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Biocidal Activity of Some Selected Phytoextracts and Fruits of Different Citrus Cultivars against Fruit Fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae)

SJA_38_3_800-811

Research Article

Biocidal Activity of Some Selected Phytoextracts and Fruits of Different Citrus Cultivars against Fruit Fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae)

Muhammad Ismail1,*, Abu Bakar Muhammad Raza1, Muhammad Zeeshan Majeed1 and Umair Abbas1 and Riaz Hussain2

1Department of Entomology, College of Agriculture, University of Sargodha, Pakistan; 2Department of Entomology, The University of Agriculture, Peshawar, Pakistan.

Abstract | Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is one of the economic pests of horticultural crops. This invasive species causes substantial economic loss to citrus produce each year in Pakistan. Farmers rely on persistent synthetic insecticides for fruit fly control. Insecticidal phytoextracts are biorational alternates to hazardous synthetic insecticides. This study evaluated the efficacy of aqueous extracts of neem (Azadirachta indica A. Juss), garlic (Allium sativum L.), ginger (Zingiber officinale Roscoe) and lime citrus (Citrus aurantifolia (Christm.) Swingle) on the fruits of five citrus cultivars (i.e. bitter orange (Citrus aurantium L.), grapefruit (Citrus paradisi Macfad), lime (Citrus aurantifolia Christm), mandarin (Citrus reticulata Blanco) and sweet orange (Citrus sinensis (L.) Osbeck) against B. dorsalis using choice and no-choice fruit-dip bioassays. Results revealed a significant reduction of pupal weight and adult emergence of B. dorsalis by 4% extracts of A. indica, A. sativum and C. aurantifolia. Moreover, a significantly higher male to female adult sex ratio was observed in case of A. indica treatment. It is concluded from overall study results that the extracts of A. indica and C. aurantifolia exhibited significant anti-insect effects on the pupal recovery, pupal weight, adult emergence and male to female ratio of B. dorsalis on all five citrus host fruits under laboratory conditions, and hence are recommended to be further evaluated under field conditions and to consider their potential incorporation in IPM programs against fruit fly infestations on citrus crop.


Received | November 26, 2021; Accepted | January 15, 2022; Published | June 11, 2022

*Correspondence | Muhammad Ismail, Department of Entomology, College of Agriculture, University of Sargodha, Sargodha 40100, Pakistan; Email: ismailbilu2643@gmail.com

Citation | Ismail, M., A.B.M. Raza, M.Z. Majeed, U. Abbas and R. Hussain. 2022. Biocidal activity of some selected phytoextracts and fruits of different citrus cultivars against fruit fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). Sarhad Journal of Agriculture, 38(3): 800-811.

DOI | https://dx.doi.org/10.17582/journal.sja/2022/38.3.800.811

Keywords | Citrus cultivars, Bactrocera dorsalis, Botanical extracts, Azadirachta indica, Citrus aurantifolia, Pupal and adult emergence

Copyright: 2022 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).



Introduction

Oriental fruit fly Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is one of the world’s most damaging and economic pests of horticultural crops. It is an invasive polyphagous species with more than 250 host plants including vegetables and fruits (Shi, 2017;). This species causes damage through ovipositioning and subsequent larval development within the infested fruits resulting in considerable economic loss (). Female flies lay eggs inside the fruits, thereby rendering the maggots inaccessible to contact insecticides. Once eggs are laid, no effective control is possible except the removal and destruction of infested fruits ().

Primarily conventional synthetic insecticides are being used by the local farmers to combat fruit fly infestations. Frequent and intensive use of such chemicals cause many non-target effects including eradication of beneficial fauna, insecticide resistance in insect pests, contamination of environment and human health hazards due to persistent insecticidal residues (Desneux et al., 2007; Naeem et al., 2016; Deng et al., 2020; Dhananjayan et al., 2020; Haddi et al., 2020). These ecological consequences of synthetic chemical insecticides necessitate seeking alternative fruit fly management practices such as botanical insecticides (Umeh, 2016; Isman, 2020).

