Exploring the potential of Delphastus davidsoni (Coleoptera: Coccinellidae) in the biological control of Bemisia tabaci MEAM 1 (Hemiptera: Aleyrodidae)

1 Introduction

Over the past two decades the whitefly Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae), a worldwide pest, has caused substantial economic damage to major vegetables, fruits, legumes, and ornamental crops (De Barro et al. 2011; Perring et al. 2018). As a polyphagous phloem feeder, B. tabaci has reportedly colonized more than 900 plant species (Simmons et al. 2008). At high infestations, B. tabaci feeding results in stunted or dead plants, significantly reducing yield. The insect is also a vector to over 300 plant viruses, further exacerbating economic losses (Polston et al. 2014; Gilbertson et al. 2015).

The first report of B. tabaci in Brazil was in the 1920s (Bondar 1928). As a complex of cryptic species, B. tabaci consists of 44 species that are morphologically indistinguishable (De Barro et al. 2011; Kanakala and Ghanim 2019). The species Middle East-Asia Minor 1 (MEAM1, formerly B biotype) was initially reported in the 1990s and is now the most prevalent species on agricultural crops in Brazil (Lourenção and Nagai 1994; Kanakala and Ghanim 2019; Moraes et al. 2018). Due to its ability to cause economic damage to both food and ornamental crops, insecticides became the primary method to control B. tabaci MEAM1. However, overreliance on insecticides has resulted in high levels of resistance and reduced control of B. tabaci MEAM1 (Naveen et al. 2017; Dângelo et al. 2018). Costly insecticide applications, environmental contamination, direct and indirect effects of insecticide application on non-target organisms, human health safety, and increasing demand for more sustainable food production continue to drive the search for an efficient integrated pest management (IPM) program for B. tabaci MEAM1.

The use of biological control to manage B. tabaci MEAM1 has received increased attention due to its ability to provide cost effective pest control without the downsides of using synthetic insecticides (van Lenteren et al. 2018; Togni et al. 2019; Sani et al. 2020). Predacious coccinellids (Coleoptera) are widely used as biological control agents of hemipterans, such as whiteflies and aphids. At least 40 coccinellid species with various degrees of oligophagy prey on immature B. tabaci (Gerling et al. 2001; Arnó et al. 2010; Kheirodin et al. 2020; Kumar et al. 2020). Coccinellids in the subfamily Microseismical, tribe Seranguiini, which includes genera Delphastus and Serangium, are efficient predators of whiteflies (Frank and Mizell 2020; Kheirodin et al. 2020). Delphastus catalinae (Horn), Delphastus pusillus (LeConte), and Delphastus pallidus (LeConte) are the most prevalent species along the eastern coast of the United States (Gordon 1994; Kheirodin et al. 2020; Kumar et al. 2020). D. pusillus also is present in the northeastern U.S., including New Hampshire and Maine (Hesler 2021). Both D. catalinae and D. pusillus have been applied to IPM programs of whiteflies in tropical plants, semi-tropical plants, and commercial greenhouses (Hoelmer et al. 1993; Liu 2005; Legaspi et al. 2006, 2008; Perring et al. 2018). These species can consume up to 10,000 whitefly eggs or 700 fourth instar nymphs during an adult lifetime, although numbers could be much greater under greenhouse conditions (Hoelmer et al. 1993). Inside exclusion cages placed in an open cotton field, D. catalinae reduced B. tabaci infestation by 55–67 % (Heinz et al. 1994), prompting its introduction into the east Mediterranean region of Turkey.

Delphastus davidsoni Gordon is a South American species (Gordon 1994). It was first reported preying on B. tabaci in a two-year survey conducted on a variety of agricultural crops in Central Brazil (Oliveira et al. 2003). D. davidsoni adults are small, glossy black beetles with pale legs, measuring about 1.4 mm in length (Baldin et al. 2011). Adult males are distinguished by an orange-colored head, while females are entirely black. Larvae are elongated with fine short setae and pupae are yellowish and spherical (Legaspi et al. 2008; Baldin et al. 2011). Given its similarity with other Delphastus species, morphological identification of D. davidsoni requires careful examination of the genitalia.

