Management of Asian Citrus Psyllids, Diaphorina citri Kuwayama, The Direct and Vector Pest of Citrus Via Synthetic Insecticides in Khyber Pakhtunkhwa, Pakistan
Research Article
Management of Asian Citrus Psyllids, Diaphorina citri Kuwayama, The Direct and Vector Pest of Citrus Via Synthetic Insecticides in Khyber Pakhtunkhwa, Pakistan
Ashraf Khan1*, Suliman Shah2, Maid Zaman3 and Komal Habib2
1National Tea and High Value Crops Research Institute, PARC, Shinkiari Mansehra, Pakistan; 2Department of Entomology, The University of Agriculture, Peshawar, Khyber Pakhtunkhwa, Pakistan; 3Department of Entomology, the University of Haripur, Pakistan.
Abstract | Asian citrus psylla, Diaphorina citri Kuwayama, is considered to be the most noxious pest of almost all species and varieties of citrus and its infestation found throughout the world. It is becoming serious threat to the brightening future of citrus growing areas of Pakistan. Thirteen different insecticides were usedfor effective control against citrus psylla under field conditions. Population density of pest was recorded as number of adults per branch. Efficacy of the insecticides was evaluated as percent mortality (%) of citrus psylla. Overall highest percent mortality was observed in plants treated with combination of Nitenpyram + Chlorfenapyr (99.20 and 99.89 %) followed by Flubendiamide (89.83 and 99.39 %) and Imidacloprid (89.31 and 98.77 %) after spray 1 and 2, respectively. Least effective insecticide was proved to be Melathion with 39.79 and 65.43 percent reduction in citrus psyllidspopulation except untreated plants with 9.27 and 15.94 percent decrease after first and second spray, respectively. Decline in overall population recorded from 91.73 to 13.20 and 17.40 to 4.43 percent after multiple sprays, respectively. All the insecticides endowed withstatistically significant control of citrus psylla comparable to untreated plants.
Received | March28, 2018; Accepted | September 1, 2018; Published | October 29, 2018
*Correspondence | Ashraf Khan, National Tea and High Value Crops Research Institute, PARC, Shinkiari Mansehra, Pakistan; Email: ashraf_ento60@yahoo.com
Citation | Khan, A., S. Shah, M. Zaman and K.Habib. 2018. Management of Asian citrus psyllids, Diaphorina citri Kuwayama, The direct and vector pest of citrus via synthetic insecticides in Khyber Pakhtunkhwa, Pakistan. Pakistan Journal of Agricultural Research, 31(4): 300-305.
DOI | http://dx.doi.org/10.17582/journal.pjar/2018/31.4.300.305
Keywords | Insecticides, Percent mortality, Nitenpyram + Chlorfenpyr, Flubendiamide, Imidacloprid
Introduction
Among the major insect pests of citrus, Asian citrus psylla (ACP) Diaphorina citri Kuwayama (Hemiptera: Psyllidae), is the most destructive and consequently the most annoying pest as it vectors the phloem-limited bacterium,Candidatus Liberibacterasiaticus, the causal organism of “huanglongbing” (HLB) or citrus greening disease (Halbert and Manjunath, 2004; Catling, 1969). HLB is one of the world’s most devastating diseases of citrus, responsible for the decline and death of infected trees (Bové, 2006; Roistacher, 1996). After attack of both nymphs and adults of D. citri on buds and soft young shoots, curling, defoliation and distortion of the leaves starts, production of honey dews take place and ultimately infection of sooty mould fungus resulting in premature fruit drops (Shah and Saleem, 2000). Death of the plant may occur as a result of distortion by heavy infestation of the pest within 4-5 years (Bove, 2006). Saliva of the pest is thought to be toxic which probably induce such distortion (Dennis, 1983). Nearly worldwide extension of Asian citrus psyllid and HLB to citrus growing regions (Halbert and Manjunath, 2004; Halbert and Nunez, 2004; Pluke et al., 2008), have increased research efforts on ACP and HLB over the past 85 years and making expanded our comprehension of the insect, the disease and their interactions.
