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Virulence of Beauveria bassiana and Metarhizium anisopliae on different stages of the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae)

Abstract

Background

The pink bollworm, Pectinophora gossypiella, is the most destructive pests of the cotton plant in Egypt. Due to the several problems of insecticides, the present study was conducted to evaluate the toxicity effect of the entomopathogenic fungi (EPF), Beauveria bassiana and Metarhizium anisopliae, against the different stages of the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae)

Results

The fungal isolates exhibited a toxic effect against the treated stages, egg, larva, and pupa. According to the obtained data of LC50, B. bassiana was more potent in inducing toxicity than M. anisopliae. However, eggs of P. gossypiella were less susceptible to the EPF than the other stages. Based on total mortality, LC50 was 4.97×1011, 6.03×1012 spores/ml for egg; 8.25×108, 6.03×109 spores/ml for neonate; 2.52×108, 1.29×1010 spores/ml for early 4th instar larvae; and 6.79×108, 8.36×109 spores/ml for pupae after treatment with B. bassiana and M. anisopliae, respectively.

Conclusions

Entomopathogenic fungi exhibited an activity in inducing mortality against different stages of P. gossypiella.

Background

The pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae), is one of the most injurious cotton pests worldwide (Parmar and Patel 2016). It decreases quantities and qualities of the cotton yield (Moustafa et al. 2019).

Because of the adverse effects of chemical insecticides to human and environment generally, there is a serious need for insecticidal alternatives. Microbial insecticides such as fungus, bacterium, virus, or protozoan are one of such alternatives characterized by not having chemical residues and/or insect resistance (Dhakal and Singh 2019).

More than 700 species of EPF were widely used as biopesticides (e.g., B. bassiana, M. anisopliae, Verticillium lecanii, Purpureocillium lilacinum, and Isaria fumosorosea) against many agricultural pests (Rizwan et al. 2019). EPF are present within natural insect populations and are often considered as an effective microbial control agent in integrated pest management (Vega et al. 2009). The mode of action of the EPF is through invading the insect cuticle and production of toxic enzymes that overcome the insect immune system (Niu et al. 2019).

EPF proved its effect against eggs, immature stages, and adult stage of many insect species (Hanem 2012) in both natural and artificial ecosystem (Cuthbertson and Audsley 2016). There is a growing interest to use them as a biocontrol agent in integrated pest management programs (Ali et al. 2017). The present study aimed to evaluate the virulence of EPF, B. bassiana and M. anisopliae, against the P. gossypiella different stages under laboratory conditions.

Methods

Rearing of insect

A culture of P. gossypiella was established under constant laboratory conditions of (27±1 °C and 65% R.H) in a rearing room at the Bio Insecticides Production Unit, Plant Protection Research Institute, Giza, Egypt. The neonate larvae were reared on an artificial diet described by Rashad et al. (1993). The pupae were placed in clean glass vials plugged with cotton until moth emergence.

Entomopathogenic fungi

Entomopathogenic fungi isolates, used in the present study, were B. bassiana and M. anisopliae. B. bassiana was isolated from the red palm weevil, Rhynchophorus ferrugineus in Ismailia governorate, while M. anisopliae was isolated from the white fly, Bemisia tabaci (Genn.) in Sharkia governorate (Ibrahim 2006).

Mass production of entomopathogenic fungi

The obtained conidia from fungal culture of B. bassiana and M. anisopliae were grown at 25 °C, in dark, on Sabouraud dextrose agar (SDA), consisting of peptone 10 g/l, glucose 20g/l, and agar-agar 20 g/l, (constant volume of 15 ml) in standard Petri-dishes (9-cm diameter). Conidia were harvested from 15-day-old plates by scraping into sterile Triton-X. The suspension was vortexed for 2 min and agitated for 1.5 h on a flask shaker at room temperature before filtering through 4 layers of sterile muslin. The conidial concentrations were estimated stock suspension were estimated using an improved Neubauer bright line hemocytometer (Reichert) under a Leitz Dialux × 40 EB microscope (400× magnification). A series of dilutions were made to give range concentrations of 108, 109, 1010, 1011, and 1012 spores/ml.

