The spiraling whitefly, Aleurodicus dispersus Russell (Hemiptera: Aleyrodidae), is a polyphagous pest with an extensive host range (Srinivasa 2000, Boopathi et al. 2014). A direct damage is caused when immature and adult stages of the whiteflies pierce and the suck sap from foliage. As a byproduct of feeding, dense populations of this polyphagous pest cause premature leaf drop along with production of honeydew, which serves as a substrate for the growth of sooty mold (Akinlosotu et al. 1993, Boopathi et al. 2014). Sooty mold blackens the leaf, decreases photosynthetic activity and vigor, resulting in disfigurement of the host (Kumashiro et al. 1983, John et al. 2007). A. dispersus is difficult to control via use of conventional insecticides largely because the body of the insect is covered with heavy waxy flocculent materials (Waterhouse and Norris 1989). Additionally, the wide host range of this insect along with characteristics such as the ability to quickly infest and adapt to different habitats so as to inflict rapid damage, further complicate the management of A. dispersus using conventional chemical insecticides (Waterhouse and Norris 1989, Boopathi et al. 2013). Hence, in an attempt to control A. dispersus infestations, one prime area of interest wherein efforts have been focused off late is the biological control (Huffaker and Messenger 2012). Several reports in India have investigated the utility of common natural enemies of the spiraling whitefly such as predators like Mallada astur (Banks) and Cybocephalus spp., and parasitoids, like Encarsia guadeloupae Viggiani and Encarsia sp. nr. meritoria Gahan, as agents for biological control (Joshi and Yadav 1990, Mani and Krishnamoorthy 1999, Boopathi et al. 2015a).

In India, among the known natural enemies of A. dispersus that can be used in order to regulate its population are the commonly found and widespread green lacewings (Geetha 2000, Mani and Krishnamoorthy 1999). Many studies have documented the potential of green lacewings to function as natural enemies that can regulate the A. disperses population (Geetha 2000, Boopathi et al. 2013, Boopathi et al. 2015a). The green lacewings are considered as one of the most effective generalist predators that can be used for biological control. Green lacewings are an important group of predatory insects (Dean and Satasook 1983) that can be mass reared in the laboratory and used for the purpose of pest control (Syed et al. 2008). Their ability to adapt to a wide range of ecological conditions (Ulhaq et al. 2006) and tolerance to insecticides (Bigler 1984) has made them important in terms of both research as well as field applications (Nasreen et al. 2003).

Mallada desjardinsi (Navas) (Neuroptera: Chrysopidae) is a generalist predator that has been reported to prey on a wide variety of pests such as mealy bugs (Mani and Krishnamoorthy 1989), white flies (Joshi and Yadav 1990, Selvakumaran et al. 1996), bollworms, aphids viz., Lipaphis erysimi (Kalt.), Brevicoryne brassicae (L.) and Uroleucon carthami (H.R.L.) (Kabissa et al. 1996, Gade et al. 2011), neonates of Helicoverpa armigera (Hübner), Spodoptera litura F. and Earias vitella (F.) (Nagamallikadevi et al. 2013) as well as the red spider mite (Babu et al. 2011). Although generalist predators lack prey specificity, they can exert a significant impact on various pest complexes (Symondson et al. 2002). The larvae of green lacewings feed on plant-infesting pests such as aphids, whiteflies, scales, caterpillars, spider mites, etc. (McEwen et al. 2001). Green lacewing adults are commonly considered nonpredatory, as they generally feed on nectar, pollen, or honeydew although a few of them are known to be predatory in their eating habits (Coppel and Mertins 1977). Project Directorate of Biological Control ([PDBC] 1998), Mani and Krishnamoorthy (1999), and Geetha (2000) reported that the larvae of Mallada astur (Banks) prey on A. dispersus, but no information is available in literature regarding the feeding potential and biology of M. desjardinsi on A. dispersus. In recent years, green lacewings have begun to be regarded as an exceptional addition to any IPM (Integrated Pest Management) program. Other natural enemies or predators and parasitoids of A. dispersus suffer from crucial shortcomings that prevent them from controlling this pest efficiently. This study therefore was conducted in an attempt to study the distribution and biology of M. desjardinsi in order to analyze its predatory potential against A. dispersus with the view of exploiting it as a potential biological control agent for regulation of the whitefly population.