In the management of pest and disease, soil and foliar applied insecticides are essential tools (McCoy et al., 2009). Foliar sprays are considered most effective against adult psyllids because they are more exposed than the immature psyllids which are secluded in the young shoots and are more susceptible to systemic poisons. In addition to that adult psyllids are responsible for the spread of C. Liberibacterasiaticus from infected trees to the adjoining healthy trees (McCoy, 1985; Stansly and Qureshi, 2008).
Pakistan prostrate among the leading citrus growing countries of the world where citrus is cultivated on a land of 194.5 million hectares with 1982.2 million tons production (MINFA, 2010-11) in different districts of Punjab, and many districts of Khyber Pakhtunkhwa such as Malakand, Haripur, Swat, Mardan, Dir Upper and Lower and Peshawer (Jillani et al., 1989). Citrus have been observed under severe infestation of citrus psylla since the last few years resulting in high reduction of production. Keeping in view the great commercial importance of citrus fruit all over the world and especially in Khyber Pakhtunkhwa whose climatic conditions are most congenial for the production of different citrus species cultivated since ancient times in the sub content (MINFA, 2010-11), the current study was conducted for the management of its noxious pest via insecticides application.
Materials and Methods
Selection of experimental plants
The experiment was carried out at New Developmental Farm of the University of Agriculture, Peshawar, during 2016. For this purpose, 42 sour orange plants bearing equal size were randomly selected. The number of treatments were kept 14 including control (untreated plants). A single plant was left untreated between all the two treatments supposed to be buffer zone. The experiment was designed as randomized complete blocks. No artificial interventions were involved to trigger the infestation of Asian Citrus Psylla (ACP).
Population density/ Infestation
Seven reference points (top, middle, bottom, east, west, north and south) bearing adults of ACP were randomly selected and tagged prior to application of the treatments for evaluation of their efficacy on each plant. High infestation of citrus psylla was observed in the month of August. The population of pest was counted on 05 leaves of each tagged branch (total 35 leaves/ tree). Infestation of Asian citrus psylla was observed on both the upper and lower surface of each leaf. Percent decrease over control was calculated using the following formula: (Khattak et al., 1987);
C = A/B *100
Where;
A = population infestation in treated plants
B = population infestation in control
C = decrease over control
Percent decrease = 100 – C
Chemical control
To study the efficacy of insecticides against citrus psylla population, the following 13 insecticides were tested along with control. Water spray was used as control. Trees were sprayed twice at four weeks interval early in the morning leaving the control untreated. Application of insecticides was made when infestation of the pest was confirmed on both sides of the leaves.
| S. No | Treatments |
| 1 | Thaiachloprid |
| 2 | Emamectin benzoate |
| 3 | Nitenpyram + Bimetrozen |
| 4 | Deltamethrin |
| 5 | Flubendiamide |
| 6 | Lambda cyhalothrin |
| 7 | Melathion |
| 8 | Pyriproxifen |
| 9 | Nitenpyram (20%) + Chlorfenapyr (30%) |
| 10 | Fenpyroxymate |
| 11 | Chlorpyrifos |
| 12 | Acetamaprid |
| 13 | Imidacloprid |
| 14 | Control |
Statistical analysis
The recorded data were subjected to ANOVA by repeated measurement analysis using Statistix 8.1 taking spray as repeated measure factor, whereas time and treatments were arranged in randomized complete block design. Means were separated using DMRT contingent on a significant treatment effect (P<0.05) (SAS Institute, 2004).
