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Pathogenicity and persistence of entomopathogenic fungi against Asian citrus psyllid, Diaphorina citri Kuwayama
*Corresponding author: E-mail address: mamoon@gu.edu.pk (M Mamoon-ur-Rashid)
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Received: ,
Accepted: ,
Abstract
The increased development of insecticide resistance has necessitated the development of alternative control strategies against citrus psyllids. Entomopathogenic fungi are viewed as complementary and effective alternatives to synthetic insecticides. These investigations aim to determine the pathogenic potential of two different fungal strains, viz., Beauveria bassiana and Metarhizium anisopliae, against citrus psyllid under laboratory and natural field conditions. Both fungal strains were used at five different concentrations consisting of 1 × 104, 1 × 105, 1 × 106, 1 × 107 and 1 × 108 conidia mL-1. The mortality of D. citri was recorded 3, 7 and 14 days after fungal treatment, which was dose and time-dependent. Under laboratory environment at 14 days after treatment, the M. anisopliae used at higher concentrations of 1 × 107 and 1 × 108 conidia mL-1 caused > 80% mortality of D. citri having significant variation from 61.8 and 66.4% corrected mortality on plants treated with B. bassiana at similar concentrations, respectively. Additionally, under natural field conditions, M. anisopliae was more pathogenic and caused maximum (80%) mortality of D. citri at the maximum concentration of 1 × 108, having a significant difference from 64% cumulative mortality on plants treated with B. bassiana at the same concentration. Among the two tested fungal strains, M. anisopliae caused higher mortality of D. citri adults compared with B. bassiana and persisted up to 14 days after being applied. The present study highlights the potential of both tested entomopathogenic fungi strains as effective biological control agents against citrus psyllids.
Keywords
Biocontrol
Citrus crop
D. citri
Fungal strains
Mortality
Pest management
1. Introduction
The Asian citrus psyllid (ACP), Diaphorina citri Kuwayama, is the most devastating insect pest of all citrus species. It is a vector of bacterium, Candidatus Liberibacter asiaticus (CLas), the fundamental organism of Huanglongbing (HLB) also called citrus greening, a lethal and incurable disease of many citrus species (Hoddle, 2012; Grafton-Cardwell et al., 2013; Boina & Bloomquist, 2015; Khan et al., 2018). ACP is a serious threat to the future of citrus industry around the globe (Khan et al., 2018). The nymphs and adults suck cell sap from leaves, buds and tender shoots and remain active throughout the year. The attack of psyllids leads to wilting and distortion of leaves, buds and shoots. Moreover, due to the secretion of honeydew, sooty mold (black fungus) develops, resulting in premature fruit drop. Fruit size, quality and juice content are significantly reduced due to toxins present in the saliva of psyllids (Shah and Saleem, 2016). Three species of gram-negative bacteria (Candidatus Liberibacter spp.) mainly cause citrus greening disease by plugging of the phloem filter tubes of the plant (Bové, 2006). Fourth and fifth instar nymphs of ACP are capable of transmitting bacteria to the citrus plants; however, adults can spread the disease to larger areas due to their flying ability (Inoue et al., 2009; Boina & Bloomquist, 2015).
Diaphorina citri was first described in Taiwan in 1907 (Kuwayama, 1910), and the infectious nature of HLB was later demonstrated in South China (Lin, 1956). Most of the varieties of commercially cultivated citrus are susceptible to the attack of citrus psyllid all over the world (except in Australia and New Zealand). Citrus greening disease cannot be detected easily due to a concealed period of inoculation before inception (Grafton-Cardwell et al., 2013). HLB can cause severe yield losses ranging from 30% to 100%, based on the disease severity (Meyer et al., 2008). In Pakistan, up to 90% yield losses have been reported caused by ACP to citrus crops (Ahmad, 1961). In heavily infested areas, high yield losses and ultimately plant death within two years have been observed (Qasim et al. 2024). Rapid increase and spread of citrus psyllids and HLB in citrus growing areas of the world have necessitated extensive research on the ecology, biology and management of this pest (Grafton-Cardwell et al., 2013). Application of synthetic pesticides is the most commonly used method for the management of psyllids; however, due the development of resistance against many insecticides, it is vital to search for alternative measures of pest management (Khan et al., 2018; Grafton-Cardwell et al., 2013). Researchers are focusing on various options for the sustainable management of ASP and HLB like the use of biological agents, the development of resistant varieties, and biological and novel pesticides. Integrated pest management (IPM) agendas based on preservation of natural enemies of citrus psylla through cautious use of insecticides and releases of parasitoids are needed for sustainable management of pest and disease (Qureshi and Stansly, 2009). A combination of all possible control measures against ACP is of utmost importance to safeguard citrus plantations around the world (Qasim et al., 2024).
