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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