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Research paper

Toxicity, antifeedant and growth regulating potential of three plantextracts against the desert locust Schistocerca gregaria Forskal(Orthoptera: Acrididae)

AbstractThe main objective of this investigation was to assess the toxicity andgrowth regulating potential of Jatropha (Jatropha curcas), neem(Azadirachta indica) and argel plant, (Solenostemma argel) against thedesert locust, Schistocerca gregaria. The effect on fecundity, feedingbehavior and egg hatchability was also studied. Argel of 5% concentrationinduced a significantly less (56%) antifeedant effect on desert locust nymphscompared with 79.62 and 78.92% for neem and Jatropha oils respectively.Significant mortality of 40.54 and 43.39% was recorded, 7 days aftertreatment, in insects treated with 10% concentration of neem and Jatrophaoils respectively compared to 15.19% in the control. Argel resulted in thelowest mortality of 20.70% which was not significantly different from thecontrol. There was a significant difference between treatments for the time ittook surviving nymphs to moult to the next instar. Nymphs in the controlgroup took significantly less time (11.3 days) to develop from the 5th instarto the 6th instar than those treated with neem and Jatropha oils where thytook 17.5 and 16.5 days respectively. Argel was not significantly differentfrom the control. Jatropha oil significantly reduced the fecundity of femalesdeveloped from nymphs treated in the 3rd instar by 42.2% compared with58.54% due to neem treatment. Argel caused no significant effect onfecundity of treated insects. Both Jatropha and neem oils resulted in 99.71%egg unhatchability while argel had no significant effect. Of the three testproducts, only Jatropha and neem oil have shown growth regulating effect.

Keywords: Jatropha oil, neem, Solenostemma argel, desert locust,nymphal mortalityIntroductionLocusts and grasshoppers are major economic pests of crops and grasslandsthroughout the world's dry zones (Steedman, 1990). The desert locust

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Schistocerca gregaria (Forskal) has been a most serious crop pest in manycountries of Africa and Asia (Ceccato et al., 2007). It is characterized by aremarkable phase polyphenism, a form of phenotypic plasticity in which theexpression of numerous physiological, morphological and behavioral traitsoccurs in response to changes in local population density (Uvarov, 1921).During the 2003-2004 desert locust campaigns and throughout the lastinvasion areas, control teams applied some 13 million liters of mainlyorganophosphorus pesticides to roughly 13 million ha of land (Lecoq, 2010).Current locust control operations are mainly based on organophosphoruspesticides as a result of the banning of organochlorine and especiallydieldrin (Lecoq, 2001). Rembold (1994) adverted to the rapidly increasinginsect tolerance against any type of neurotoxic insecticide, and allinsecticides given their wide spectrum of action undoubtedly had substantialside-effects on the non-target fauna (Müller, 1988). A preventive controlstrategy for locusts was developed as of 1960s and was recommended byFAO and applied by national and regional locust control units (FAO, 1968).The strategy requires monitoring ecological conditions and locustpopulations in outbreaks areas and conducting preventive treatments againstthe first gregarious locusts. Due to the regular application of this strategy,the frequency and duration of desert locust invasion were reduced since1960s (Lecoq, et al. 1997). Peveling, et al. (1994) showed that, there was noevidence of serious side-effects of alternative control agents (microbialinsecticides) on epigeal arthropods when compared with conventional ones.Mycopesticides, particularly Metarhizium anisopliae should have a role inan integrated control strategy alongside classic insecticides (Lomer et al.2001). It is now available on the locust control market and part of FAO(1999) list of products recommended for locust control. Other potentialalternative is the pheromone phenylacetonitrile (PAN) which inhibitspheromonal communication among gregarious hoppers and induces stressesthat lead to high mortality (Hassanali and Bashir 1999). Various researcheson the effect of botanical bio-pesticides including neem on desert locusthave been or are being carried out as alternatives to the currently usedharmful pesticides (Krall and Wilps, 1994). These botanicals are still at theexperimental stage as far as locust control is concerned and large scaleproduction is problematic and difficulties with the registration of variable

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products will limit adoption (Meinzingen and Kooyman 1997). Accordingly,the use of such products may be aimed at protecting crops locally (Lecoq2001).The Jatropha curcas (physic nut) is a drought-resistant multipurpose shrubor a small tree belonging to the Family Euphorbiaceae; it is a native oftropical America, but now thrives in many parts of the tropics and sub-tropics in Africa, Asia and southern America (Gübitz et al., 1999). Theextracts of Jatropha showed nematicidal, fungicidal (Sharma and Trivedi2002), molluscicidal (Liu et al. 1997) effects. It also exhibited insecticidalactivities against moths, butterflies, aphids, bugs, beetles, flies, andcockroaches (Wink et al. 1997). Toxicity of J. curcas seeds is attributed toseveral components, including saponins, lectins (curcin), phytates, proteaseinhibitors, curcalonic acid and phorbol esters (Makkar et al. 1997). Theinsecticidal properties of neem were first observed in 1959 when it wasnoticed that neem trees in Africa were undamaged during a plague of locusts(Schmutterer, 1990). Most work has been focused on azadirachtin, alimonoid from the seeds of the Indian neem tree, Azadirachta indica. Neemacts both as potent antifeedant and insect growth regulator (Koul, 1992;Kraus 2002).Argel plant, Solenostemma argel belongs to the family Apocynaceae, isindigenous to Africa and valued for its medicinal and aromatic qualities. It iswidely distributed in Sudan and throughout North Africa (Egypt, Libya andAlgeria) and the Saudi Arabia (Ahmed, 2004). It has many activecompounds that have been shown to act as potent acute or chronicinsecticides (Sammour, 1996 and Talukader, 2006), antifeedants and insectgrowth regulators (Abo El-Ghar et al., 1996) against a variety of insectspecies.The present study was carried out with the objective of illustrating thebiological activity of Jatropha oil, neem oil and argel extract against thedesert locust Schistocerca gregaria.