Some species of entomo-pathogenic fungi (EPF) are effective against psyllids under humid conditions (Subandiyah et al., 2000; Meyer et al., 2007; Hoy et al., 2010; Casique-Valdes et al., 2011; Hunter et al., 2011). However, there are some constraints with the application of fungal entomo-pathogens like unequal growth limit conidia production in the laboratory, slime production by mycelia, low sporulation rates and inhibitory effect of chemical insecticides, including horticultural oil, copper hydroxide and elemental sulfur (Meyer et al., 2007; Casique-Valdes et al., 2011; Hall et al., 2012).
Isolates of Beauveria basiana have been found effective against more than 700 insect species across the globe (Zimmermann, 2007; Mascarin & Jaronski, 2016). Entomopathogenic fungi have been considered a vital addition as well as a good substitute to synthetic insecticides (Meyling and Hajek, 2010; Malik et al., 2016). Entomopathogenic fungi were found as an effective control agent against pear psyllids (Cacopsylla pyricola Foerster) (Puterka et al., 1994). Moreover, EPF are also being used as a potential biotic agent against Asian citrus psyllids. A strain of C. fumosorosea was found naturally infecting adult citrus psyllids in the USA (Meyer et al., 2008), and C. fumosorosea is also being used augmentatively against citrus psylla around the world (Hoy et al., 2010).
Before the application of entomopathogenic fungi for the management of insect pests, it is imperative to screen out different isolates to determine the most virulent pathogens. Considering the limited information regarding the efficacy of various fungal isolates against citrus psyllids, the current study aimed to investigate the pathogenic potential of B. bassiana and M. anisopliae against D. citri under controlled laboratory and natural environments.
2. Materials and Methods
2.1 Fungal culture and preparation of conidial suspensions
The studies were conducted to determine the efficacy of two fungus isolates, including Beauveria bassiana and Metarhizium anisopliae against citrus psyllid. The initial fungal isolates were obtained from the Department of Entomology, University of Sargodha, Punjab, Pakistan. The Beauveria bassiana isolates were cultured on potato dextrose agar (PDA) while Metarhizium anisopliae isolates were cultured on Sabouraud dextrose agar (SDA). Both cultures were maintained at 25 ± 2°C under dark conditions. After two to three weeks, the fungal conidia were harvested from the sporulated cultures. The fungal conidia were suspended in 10 mL of distilled water with 0.05% Triton X-100 in universal bottles containing glass beads. To break the conidial clumps, the suspension was vortexed for 5 min at 700 rpm to ensure homogeneous mixtures. According to the modified method of Ullah et al. (2018), both EPF were tested at five different concentrations of 1×104, 1×105, 1×106, 1×107 and 1×108, conidia mL-1. The treatments were used when the population of citrus psyllids reached the economic threshold level (ETL). The quality control of conidial concentration was evaluated by using a haemocytometer in a Neubauer chamber. The data on the mortality of citrus psyllids were recorded at 3, 7 and 14 days after the application of entomopathogenic fungi and were converted into percent mortality.
2.2 Laboratory bioassay
Twenty adult psyllids were collected in the sex ratio of 1:1 from the rearing culture. In the laboratory experiment, each fungal treatment was sprayed with 400 µL. The experiment was conducted in glass vials in which young seedlings were already inoculated with M. anisopliae and B. bassiana. The control group was treated with distilled water in equal quantity. Each fungal isolate was used at aforementioned five constant concentrations. The experiment was performed following a completely randomized design under controlled conditions of 28 ± 2°C and 75 ± 2% relative humidity with a photoperiod of 14-h light and 10-h dark period with three replications. The tests were repeated on different dates. The data on the mortality of citrus psyllids were recorded after 3, 7 and 14 days after fungal application.