Materials and Methods

Biology and Feeding Potential of M. desjardinsi on the A. dispersus Populations

Laboratory experiments were conducted in order to determine the feeding potential and biology of M. desjardinsi. M. desjardinsi individuals were placed separately in small plastic containers (10 by 5 cm) that were covered with a khada cloth (0.3531 mm). Each M. desjardinsi individual was examined daily and fresh leaves infested with 150 A. dispersus were provided so as to ensure that the predator always had an excess of prey. The leaves along with life stages of A. dispersus used in the experiment were examined under microscope, and the number and life stages of A. dispersus fed to each M. desjardinsi individual was counted. The study was continued till the predator died and the experiment was maintained as described previously by Gautam (1994). The stage-specific predatory potential of different larval stadia of M. desjardinsi on different life stages of A. dispersus was also studied. For this, each stage of A. dispersus (eggs, nymphs, pupae, and adults) were introduced separately into small plastic containers (10 by 5 cm) covered with a khada cloth (0.3531 mm) and a single larva of M. desjardinsi was introduced. The larvae used for each of the experiments were less than a day old and starved for 6 h prior to the start of the experiment by keeping them individually in separate plastic containers. The number of A. dispersus life stages consumed in 24 h was counted using a stereo binocular microscope (Olympus 10 X). The experiment was replicated 10 times. The data on incubation period of eggs, developmental period of each larval stadium, prepupal period, pupal period, adult longevity, and fecundity were recorded. The larvae were provided with A. dispersus nymphs in plastic containers as described above. The experiment was replicated 10 times.

Table 1.

A. dispersus and M. desjardinsi samples collected from seven different geographic regions of India

Table 2.

Standard evaluation system based on the intensity of damage (%) by A. dispersus

Results

Feeding Efficiency of M. desjardinsi

This is the first report that documents the predatory potential of M. desjardinsi for A. dispersus. The mean consumption for different stages of M. desjardinsi on different prey stages of A. dispersus is statistically significant (Table 5). The feeding efficiency of M. desjardinsi increased with advancement in each developmental stage. The first instar of M. desjardinsi consumed significantly less A. dispersus eggs (54.0 ± 0.316), first-instar nymph (58.0 ± 0.316), second-instar nymph (57.8 ± 0.490), third-instar nymph (50.6 ± 0.678), fourth-instar nymph (45.0 ± 0.447), pupae (40.2 ± 0.583), and adults (20.8 ± 0.374) as compared to the second instar and third instar of M. desjardinsi. The second instar of M. desjardinsi consumed more number of A. dispersus eggs (77.8 ± 0.663), first-instar nymph (77.6 ± 0.510), second-instar nymph (79.2 ± 0.374), third-instar nymph (78.6 ± 0.510), fourth-instar nymph (67.2 ± 0.860), pupae (78.6 ± 0.748), and adults (59.8 ± 0.490) as compared to the first instar but significantly less than the third instar of M. desjardinsi. The third instar of M. desjardinsi consumed significantly more number of A. dispersus eggs (79.8 ± 0.374), first-instar nymph (78.2 ± 0.583), second-instar nymph (124.0 ± 0.775), third-instar nymph (78.8 ± 0.374), fourth-instar nymph (79.2 ± 0.374), pupae (78.8 ± 0.374), and adults (62.2 ± 0.800) than any of the previous stages. The differences between different developmental stages of A. dispersus (F = 1350.75; df = 6; P < 0.000), different developmental stages of M. desjardinsi (F = 8237.26; df = 2; P < 0.000), and the interaction between different developmental stages of A. dispersus × different developmental stages of M. desjardinsi (F = 320.91; df = 12; P < 0.000; Table 6) were statistically significant.

A significant difference was observed when consumption of different developmental stages of A. dispersus by M. desjardinsi was analyzed. The mean consumption of the second-instar nymphs of A. dispersus by M. desjardinsi was the highest (261.0 ± 1.6856) as compared to all the other developmental stages. The average number of A. dispersus adults consumed by M. desjardinsi was significantly less (142.8 ± 2.4713) as compared to other developmental stages (Fig. 1). Significant variations in the predatory potential of M. desjardinsi were observed. These variations were found to be dependent upon the size and quantity of food (A. dispersus) offered to different developmental stages of M. desjardinsi as well as the size and longevity of different developmental stages of M. desjardinsi. The third larval instar of M. desjardinsi was observed to be voracious feeder and found to consume maximum number A. dispersus of all the stages during its life span (578.4 ± 2.0396) as compared to the first (326.4 ± 1.0296) and second (521.4 ± 1.7493) instars (Fig. 2).

Table 3.

