choice, with both male and female adults preferring large-sized partners over small-sized possibilities for mating. Mating pairs with large-sized individuals have been shown to be more fecund; however, egg viability was affected only by the size of the male partner (Braga Gonçalves et al. Reference Braga Gonçalves, Mobley, Ahnesjo, Sagebakken, Jones and Kvarnemo2010; Omkar and Afaq, Reference Afaq2012). The progeny of the abovementioned mating pair had better fitness, which suggests possible superior nutrient allocation by females and higher supply of accessory gland proteins and sperm by males, in addition to superior quality of genes from both the parents (Bissoondath and Wiklund Reference Bissoondath and Wiklund1996; Helinski and Harrington Reference Helinski and Harrington2011; Omkar and Afaq Reference Afaq2012).

Mate selection in relation to mating status

Zygogramma bicolorata exhibits both polyandry and polygyny, with both males and females of the species preferring to mate with more than one individual of the opposite sex. Omkar and Pandey (Reference Pandey2010) and Afaq and Omkar (Reference Afaq2017a) have confirmed that mating status greatly influenced not only the reproductive performance of the adult beetles but also the fitness of their offspring. The studies revealed that twice-mated females and unmated males were preferred as mates for their superior reproductive performance and proven survivability. In addition, Afaq (Reference Afaq2012) showed that females that had mated with previously mated males appear to be willing to mate again sooner than females that had mated with unmated males.

Mate selection in relation to age

Omkar et al. (Reference Omkar, Pandey, Rastogi and Mishra2010) revealed that Z. bicolorata adults show some degree of age-based mate preference. Middle-aged adults were chosen as mates by middle-aged beetle of opposite sex. Conversely, young and old females showed no preference for males of any age group, young males were found to prefer older females as their mating partners, and older males exhibited no preference (Pandey and Omkar Reference Pandey2013). Pandey and Omkar (Reference Pandey2013) also confirmed that the growth, development, and survival of progeny resulting from the adults’ mate choices were affected by the age of their mother.

Mate guarding behaviour

Mate guarding can be defined as a period of mating that extends beyond the time required for the transfer of ejaculate (Simmons Reference Simmons2001). Such postmating interactions may confer numerous benefits for the mating pair (Alcock Reference Alcock1994) by decreasing sperm competition (Vahed et al. Reference Vahed, Parker and Gilbert2011). The purpose can be achieved either by preventing the remating of a female partner (Parker Reference Parker1984) or by inserting the male copulatory organ into female genitalia to prevent flushing of ejaculate after mating (Chaudhary et al. Reference Chaudhary and Mishra2015). Bhaisare et al. (Reference Bhaisare, Paraste, Kaushik, Chaudhary, Al-Misned and Mahboob2021) reported that Z. bicolorata exhibits mate guarding behaviour to increase reproductive output. Bhaisare and Chaudhary (Reference Bhaisare and Chaudhary2023) also showed that developmental temperature significantly affects mate guarding behaviour in Z. bicolorata, as well as the reproductive attributes of the mating pair.

Ecotoxicological threat of herbicides and insecticides to Zygogramma bicolorata’s biological attributes

Biological control agents that infesting pests and weeds in agricultural fields are vulnerable to insecticides and herbicides applied to manage pests. Several studies have demonstrated the harmful effects of such pesticides on Z. bicolorata (Sushilkumar et al. Reference Sushilkumar, Vishwakarma and Ray2003; Siddhapara et al. Reference Siddhapara, Patel and Patel2012; Hasan and Ansari Reference Hasan and Ansari2016c, Reference Hasan and Ansari2017). Hasan and Ansari (Reference Hasan and Ansari2016c) evaluated the ecotoxic effects of glyphosate (0.44%), atrazine (0.142%), metribuzin (0.075%), alachlor (0.6%), and 2,4-D (0.208%) within the lowest range of their recommended field doses. Their findings show that none of the tested herbicides are safe and that both 2, 4-D and alachlor as extremely toxic to the third-instar larvae of Z. bicolorata. Of the five tested pesticides, glyphosate was found to be the least toxic and might be used for field applications, but this would need to be done under natural field conditions. In addition, Hasan and Ansari (Reference Hasan and Ansari2017) investigated the acute toxicity and sublethal effects of six commonly used insecticides on Z. bicolorata’s biological attributes and life table parameters. Monocrotophos and imidacloprid yielded the highest mortality of third-instar Z. bicolorata larvae and increased the developmental time of other immature stages. None of the tested insecticides was shown to be safe, but of the six, malathion was found to be the least toxic. These studies suggest that selecting the right pesticide and applying the right dose play a critical role in maintaining Z. bicolorata populations and their biocontrol services.