2.3 Bio-efficacy of EPF on commercial citrus grove
The insecticidal bio-efficacy of both fungal isolates was tested against D. citri under field conditions in all selected locations/sites. The field experiments were conducted with a one-month interval between two successive applications. The aerial conidia of both EPF were produced on precooked parboiled rice. Each fungal isolate was used at five constant concentrations as described above. The citrus plants infested with citrus psyllids were selected for M. anisopliae and B. bassiana applications. No chemical/pesticide was applied before or after the fungal application. The experiment was initiated using a randomized complete block design (RCBD). The experiment was continued for a period of twelve months; a total of twelve experiments were conducted (1 per month) in the same area. The experiments were conducted on randomly chosen plants to assess the performance of both fungal isolates.
The data were recorded after 3, 7 and 14 days of application, the citrus branches restrained in the voile bags/cotton wool were cut off and brought to the laboratory for the observation of dead and healthy adults. The mortality data were noted and the corpses were incubated in humid chambers to check the presence of sporulation.
2.4 Statistical analysis
Prior to analysis, the percent mortality data were arcsine square root transformed. These transformed data were used for statistical analysis by one-way analysis of variance using the computer software “Statistix Version 8.1. The Tukey Honestly Significant Difference (HSD) test was applied at a 0.05 significance level to compare the treatment means.
3. Results
3.1 Laboratory studies
3.1.1 Population reduction after three days
The tested entomopathogenic fungi possessed a high level of pathogenicity against D. citri used at different concentrations, however, the population reduction was negligible after 3 days of application. The insecticidal effect of both fungal isolates gradually increased and reached at a peak after two weeks of application.
The significant differences were observed between two different species of EP fungi at three days after the application (1 × 104: F1 = 39.2; P < 0.0002), (1 × 105: F1 = 22.2; P < 0.0015), (1 × 106: F1 = 34.1; P < 0.0004), (1 × 107: F1 = 30.0; P < 0.0004) and (1 × 108: F1 = 30.1; P < 0.0006). After 3 days of fungal application, the maximum reduction (14%) in psyllid population was observed on plants treated with the maximum concentration (1 × 108 conidia mL-1) of M. anisopliae having significant variation from 10% population reduction recorded on plants treated with B. bassiana at the same concentration (Fig. 1). The least reduction in the D. citri population was observed on plants treated with the minimum concentration of the EP fungi.
- Pathogenicity of two entomopathogenic fungi against D. citri under laboratory conditions at three days after application.
3.1.2 Population reduction after seven days
A substantial increase in the mortality of D. citri was observed at seven days after treatment. The maximum mortality (79.20%) was documented on plants treated with the maximum (1 × 108 conidia mL-1) concentration of M. anisopliae having significant variation from 56.4% mortality of D. citri observed on plants treated with B. bassiana at the same concentration (1 × 104: F1 = 36.0; P < 0.0003), (1 × 105: F1 = 964; P < 0.0000), (1 × 106: F1 = 74.9; P < 0.0000), (1 × 107: F1 = 294; P < 0.0000) and (1 × 108: F1 = 217; P < 0.0000). The M. anisopliae caused more than 50% mortality of D. citri at all the evaluated concentrations except the lowest concentration; however, B. bassiana caused more than 50% reduction in the population of D. citri at the higher concentrations of 1 × 107 and 1 × 108 conidia mL-1 (Fig. 2).
- Pathogenicity of two entomopathogenic fungi against D. citri under laboratory conditions at seven days after application.
3.1.3 Population reduction after fourteen days
A negligible increase in the mortality of D. citri was observed at 14 days after the application of entomopathogenic fungi. Among the two tested entomopathogenic fungal isolates, the M. anisopliae caused significantly higher mortality of D. citri compared with B. bassiana. At 14 days after treatment, M. anisopliae used at higher concentrations of 1 × 107 and 1 × 108 caused > 80% mortality of D. citri having significant variation (1 × 104: F1 = 135; P < 0.0000), (1 × 105: F1 = 599; P < 0.0000), (1 × 106: F1 = 298; P < 0.0000), (1 × 107: F1 = 498; P < 0.0000) and (1 × 108: F1 = 158; P < 0.0000) from 61.8 and 66.4% corrected mortality noted on plants treated with M. anisopliae at the similar concentrations, respectively. Overall, the minimum corrected mortality (41.8%) was recorded when citrus leaves were treated with B. bassiana at the minimum concentration of 1 × 104, having a significant difference from the 57.4% corrected mortality observed on leaves treated with M. anisopliae at the same concentration (Fig. 3).
- Pathogenicity of two entomopathogenic fungi against D. citri under laboratory conditions at fourteen days after application.