Results and Discussion
A total of 13 insecticides efficacy was investigated against Asian citrus psylla for evaluation of most suitable active ingredient(s) (Table 1). After application, data recorded after one week indicated significantly high reduction (97.72 %) in plants treated with Nitenpyram + Chlorfenpyr followed by Pyriproxifen and Flubendiamide with 81.02 and 78.06 %, respectively. Lowest and statistically non-significant decrease in the percent pest density was observed in Thaiacloprid, Melathion and Control (Untreated) which was 2.6, 3.36 and 6.02 percent, respectively. Similarly, highest butnon significant decrease in week 2 (post treatment) was indicated between Nitenpyram + Chlorfenpyr and Flubendiamide treated plants with 99.90 and 98.81 percent, respectively, but was statistically significant from rest of the treatments. These highly effective insecticides were followed by Imidacloprid (95.79%) and Nitenpyram + Bimetrozen (95.03 %). After the same duration, lowest decrease (0.66%) in percent pest infestation was noted in untreated plants (control). After week 3, complete elimination of the pest from the plants was occurred which were treated with Nitenpyram + Chlorfenpyr (100 %) followed by Flubendiamide with 99.98 percent reduction. Both the treatments were significantly different from untreated plants (control), Melathion, Thaiaclopridand Deltamethrin and were non-significant with rest of the treatments.
Results regarding percent decrease of Citrus psylla after second application of the treatments are given in Table 2, which indicated that various treatments, Nitenpyram + Chlorfenpyr, Flubendiamaide, Imidacloprid, Fenpyroximate, Nitenpyram + Bimetrozen and Emamectin benzoate proved to be most effective with more than 90%reduction of the pest after 1 week of application, which were non-significant among themselves but significantly different from rest of the treatments. Maximum numbers of adults were found in the untreated plot (control) with 14.28 percent reduction in their number after the same duration. Highest significant reduction in population was again recorded in the plants treated with Nitenpyram + Chlorfenpyr, Imidacloprid, Flubendiamide, Emamectin benzoate, Deltmethrin, lamdacyhalothrin, Nitenpyram + Bimetrozen, and Fenpyroximate, respectively, fluctuating the pest from 99.09 to 96.11 percent 2 weeks post application of the treatments. A 16.36 percent reduction was recorded in untreated plants after the same duration. After week 3, similar insecticides were observed to be effective with the exception of Emamectin benzoate bearing the lowest number of adults with 99.93 percent decrease and untreated plants (control) with the highest number of adults showing 17.18 percent reduction in their population.
Table 1: Percent reduction in number of Asian citrus psylla per branch (5 leaves) at various time intervals on citrus after first application of different insecticides.
| S. No | Treatment | Dose/100 LOW | Post spray timings | ||
| Week 1 | Week 2 | Week 3 | |||
| 1 | Thaiachloprid | 125 ml | 2.65h | 64.35g | 80.79d |
| 2 | Emamectin benzoate | 80 ml | 49.47ef | 88.21c | 97.92ab |
| 3 | Nitenpyram + Bimetrozen | 100 gm | 56.95de | 95.03b | 97.46ab |
| 4 | Deltamethrin | 200 ml | 27.55g | 68.36f | 87.34cd |
| 5 | Flubendiamide | 30 gm | 78.06bc | 98.81a | 99.98a |
| 6 | Lambda cyhalothrin | 250 ml | 46.75f | 76.33e | 92.90abc |
| 7 | Melathion | 500 ml | 3.36h | 55.96h | 65.56e |
| 8 | Pyriproxifen | 350 ml | 81.02b | 86.59c | 94.59ab |
| 9 | Nitenpyram (20%) + Chlorfenapyr (30%) | 150 gm | 97.72a | 99.90a | 100.00a |
| 10 | Fenpyroxymate | 180 ml | 45.05f | 76.00e | 93.36abc |
| 11 | Chlorpyrifos | 500 ml | 41.00f | 82.01d | 91.67bc |
| 12 | Acetamaprid | 85 g | 59.38d | 86.04c | 94.76ab |
| 13 | Imidacloprid | 150 ml | 74.45bc | 95.70b | 97.79ab |
| 14 | Control | 6.02h | 0.66i | 21.14f | |
| LSD Value | 9.44 | 2.61 | 7.14 | ||
Values in columns followed by different letter(s) are significantly different at 5 % level of probability using DMR test.