Efficacy against Parthenium hysterophorus

Research conducted by Sushilkumar and Ray (Reference Ray2011) and Kanagwa et al. (Reference Kanagwa, Kilewa and Treydte2020) on the biocontrol efficacy of Z. bicolorata demonstrates that the beetle is a satisfactory potential candidate to reduce P. hysterophorus density in field conditions. In particular, Sushilkumar and Ray (Reference Ray2011) verify that the beetle is capable of defoliating approximately 85% of the weed plant and reducing plant density in Indian agro climatic conditions. The beetle-caused defoliation significantly reduced P. hysterophorus leaf and flower production, plant density, weed biomass, plant height, and seed production. To accomplish successful biological control of the weed, a satisfactory population build-up of Z. bicolorata is essential, this can be achieved by timely releases of the beetle in the target fields. Several such augmentative releases may be necessary to ensure the beetle’s early establishment, but once the beetle becomes established, the population will sustain itself. The damage inflicted on P. hysterophorus by the beetle was more prominent when the biological control agent was released in higher densities and at Parthenium’s early growth stages (Shabbir et al. Reference Shabbir, Sheema and Iram2016). The developmental stage of the beetle at the time of release has also been shown to play a key role during field releases, but the weed’s defoliation and injuries also depend on geographic location (McFadyen and McClay Reference McFadyen and McClay1981). Nonetheless, Z. bicolorata larvae are known to be more effective defoliators than adults are, but adults build up effective populations and propagate new colonies in less time, which results in quick and effective control of Parthenium weed (Hasan et al. Reference Hasan, Al-Ghanim, Al-Misned and Mahboob2020a).

Conclusions and future prospects

Research into Z. bicolorata has shown that the beetle is host specific and has great potential to neutralise and metabolise the toxicants present in Parthenium. The beetle’s adults and larval stages are voracious defoliators of P. hysterophorus. The beetle serves as an alternative to chemical-based herbicides and labour-intensive uprooting, burning, and ploughing to control Parthenium weed. Biotic and abiotic factors, such as temperature, crowding, photoperiod, light wavelength, age, mating status, natural enemies, and quality and quantity of food, affect and influence the beetle’s growth and development. Because of this, it is recommended to monitor these factors during mass rearing of the beetle in laboratory and before the beetle’s release in the field to obtain the best results. Monitoring after release and seasonally is also recommended in order to verify and confirm the level of population build-up and spread necessary for the beetle to act effectively as a biocontrol agent, particularly after extreme environmental conditions.

Future studies that investigate the beetle’s feeding and diapause behaviour are recommended. Molecular studies can be undertaken to identify the specific proteins or genes responsible for specific actions. More studies are also required to better understand Z. bicolorata’s natural enemies and how they affect the beetle’s successful mass rearing in the laboratory and establishment in the field. Research into the nontarget and harmful effects of pesticides on Z. bicolorata would help crop managers better plan and support mass releases of the beetle into agricultural fields. Furthermore, the potential of antimicrobial proteins purified from this beetle for use in antibiotics and other pharmaceutical products remains an area deserving of researchers’ attention.

Acknowledgements

The authors thank the Department of Biosciences, Faculty of Science, Integral University, Lucknow, Uttar Pradesh, India. The manuscript has been approved by a competent authority of the university; the assigned communication number is IU/R&D/2023-MCN0001961.

Competing interests

The authors declare that they have no competing interests.

Footnotes

Subject Editor: Michele Tseng

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Figure 0

Figure 1. Distribution of Zygogramma bicolorata on world map (India and Mexico). (Source: https://www.cabi.org/isc/datasheet/57506).

Figure 1

Table 1. Previous studies on Zygogramma bicolorata

Figure 2

Figure 2. Life cycle of Zygogramma bicolorata on Parthenium weed.

Figure 3

Table 2. Ecological efficiencies of larvae of Zygogramma bicolorata fed on Parthenium leaves (Omkar and Afaq 2011). Values are mean ± standard error; L1, first instar; L2, second instar; L3, third instar; L4, fourth instar; and E.C.I., efficiency of conversion of ingested food; * and **, F-values significant at P < 0.01 and P < 0.001, respectively; NS, F-values nonsignificant at P > 0.05.