Bioassay

To study the virulence of M. anisopliae and B. bassiana against the different stages of pink bollworm P. gossypiella, 5 concentrations of each fungus (108, 109, 1010, 1011, and 1012 (spores/ml)) were prepared. All studies were carried out and incubated at 27±1°C and 65% R.H.

Treatment of eggs

Egg cards of P. gossypiella were sprayed using air brush directly with 5 concentrations of each EPF through laboratory bioassays then placed into plastic container measuring 7×5 cm and observed daily for the number of hatched larvae in each treatment. Four replicates (50 eggs/replicate). Control eggs were treated with water only.

Treatment of newly hatched larvae (neonate)

Concentrations of fungi were homogeneously mixed with artificial diet (without the antimicrobial agents). Four replicates (each replicate contained 10 newly hatched larvae P. gossypiella). A control experiment was done, but diet was mixed with distilled water. Newly hatched larvae at all treatments were allowed to feed on the treated diet for 48 h; then, alive larvae were transferred individually to glass tubes (2×7 cm) containing untreated artificial diet. Tubes were plugged with cotton wool and incubated at the above concentrations.

Treatment of early 4th instar larvae

Early 4th instar P. gossypiella larvae were immersed in 5 concentrations of fungi for 30–60 s, and then transferred to a sterile filter paper to dry. Four replicates (each replicate contained 10 individuals of 4th instar larvae). A control experiment was done, but larvae were immersed in distilled water. The 4th instar larvae were transferred by sterile forceps to glass tubes (2×7 cm) containing untreated artificial diet. Tubes were plugged with cotton wool and incubated at the above conditions. Mortality rate was recorded daily until pupation and adult emergence.

Treatment of pupae

One-day-old pupae P. gossypiella were immersed in different concentrations of fungi for 30–60 s, and then transferred to a sterile filter paper to dry. Four replicates at each concentration treated contained 10 pupae. Pupae were incubated at the above conditions. The mortality rate was recorded daily until adult emergence.

Studied criteria

  • Mortality rate was recorded daily and calculated as percentages.

  • Pupation rate was expressed as percent of the successfully developed pupae.

  • Emergence rate was expressed as percent of the successfully emerged adults.

  • Total mortality percentages were corrected against those of the control by Abbott’s formula (Abbott 1925).

  • LC50 calculation: corrected percentages of total mortality (between 20 and 84% mortality) were plotted versus the corresponding concentrations on logarithmic probability paper to obtain the corresponding log-concentration probit lines. The median lethal concentration (LC50) of treated insects was determined from the established regression lines (Finney 1971).

Results

Virulence of EPF against eggs

Table 1 displays the virulence of M. anisopliae spore suspensions against the egg of P. gossypiella. Egg mortalities were recorded at all concentration levels (41, 33, 22, 17, and 9% at 1012, 1011, 1010, 109, and 108 spores/ml, respectively, compared to 1.50% of control eggs). Also, egg hatchability was gradually decreased with the increase of concentration levels. The used concentration levels decreased the egg hatchability to 59, 67, 78, 83, and 91 than 98.50% in the control eggs.

Table 1 Effect of the fungal isolates against the egg stage of Pectinophora gossypiella

B. bassiana spore suspensions exhibited also a mortality effect against the egg of P. gossypiella (Table 1). The highest egg mortality was recorded by 53% at concentration level 1012 spores/ml than 2.5% in the control egg. The same concentration level decreased the egg hatchability to 47% compared to 97.5% of control egg.

No latent toxicity effect was recorded for the 2 EPF. According to the LC50 values, B. bassiana exhibited the lowest 4.97×1011 spores/ml, whereas 6.03×1012 spores/ml for M. anisopliae (Table 5).