Botanical insecticides are one of the biorational tools to control insect pests and are usually safer for the environment, non-target species and for human health than the synthetic insecticides (Isman, 2020). Some plant species are rich source of bioactive compounds such as plant secondary metabolites that can defend plants against insect pests (Prakash and Rao, 2018). Many plant-based compounds and botanical extracts have been demonstrated to exhibit growth inhibition, feeding deterrence and repellency against a wide array of insect pests including fruit flies (Campos et al., 2019; Isman, 2020).

Moreover, the advantages of insecticidal botanical extracts include their quick and easy preparation by local farmers, cost-effectiveness and lower mammalian toxicity (Turek and Stintzing, 2013; Isman, 2020). Besides, whereas synthetic insecticides are based on a particular active ingredient, plant-derived insecticides are composed of various compounds that work on both behavioural and biochemical processes of insect pests. Therefore, it is less feasible that pests gain resistance to these substances (Marrone, 2019). Similarly, some studies have demonstrated that different host plants exert differential impact on fruit fly ovipositioning preference, egg and maggot development and pupal and adult life parameters (Brévault and Quilici, 2007; Muthuthantri and Clarke, 2012).

Keeping in view the aforementioned background, this laboratory study was aimed to determine the bioactivity of aqueous extracts of four local plant species on the ovipositional preference and development of fruit fly B. dorsalis on the fruits of five locally available citrus cultivars.

Materials and Methods

Insect rearing

The experiment was conducted in laboratory of the Department of Entomology, University of Sargodha. Culture of fruit fly B. dorsalis was obtained from the fruit fly rearing laboratory and was maintained at 27 ± 1ºC temperature, 60 ± 5% relative humidity and at 16 h:10 h light and dark photoperiod. Adults were fed on a banana-based artificial diet with ingredients including egg yolk, sugar, honey, yeast, syrup and vitamin B complex blended in a ratio of 2:4:8:2:1, respectively, and was placed in a freezer for subsequent use (Ahmad et al., 2010). Fifty newly emerged pairs of B. dorsalis adults from stock culture were sexed and transferred into a new adult rearing cage (40 × 45 × 45 cm). Twenty-one day old female flies were used in the bioassays as this is the optimum age for them to oviposit. Moreover, cleaning of rearing cages and adjustment of diet slides were done daily to avoid any microbial contamination (Rattanapun et al., 2009).

 

Table 1: Detail of plants used in the study.

Common / Vernacular Name

Botanical name

Family

Parts used

Neem

Azadirachta indica A. Juss

Meliaceae

leaves

Ginger

Zingiber officinale Roscoe

Zingiberaceae

rhizomes

Garlic

Allium sativum L.

Liliaceae

tubers

Citrus lime

Citrus aurantifolia (Christm.) Swingle

Rutaceae

peel

 

Botanical extracts preparation

Extracts of four local plant species were used in this research for assessing their effectiveness against B. dorsalis. The detail of these plants is mentioned in Table 1. Different parts of these plants, as mentioned in Table 1, were rinsed thoroughly with tap water and were let to dry under sunshine for one day, followed by an oven drying at 50 °C for two days. The dry samples were grinded into powder by an electric blender. For extraction, a 200 mL conical flask was loaded with 20 g of each plant powder along with 100 mL of distilled water. The conical flasks were wrapped with aluminum foil and were kept on an electric shaker set at 150 rpm for 24 h. The samples were then sieved through a fine mesh muslin cloth followed by filtering through Whatman No 1 filter paper sheets.

 

Table 2: Recovered pupae (number/fruit) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

4.00±0.342b

5.00±0.233b

4.70±0.321b

3.30±0.345b

2.0

3.00±0.284bc

3.00±0.523c

3.30±0.123bc

2.30±0.034b

4.0

1.70±0.183c

1.30±0.084d

2.30±0.241c

1.30±0.075b

Control

7.70±0.428a

8.00±0.992a

8.30±0.923a

6.00±0.783a

Sign.

29.8***

42.3***

29.7***

9.67**

Sweet orange

1.0

3.33±0.347b

3.67±0.157b

4.33±0.231b

3.33±0.083b

2.0

2.33±0.238c

3.67±0.154b

3.00±0.342b

2.33±0.783bc

4.0

1.00±0.289d

1.00±0.092c

1.33±0.082c

1.00±0.093c

Control

7.67±0.634a

8.00±0.923a

8.33±0.923a

6.00±0.345a

Sign.