D. davidsoni has been observed in several Brazilian regions. Baldin et al. (2011) found larvae and adults preying on B. tabaci MEAM1 reared on collard greens (Brassica oleracea L. var. acephala; Brassicaceae) in southeast Brazil, while Petenusso and Giorgi (2018) observed the insect preying on psyllids, Euphalerus clitoriae (Burckhardt and Guajará; Hemiptera: Psyllidae) in northeast Brazil. Despite evidence of widespread distribution in South America, the insect, and its feasibility in the IPM of key pests such as B. tabaci MEAM1, remains understudied. In this context, the main goal of this research was to provide an initial assessment of the potential of D. davidsoni to consume eggs and larvae of B. tabaci MEAM1. Food preference and predatory capacity of both adults and larvae of the lady beetle were evaluated on B. tabaci MEAM1 on collard greens. In addition, we report the biological performance of D. davidsoni larvae preying on immature stages of B. tabaci MEAM1.

2 Materials and methods

3 Results

3.1 Predatory capacity of D. davidsoni adults

One hour after the release of D. davidsoni adults, no statistical differences were observed among the treatments (Table 1). At time points 2 h through 12 h, there were significantly higher number of adults consuming fourth instar B. tabaci than eggs or first–third instars. Within 2 h of beetle release, there were approximately six times more adults consuming fourth instars than other B. tabaci developmental stages. At 24 h after adult release, there were significantly more adults consuming fourth instars than eggs, but no significant difference was observed between adults consuming fourth and first–third instars. In terms of cumulative consumption, fourth instar B. tabaci were the most consumed by D. davidsoni adults (64.40 nymphs), followed by eggs (30.50 eggs), and by first–third instar (3.50 nymphs) treatments (Figure 1).

Table 1:

Number of Delphastus davidsoni adults (mean ± SE) consuming different stages of Bemisia tabaci at 1, 2, 3, 6, 12, and 24 h after release in multi-choice test.

Treatment	Evaluation period
	1 h	2 h	3 h	6 h	12 h	24 h
Eggs	0.10 ± 0.06	0.10 ± 0.03b	0.10 ± 0.01b	0.20 ± 0.05b	0.10 ± 0.04b	0.00 ± 0.00b
First–third instar	0.00 ± 0.00	0.00 ± 0.00b	0.20 ± 0.07b	0.20 ± 0.08b	0.10 ± 0.05b	0.20 ± 0.03ab
Fourth instar	0.10 ± 0.04	0.60 ± 0.12a	0.80 ± 0.16a	1.00 ± 0.07a	0.80 ± 0.17a	0.70 ± 0.14a
P	0.0742	0.0264	0.0372	0.0214	0.0219	0.0405

1. Means followed by the same letter in each column do not differ by Tukey’s test (P > 0.05).

Figure 1:

Cumulative consumption (mean ± SE) of different stages of Bemisia tabaci by Delphastus davidsoni adults 24 h after release in multi-choice test. Means followed by the same letter do not statistically differ by Tukey’s test (P > 0.05).

3.2 Prey consumption of D. davidsoni larvae

At 24 h, D. davidsoni larvae consumed significantly more fourth instar B. tabaci (14.60 nymphs) than eggs (7.28) (Figure 2). At 10 days after release, there were no significant differences in number of first–third and fourth instar consumed by D. davidsoni larvae (148.30 and 115.30 nymphs, respectively), but there were significantly fewer eggs consumed (86.60 eggs) than the other developmental stages.

Figure 2:

Cumulative consumption (mean ± SE) of different stages of Bemisia tabaci by Delphastus davidsoni larvae at 24 h (A) and 10 days (B). Means followed by the same letter do not statistically differ by Tukey’s test (P > 0.05).

3.3 Biological performance of D. davidsoni

D. davidsoni developmental time was significantly influenced by diet (Table 2). First instar D. davidsoni development was completed within 1.9 days when consuming fourth instar B. tabaci, differing significantly from when consuming first–third instar B. tabaci (4.25 days). Similarly, second instar D. davidsoni developmental time was significantly reduced when consuming fourth instar B. tabaci (1.10 days) than when consuming first–third instar (2.16 days). At the third D. davidsoni instar, developmental time was reduced when consuming fourth instar B. tabaci (1.8 days), differing significantly from when consuming first–third instar (3.20 days), and eggs (3.00 days). Fourth instar D. davidsoni likewise had reduced developmental time when consuming fourth instar B. tabaci (2.87 days) differing significantly from when consuming B. tabaci first–third instar or eggs, with 4.40 and 5.50 days, respectively. Overall, the time for complete D. davidsoni larval development was shorter when consuming fourth instar B. tabaci (7.87 days) compared to when consuming B. tabaci first–third instar or eggs, requiring on average an additional 4.73 and 6.13 days to complete the larval stage, respectively.

