Insecticidal activities of the local entomopathogenic nematodes and cell-free supernatants from their symbiotic bacteria against the larvae of fall webworm, Hyphantria cunea

https://doi.org/10.1016/j.exppara.2022.108380Get rights and content

Highlights

  • The fall webworm (FWW) is considered one of the invasive pests of many plants.

  • The chemical control is the most preferred method by farmers in severe infestations of FWW.

  • We tested the efficacy of entomopathogenic nematodes (EPNs) and their bacterial cell-free superatants (CFSs) against the larvae of FWW.

  • Foliar applications of EPNs and their CFSs could play an important role in the management of larvae of Hyphantria cunea.

Abstract

The fall webworm (FWW), Hyphantria cunea Drury (Lepidoptera: Erebidae), is an invasive and polyphagous insect pest of many economically important crops such as hazelnuts, apple, and mulberry. Recently, there have been an increasing number of reports about the damaging activities of FWW from hazelnut growing areas of Turkey indicating that currently existing control methods fail to satisfy the expectations of growers. Entomopathogenic nematodes (EPNs) in the Steinernematidae and Heterorhabditidae (Nematoda: Rhabditida) families and the symbiotic bacteria they carry in their intestine have a great potential for the management of many agriculturally important pests. In this study, the symbiotic bacteria of local EPN species (Heterorhabditis bacteriophora AVB-15, Steinernema feltiae KCS-4S, and Steinernema bicornotum MGZ-4S) recovered from the central Anatolia region was characterized using recA gene region as Photorhabdus luminescens, Xenorhabdus bovienii and Xenorhabdus budapestensis. The contact (25, 50, 100, 200 IJs/Petri) and oral efficacies of the infective juveniles (IJs) (25, 50, 100, 200 IJs/leaf) of these EPN isolates determined on 3rd/4th instar larvae, and cell-free supernatants from the identified symbiotic bacteria were evaluated separately on the 3rd and 4th larval instars of FWW in Petri dish environment under laboratory conditions (25 ± 1 °C, 60% of RH). In the Petri dish bioassays of EPN species, the most pathogenic isolate at the 1st DAT and 4th DAT was S. feltiae which caused 50% mortality at the highest concentration (200 IJs/Petri) and the highest mortality rate (97.5%) were achieved at 4th DAT by H. bacteriophora AVB-15 isolate. Surprisingly, the mortality rates were generally higher at the lowest concentrations and 82.5% mortality were reached 4th DAT by S. bicornotum at the lowest concentration (25 IJs/leaf) in the leaf bioassays. Mortality rates were higher in both Petri dish and filter paper efficacies of cell-free supernatants at the 2nd DAT and the highest mortality (87.5%) was reached in the contact efficacy studies when applied X. bovienii KCS-4S strain. The results suggest that the tested EPN species and CFSs have good potential for biological control of the larvae of FWW and can contribute to the IPM programs of FWW. However, the efficacy of both IJs of EPNs and CFSs of their symbiotic bacteria on larvae of FWW requires further studies to verify their efficiency in the field.

Introduction

The fall webworm (FWW), Hyphantria cunea Drury (Lepidoptera: Erebidae), is considered one of the invasive pests of many plants. FWW has been recorded on over 600 plant species including forest, stone, and pome fruits (Yarmand et al., 2009). Although FWW is a native pest of North America, it has found its way onto four continents over 30 countries and become a major pest of many economically important crops (İren, 1977; Kim and Kil, 2012; Mouloudis et al., 1980; Japoshvili et al., 2006; Kaçar et al., 2019). The female of this pest can lay up to 2000 eggs on the undersurface of leaves of host plants under favorable conditions. Newly hatched larvae start feeding en masse on the leaves within a protective nest-web which they constructed the following hatching. They continue feeding inside the web by enlarging it through larval stages (Yarmand et al., 2009). The larval stages of FWW damage the foliage of host plants by defoliating and in high population levels, the larvae cause serious losses leaving the host vulnerable to secondary pests and pathogens and thus leading the plant to complete destruction (Zhao, 2005; Ge et al., 2019). The fall webworm, which has been in Turkey for nearly half a century, has settled widely into the black sea region that accounts for 70% of the world's hazelnut production and becomes a major destructive pest of hazelnuts and mulberry in the region (Işık and Yanılmaz, 1992; Kaçar et al., 2019; Avcı and Öztemiz, 2020). In addition to its damage to the plants, the last instar larvae also cause a nuisance to people in late September by invading surrounding living spaces due to their overwintering behaviors (Wagner, 2005; Akkuzu and Torul, 2006; Yarmand et al., 2009).