99.9***

60.5***

35.7***

11.5**

Grapefruit

1.0

2.33±0.237b

3.33±0.183b

3.33±0.042b

2.67±0.893b

2.0

1.67±0.428bc

3.33±0.132b

2.67±0.023b

2.00±0.985b

4.0

0.67±0.087c

0.67±0.023c

0.33±0.002c

2.33±0.991b

Control

7.67±0.723a

8.00±0.989a

8.33±0.941a

6.00±0.898a

Sign.

88.3***

55.8***

102.0***

14.8**

Lime

1.0

1.33±0.182b

1.33±0.097b

1.67±0.023b

0.67±0.072b

2.0

0.67±0.094bc

0.67±0.082bc

1.33±0.042b

0.67±0.066b

4.0

0.00c

0.00c

0.00c

0.00b

Control

7.67±0.742a

8.00±0.923a

8.33±0.892a

6.00±0.872a

Sign.

151.0***

247.0***

168.0***

20.1***

Bitter orange

1.0

2.33±0.238b

3.00±0.384bc

3.00±0.231b

2.00±0.034b

2.0

1.67±0.271b

3.33±0.281b

2.33±0.324b

1.67±0.038b

4.0

0.00c

1.67±0.128c

0.33±0.039c

0.00b

Control

7.67±0.548a

8.00±0.923a

8.33±1.023a

6.00±0.823a

Sign.

65.9***

34.3***

70.0***

14.6**

***: significant at P < 0.001; **: significant at P < 0.05

 

The solvent was evaporated by a rotary vacuum evaporator (Laborota 4001, Heidolph, U.S.A.) set a temperature of 50 °C in the water bath. Three concentrations of each botanical extract i.e. 1.0, 2.0 and 4.0% were made through serial dilution process.

Fruit-dip bioassays

Fruits of almost similar size and color were picked from the orchard trees of five locally available citrus cultivars (i.e. bitter orange (C. aurantium), grapefruit (C. paradisi), lime (C. aurantifolia, mandarin (C. reticulata) and sweet orange (C. sinensis) with no previous application of any insecticide during the season. Fruits were thoroughly washed with tap water and were air-dried at room temperature (28 °C). These fruits from each cultivar were used as an oviposition medium. The fruits were then dipped in each concentration of each botanical for 60 sec, and were air-dried and labelled. Oviposition preference of B. dorsalis adults was tested by performing following two types of bioassays.

Choice test

For oviposition, three fruits of each citrus cultivar were offered collectively as free choice. Twenty pairs of B. dorsalis adults were placed in an insect rearing cage (40 × 45 × 45 cm). After 24 h of egg deposition, the fruits were gathered individually in plastic jars (25 × 12 cm) lined with sterilized sand and sawdust at the bottom for pupation. Pupae were obtained after 6–8 days by sieving the pupation medium. The experiment was replicated independently three times. Fruit-wise observations were recorded regarding the ovipositional preference and biological parameters such as pupal recovery, pupal weight, pupal deformity, adult emergence and adult sex ratio. 

No-choice test

In this test, oviposition preference was determined with three fruits of each cultivar placed separately in a separate cage. Fruits of each cultivar were treated with each botanical extract individually. Ten pairs of B. dorsalis adult flies were placed in each cage and were permitted for 24 h for ovipositioning. A similar series of experiments were carried out using each cultivar’s fresh fruits as controls. In case of no-choice test, same observations were recorded as described above for choice test. The experiment was replicated three times.

Statistical analysis

A factorial analysis of variance (ANOVA) was performed to assess the impact of different concentrations of botanical extracts on B. dorsalis performance. Means were compared using Fisher’s least significant difference (LSD) test at 5% probability level. Statistical interpretations were done using Minitab 17.0 software.