Distribution of A. dispersus and its predator, M. desjardinsi, in the seven geographic regions of India

Table 4.

Analysis of variance (ANOVA) of data on distribution of A. dispersus and its predator, M. desjardinsi, from seven different geographic regions of India

Table 5.

Predatory potential of M. desjardinsi feeding on A. dispersus (n = 150)

Table 6.

Analysis of variance (ANOVA) of data on predatory potential of M. desjardinsi feeding on A. dispersus

Discussion

To the best of our knowledge this is the first report of its kind regarding the occurrence and distribution of M. desjardinsi feeding on A. dispersus in India (2012–2013) under field conditions. In the current investigation, Bengaluru, Karnataka, was observed to have the highest density of M. desjardinsi population (26.6% and 5.05 ± 0.108 per plant). Earlier, Geetha (2000) reported the occurrence of a related species, M. astur, to be preying on all stages of A. dispersus in Coimbatore, Tamil Nadu, and Mani and Krishnamoorthy (1999) reported the same in Bengaluru, Karnataka, India.

Fig. 1.

Total number (±SE) of different stages of prey (A. dispersus) consumed by a single individual of M. desjardinsi during its entire life cycle.

Fig. 2.

Total number (±SE) of prey (A. dispersus) consumed by different stages of M. desjardinsi during its entire life cycle.

Fig. 3.

Life cycle of M. desjardinsi feeding on A. dispersus.

Furthermore, this is the first report that analyzes the predatory potential of M. desjardinsi feeding on different stages of A. dispersus under laboratory conditions. Studies by Joshi and Yadav (1990) reported the feeding potential of M. desjardinsi (=M. boninensis) on Bemisia tabaci (Gennadius) under laboratory conditions. In the current investigation, the third stadium of M. desjardinsi was seen to be the most voracious predator of all life stages of A. dispersus, but it is to be noted that second stadium demonstrated an equal propensity for the consumption of the first and third instar as well as pupae of A. dispersus. As expected, M. desjardinsi first stadium presented with the least capacity to consume various life stages of A. dispersus. Our findings are largely in agreement with the observations reported by Huang and Enkegaard (2009) and Babu et al. (2011) who claimed that the first stadium of M. desjardinsi (=M. boninensis) consumed the least numbers of red spider mites. M. desjardinsi larvae easily removed the waxy material covering of A. dispersus by using their well-developed setae and mandibles, and thus demonstrated a great efficiency in prey searching and predatory potential on A. dispersus. The M. desjardinsi larvae consumed on an average 487.4 A. dispersus individuals. This is in parallel with a study conducted by Joshi and Yadav (1990) who reported that an M. desjardinsi (=M. boninensis) larva consumes on an average 453 nymphs of B. tabaci. It has also been reported that a single larva of M. astur can consume a total of 200 nymphs (Mani and Krishnamoorthy 1999). Earlier, it was reported that a single individual of the Mallada sp. can consume on an average 23,490 whiteflies during its entire life cycle (PDBC 1998). Ingole et al. (2005) reported that the release of M. desjardinsi (=M. boninensis) had reduced the Aleurocanthus woglumi Ashby population in citrus plants by 34.6–36.7%.

Table 7.

Life cycle parameters of M. desjardinsi on A. dispersus (each datapoint is an average of 10 replicates)

Kabissa et al. (1996), Nehare et al. (2004), and Huang and Enkegaard (2009) have reported that the prey consumption of lacewings increases with advancement in larval instars. Second and third stadia of M. desjardinsi consumed a much larger number of A. dispersus individuals. This clearly demonstrates that the third-instar lacewings are far more voracious than the second and first instars (Atlihan et al. 2004, Huang and Enkegaard 2009). In the present study, when the prey stages were offered separately, the third stadium of M. desjardinsi was seen to consume more eggs and more first and second instar of A. dispersus than any other stage of M. desjardinsi. These findings are largely in agreement with the observations reported by Joshi and Yadav (1990) regarding the predation by M. desjardinsi (=M. boninensis) on B. tabaci. A possible reason for the higher consumption of eggs as well as first and second instar nymphs of A. dispersus could be that the size of the prey is smaller and has less waxy flocculent substance as compared to the body size of third and fourth instar nymphs and adults, and also the static state.