Comparison of overall percent reduction among various insecticides reveals that maximum percent decrease of 99.20 was recorded in Nitenpyram + Chlorfenpyr followed by Flubendiamide (89.83), Imidacloprid (89.31) and Pyriproxifen reducing the pest by 89.83, 89.31 and 87.40 percent, respectively, which were significantly effective than the rest of the treatments while minimum percent decrease of 9.27 percent was recorded in control (untreated plants) after first spray (Table 3). Nitenpyram + Chlorfenpyr (99.89%), Flubendiamide, Imidacloprid, Emamectin benzoateand Fenpyroximate recorded highest population reduction ranged upto 99.39 percent after second spay while minimum decrease was recorded in untreated plants with overall 15.94 percent mortality. The least effective insecticide was observed to be Melathion with 38.79 and 65.43 percent reduction in citrus psyllids population after both the sprays, respectively.
Table 2: Percent reduction in number of Asian citrus psylla per branch (5 leaves) at various time intervals on citrus after second application of different insecticides.
| S. No | Treatment | Dose/100 LOW | Post spray timings | ||
| Week 1 | Week 2 | Week 3 | |||
| 1 | Thaiachloprid | 125 ml | 78.12f | 80.67f | 76.96f |
| 2 | Emamectin benzoate | 80 ml | 96.92ab | 97.41ab | 99.93a |
| 3 | Nitenpyram +bimetrozen | 100 gm | 97.00ab | 96.96b | 98.45b |
| 4 | Deltamethrin | 200 ml | 93.88c | 97.34ab | 98.10ab |
| 5 | Flubendiamide | 30 gm | 98.91ab | 98.10a | 98.21a |
| 6 | Lambda cyhalothrin | 250 ml | 92.94cd | 97.07ab | 99.24ab |
| 7 | Melathion | 500 ml | 31.19g | 75.89g | 89.23d |
| 8 | Pyriproxifen | 350 ml | 90.12de | 94.62c | 76.06fg |
| 9 | Nitenpyram + Chlorfenpyr | 150 gm | 99.99a | 99.09a | 99.10a |
| 10 | Fenpyroxymate | 180 ml | 97.05ab | 96.11abc | 98.45ab |
| 11 | Chlorpyrifos | 500 ml | 80.91f | 91.57e | 79.89e |
| 12 | Acetamaprid | 85 g | 87.73e | 94.94d | 91.23d |
| 13 | Imidacloprid | 150 ml | 98.51ab | 98.76a | 98.85a |
| 14 | Control | 14.28h | 16.36h | 17.18h | |
| LSD Value | 3.03 | 1.75 | 1.41 | ||
Values in columns followed by different letter (s) are significantly different at 5 % level of probability using DMR test.
As indicated in Figure 1, decline in the population of the pest with time was recorded from 91.73 to 13.20 percent after first application. After first week of spray, change in overall population of citrus psyllids seemed to be magnificent and reduced to 52.38 percent. After week 2, the population fluctuated to 13.20 percent of pests/ branch. When the plants were treated for the 2nd time the initial population was recorded 17.11 percent/ branch where no reasonable changes were noted after week 1 of the spray and the population decreased slightly to 17.40 percent/branch. The population declined to 10.48 percent/branch after week 2 and minimum population of the pest was observed 3 weeks after the spray which was recorded to be 4.43 percent /branch.
Figure 2 indicated the percent fluctuation in number of citrus psylla for each treatment applied to plants. Slight changes were observed in population density of the pest in untreated plants throughout the treated intervals. All the treatments illustrated significant decline in number of pest with maximum control observed in Nitenpyram + Chlophenpyr and Flubendiamide followed by Imidacloprid. The figure also demonstrated that sufficient number of pests were present after first spray which was brought under control with the second application of insecticides.