Results and Discussion

Choice test

As compared to control, all botanical extracts particularly at higher (4%) concertations exhibited significant effect (P < 0.05) on B. dorsalis pupal recovery under choice test and this effect was found concentration-dependent. Control treatment showed maximum pupal recovery (6.0–8.3 pupae/fruit) in all citrus host fruits (Table 2). No pupae were recovered at 4% concentration of all botanicals from the fruits of lime and bitter orange cultivars. In general, A. indica and C. aurantifolia extracts showed significantly reduced ovipositional preference on each citrus cultivar than the extracts of A. sativum and Z. officinale.

A similar concentration-dependent response was observed in case of pupal weight (mg) for all botanicals. Pupal weight varied less significantly with mandarin

 

Table 3: Pupal weight (mg) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

4.32±0.573a

4.10±0.304a

4.32±0.452ab

3.53±0.653ab

2.0

4.10±0.734ab

3.10±0.623a

4.10±0.561ab

3.51±0.783ab

4.0

4.32±0.823b

4.10±0.642a

2.74±0.358b

2.53±0.732b

Control

3.53±0.572a

3.50±0.452a

4.67±0.562a

4.85±0.653a

Sign.

2.94**

2.17NS

2.95**

5.69**

Sweet orange

1.0

4.00±0.532a

3.68±0.303ab

3.69±0.542ab

3.53±0.733bc

2.0

4.10±0.653a

3.03±0.360b

3.03±0.234b

4.18±0.743ab

4.0

2.35±0.632b

2.39±0.624b

2.39±0.236b

3.07±0.465c

Control

4.60±0.345a

4.50±0.632a

4.67±0.526a

4.85±0.743a

Sign.

6.95**

4.68**

5.27**

7.67**

Grapefruit

1.0

4.00±0.632a

3.69±0.673ab

3.89±0.456a

3.78±0.456a

2.0

4.10±0.636a

2.55±0.562bc

3.35±0.563a

3.39±0.245ab

4.0

1.73±0.085b

1.72±0.636c

0.81±0.034b

1.73±0.254b

Control

4.60±0.587a

4.50±0.632a

1.73±0.453a

4.85±0.657a

Sign.

5.27**

5.31**

10.3**

5.42**

Lime

1.0

3.50±0.452a

2.77±0.542b

2.77±0.732b

3.08±0.653ab

2.0

2.87±0.146a

1.37±0.073bc

2.27±0.562b

2.87±0.034ab

4.0

0.59±0.037b

0.47±0.027c

0.56±0.028c

0.71±0.005b

Control

4.60±0.632a

4.50±0.532a

4.67±0.734a

4.86±0.633a

Sign.

6.15**

19.2***

39.2***

4.10**

Bitter orange

1.0

3.43±0.353b

3.77±0.632ab

3.77±0.453a

2.67±0.234b

2.0

2.70±0.653b

3.57±0.435b

3.23±0.457a

2.70±0.456b

4.0

0.48±0.037c

3.23±0.652ab

0.97±0.045b

0.58±0.082c

Control

4.60±0.653a

4.50±0.532a

4.67±0.653a

4.85±0.654a

Sign.

45.5***

2.85**

7.76**

60.2***

***: significant at P < 0.001; **: significant at P < 0.05; NS: non-significant.

 

Table 4: Adult emergence (%) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

85.0±5.523ab

46.7±3.863b

77.8±4.736ab

69.4±7.743a

2.0

55.6±5.363b

55.5±5.565b

58.3±7.343bc

72.2±7.342a

4.0

50.0±5.562b

100a

50.0±4.746c

66.8±4.764a

Control

100a

96.8±2.545a

100a

77.8±7.343a

Sign.

2.47**

50.3***

6.95**

0.743NS

Sweet ornage

1.0

69.4±6.338a

68.9±7.344a

71.1±5.672a

69.4±7.343a

2.0

72.2±6.238a

72.2±6.348a

72.2±5.433a

44.4±4.733ab

4.0

66.7±6.344a

71.2±7.638a

0.00b

16.7±2.346b

Control

82.1±7.363a

84.3±6.344a

87.5±4.566a

86.1±6.734a

Sign.