When all the life stages of A. dispersus were offered together, all three stadia of M. desjardinsi were seen to accept every stage of prey. The foraging behavior of many predators is observed to be dependent on the relation between the body size of the predator and prey (Sabelis 1992). Mean prey size increases with the body size of the predator (Werner and Gilliam 1984, Cisneros and Rosenheim 1997). In our study, we found that all three instars of M. desjardinsi accepted all life stages of A. dispersus including the adults. The reason for the acceptance of all life stages of A. dispersus by M. desjardinsi larvae may be that the body size of A. dispersus is much smaller than that of M. desjardinsi as has been hypothesized previously by Cheng et al. (2010) who reported that the green lacewing, Mallada basalis (Walker), larvae did not demonstrate any noticeable preference for any particular life stage of mites but rather accepted all the life stages equally.

Developmental stages of M. desjardinsi consist of an egg, three stadia, prepupae, pupae, and an adult form. The female is known to be marginally larger than male. Nagamallikadevi et al. (2013) studied the biology of M. desjardinsi on three different neonates of H. armigera, S. litura and E. vitella. Larval stages of many chrysopids cover the dorsum with debris including their own cast cuticles, remains of prey, and the fragments of vegetables or other materials; such larvae are called trash carriers or debris carriers. This is hypothesized to be a protective mechanism employed by larvae to guard against other predators (Canard and Principi 1984). Similarly, in our study we also noticed this camouflaging behavior in M. desjardinsi. The third stadium of M. desjardinsi spins a silken cocoon within which it becomes enclosed. In the present investigation, the total developmental period of M. desjardinsi averaged 24.1 ±0.99 d on A. dispersus. Studies by Joshi and Yadav (1990) have reported that the total developmental period of M. desjardinsi (=M. boninensis) feeding on B. tabaci averaged 32.64 d. Similarly, Babu et al. (2011) have reported that the developmental period of M. desjardinsi (=M. boninensis) on red spider mites is around 31.7 d. Earlier research indicated that the average developmental periods of a related species, M. astur, on nymphs of A. dispersus were 13.5 d (PDBC 1998) and 14.2 d (Geetha 2000). The larval duration of M. desjardinsi averaged 12.1 ±0.57 d. Similarly, the larval duration of C. zastrowi sillemi is reported as 24.8 d (Gerling 1986) for M. astur it is known to be 11.6 d (Venkatesan et al. 2002) and for M. basalis the same is computed to be 11.8 d (Chang 2000). The latter value is closer to our observations in this study. We found that the longevity of M. desjardinsi female was 27.6 ± 1.69 d on A. dispersus population. However, Joshi and Yadav (1990) have reported that the average longevity of M. desjardinsi (=M. boninensis) females and males was 64.8 ± 15.97 and 27.36 ± 8.03 d, respectively, which is higher than our findings. Nagamallikadevi et al. (2013) observed that the male and female longevity of M. desjardinsi (=M. boninensis) is superior over that for neonates of S. litura (21.16, 35.58 d, respectively) rather than H. armigera and E. vitella. The average number of eggs laid by the M. desjardinsi female was 211.1 ± 6.35 eggs. Joshi and Yadav (1990) reported that the total number of eggs laid by the M. desjardinsi (=M. boninensis) female averaged 431 ± 38.62 eggs when fed with B. tabaci nymphs which is higher than those obtained in our investigations. Nagamallikadevi et al. (2013) observed that reproductive potential of M. desjardinsi (=M. boninensis) (94.50 eggs per female) was enhanced by the neonates of S. litura. However, Gerling (1986) reported that the fecundity of M. astur ranged from 315 to 386 eggs per female. This difference in the fecundity of green lacewings might be due to different species of chrysopids, host insects, and environmental conditions used in the different studies.

Biological pest control is an exciting and promising alternative to chemical control (Huffaker and Messenger 2012). In our study results clearly demonstrated that the M. desjardinsi larvae are able to easily remove the waxy material covering of A. dispersus by using their well-developed setae and mandibles, and thus they were observed to demonstrate great efficiency in prey searching as well as predatory potential on A. dispersus. Our findings proved conclusively that M. desjardinsi is an efficient predator of A. dispersus under laboratory conditions, which corroborates the findings of Joshi and Yadav (1990) and Babu et al. (2011), who reported that M. desjardinsi (=M. boninensis) is the best biological control agent against B. tabaci and red spider mites, respectively. Lastly, larval instars of M. desjardinsi were the most voracious feeders of spiraling whiteflies. Thus, this predatory green lacewing has the potential to be exploited for the management of A. dispersus by mass rearing and release on different crops in southern India. However, before drawing firm conclusions about the effectiveness of M. desjardinsi on A. dispersus, further experiments, under field conditions are warranted.