Asian citrus psylla is considered to be the serious pest of citrus in terms of direct attacking the leaves as well as serving as vector for Huang Long Bing (HLB), the citrus greening disease. Insecticidal application provides quick control of pest and is more effective in case of severe infestation which otherwise may not be control with conventional methods. Applying insecticides at critical flushing periods and during winter can greatly reduce populations of ACP. Surveys in Brazil indicated reduction in the rate of newly infested trees by intensive chemical programs and belligerent removal eradication of infested tress with ACP.
Table 3: Percent reduction of Citrus psylla per branch (5 leaves) overtime in citrus in comparison to control after both sprays.
| S. No | Treatment | Dose/100 LOW | Spray 1 | Spray 2 |
| 1 | Thaiachloprid | 125 ml | 49.26g | 78.58g |
| 2 | Emamectin benzoate | 80 ml | 78.53d | 98.75ab |
| 3 | Nitenpyram+bimetrozen | 100 gm | 83.15cd | 97.47bcd |
| 4 | Deltamethrin | 200 ml | 61.09f | 96.77cd |
| 5 | Flubendiamide | 30 gm | 89.83b | 99.39a |
| 6 | Lambda cyhalothrin | 250 ml | 71.99e | 96.42d |
| 7 | Melathion | 500 ml | 39.79h | 65.43h |
| 8 | Pyriproxifen | 350 ml | 87.40bc | 86.93e |
| 9 | Nitenpyram+Chlorfenpyr | 150 gm | 99.20a | 99.89a |
| 10 | Fenpyroxymate | 180 ml | 71.47e | 98.34abc |
| 11 | Chlorpyrifos | 500 ml | 71.56e | 84.13f |
| 12 | Acetamaprid | 85 g | 80.06d | 85.97e |
| 13 | Imidacloprid | 150 ml | 89.31b | 98.77ab |
| 14 | Control | 9.27i | 15.94i |
Values in columns followed by different letter (s) are significantly different at 5 % level of probability using DMR test. *LSD value for Spray 1: 4.92; *LSD value for Spray 2: 1.80
Scheduled insecticides have also been recommended in Florida against ACP (Rogers, 2008; Stanlsy et al., 2010b). Different insecticides showed different behavior at various intervals after spraying. Immediate reduction in population of the pest demonstrated quick knock down effect of Nitenpyram + Chlofenpyr just after application. The same was continued in later intervals as well which was followed by Flubendiamide and Imidacloprid. Complete removal was observed for Nitenpyram in combination with Chlorfenpyr after a week and nearly the same results were recorded after the second application. Neonicotinoids proved to be a better solution for ACP and hence HLB. Our results are in agreement with Dahiyaet al. (1994) and Chakrvarthy (1998). Similarly, Shivankaretal. (2000) also reported almost complete removal of psyllids by treating with Imidacloprid. Our findings are also in coincidence with that of Ahmed et al. (2004) and Sharma (2008) who investigated that neonicotinoids were significantly effective against citrus psylla. Similarly, Arora and Sharma (2011) also reported the latest group of insecticides to be more efficient against this pest. After first spray the fluctuation in overall population was reasonable in terms of time intervals after application of the treatments. Slight decrease during the first-time interval was observed in the population after second spray however it significantly increased in the later stages. Overall results revealed that negligible pests were present in the recorded duration after two times application of the insecticides.
Conclusions and Recommendations
All the insecticides were influential in regulating the population of Diaphorina citri, and revision of spray significantly reduced their occurrence. Although some insecticides affected the pest gradually. Nitenpyram + Chlorphenfyr proved to be highly effective and it should be sprayed twice with an interval of at least 4 weeks. Further studies should be conducted at various agro-climatic conditions for the effectiveness of these insecticides and identification of other species of citrus psylla.
Author’s Contribution
Ashraf Khan: Coceived, supervised and conducted research, wrote manuscript and is the corresponding author.
Suliman Shah: Conducted Research and Wrote manuscript.
Maid Zaman: Proof checking and provided technical assistance.
Komal Habib: Analyzed and Incorporated reviewers comments.
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