1.75NS

0.17NS

21.3***

4.96**

Grapefruit

1.0

66.7±7.384ab

69.4±5.346a

83.3±6.344a

100a

2.0

33.3±5.635bc

66.7±5.324a

41.7±6.342b

83.3±7.342a

4.0

0.00c

0.00b

16.7±3.634b

11.1±1.346b

Control

100a

100a

100a

77.8±7.345a

Sign.

13.3**

9.49**

9.30**

4.22**

Lime

1.0

16.7±2.344a

66.7±6.348a

50.0±3.643ab

83.3±6.342a

2.0

0.00b

16.7±2.563b

66.7±4.734ab

33.3±3.264ab

4.0

0.00b

0.00b

0.00b

0.00b

Control

100a

100a

95.8±4.743a

94.4±6.345a

Sign.

33.0***

15.2**

3.29**

5.48**

Bitter orange

1.0

50.0±3.677ab

38.9±3.533bc

72.2±5.743a

33.3±1.734b

2.0

44.4±5.384ab

61.1±5.352ab

27.8±6.342b

11.1±1.435b

4.0

0.00b

0.00c

0.00b

0.00b

Control

100a

100a

95.8±4.732a

77.8±3.634a

Sign.

5.05**

8.72**

16.6***

7.67**

***: significant at P < 0.001; **: significant at P < 0.05; NS: non-significant.

 

showing the highest pupal weight 2.5–4.4 mg at 4% concentration application of each botanical, while grapefruit resulted into the least pupal weight of 0.81 mg when treated with a 4% Z. officinale extract as compared to other treatments (Table 3). Among the host citrus fruits, the least pupal weight was recorded for the fruits of lime and bitter orange fruits.

Similarly, the effect of all botanical extracts on B. dorsalis adult emergence was dose-dependent. Higher concentrations of all botanicals showed fewer adults’ emergence. Particularly, no emergence of adults was observed from the pupae recovered from the fruits of lime, grapefruit and bitter orange treated with 4% extracts of A. indica and A. sativum (Table 4). Among host citrus cultivars, lime and bitter orange fruits revealed the minimum adult emergence of B. dorsalis.

In the case of adult sex ratio, A. indicaA. sativum, Z. officinale, and C. aurantifolia treatments significantly altered the adult sex ratio in all citrus cultivars under the choice test. Male to female adult sex ratio was close to one for the lowest concentration of A. indica extract. However, it was consistently higher with 1.0, 2.0 and 4.0% concentration of each extract. Among the different host fruits, the female ratio was higher in grapefruit, lime and bitter orange than in mandarin and sweet orange (Figure 1). 

No-choice test

All four botanical extracts under no-choice test with each citrus cultivar showed a concentration-dependent response regarding the pupal recovery as the number of recovered pupae decreased with the increase in botanical concentration (Table 5). Highest concentration of all tested extracts adversely affected the oviposition of B. dorsalis. Minimum recovery (0.0–0.33 pupae/fruit) was from the fruits of lime

 

and bitter orange, and maximum (1.00–1.67 pupae/fruit) from the fruits of mandarins and sweet orange cultivar which were significantly lower than the pupae in their respective controls (Table 5).

Similar trend was observed regarding the impact of different botanical extracts and citrus cultivars on the pupal weight of B. dorsalis under the no-choice test. Mandarins and lime showed highest (1.95–2.97 mg) and lowest (0.33–0.49 mg) pupal weight, respectively.

 

Table 5: Recovered pupae (number/fruit) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under no-choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

3.33±0.523b

3.33±0.927b

4.00±0.592b

3.00±0.348b

2.0

1.67±0.047c

3.00±0.782b

3.33±0.382b

2.00±0.583bc

4.0

1.00±0.034c

1.33±0.382c

1.67±0.328c

1.33±0.034c

Control

7.33±0.623a

7.67±0.993a

7.00±0.943a

7.00±1.082a

Sign.

96.9***

87.6***

35.7***

33.1***

Sweet ornage

1.0

3.67±0.532b

3.33±0.347b

4.00±0.348b

3.00±0.634b

2.0

2.67±0.623c

2.67±0.724bc

2.67±0.682c

2.67±0.047b

4.0

1.00±0.348d

1.00±0.084c

1.33±0.238d

1.67±0.073b

Control

7.33±0.823a

7.67±0.989a

7.00±0.996a

7.00±0.943a

Sign.