3.2 Pathogenicity of entomopathogenic fungi against D. citri under field conditions
3.2.1 Population reduction after three days
The entomopathogenic fungi species tested at five different concentrations could not control D. citri populations under field conditions at 3 days after treatment. However, the differences among the two species of entomopathogenic fungi were significant (1 × 104: F1 = 19.6; P < 0.0022), (1 × 105: F1 = 23.1; P < 0.0014), (1 × 106: F1 = 12.1; P < 0.0083), (1 × 107: F1 = 12.5; P < 0.0077) and (1 × 108: F1 = 34.4; P < 0.0004). The maximum reduction (14.4%) was observed on plants treated with M. anisopliae at the maximum concentration of 1 × 108, having a significant difference from 10.6% reduction in D. citri infestation on plants treated with B. bassiana at the same concentration (Fig. 4).
- Pathogenicity of two entomopathogenic fungi against D. citri under field conditions at three days after application.
3.2.2. Population reduction after seven days
A significant (1 × 104: F1 = 141; P < 0.0000), (1 × 105: F1 = 520; P < 0.0000), (1 × 106: F1 = 346; P < 0.0000), (1 × 107: F1 = 565; P < 0.0000) and (1 × 108: F1 = 488; P < 0.0000) increase in the efficacy of the both entomopathogenic fungi was observed at 7 days after treatment. The M. anisopliae caused > 50% reduction in the infestation of D. citri when used at all the evaluated concentrations except the lowest concentration, whereas B. bassiana registered more than 50% reduction of citrus psyllids when used at the maximum concentration of 1 × 108. The maximum (72.6%) reduction in the infestation of D. citri was observed when citrus plants were treated with M. anisopliae at the maximum concentration, having a significant difference from the 52.6% reduction on plants treated with B. bassiana (Fig. 5).
- Pathogenicity of two entomopathogenic fungi against D. citri under field conditions at seven days after application.
3.2.3 Population reduction after fourteen days
Both the tested entomopathogenic fungi caused significant mortality of D. citri at all the evaluated concentrations (1 × 104: F1 = 218; P < 0.0000), (1 × 105: F1 = 363; P < 0.0000), (1 × 106: F1 = 509; P < 0.0000), (1 × 107: F1 = 214; P < 0.0000) and (1 × 108: F1 = 320; P < 0.0000). The pathogenicity of both the tested fungi increased by increasing the concentrations and reached a peak at the maximum concentration of 1 × 108. The M. anisopliae was more pathogenic against D. citri compared with B. bassiana. Overall, maximum (80%) mortality of D. citri was observed when citrus plants were treated with M. anisopliae at a maximum concentration of 1 × 108, having a significant difference from 64% cumulative mortality observed on plants treated with B. bassiana at the same concentration (Fig. 6).
- Pathogenicity of two entomopathogenic fungi against D. citri under field conditions at fourteen days after application.
4. Discussion
Control of many insect pests relies heavily on the frequent use of chemical insecticides, but due to increasing issues of reduced efficacy and increased resistance in field populations, biological control is considered as the most viable alternative. Entomopathogenic fungi are viewed as effective bio-control agents in pest management. Varying degrees of pathogenicity have been reported against various insect pests depending upon the isolates of entomopathogenic fungi (Wakil et al., 2021; Chepkemoi et al., 2024). The present study confirmed the pathogenicity and persistence of two fungal isolates including B. bassiana and M. anisopliae against citrus psyllids under laboratory and field conditions. The higher concentrations of both the fungal isolates showed higher efficacy as more conidia result in successful infection, leading to mortality of target insect pests.
The pathogenicity of both the tested fungal isolates increased with the increase in the concentration and exposure duration. In the present investigations, the population reduction was negligible after 3 days of application, however the insecticidal efficacy of both the tested isolates gradually increased and reached at peak after 2 weeks of application. Among the two tested entomopathogenic fungi species, the M. anisopliae caused significantly higher mortality of D. citri compared with B. bassiana at all the exposure durations. At 7 days after the exposure period, in laboratory conditions, M. anisopliae caused more than 50% mortality of D. citri at all the evaluated concentrations except the lowest concentration; however, B. bassiana caused more than 50% reduction in the infestation of D. citri at the higher concentrations of 1 × 107 and 1 × 108 conidia mL-1 suspension. A negligible increase in the mortality of D. citri was observed at 14 days after the application of entomopathogenic fungi. During this period, the M. anisopliae used at higher concentrations of 1 × 107 and 1 × 108 conidia mL-1 caused > 80% mortality of D. citri having significant variation from 61.8 and 66.4% corrected mortality observed on plants treated with B. bassiana at similar concentrations, respectively. Similar trends were also demonstrated in previous studies like Akutse et al. (2020), they documented that M. anisopliae were most effective compared with other tested strains and caused more than 80% reduction in the infestation of fall army worm. Saldarriaga Ausique et al. (2017) validated our findings. They found 77.8% and 78.4% adult mortality of citrus psyllids by using Isaria fumosorosea ESALQ-1296 and Beauveria bassiana ESALQ-PL63 under laboratory conditions.