Table 2:

Developmental time (mean ± SE) of Delphastus davidsoni consuming different immature stages of Bemisia tabaci.

Treatment	Time (days)
	First instar	Second instar	Third instar	Fourth instar	Total developmental time
Eggs	3.75 ± 0.26ab	2.00 ± 0.19ab	3.00 ± 0.18a	5.50 ± 0.32a	14.00 ± 2.25a
First–Third instar	4.25 ± 0.65a	2.16 ± 0.14a	3.20 ± 0.21a	4.40 ± 0.20a	12.60 ± 1.42a
Fourth instar	1.90 ± 0.11b	1.10 ± 0.23b	1.80 ± 0.17b	2.87 ± 0.16b	7.87 ± 1.09b
P	0.0441	0.0278	0.0369	0.0159	0.0338

1. Means followed by the same letter in each column do not differ by Tukey’s test (P > 0.05).

The consumption of fourth instar B. tabaci resulted in D. davidsoni larval survival of 82.25 % (Figure 3). Larval survival was reduced to 48.44 % and 19.44 % when D. davidsoni consumed B. tabaci first–third instar or eggs, respectively. However, pupal survival was not significantly different between D. davidsoni consuming fourth (94.43 %) or first–third instar B. tabaci (85.75 %) (Figure 4).

Figure 3:

Larval survival (% mean ± SE) of Delphastus davidsoni preying on different stages of Bemisia tabaci. Means followed by the same letter do not statistically differ by Tukey’s test (P > 0.05).

Figure 4:

Pupal survival (% mean ± SE) of Delphastus davidsoni preying on different stages of Bemisia tabaci. Means followed by the same letter do not statistically differ by Tukey’s test (P > 0.05).

4 Discussion

For coccinellids, prey size and abundance are considered primary factors in food preference (Dixon 1959; Albuquerque et al. 1997; Dixon and Dixon 2000). In this study, adult D. davidsoni were more attracted to fourth instar B. tabaci, resulting in greater consumption (Figure 5). Both D. davidsoni larvae and adults exhibited a lower predatory performance and delayed larval development when B. tabaci eggs were offered. These findings contrast with existing literature for Delphastus spp., where B. tabaci eggs were the most consumed by D. catalinae and D. pusillus. Interestingly, in previous research the consumption of B. tabaci by Delphastus spp. decreased as prey aged and became larger (Hoelmer et al. 1993; Liu 2005; Oriani and Vendramim 2014). Under optimal survival conditions, Hoelmer et al. (1993) reported D. catalinae (reported as D. pusillus) may consume up to 10,000 eggs or 700 fourth instar nymphs during its life span, and rarely attacked older nymphs when younger stages were available. Most recently, a study by Kumar et al. (2020) compared consumption of two B. tabaci biotypes, MEAM1 and Mediterranean, eggs and nymphs by adult D. catalinae and D. pallidus. It was identified that both species preferred B. tabaci eggs over nymphs with no evident preference over biotype, consuming over 50 eggs daily. It is possible that the quantity of eggs offered in this study was below the optimal nutritional requirements for D. davidsoni, triggering the predator to consume and thrive on larger forms of the prey, but these differences also could be attributed to species preference. Another point for consideration is that studies investigating the predatory capacity and preference of D. catalinae and D. pallidus were primarily done using early nymphal stages (first–third instar) of B. tabaci. As B. tabaci nymphs are immobile at the fourth instar, concentrating on this stage as prey is advantageous for feeding and stimulates oviposition in the vicinity (Seagraves 2009).

Figure 5:

Delphastus davidsoni life stages and predation on Bemisia tabaci MEAM1. (a) Fourth larval instar of Delphastus davidsoni; (b) fourth larval instar of D. davidsoni preying on a Bemisia tabaci nymph on collard greens; (c) pupa of D. davidsoni; (d) adult emergence of D. davidsoni; (e and g) adult of D. davidsoni; (f) adult of D. davidsoni preying on B. tabaci nymphs on collard greens; (h) predation of B. tabaci MEAM1 by larvae and adults of D. davidsoni.

D. davidsoni larvae consumed relatively fewer B. tabaci than did D. davidsoni adults, which aligns with the sedentary behavior commonly exhibited by ladybeetle larvae (Ferran and Dixon 1993; Ferrer et al. 2008). With low mobility, younger larvae tend to remain near the place of hatching or near their prey and spend more time consuming their prey. Conversely, adults are highly mobile, spending most of their time searching for food and mates. Adult females are focused on searching for a suitable oviposition site, where prey quantity and quality are the most important cues. This ensures that neonates do not have to travel too far before locating food. Interestingly, Liu and Stansly (1996) reported that D. pusillus commonly lays a single egg or small groups of eggs (2–4) where whiteflies nymphs and eggs are abundant. This is apparently a strategy to prevent progeny starvation and potential loss to cannibalism or predation eggs laid in proximity (Michaud and Jyoti 2007).

