Studies on the predator Apertochrysa astur (Banks) (debris carrying green lacewing) on invasive coconut whiteflies

The invasive whitefly species, rugose spiralling whitefly (RSW) and Bondar’s nesting whitefly (BNW) (Hemiptera: Aleyrodidae) were reported on coconut in 2016 at Pollachi, Tamil Nadu, India and in 2019 in Kerala, India, respectively. Among the natural enemies of whiteflies, Apertochrysa astur (Banks) is the predominant predator observed in the coconut ecosystem. The population effect of RSW and BNW in different host plants, viz., coconut, banana and custard apple, on the growth and development of the A. astur were studied. Further, the effects of A. astur and yellow sticky traps (YSTs) were evaluated against the invasive whiteflies of coconut. The growth and development of the grubs of A. astur were better when fed with the RSW and BNW reared in coconut, followed by custard apple and banana. The weight of the 1 st , 2 nd and 3 rd instar grubs were 0.25 mg, 0.62 mg and 2.46 mg, respectively. The pre-pupal weight was 7.41 mg, and that of the pupa and adult were 8.35 mg and 12.27 mg when fed with RSW. Similarly, when A. astur was fed with BNW reared on coconut, the weight of the 1 st , 2 nd and 3 rd instar grub of A. astur was 0.22 mg, 0.59 mg and 2.24 mg, respectively. The pre-pupal weight was 7.06 mg, and that of the pupa and adult were 8.22 mg and 12.01 mg, respectively. Among the different treatment dosages of A. astur eggs and YSTs evaluated, 3 YST and 10 A. astur eggs palm -1 were highly effective as they reduced RSW and BNW population by 59.7 per cent and 56.7 per cent per cent, respectively. The grubs of A. astur were observed to be extremely efficient in reducing the population of A. rugioperculatus and P. bondari . The results supported that A. astur can be employed as an efficient biological control agent for managing invasive whitefly species in the coconut ecosystem.

Introduction mealybugs constitute major invasions. In India, 469 whitefly species belonging to 71 genera are known to feed on many agricultural, horticultural, and forestry crop plants (Sundararaj et al., 2021). The first report on the incidence of RSW occurred in 2016 at Pollachi, Coimbatore district, western agroclimatic zone of Tamil Nadu (Sundararaj and Selvaraj, 2017) and that of BNW in 2019 in Kerala (Josephrajkumar et al., 2019). These whiteflies suck sap from under the surface of the palm leaves, thereby causing stress to the host plant. Farmers prefer chemical insecticides to manage the whiteflies. However, frequent applications of insecticides result in the problem of resistance, resurgence and residues. Under these circumstances, natural enemies are the best option for managing the whitefly population in the coconut ecosystem.
Lacewings are economically important biocontrol agents which predate on different developmental stages of mealybugs, aphids, thrips, whiteflies and mites under different agroecosystems . Their wide host range, geographical distribution, insecticide resistance, voracious feeding ability and amenability to rearing with the UV sterilized Corcyra cephalonica eggs make them a good bio-agent for pest management (Syed et al., 2008). The adults are free-living and feed only on nectar, pollen, and honeydew (Coppel and Mertins, 1977). Among the natural enemies of RSW and BNW occurring in coconut, banana and custard apple, A. astur is the predominant predator.
Yellow sticky traps (YSTs) are commonly used for monitoring pest populations, including whiteflies, leaf miners, and aphids (Gu et al., 2008). Abdel-Megeed et al. (1998) also demonstrated that yellow sticky traps could significantly reduce the density of B. tabaci in the field for control purposes. The combination of YSTs and parasitoids has proven to be effective in controlling B. tabaci in a greenhouse (Shen and Ren, 2003). With this background, we have studied the influence of RSW and BNW in different host plants on the development of A. astur and fixed the host plant for mass culturing RSW and BNW to rear A. astur. Also, the combination of A. astur and YST on the population reduction of A. rugioperculatus and P. bondari was investigated.

Influence of RSW and BNW in different host plants on the growth and development of A. astur
A laboratory experiment was conducted to study the effect of RSW and BNW in different host plants on the growth and development of A. astur. In greenhouse conditions, the culture of RSW was maintained in host plants, viz., coconut, banana and custard apple. A newly emerged 1 st instar grub of A. astur was released individually in each insectrearing dish of dimension (90 × 40 mm) dish and provided 40 numbers of 2 nd instar nymphs of RSW reared on coconut, banana and custard apple daily until their adult stage. The host plants used for culturing RSW were considered treatments and replicated eight times. The weight of the grubs, prepupa, pupa and adults of A. astur were measured using the weighing balance. Observations on the grub period, pupal period and adult longevity were also recorded. The experimental procedure mentioned above for RSW was followed to assess the effect of BNW reared on different host plants on A. astur.