86.2***

24.2***

42.3***

18.0***

Grapefruit

1.0

4.00±0.237b

4.67±0.082b

4.33±0.348b

3.67±0.634b

2.0

3.00±0.348b

2.67±0.194c

3.33±0.634bc

3.33±0.348b

4.0

0.67±0.007c

1.33±0.083c

1.33±0.234c

1.33±0.238c

Control

7.33±0.932a

7.00±0.974a

7.00±0.893a

7.00±0.834a

Sign.

34.5***

27.3***

13.3**

22.1***

Lime

1.0

1.00±0.093b

1.67±0.189b

1.67±0.238b

0.67±0.009b

2.0

0.33±0.006b

1.33±0.037b

0.67±0.007bc

0.67±0.006b

4.0

0.00b

0.00c

0.00c

0.33±0.003b

Control

7.33±0.728a

7.67±0.892a

7.00±0.348a

7.00±0.993a

Sign.

86.7***

140.0***

73.1***

62.4***

Bitter orange

1.0

2.67±0.238b

2.00±0.238b

3.00±0.374b

2.67±0.539b

2.0

1.00±0.093c

1.00±0.072bc

2.33±0.238b

1.00±0.348c

4.0

0.00d

0.33±0.002c

0.00c

0.00c

Control

7.33±0.998a

7.67±0.992a

7.00±0.638a

7.00±1.093a

Sign.

190.0***

80.7***

43.6***

86.0***

***: significant at P < 0.001; **: significant at P < 0.05.

 

A. indica and C. aurantifolia extracts exhibited maximum and significant reduction of pupal weight in all citrus cultivars (Table 6).

Similarly, highest adult B. dorsalis emergence was recorded for untreated fruits of all cultivars as compared to those treated with different botanical extracts. Higher concentration of botanicals results exhibited statistically a fewer number of adult emergence. The emergence rate was higher in the mandarin fruits as compared to other cultivars. A. indica, A. sativum and C. aurantifolia extracts at 4% concentration resulted in zero adult emergence in fruits of lime and bitter orange cultivars (Table 7).

Male to female adult sex ratio of B. dorsalis was also affected by different concentrations of C. aurantifolia, A. indicaA. sativum and Z. officinale. It was close to one in the lowest concentration of A. indica extract. However, it was consistently higher with 1.0, 2.0 and 4.0% concentration of each extract (Figure 2).

Fruit fly infestations are one of the detrimental factors for fruit production in Pakistan. B. dorsalis is an economic pest of citrus and other horticultural crops in Pakistan. Obscured feeding nature of its maggots renders this pest very difficult to control with conventional synthetic insecticides. This laboratory study assessed the biocidal activity of four local botanical extracts (i.e. of A. indica, A. sativumZ. officinale and C. aurantifolia) against B. dorsalis on the fruits of five commonly grown citrus cultivars.

Results demonstrated a differential and significant effect of all four botanical extracts on the pupal recovery, pupal weight, adult emergence and male to female adult sex ratio of B. dorsalis on the fruits of all citrus hosts. Among these botanicals, extracts of

 

Table 6: Pupal weight (mg) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under no-choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

4.14±0.572a

3.43±0.583a

4.33±0.683ab

4.14±0.682a

2.0

3.40±0.672ab

3.26±0.587ab

3.50±0.632bc

2.77±0.298b

4.0

2.73±0.582b

1.95±0.036b

2.97±0.387c

2.73±0.295b

Control

3.20±0.327ab

3.23±0.587ab

4.68±0.523a

3.36±0.634ab

Sign.

2.01**

2.63**

5.1**

3.08**

Sweet ornage

1.0

3.43±0.347a

3.24±0.637a

3.70±0.378a

3.71±0.678a

2.0

2.73±0.348ab

3.00±0.683ab

3.60±0.582a

2.73±0.298ab

4.0

1.73±0.118b

1.21±0.587b

2.70±0.183a

2.20±0.284b

Control

3.26±0.732ab

3.23±0.583a

4.60±0.658a

3.36±0.683a

Sign.