Virulence of EPF against newly hatched larvae

M. anisopliae exhibited a mortality effect against the newly hatched larvae (neonate) of P. gossypiella that increased with the increased of concentration levels (Table 2). Obtained data indicated that the highest mortality percent (92.5%) was recorded by the highest concentration (1012 spores/ml) while the lowest mortality percent (15.0%) was caused by the lowest concentration (108 spores/ml) compared to 7.5% of control larvae. The mortality effect of M. anisopliae extended from the larval treatment to the resulted pupae and adults. Pupal mortality appeared at the highest 3 concentrations: 66.7, 20.0, and 4.5% at 1012, 1011, and 1010 spores/ml, respectively than 0.0% in the control pupae. However, M. anisopliae induced adult mortality to 37.5, 14.3, and 6.90% at 1011, 1010, and 109, respectively compared to 0.0% of control adults. Total mortality was increased gradually by increasing the concentration (97.50, 87.5, 55.00, 32.50, and 15.00 at 1012, 1011, 1010, 109, and 108 spores/ml, respectively compared to 07.50% of control insects). Pupation and adult emergence percentages were concentration dependent. Application of the highest concentration level (1012 spores/ml) decreased the pupation percent to 07.50% vs. 92.50 of the control pupae and adult emergence percent to 02.50% vs. 100.00% of control adults.

Table 2 Effect of the fungal isolates against the newly hatched larvae (neonate) of Pectinophora gossypiella

B. bassiana showed the same effect of M. anisopliae on treatment of the newly hatched larvae (neonate) of P. gossypiella (Table 2). Complete mortality (100%) was recorded at the highest concentration level (1012 spores/ml) compared to control larvae (10.0%) whereas other tested concentrations caused mortality of 82.5, 70.0, 47.5, and 32.5% at 1011, 1010, 109, and 108 spores/ml, respectively. Mortality effect of B. bassiana was extended in the resulted pupae and adults. In pupal stage, only 2 concentration levels (1011 and 1010 spores/ml) revealed a mortality rate of 28.60 and 8.0% compared to control (0.0%). In the adult stage, mortality rates were revealed at all concentration levels with the highest mortality 60.0% at 1011 spores/ml. Total mortality percent was recorded in a concentration-dependent manner (100.00, 95.50, 77.50, 52.50, and 37.50% at 1012, 1011, 1010, 109, and 108 spores/ml, respectively vs. 10.00% of control insects). Pupation and adult emergence percent decreased with increasing the concentration levels (Table 2).

According to the LC50 values of total mortality, B. bassiana exhibited the lowest LC50, 8.25×108 spores/ml, whereas it was 6.03×109 spores/ml at M. anisopliae (Table 5).

Virulence of EPF against early 4th instar larvae

Obtained data exhibited that the highest mortality percent in the treated larvae (57.5%) was caused by the highest concentration level of 1012 spores/ml whereas the concentrations of 1011, 1010, 109, and 108 spores/ml induced mortality of 45.0, 32.5, 22.5, and 15.0%, respectively, compared to 0.00% in control larvae (Table 3). The mortality effect of M. anisopliae extended to the pupae and adults that resulted from the treatment. Pupal and adult mortalities were recorded at all concentration levels except the lowest concentration. Pupal mortality rates were 52.9, 31.8, 18.5, and 6.5% at 1012, 1011, 1010, and 109 spores/ml, respectively, vs. 0.00% mortality in control. Also, 25.0% of adult mortality that formed the highest percent was recorded at the highest concentration level (1012 spores/ml) compared to 2.5% in control. Total mortality increased with the increased concentration levels to 85.0, 67.5, 50.0, 30.0, and 15.0%, respectively, against 2.5% in control. The highest concentration (1012 spores/ml) decreased pupation and adult emergence percent with the highest percent to 42.5 and 20.0%, respectively vs. 100% of control insects.