Effect of yellow sticky trap and A. astur on coconut trees
A field trial was conducted in the New Area at the Tamil Nadu Agricultural University, Coimbatore, from March to May 2021. Three-yearold coconut palms infested with invasive whitefly species were selected. The treatments fixed were 10 eggs of A. astur palm -1 , 20 eggs of A. astur palm -1 , 30 eggs of A. astur palm -1 , 1 YST palm -1 , 2 YST palm -1 , 3 YST palm -1 , 1 YST+ 30 eggs palm -1 , 2 YST+ 20 eggs palm -1 and 3 YST+ 10 eggs palm -1 . Control was not provided with either YST or eggs of A. astur. The YSTs used were 1 × 1 feet in dimension and were smeared with castor oil as adhesive on both sides. These treatments were replicated thrice. A total of 30 trees were utilized for the experiment. The incidence of RSW and BNW was assessed from ten leaflets in three bottommatured fronds once a week. The per cent reduction of the whitefly population was computed using Abbott's formula (Abbott, 1925).

Statistical analysis
The data collected under laboratory and field experiments in a completely randomized design were analyzed using analysis of variance (ANOVA) using AGRES 3.01 and AGDATA software. Data in the form of numbers were transformed to square root values. The mean values of the treatments were compared using DMRT at a 5 per cent level of significance.