Several studies have reported the efficacy of various fungal isolates against nymphal and adult stages of psyllids under controlled laboratory conditions (Hunter et al., 2011; Stauderman et al., 2012). However, studies investigating the efficacy of entomopathogenic fungi under natural field conditions are limited and inconsistent. In the current investigation, under natural field conditions, both the fungal isolates were effective against psyllids in a commercial citrus grove and caused significant mortality at all the post-treatment exposure periods, except three days exposure duration. The entomopathogenic fungi species tested at five different concentrations could not control D. citri populations at three days after treatment. At seven days after treatment, there was a significant increase in the efficacy of both fungal isolates. The maximum (72.6%) reduction in the infestation of D. citri was observed when citrus plants were treated with M. anisopliae at the maximum concentration, having a significant difference from 52.6% reduction on plants treated with B. bassiana. The pathogenicity of both the tested fungi increased with increasing concentrations and exposure periods.
Both the tested fungal isolates persisted up to fourteen days and caused maximum population reduction at the maximum concentration of 1 × 108 conidia mL-1. These data are in line with previous research as many researchers observed that the efficacy of different fungal isolates increases by increasing the conidial concentrations, leading to decreased duration required for causing mortality lethal timings (Kocaçevik et al., 2016 and Kushiyev et al., 2018). M. anisopliae was more pathogenic compared with B. bassiana. Overall, there was a maximum (80%) mortality of D. citri when citrus plants were treated with M. anisopliae at maximum concentration having a significant difference from 64% cumulative mortality on plants treated with B. bassiana at the same concentration. Similar findings by Corallo et al. (2021) reported that M. anisopliae caused higher (78.9%) mortality of psyllids under semi-field conditions compared with B. bassiana (51%). Previous studies have documented that entomopathogenic fungi, B. bassiana and I. fumosorosea used at 1 × 108 conidia mL-1 caused mortality of adult psyllids at 64.4 and 73.8%, respectively, under laboratory conditions (Ullah et al., 2018). These data are in accordance with those of Tuncer et al. (2019). The efficacy of M. anisopliae was higher than B. bassiana against Xylosandrus germanus Blandford under laboratory conditions. In another study, Liu et al. (2017) observed that B. bassiana (12,108 isolates) was more effective against adults of Curculio nucum (Coleoptera: Curculionidae) compared with M. anisopliae (3.4607 isolate). The differences in the results regarding the efficacy of the entomopathogenic fungi are attributed to the differences in the isolates and insect species. The efficacy of entomopathogenic fungi varies between species and even between different isolates of the same species (Goettel et al., 2005).
5. Conclusions
The present findings confirmed that M. anisopliae and B. bassiana caused significant mortality of psyllids under laboratory and field environments and had significant potential as biological control agents. The tested fungal isolates are recommended for safer and sustainable management of citrus psylla.
CRediT authorship contribution statement
Yasir Ishfaq: Conducted the experiment, contributed to writing the original draft; Muhammad Mamoon-ur-Rashid: Conceptualization and study design, supervision of the study; Azhar Abbas Khan: Conceptualization and study design, supervision of the study; Mohammad Safdar Baloch: Contributed to writing the original draft; Asif Latif Baloch: Contributed to writing the revised draft; Asghar Ali Khan: Conducted the experiment; Hussan Ara Begum: Contributed to writing the original draft; Muhammad Umair Sardar: Contributed to writing the revised draft; Muhammad Naeem: Contributed to writing the revised draft; All authors revised the manuscript and approved the final version.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Data availability
The datasets generated during and/or analyzed during the current study are available within the manuscript.
Declaration of generative AI and AI-assisted technologies in the writing process
The authors confirm that there was no use of artificial intelligence (AI)-assisted technology for assisting in the writing or editing of the manuscript and no images were manipulated using AI.
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