Table 3 Effect of the fungal isolates against the early 4th instar Pectinophora gossypiella larvae

The fungal isolate B. bassiana showed the same trend with M. anisopliae but with somewhat high effect (Table 3). All spore suspensions exhibited mortal effects against the treated larvae (65, 55, 47.5, 35, and 22.5% at 1012, 1011, 1010, and 109 spores/ml, respectively) vs. 2.5% mortality in control larvae. The virulence activity of the fungus B. bassiana was continued in the resulted pupae and adults from larval treatment. Pupal mortality was in a concentration dependent manner. The highest pupal mortality was recorded at the 2 highest spore suspensions, 78.6 and 55.6% at 1012 and 1011 spores/ml than 0.0% mortality in control pupae. The highest 3 spore suspensions induced adult mortality; the highest mortality was 66.7% at 1012 spores/ml vs. 0.0% mortality in control adults. The total mortality was gradually increased by increasing spore suspensions as 97.5, 84.6, 69.2, 51.3, and 33.3% vs. 2.2% mortality in control insects. All concentrations decreased pupation and adult emergence percent in a concentration-dependent manner.

According to LC50 values of total mortality, B. bassiana was more effective than M. anisopliae against the early 4th instar larvae of P. gossypiella. The entomopathogenic fungus B. bassiana exhibited the lowest LC50, 2.52×108 spores/ml, whereas the LC50 of M. anisopliae recorded 1.29×1010 spores/ml (Table 5).

Virulence of EPF against the pupae

The highest spore suspension of M. anisopliae, 1012 spores/ml, caused a high percent of pupal mortality, 72.5% and 45.6% of adult mortality after treatment of P. gossypiella pupae, compared to 5.0 and 2.5%, respectively, for control (Table 4), whereas the other concentrations of 1011, 1010, 109, and 108 spores/ml caused 65.0, 47.5, 32.5, and 17.5% pupal mortality rates and 24.6, 14.3, 11.1, and 3.0% adult mortalities. Total mortality was increased with the increase of concentration levels as 85.0, 75.0, 55.0, 40.0, and 20.0% at 1012, 1011, 1010, 109, and 108 spores/ml, respectively, compared to 7.5% of control insects. The percent of adult emergence decreased gradually to 82.5, 67.5, 52.5, 35.0, and 27.5% at the same ascending fungal concentrations than 95.0% of control adults.

Table 4 Effect of the fungal isolates against pupal stage of Pectinophora gossypiella

The effect of B. bassiana treatment against P. gossypiella pupae and its extended to the emerged adults is showed in Table 4. B. bassiana showed pupal mortality rates of 85.0, 77.5, 70.0, 47.5, and 35.0% at concentrations of 1012, 1011, 1010, 109, and 108 spores/ml, respectively, compared to 2.5% for control pupae. Also the effect was spread in the emerged adults, where the same spore suspensions exhibited a slight activity by 5.0, 7.5, 7.5, 5.0, and 2.5% vs. 2.5% for control adults. Total mortality was in a concentration-dependent manner as 90.0, 85.0, 77.5, 52.5, 37.5% at 1012, 1011, 1010, 109, and 108 spores/ml, respectively, compared to 5.0% for control insects. Adult emergence was inhibited by the highest percent to 15.0, 22.5, 30, 52.5, and 65.0% at the used fungal concentrations vs. 97.5% of control adults.

Based on LC50 values for total mortality, B. bassiana was more potent than M. anisopliae against P. gossypiella after treatment of the early pupal stage. Obtained data exhibited that the B. bassiana recorded the lowest LC50, 6.79×108 spores/ml, whereas the LC50 of M. anisopliae was 8.36×109 spores/ml (Table 5). Depending on the previous data of LC50 values for EPF, the lowest affected immature stages were eggs.

Table 5 LC50 values of the fungal isolates on different stages of Pectinophora gossypiella

Discussion

Entomopathogenic fungi currently present as an alternative tool for pest control. Several strains of B. bassiana, M. anisopliae, and other fungal isolates have been evaluated against P. gossypiella (El-Akad et al. 2016; Moustafa et al. 2019) and several other insect pests.