Results and discussion
The quantity and quality of the prey were observed to greatly impact the reproductive potential of the adults (Canard, 2001). The host plants used had a significant effect on the growth and development of A. astur. Among them, whiteflies reared on coconut enhanced the growth and development of A. astur.
All three instars of the grub were healthier in terms of weight when provided with RSW, and BNW was reared on coconut plants. The weights of the 1 st , 2 nd and 3 rd instars, when fed with RSW reared on coconut, were 0.25 mg, 0.62 mg and 2.46 mg; their developmental period was 3.6, 5.4 and 6.2 days, respectively. The duration of pre-pupa of A. astur was recorded as 2.3 days, and their weight was 7.41 mg. The pupa weighed 8.35 mg, and the adult weight was 12.27 mg. The period of pupa stage and adult longevity was 9.2 and 16.9 days, respectively ( Table 3). The grub weight was 0.19 mg in 1 st instar, 0.57 mg in 2 nd instar, 2.13 mg in 3 rd instar, 7.14 mg in pre-pupal, 8.08 mg in pupal and 12.02 mg in adult stages when fed with RSW cultured in the custard apple (Table 1). The duration of the 1 st , 2 nd , 3 rd , pre-pupa, pupa and adults were 3.9, 5.8, 6.9, 2.4, 9.3 and 17.1 days, respectively. The growth of the grubs was least when provided with the RSW infested in banana leaves. The weights of the 1 st , 2 nd and 3 rd instars were 0.16 mg, 0.51 mg and 2.04 mg; their duration was 4.2, 6.5, and 7.0 days, respectively. The weight of pre-pupa was 6.83 mg, with a development duration of 2.6 days. The duration of the pupa and adult were 9.8 and 17.8 days, along with their weight of 7.87 mg and 11.83 mg, respectively.
Similarly, when A. astur was fed with BNW reared in coconut, the weight of the 1 st , 2 nd and 3 rd instar grub was 0.22 mg, 0.59 mg and 2.24 mg with the duration of 3.8, 6.0 and 6.8 days, respectively ( Table 2). The pre-pupal weight was 7.06 mg, and their duration was 2.3 days. The weight of the pupa and adult was 8.22 mg and 12.01 mg, and their duration was 9.2 and 17.3 days, respectively. The weight of grubs was 0.16 mg in 1 st instar, 0.52 mg in 2 nd instar, 2.01 mg in 3 rd instar, 6.89 mg in pre-pupal, 7.88 mg in pupal and 11.97 mg in the adult stage when fed with BNW reared on custard apple. Their duration was 4.3, 6.4, 7.1, 2.5, 9.5 and 17.7 days, respectively. The growth of the grubs was least when provided with the BNW infested in banana leaves; the duration of the 1 st , 2 nd and 3 rd instars was 4.8, 6.9 and 7.7 days and weighed 0.12 mg, 0.46 mg and 1.83 mg, respectively. The weight of the pre-pupa was 6.54 mg, and their duration was 2.6 days. The weights of the pupa and adult were 7.51 mg and 11.48 mg, and the duration was 9.9 and 18.4 days (Table 4.), respectively. The findings showed that the grubs favoured the RSW life stages over those of the BNW when reared on different host plants.
The duration of development and weight of the A. astur grubs varied significantly among the three host plants, coconut, banana, and custard apple. Coconut was found to be an appropriate host since it had the lowest developmental time and the heaviest grub weight. Similar results were also reported on another species of green lacewing when C. rufilabris fed on Bemisia argentifolii reared on cucumber and melon had the quickest development, much longevity and heavy in weight than when it was reared on poinsettia and bean (Legaspi et al., 1994). Moreover, Giles et al. (2009) also reported that the grubs of C. rufilabris when supplied with pea aphids reared on alfalfa, had faster developmental rates than with the pea aphids reared on faba bean. Almost all whiteflies of economic importance can be monitored using yellow sticky traps (Yano, 1987). The population of RSW and BNW were   drastically reduced when the yellow sticky trap and eggs of A. astur were used together. The highest per cent reduction of the RSW population was observed to be 59.7 per cent when three YST and 10 eggs palm -1 were used in the palms. On the other hand, when two YST and 20 eggs palm -1 were used, 55.8 per cent of the whitefly population was reduced. The population was reduced to 54.2 per cent when one YST and 30 eggs palm -1 were used. The YSTs, when used @ three, two and one palm -1 , resulted in the reduction of the whitefly population to the tune of 50.5, 46.0 and 39.7 per cent, respectively (Table 5). Similarly, the eggs of A. astur, when stapled in the underside of the coconut leaflet @ 10 eggs, 20 eggs and 30 eggs palm -1 , 8.9, 18.8 and 24.8 per cent of the RSW population were reduced within a period of eight weeks, respectively. Similar to our observations, Elango et al. (2021) had reported that the maximum number of whitefly adults was attracted when traps were smeared with castor oil @ 270.59 adults trap -1 week -1 in coconut. Similarly, Premalatha and Rajangam (2011) reported that using YST had reduced Trialeurodes vaporariorum in gerbera. The highest per cent reduction of BNW was observed to be 59.7 per cent when three YSTs and 10 eggs palm -1 were used. On the other hand, when 2 YST and 20 eggs palm -1 were used, 53.5 per cent of the whitefly population was reduced. The YSTs, when used @ three, two and one palm -1 , the whitefly population reduced to the tune of 46.5, 42.3 and 37.0 per cent, respectively (Table 6.). The BNW population was reduced to 6.7, 13.3 and 16.9 per cent when 10 eggs, 20 eggs and 30 eggs palm -1 were used. Duelli (2001) and Nordlund et al. (2001) reported that when the mated female adults of the chrysopids were released into the field, they dispersed and left the target site. To overcome this issue, the eggs of A. astur were stapled in the undersurface of the infected coconut leaflets. The grub stages of A. astur were found efficient in the field conditions which was previously reported by (Rao et al., 2020) that in four years old hybrid Godavari Ganga plantation, the RSW population was reduced to 3 spirals per leaflet in the palms after 20 days when 500 eggs of Dichochrysa astur were clipped in five palms.
Results from the field trials could also be compared with the reports on the effect of Chrysoperla spp. on aphids and whiteflies. Alghamdi et al. (2018) observed that, after the second release of five grubs of C. carnea per plant, there was a 90 and 97 per cent reduction of aphid and whitefly populations in squash and a cent per cent reduction in sweet pepper plants. Similarly, El-Arnaouty et al. (2000) obtained the best results when second-instar grubs of C. carnea were released on green pepper plants under greenhouse conditions against M. persicae.

Conclusion
Invasive whiteflies reared on coconut significantly influenced the growth and development of A. astur when compared to the whiteflies reared on other host plants like banana and custard apple. The data obtained from the field trials showed that the YSTs and releases of A. astur successfully suppressed the invasive whitefly populations in coconut fields. Control of two whitefly species under investigation differed according to the number of eggs released and the number of yellow sticky traps used. Therefore, the predatory green lacewing, A. astur, and YST can be exploited as an efficient strategy for managing invading whiteflies in the coconut ecosystem.