The control of FWW is challenging due to their feeding habits, wide host range, adaptation capability, and reproduction rate (Yarmand et al., 2009; Saruhan et al., 2014; Kaçar et al., 2019). The chemical insecticides have been the most preferred control methods by farmers in severe infestations although the treatments do not give satisfactory results (Yarmand et al., 2009). It is also a well-known fact that there are many unwanted and irreversible effects of chemicals on both biotic and abiotic environments. Therefore, numerous researchers all around the world are currently looking for alternative control strategies to control FWW (Chkhubianishvili et al., 2007; Aker and Tuncer, 2016; Albayrak İskender et al., 2017; Gokturk et al., 2017; Saruhan et al., 2017; Gözel, 2019).

Entomopathogenic nematodes (EPNs), which are one of the successful groups of entomopathogens, have been getting the attention of many researchers around the world due to some features such as high speed of kill, their capability to reach pests in cryptic habitats by active host-seeking behavior of infective juveniles (IJs), and compatibility with many insecticides (Kaya and Gaugler, 1993; Grewal et al., 1998; Lacey, 2017; Kwizera and Susurluk, 2017; Özdemir et al., 2020). Although EPNs are soil-dwelling organisms, foliar applications of EPNs which are applied directly against the target pests yielded promising results thanks to enhanced application technology and formulations (Shapiro-Ilan et al., 2006; Laznik et al., 2012; Beck et al., 2013; Acar, 2019).

Symbiotic bacteria of EPNs from the genera Xenorhabdus and Photorhabdus play a key role in the virulence of EPNs by releasing toxic substances into the hemolymph and multiplying in there (Forst et al., 1997; Boemare, 2002; Snyder et al., 2007). Previous studies have shown that cell suspension of in vitro culture of Xenorhabdus spp. And Photorhabdus spp. have lethal properties against some economically important agricultural pests (Mohan et al., 2003; Sergeant et al., 2006; da Silva et al., 2013, Shawer et al., 2018; Eroglu et al., 2019). However, the efficacy of both native EPNs and their symbionts on FWW has not been studied in Turkey. It is essential to reveal the separate efficacy of EPNs and their symbiotic bacteria on the target host due to the varying pathogenicity of both EPNs and their symbiotic bacteria depending on species and strains. Therefore, a laboratory study was conducted to evaluate the contact and oral efficacy of both local isolates of IJs and cell-free supernatant of in vitro cultured symbiotic bacteria on the larvae of FWW in the Petri dish.

Section snippets

Production of entomopathogenic nematode isolates for pathogenicity bioassays

Three different EPN species (Heterorhabditis bacteriophora AVB-15, Steinernema bicornotum MGZ-4S, and Steinernema feltiae KCS-4S) originating from Central Anatolia and the Mediterranean region of Turkey were used for the experiments (Canhilal et al., 2017). The last instar larvae of Galleria mellonella (Linnaeus) (Lepidoptera: Pyralidae) were used to establish a laboratory culture after obtaining EPN isolates as described by Woodring and Kaya (1988). IJs collected with modified White's traps

Virulence of entomopathogenic nematodes

The differences in the mortality rates of FWW larvae were significantly affected by all main factors [Nematode species (N), exposure time (T), and bioassays (B)] except for concentrations of IJs (C) (Table 1). The interactions of all the main factors (4-way interaction; NxTxCxB) had also a significant effect on the mortality rates of FWW larvae.

All nematode species were able to penetrate and kill the larvae of FWW with varying levels of virulence and the mortality rates of FWW larvae increased

Discussion

This study shows the potential of entomopathogenic nematodes and cell-free supernatants of their symbiotic bacteria to control the larvae of FWW. Although several studies were conducted to assess the usage potential of EPNs on different pests, there is a limited number of studies examining the effects of EPNs on the larvae of FWW. However, to our knowledge, we evaluated, for the first time, the insecticidal activity of Xenorhabdus and Photorhabdus cell-free supernatants against FWW.

The previous

Conclusion

The results of this study show that the entomopathogenic nematode isolates and cell-free supernatants of their symbiotic bacteria might have potential to control FWW. These results will have also importance to the arrangements of further semi-field and field experiments which might help to determine the EPN/CFS potential to control FWW. Considering that FWW eggs are laid in leaves, additional studies could be conducted at the beginning of oviposition. Foliar application of IJs in this study

Author statement

EY and EÖ conceived, designed and conducted the experiments. RAD and EÖ analysed the data. EÖ and EY wrote the manuscript. RC helped in the interpretation and integration of the results. EÖ revised the manuscript. All authors read and approved the manuscript.

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