Repellent and Toxic Effects of some Plant Extracts on Subterranean Termite Psammotermes hybostoma (Isoptera: Rhinotermitidae)

 

Khalid A Asiry1*, Abir S Al-Nasser2 and Refaat A Abohassan3

1Department of Arid Land Agriculture, Faculty of Meteorology, Environment and Arid Land Agriculture, King Abdulaziz University. Jeddah, Saudi Arabia

2Department of Biology, Faculty of Science, University of Jeddah, Jeddah, Saudi Arabia

3Department of Arid Land Agriculture, Faculty of Meteorology, Environment and Arid Land Agriculture, King Abdulaziz University. Jeddah, Saudi Arabia

*For correspondence: Kasiry@kau.edu.sa; aalnasser@uj.edu.sa; rabuhasan@kau.edu.sa

Received 04 October 2021; Accepted 28 December 2021; Published 28 February 2022

 

Abstract

 

The current study was conducted to evaluate the toxicity and repellent effects of ethanolic extracts of Lantana camara, Moringa oleifera, Rhazya stricta and Ruta chalepensis on subterranean termite, Psammotermes hybostoma. All the tested extracts demonstrated noticeable toxicities, however, L. camara and R. stricta showed relatively more toxic effects, at 24 h and 48 h with LC50s of 177.5, 131.5 mg.kg-1 and 199.8, 140.3 mg.kg-1, respectively. Toxic effect was observed to be dependent on dose as well as exposure-time. No significant differences were observed between L. camara, R. sricta and positive control fipronil 2.5EC. Moreover, L. camara and R. stricta extracts, at 500 mg.kg-1, showed potential repellent effects on P. hybostoma (Desneux) with repellency of 88.3 and 81.67%, respectively. Our work highlights the importance of screening the plant-based products for anti-termites’ activity. We suggest that tested plants could possibly provide an alternative means for termite control strategies in protecting the economically important crops. © 2022 Friends Science Publishers

 

Keywords: Lantana camara; Moringa oleifera; Plant extracts; Repellent; Acute and Chronic Mortality; Termites; Psammotermes hybostoma; Rhazya stricta; Ruta chalepensis; Termiticide

 


Introduction

 

Termites are social insect pests present in a wide-ranging terrestrial environment scattered all over the globe. Termites are the most detrimental pest in the tropics which cause significant challenges in housing and agriculture. Subterranean termites are highly destructive polyphagous insect pests and it is anticipated that billions of dollars are expended annually to manage termites worldwide (Tsunoda 2003; Buczkowski and Bertelsmeier 2017). Colonies of Psammotermes hybostoma (Desneux) are common subterranean termites prevalent in rural and suburban areas in Saudi Arabia and are held responsible for largely damaging agricultural crops, forestry and household wooden structures (Adeyemi 2010; Alshehri et al. 2014; Buczkowski and Bertelsmeier 2017; Ahmad et al. 2021). Termites feed on the decaying organic wastes (Kambhampati and Eggleton 2000). They can also feed on live plants parts of groundnuts, maize, and millets (Ravan et al. 2015; Ahmad et al. 2021). In general, several chemical insecticides like aldrin, BHC, DDT and dieldrin are being used for long term to provide safety from termite invasion. However, these has now been barred in various countries because their residues have adversely influenced the terrestrial and aquatic environment (Elango et al. 2012; Bakaruddin et al. 2018). The destructive effects of chemical-based termiticides and the enhanced prevalence of termite-resistance have led to the necessity of discovering alternate bio-pesticides which are safer and more effective termiticides.