2.43**

2.67**

2.1NS

3.87**

Grapefruit

1.0

2.80±0.285a

3.19±0.673a

2.76±0.283b

3.20±0.099a

2.0

2.63±0.198a

1.87±0.683b

1.41±0.093c

2.41±0.048ab

4.0

0.98±0.073b

2.21±0.298ab

1.54±0.285bc

1.36±0.039b

Control

3.20±0.285a

3.23±0.386a

4.68±0.387a

3.36±0.386a

Sign.

4.99**

415**

15.7***

3.29**

Lime

1.0

1.40±0.089ab

2.12±0.376b

2.12±0.284b

1.40±0.007b

2.0

0.81±0.005b

2.76±0.218ab

0.96±0.009c

1.14±0.003b

4.0

0.37±0.023b

0.49±0.037c

0.45±0.032d

0.33±0.083b

Control

3.19±0.237a

3.23±0.568a

4.68±0.736a

3.36±0.593a

Sign.

5.64**

19.7***

55.7***

5.96**

Bitter orange

1.0

2.77±0.385ab

2.57±0.835ab

2.71±0.285b

2.52±0.275b

2.0

2.34±0.285b

2.74±0.285a

2.50±0.382b

2.20±0.386b

4.0

0.34±0.037c

0.96±0.073b

0.67±0.057c

0.41±0.087c

Control

3.17±0.398a

3.23±0.683a

4.68±0.682a

3.36±0.285a

Sign.

45.1***

3.55**

68.1***

61.0***

***: significant at P < 0.001; **: significant at P < 0.05; NS: non-significant.

 

A. indica (neem) and C. aurantifolia (citrus lime) exhibited a significant and maximum suppression of B. dorsalis pupal recovery, average pupal weight and adult emergence percentage and male to female adult sex ratio as compared to other extracts and control treatments. Many studies reported the deterrence of ovipositioning and suppression of ovary development in different Bactrocera species by A. indica extracts (Ignacimuthu and Vendan, 2008; Khan et al., 2016; Ilyas et al., 2017).

Similarly, some previous research reported negative and suppressive effects of neem seeds extract on the landing, preference and oviposition by B. dorsalis fruit flies on their guava fruits in both choice and no-choice tests (Sandeep and Desraj, 2016; Singh and Singh, 1998). Another study by Stark et al. (1990) showed adverse effects of A. indica extract based diets on the pupae formation and adult emergence of three Tephritid flies. Moreover, our results regarding the ovipositional deterrence by extracts of A. indica and C. aurantifolia are consistent with those of previous studies on B. zonata (Mahmoud and Shoeib, 2008; Papachristos et al., 2008). Later study has demonstrated that lime peel extract confers resistance to citrus fruits against B. dorsalis. Essential oil and extract of this citrus species have been shown ovicidal, larvicidal and adulticidal effects against Aedes mosquitoes (Sarma et al., 2019).

Among five citrus cultivars evaluated in this study, fruits of Lime and bitter orange were least preferred and most suppressive against B. dorsalis adults followed by the fruits of grapefruit, while fruits of sweet orange and kinnow mandarin were found most preferred and susceptible for fruit fly in both choice and no-choice tests. This differential oviposition preference and development of fruit flies could be due to

 

the differential olfactory bio-constitutions (volatile oils) of different citrus cultivars which would trigger and affect the fruit fly olfactory response towards these cultivar fruits (Papachristos and Papadopoulos, 2009; Liu and Zhou, 2016). Our results are in line with the findings of Diatta et al. (2013) showing that fruits of lime (C. aurantifolia) were not preferred at all by the adults of fruit fly B. invadens. Similarly, disturbance in the sex ratio due to botanical treatments and due to different citrus cultivars are sub-lethal effects as reviewed by Isman (2020).

Conclusions and Recommendations

It is concluded that the fruits of citrus cultivars kinnow mandarin and sweet orange appeared as most

 

Table 7: Adult emergence (%) of Bactocera dorsalis from fruits of different citrus cultivars treated with different botanical extracts under no-choice test.