In the present study, the 2 fungal isolates, B. bassiana and M. anisopliae, proved their virulence against P. gossypiella irrespective of the treated stage. The newly hatched larvae were more susceptible than the 4th instar larvae after treatment with B. bassiana than M. anisopliae. Accordingly, the LC50, B. bassiana isolate was more potent than M. anisopliae isolate in inducing mortality. Farooq et al. (2020) found that B. bassiana, V. lecanii, and M. anisopliae concentrations and A. indica extract (alone and in combination) at different exposure intervals caused high mortality rates among the treated 2nd instar P. gossypiella larvae. Also, LC50 values for P. gossypiella larvae treated with different concentrations of B. bassiana and M. anisopliae were 1.42 and 0.98 g/l, respectively (El-Akad et al. 2016). Moustafa et al. (2019) showed that the virulence of Paecilomyces lilicanus was high on P. gossypiella whereas the toxicity of M. anisopliae was high in case of Earias insulana after treatment of the newly hatched larvae. Trichoderma harzianum spores induced mortalities against the larvae of E. insulana and P. gossypiella (El-Massry et al. 2016).

The present study revealed that the treated eggs of P. gossypiella were less susceptible to the EPF than the other treated immature stages including the pupal stage depending on the LC50. It is broadly accepted that insect eggs are more difficult to be infected than the larval stage (Skinner et al. 2014) and that the pupal stage is typically very resistant to succumb to injury (Vestergaard et al. 1995). However, the tested EPF, B. bassiana and M. anisopliae, decreased the egg hatchability of P. gossypiella. This result agrees with the study of Ullah et al. (2019) who reported that the EPF, I. fumosorosea and B. bassiana, significantly affected the egg hatchability of Spodoptera litura. Obtained data corroborated the findings of other studies that recorded pupal mortalities that extended after treatment of the larvae of some insects by some fungal isolates as in E. insulana (Abd-ElAzeem et al. 2019). In addition, the toxic effect of the 2 fungal isolates was reflected on the percent of pupation and adult emergence that decreased. These data are in accordance with other studies on certain insects by fungal isolates as in P. gossypiella (El-Akad et al. 2016) and E. insulana (Abd-ElAzeem et al. 2019).

Enzyme activity is considered one of the main mechanisms of fungal infection to insect host and inducing mortality by desiccation through the imperfect cuticle (Hamadah et al. 2018). Several studies revealed the presence of hydrolytic enzyme activity or cuticle-degrading enzymes, as chitinase, protease, and lipase, that play the main mechanism of fungal infection to insect host and inducing mortality. Also, some studies revealed that the virulence of EPF is associated with cuticle-degrading enzymes (Sargin et al. 2013; Cristina and Gheorghe 2017; Hamadah et al. 2018). These proteases are believed to help the fungal hyphae in penetrating the host tissue by breaking down the protein linkages in the insect cuticle and/or the utilization of the host proteins for fungal nutrition (Pozo et al. 2004). On the other hand, another suggestion that may be acceptable for the toxic effect of the fungal isolates is the complete destruction of the fat bodies; thus, the fat bodies lose their ability to synthesize and capacity to store nutrients (Mitchell and Cali 1994).

Conclusions

The study proved the activity of EPF, B. bassiana and M. anisopliae, against different stages of P. gossypiella under laboratory conditions. So, there is a possibility to use EPF as an alternative control tool to synthetic insecticides. Further study is needed to show their activity under field conditions.

Availability of data and materials

All data generated or analyzed during this study are included in this published article.

Abbreviations

P. gossypiella :

Pectinophora gossypiella

B. bassiana :

Beauveria bassiana

M. anisopliae :

Metarhizium anisopliae

I. fumosorosea :

Isaria fumosorosea

E. insulana :

Earias insulana

V. lecanii :

Verticillium lecanii

EPF:

Entomopathogenic fungi

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AI prepared fungal isolates and concentrations; GO conducted experiments and prepared statics; KH wrote the paper and interpreted the data. The authors read and approved the final manuscript.

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Correspondence to Khalid Hamadah.

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Omar, G., Ibrahim, A. & Hamadah, K. Virulence of Beauveria bassiana and Metarhizium anisopliae on different stages of the pink bollworm, Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae). Egypt J Biol Pest Control 31, 102 (2021). https://doi.org/10.1186/s41938-021-00447-w

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Keywords

  • Entomopathogenic fungi
  • Pink bollworm
  • Pectinophora gossypiella
  • Mortality