The use of chemicals costs higher, and has resulted in phytotoxicity, mammalian toxicity, pesticides residues, effects on non-target organisms, development of insect resistance and outbreaks (Elango et al. 2012). Therefore, interest has been developed among researchers to investigate the cheaper botanical insecticides to reduce the damages caused by termites and to be safe for human health (Singh et al. 2004; Senthil et al. 2005). Plants are eco-friendly and may provide alternative remedy to use of synthetic insecticides. Plants are rich sources of bioactive chemicals that act as natural insecticides against different insects and other organisms as well (Hussain et al. 2012). Recently, scientific interest for development of environment friendly plant-based pesticides and insect growth regulators has surged out (Arihara et al. 2004; Isman 2006; Cheng et al. 2007; Erb and Kliebenstein 2020). Manzoor et al. (2011) reported Curcuma longa extracts to be effective in soil treatments to protect food substrate against termites. Addisu et al. (2014) found that Macrotermes spp. can be easily managed by plant extracts as bio-termiticides in integrated pest management approach and Elsayed (2011) recorded that two desert plant extracts have a toxic effect on two termite species.

Several researchers have documented the toxic effects of plant extracts of Lantana camara (lantana or shrub verbena), Rhazya stricta (Harmal), Ruta chalepensis (fringed rue) and Moringa oleifera (horseradish tree or drumstick tree) in controlling some insect pests from different countries of the world (Ghosh et al. 2012; Ojiako et al. 2013; Addisu et al. 2014). These plants are widely distributed in the Kingdom of Saudi Arabia (Mossa et al. 1987) but their efficacy against termites is less explored.

The drawbacks related to the mismanagement and overuse of synthetic pesticides have incited the necessity for alternate pest management possibilities. In this regard, plant extracts, comprised of various bioactive compounds, are considered as promising alternative to synthetic insecticides. Therefore, this study was conducted to assess the concentration and time dependent efficacy of locally available plants. Lantana camara, Rhazya stricta, Ruta chalepensis and Moringa oleifera to contact toxicity and behavior of termite P. hybostoma (Desneux).

 

Materials and Methods

 

Termite

 

Termite species of Psammotermes hybostoma (Desneux) was obtained from the Research Station of King Abdulaziz University at Hada Elsham, Saudi Arabia. Termites were kept in plastic enamel trays and were retained and nurtured in the laboratory according to Upadhyay et al. (2010). Water and carton papers were used as a food material. Termites were kept in glass jars in dark conditions at 25°C and 75 ± 5 RH.

 

Plant materials

 

Plant materials viz., L. camara, R. stricta, R. chalepnsis and M. oleifera were collected across many parts in Saudi Arabia.

 

Preparation of plant extracts

 

Extracts of test plants were prepared by using a modified method. Leaves of the test plants were air dried for a week and then ground with micro plant grinding machine and subsequently, sieved through a 0.25 mm pore size mesh sieve to acquire uniform fine dust particles (Selase and Getu 2009). The powders obtained were kept separately in glass containers and stored at room temperature (25 ± 3ºC) in the dark. Next, 10 g of powder was mixed with 100 mL of absolute ethanol (99.9%) at room temperature (25 ± 3ºC). The mixture was stirred for 30 min with magnetic stirrer and left for 24 h. Further, it was concentrated in a rotary evaporator in a water bath at 55°C, and the residue obtained was stored at 4°C until use.

 

Mortality test

 

Stock solutions of the four plant extracts were designed by soaking 0.5 g of crude extract in 100 mL warm distill water and a range of concentrations of 100, 200, 300, 400 and 500 mg.kg-1 were obtained from stock solutions. Further, filter papers (Whatman No.1) of 9 cm diameter treated with 1 mL of different concentrations of ethanolic extracts of test plants were put in Petri dishes and allowed to dry at room temperature for 30 min. Next, twenty worker termites were arbitrarily chosen from stock population and kept in the treated Petri dishes. In all experiments, Fipronil 2.5EC (a synthetic insecticide) and water served as a positive and negative controls, respectively. All the treated Petri dishes were wrapped with a double layer of black plastic sheet to imitate the darkness for termites. Five different concentrations of each plant extract were replicated three times and placed in an incubator at 28 ± 3°C, 75 ± 2 RH. Mortality percentage of termite was recorded at 24 h and 48 h after treatment and values % for the natural mortality in the control treatment corrected by using Abbott (1925) equation.