Host Plants

Concentration (%)

Azadirachta indica

Allium sativum

Zingiber officinale

Citrus aurantifolia

Mandrins

1.0

80.2±5.233a

83.3±8.453a

58.3±3.587ab

88.9±8.452a

2.0

83.3±5.236a

61.1±6.458ab

44.4±5.734bc

61.1±4.684ab

4.0

69.6±6.234a

33.3±4.583b

16.7±2.474c

16.7±3.458b

Control

86.9±6.634a

90.5±7.453a

95.8±7.453a

95.2±7.347a

Sign.

2.34NS

3.16**

7.47**

6.20**

Sweet ornage

1.0

72.2±7.342ab

83.3±8.457a

59.1±5.874b

80.6±7.894a

2.0

33.3±2.734bc

38.9±5.784b

50.0±4.684b

33.3±3.458b

4.0

16.7±3.734c

16.7±3.657b

11.1±2.347c

11.1±3.465b

Control

95.2±8.673a

90.5±5.845a

95.8±7.874a

94.4±7.457a

Sign.

7.57**

10.7**

29.5***

9.82**

Grapefruit

1.0

76.7±4.734ab

83.3±5.843a

71.7±6.643a

88.9±8.754a

2.0

55.6±5.734b

69.4±5.784a

72.2±7.453a

77.8±8.544ab

4.0

0.00c

33.3±3.458b

16.7±2.547b

33.3±3.856b

Control

95.3±7.453a

95.2±6.747a

95.8±7.458a

100a

Sign.

25.7***

7.62**

8.23**

3.82**

Lime

1.0

66.7±7.452a

83.3±7.457ab

83.3±8.845a

83.3±6.854ab

2.0

0.00b

33.3±3.488bc

50.0±5.856ab

33.3±2.785bc

4.0

0.00b

0.00c

0.00b

0.00c

Control

96.2±6.236a

100a

95.8±8.453a

97.3±8.453a

Sign.

8.19***

6.07**

6.50**

5.57**

Bitter orange

1.0

100a

77.8±6.783a

88.9±6.845a

95.3±7.453a

2.0

66.7±6.348a

69.4±6.348a

66.7±6.458ab

88.9±7.458a

4.0

0.00b

0.00b

16.7±3.456b

0.00b

Control

100a

90.2±5.346a

95.8±8.845a

100a

Sign.

8.2**

6.83**

5.5**

61.9***

***: significant at P < 0.001; **: significant at P < 0.05; NS: non-significant.

 

preferred by B. dorsalis and favored its biology as compared to grapefruit, lime and bitter orange. Moreover, the aqueous extracts of A. indica (neem) and C. aurantifolia (citrus lime) were the most effective and exerted significant reduction of pupal development and adult emergence and sex ratio of B. dorsalis flies on the fruits of all five citrus cultivars tested under the laboratory conditions. Hence, further studies should be conducted to incorporate these botanicals extracts into IPM programs for managing B. dorsalis on the citrus crop. Moreover, these effective botanical extracts can be applied in combination with other pest control strategies to control fruit fly infestations as demonstrated by Mahmoud (2007) and Ismail et al. (2016) which have shown compatibility of entomopathogenic nematodes and fungi, respectively along with different botanical extracts against different fruit fly species.

Novelty Statement

This laboratory study has demonstrated a differential effect of the fruits of commonly grown citrus cultivars on the oviposition preference and development parameters of fruit fly B. dorsalis. Moreover, the aqueous extracts of Azadirachta indica (neem) and Citrus aurantifolia (citrus lime) can be effectively used against fruit fly infestations in citrus crop.

Authors’ Contribution

Muhammad Ismail : Conducted the bioassays, performed statistical analysis and prepared results.

Abu Bakar Muhammad Raza: Conceived the idea, planned the experiment and technically revised the manuscript.

Muhammad Zeeshan Majeed: Wrote first draft of the manuscript.

Umair Abbas: Conducted the bioassays, performed statistical analysis and prepared results.

Riaz Hussain: Helped in format setting and proofreading

Conflict of interest

The authors have declared no conflict of interest.

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