Host plant characteristics also are known to influence Delphastus spp. activity and life history parameters of using hibiscus as a host plant. Hoelmer et al. (1993) reported a developmental time of 11.6 days with 1.8, 1.4, 1.8, 1.7, 2.9, and 2.0 days for first, second, third, fourth, fourth (pupating), and fifth instars, respectively. In tomatoes (Solanum lycopersicum; Solanaceae), Oriani and Vendramim (2014) reported that larvae fed with whitefly eggs laid on the genotypes NAV1062 and LA1335 had shorter development times (10.4 and 10.8 days, respectively) than those on IAC294 (13.6 days). These findings indicated that different cultivars may also influence the biological parameters of Delphastus spp. Host plant toxicity may result in lower suitability of acceptable prey species (Hodek and Honĕk 1996).

The fifth instar of D. davidsoni did not occur in our study, differing from Oriani and Vendramim (2014). In all instances, four larval stages were observed for D. davidsoni in this study. Hoelmer et al. (1993) reported that approximately half of D. catalinae fourth instar individuals molted to a 2 days duration fifth instar while Liu (2005) did not observe the fifth instar. On cotton leaves, Kutuk and Yigit (2007) reported four larval stages, a prepupal, and a pupal stage for D. catalinae preying on B. tabaci eggs. The duration and number of larval instars could have been influenced by quality and abundance of prey (Hodek and Honĕk 1996; Castro et al. 2011; Hodek et al. 2012); however, host plant species and characteristics could be playing a larger role than previously understood.

While development and larval survival of D. davidsoni were affected by different diets (i.e. stages of B. tabaci), pupal survival appeared to be less dependent on food sources, although individuals that exclusively consumed B. tabaci eggs were less likely to survive the pupal stage than those feeding on nymphs. Diet has a direct influence on the development of most predatory insects (Guedes and Almeida 2013, Zazycki et al. 2015). Because female coccinellids generally require a higher calorie diet than males as a requirement for oviposition (Muthukrishnan and Pandian 1987; Sipos et al. 2012), we hypothesize that the numbers of B. tabaci eggs provided would have been insufficient to maintain healthy females. Future studies are needed to elucidate the impact of the same diet (i.e. different immature stages of B. tabaci) on adult emergence, sex ratio and reproduction.

Here we provide data to demonstrate the potential of D. davidsoni as a biological control agent for B. tabaci MEAM1. Both larvae and adults consumed immature B. tabaci. To date, studies investigating the role of D. davidsoni as a predator of B. tabaci eggs have been conducted in laboratory conditions (Oriani and Vendramim 2014), but to our knowledge, there are no previous estimates of age specific prey consumption. Latham and Mills (2009) found that biomass based daily consumption of sessile prey (aphids) by immature coccinellid Harmonia axyridis Pallas was underestimated in laboratory arenas compared to small field cages. Field cages could provide a more accurate estimate of consumption of prey such as immature B. tabaci, which are clustered, have low mobility and are generally undisturbed by predators (Latham and Mills 2009). Given that our daily estimates of prey consumption were age specific and included both partially and fully consumed individuals, it is possible that these estimates would translate well to field scenarios.

In North America, Delphastus spp. are commercially available and economically feasible in the biological control of B. tabaci in greenhouses (Pickett et al. 1999). Coccinellid mass release programs in South America could be even more advantageous and valuable, as costs associated with rearing and distribution are lower. It is reasonable to presume that D. davidsoni and other native species would be successful candidates for IPM programs targeting B. tabaci control in commercial greenhouses in Brazil, and potentially other countries in South America. Expanding the available tools for biological control of such an economically important pest will help reduce the overreliance on insecticides, reducing control costs and ultimately minimizing environmental impacts.

An understanding of larval and adult D. davidsoni biological performance when preying on B. tabaci on collard greens and other crops of economic importance is key for integrating this predator into existing, or for developing new, IPM practices. Although authors are unaware of undergoing mass releases of Delphastus spp. in Brazil, developing IPM strategies (e.g. selective insecticides or refuge areas) to enhance the efficacy of these predators would be beneficial.