 

Termite repellency test

 

For repellency assay, concentrations ranging from 100, 200, 300, 400 and 500 mg.kg-1 of each plant extracts were prepared. Petri dishes were spotted with Whatman No.1 filter paper (9 cm) cut into two equal parts with a distance of 2 cm. One part was treated with different concentrations of plant extracts and the other was left untreated by only distill water (Addisu et al. 2014). Twenty termites were established at the center of both treated and untreated filter papers and set in dark to reduce the effect of light on the termites. Three replications were used for each concentration of plant extracts. Number of termites on both treated and untreated filter paper in each Petri dish was recorded 30 min post-treatment. Based on the number of termites stayed on the extract-treated filter paper, repellency was determined.

 

Statistical analysis

 

The percentage mortality of P. hybostoma was calculated and were separately subject to a repeated measure ANOVA to assess the effect of the following factors: time (repeated factor with 3 observations), concentrations of four plants (17 experimental unites including control) and interactions between these factors. Before applying the repeated measure ANOVA, data were transformed by applying Log 10 (Max+1-X) to meet the normality and improve variances. Where significant treatment differences (P ≤ 0.05) were detected, the Fisher’s Least Significant Difference (LSD) tests were performed to identify differences in treatment means. In addition, LC50 was calculated according to Finney (1971). Data was corrected for control mortality using Abbott’s formula (1952). As for Repellency test, percentages of repellency rate (PR) were calculated using the method of Jilani et al. (1988). Then, obtained data (PR) were analyzed by one-way ANOVA to determine what is the best of the four used plants with tested concentrations (16 experimental unites) as a repellent for emerged adults of P. hybostoma. The mean differences were compared using Fisher's LSD test. All data analyses were performed within a SPSS ver.22 (IBM Corporation 2013).

 

Results

 

Time dependent toxicity

 

As presented in Table 1 and Fig. 1, a 100% mortality of the worker termites was recorded in the positive control (Fipronil 2.5EC) and ethanolic extract of L. camara, at 500 mg.kg-1 after 48 h. L. camara extract was the most effective among all the plant ethanolic extracts tested on P. hybostoma. At 500 mg.kg-1, the percentage of mortality after 24 h and 48 h exposure was 95.0 and 100% with L. camara extract, respectively, but it was 92.3 and 97.3% with R stricta extract, whereas it was 81.3 and 93.3% with R. Chalepensis extract and M. oleifera extract at the same concentration showed 73.3 and 77.3% mortality after 24 h and 48 h respectively.

Table 1: Percentage mortality of P. hybostoma in media containing ethanolic plant extracts

 

Plant materials

Concentration

(mg. kg-1)

 % Mortality after

  24 h    48 h

Lantana camara

100

  57.2

68.2

200

  67.5

83.3

300

  79.9

88.3

400

  90.1

98.8

500

  95.0 a

100.0 a*

Rhazya stricta

100

 53.1

63.5

200

 63.3

77.3

300

 74.8

84.3

400

 86.9

93.3

500

 92.3a

97.3 a

Ruta chalepensis

100

 48.3

56.8

200

 55.3

70.3

300

 63.5

75.9

400

 74.3

87.3

500

 81.3b

93.3 b

Moringa oleifera

100

 42.3

48.3

200

 51.3

62.3

300

 54.5

64.2

400

 64.3

70.3

500

 73.3 c

77.3 c

Fipronil (positive control)

2.5 EC

 97.5 a

100.0 a

Water (negative control)

 

 1.3 d

2.5 d

*Means not sharing the same letter with columns are significantly different (P < 0.05)

 

Table 2: LC50 values and 95% confidence limits of P. hybostoma in media containing ethanolic extracts of tested plants

 

Plant extracts

Assay time (h)

Slope

 LC50 (95% CL)

Lantana camara

24

1.96

177.5 (140.22-253.33)

48

2.11

131.5 (94.35-201.44)

Rhazya stricta

24

1.75

199.8 (161.64-297.21)

48

1.87

140.3 (101.64-220.55)

Ruta chalepensis

24

1.24

227.9 (203.77-401.33)

48

1.60

178.2 (128.32-277.11)

Moringa oleifera

24

1.11

388.1 (280.44-530.22)

48

1.51

240.2 (15.1.43-383.01)

 

Table 3: Mean Repellency percentage of P. hybostoma treated with different plant extracts

 

Plant extracts

Concentration (mg.kg-1)

Mean repellency (%)

Lantana camara

100

55.00 cd*

200

61.67 c

300

70.00 b

400

80.00 b

500

88.33 a

Rhazya stricta

100

50.00 cd

200

53.33 cd

300

63.33 c

400

75.00 b

500

81.67 a

Ruta chalepensis

100

48.33 d

200

50.00 cd

300

58.33 c

400

63.33 c

500

70.00 b

Moringa oleifera

100

43.33 d

200

48.33 d

300

51.67 cd

400

55.00 c

500

60.00 c

Fipronil (positive control)

2.5 EC

91.67 a

Water (negative control)

 

1.67

*Means with the same letter are not significantly different, P < 0.001

 

 The LC50 values for L. camara extract and R. stricta extract at 24 h and 48 h were 177.5, 131.3 and 199.8, 140.3, respectively (Table 2). whereas the LC50 values at 24 h and 48 h with R. chalepensis and M. Oleifera, were 227.9, 178.2 and 388.1, 240.2, respectively.

 

Repellency assay

 

As shown in Table 3, the maximum and significant insect repellence (91.67%) was exhibited by fipronil 2.5EC, followed by non-significant difference shown by the extract of L. camara (88.33%, at 500 mg.kg-1). R. stricta and R. chalepensis exhibited concentration dependent % repellents in the range of 48.33 to 81.67 with significantly different values of 81.67 and 70.0, respectively, at 500 mg.kg-1 each. On the contrary, M. oleifera, could show 60.0% repellents at 500 mg.kg-1.

 

Discussion

 

Economically, the termites are the most critical pest which produce substantial destruction of agricultural crops and domestic materials. The continued usage of chemical termiticides has made us to look for safety of environments and has ensued the necessity to quest for plant-based products as replacements in controlling termites. Our study

 

Fig. 1: Concentration and time dependent effects of ethanolic extracts of plants L. camara, R. stricta, R. chalepensis and M. oleifera on mortality of P. hybostoma

 

has demonstrated the biocontrol potential (termiticidal effect) of ethanolic extracts of four different plants against subterranean termites P. hybostoma worker in Saudi Arabia. All plant extracts were toxic to P. hybostoma workers in a dose dependent manner, and their efficiency varied depending on exposure-time. Although the toxic effect of L. camara was at par with positive control fipronil, toxicity was relatively low for M. oleifera. Significant differences were shown between L. camara, R. Stricta and other plant extracts, while M. oleifera exhibited less significant mortalities than other ethanolic plant extracts. The ethanolic extracts from L. camara and R. stricta showed lesser significant differences between them and showed small value of LC50s (24 h and 48 h) compared to the ethanolic extracts from R. chalipensis and M. oleifera. However, no mortality of P. hybostoma was detected for negative control over the total exposure period (48 h). In general, the ethanolic extracts of L. camara and R. stricta were more toxic than of other plants tested.

The ethanolic extracts of test plants were expected to have higher phenolic, alkaloids and flavonoid contents (Khan et al. 2016; Najem et al. 2020; Al-Solami 2021; Kumari and Sidhu 2021). These phytochemicals interfere with the behaviour, feeding, growth, moulting and reproduction in insects (Musayimana et al. 2001; Simmonds 2001).

The toxic effect of L. camara was previously reported on tobacco caterpillar Spodoptera litura (Deshmukhe et al. 2011), stored grain pests (Rajashekar et al. 2014) cabbage white butterfly, Pieris brassicae (Sharma and Gupta 2009), and the rice moth, Corcyra cephalonica. Ayalew (2020) reported that stored maize could be protected from the infestation of S. zeamais by using extracts and oils of L. camara leaf and the author suggested that this repellent and mortality effect for insects could be because of the presence of bioactive compounds like 1-Eicosano, Paromomycin, Phytol, Pyrroline and Pyrrolizin. Alvi et al. (2018) reported the toxic effect of R. stricta extract in controlling insect pests like Rhyzopertha dominica and Trogoderma granarium. The toxic effect of R. stricta extract is credited to the presence of high-level alkaloids (Ali et al. 2000).

Repellent effects of testing plant extracts on the worker P. hybostoma were significantly different; the repellent percentage dependent extracts concentrations; at 500 mg.kg-1, repellent action of L. camara was at par with fipronil, followed by R. stricta, R. chalepensis and M. oleifera. Yuan and Hu (2012) showed strong repellent and modest toxic and antifeedant activities of chloroform leaf extract of L. camara against subterranean termite, Reticulitermes flavipes. Tampe et al. (2016) have reported the repellent effect of R. chalepensis oils against the weevil Aegorhinus superciliosus. This is in agreement with our result as R. chalepensis extract showed 70% repellents to P. hybostoma. Najem et al. (2020) showed the effectiveness of R. chalepensis L. essential oil against Tribolium castaneum.

Plants based repellents are expected to impart least adverse effects on the environment because they make pests away by arousing their sensory organs ahead of attacking the plants and are also easily degraded in a short time (Addisu et al. 2014; Cespedes et al. 2014). The products of these tested plants specially, L. camara and R. stricta can be well utilized to prepare phytochemicals from which all non-target organisms can be rescued from insecticides. It has been anticipated that complex mixtures of secondary metabolites are regulator of plant defense delivering multiple mechanisms of action, as a result its use lower the predisposition of the development of insect resistance (Kortbeek et al. 2019; Erb and Kliebenstein 2020).

Various research using plant extracts in agriculture and household pest management has provided promising results towards human and animal health safety (Pascual-Villalobos and Robledo 1999; Scott et al. 2004; Pino et al. 2013; Najem et al. 2020; Al-Solami 2021). Therefore, replacing the synthetic-insecticides by bio-pesticides have become a universally accepted and suitable tactic, and is encouraged.

 

Conclusion

 

The immense crop losses experienced in Saudi Arabia are due to deterioration of crops by termites. The present study showed that all the tested plant extracts against subterranean termite, P. hybostoma possess termiticidal potential that can be exploited in the management of P. hybostoma pests. Depending on the results of our study that showed more efficacy of most plant extracts specially L. camara plant with 500 mg.kg-1 concentrate. Moreover, the common availability of these tested plants in many parts of Saudi Arabia makes them a significant natural termiticide to be exploited in integrated management of termite P. hybostoma. These findings, however, require in-depth future studies on actual assessment as biocides on pests without damaging the environment.

 

Acknowledgement

 

Authors would like to thank Prof. Dr. Ali Khalid Ahamed from the Department of Arid Land Agriculture; Faculty of Meteorology, Environment and Arid land Agriculture; King Abdulaziz University for his help on identifying the tested plants in this work.

 

Author Contributions

 

KAA designed the experiment, collected and prepared the materials, analyzes the data and drafted the manuscript. ASN prepared the plant extracts, collected data and reviewed the manuscript. RAA collected data and revised the manuscript.

Conflicts of Interest

 

Authors declare no conflict of interest.

 

Data Availability

 

Data presented in this study will be available on a fair request to the corresponding author.

 

Ethics Approval

 

Not applicable in this paper.

 

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