Materials and methodsInsect rearing

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Desert locust eggs were obtained from the International Centre of InsectPhysiology and Ecology (ICIPE), Port Sudan and mass reared in theinsectary of crop protection department, University of Khartoum. Cages (1m x 1 m x 0.35 m) fitted with wire mesh and a movable window made ofcloth, to facilitate cleaning and feeding, was used for the purpose. Thecages stood on poles one meter from the ground, 24 cups (10 cm x12cm)filled with moist soil are fitted in each cage for egg-laying. Locusts were fedon food plants such as Pennisetum typhoidium and Heliotropium spp. Thehatching nymphs were removed from the cups (10 cm x12cm) to cages (1 mx 1 m x 0.7m) fitted with cloth and wire mesh and supplied with food. The3rd and 4th instars of desert locust nymphs were used in the trials. Some ofthese nymphs were transferred into large cages (4 m x 2 m x 2 m) madefrom steel and wire mesh and were kept for breeding and continuity of thecolony.Plant materialsJatrophaFresh Jatropha curcas seeds were collected from EL-Damazein rain-fedareas in the Blue Nile State, Sudan, where the plant is grown in large scalefor the production of bio-fuel. The seeds were then cleaned, de-shelled andsubsequently the kernels and hulls were separated manually. The kernelswere dried and grounded to fine powder, stored in glass vials until used.ArgelLeaves of argel were obtained from retailer’s stores in North Sudan(Elrobatab area). The leaves samples were cleaned from foreign materials,washed with water, dried, and milled into fine powder using laboratory mill.NeemRipe neem seeds were hand-picked from mature disease-free trees inShambat area, in Khartoum University campus. The collected seeds weredepulped and thoroughly washed by hand to remove the pulp that if leftwould encourage growth of fungi. The seeds were then shade-dried on jutemats, ground to fine powder and used for different treatments.

Extraction

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The powder of each plant, as prepared above, was used to produce the crudeoil extract in a soxhlet apparatus using hexane 95% (boiling point 65–70 ºC).The hexane was removed at reduced temperature and pressure in a rotaryevaporator and the obtained oil was stored at 4ºC for subsequent use.Nymphicidal bioassayThird instars nymphs were used to study the long–term impact of the testproducts on some important biological parameters of the desert locust. A10% concentration of neem oil, Jatropha oil and argel extract was sprayedon the experimental nymphs using ultra-low volume sprayer. For eachtreatment, 60 nymphs were used and the treated insects were allowed to drybefore being transferred to rearing cages for further observation. Nymphswere checked every 24h post-treatment and mortality was recorded. Instarwas determined by checking for shed exuviae. Recording of data continueduntil nymphs became adult or died. Nymphs were considered dead whenthey failed to respond to gentle touch with a fine camel hair brush. Correctedmortality was calculated according to Abbott's (1925) formula as follows:% = 1 − ∗ 100Where n = number of insects, T = treated, Co = control. The incidence offaulty development, deformities induced by the test products was alsorecorded.Effects on fecundity and egg hatchabilityThe fecundity experiments were conducted by selecting 10 pairs of freshlyfledged adult males and females that survived treatment by the test productduring the 3rd nymphal instar. The selected insects were then transferred tothe mating and egg laying cage 75 cm x 45 cm x 45 cm. The bottom boardof the cage was made of plywood which was divided into twenty holes toaccommodate the plastic oviposition cups (7.5 cm diameter and 11 cmdeep). The plastic cups were filled with sandy soil for egg-laying. The sandwas sieved using wire mesh (2 mm), washed successively with distilledwater, dried and heat-sterilized by baking in an oven at 150°C for 24 h. Thesterilized sand was moistened by addition of water to be attractive to femalesfor egg laying. The effects of test products on fecundity were assessed onthe basis of the number of egg-pods laid during the lifetime of the female.

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The number of eggs that successfully hatched in each treatment was alsorecorded and hatchability was calculated.Phago-deterrent testThe antifeedant effects of the extracts (neem seeds oil 5%, jatropha seeds oil5% and argel extract 5%) against S. gregaria third instar nymphs, werestudied by mixing each extract in 250 g of wheat bran in a Petri dish. Therewere three replications and ten third instar nymphs were released in eachreplicate in an experimental cage. Two sets of control were included,untreated and mixed with hexane only. The bran portions left in the disheswere weighted three and six days post-treatment and the amount ofconsumed food were estimated. The antifeedant index was calculated by theformula as adopted by Abivardi and Benz (1984).( ) = × 100Where:C= Consumed wheat bran in controlT= Consumed wheat bran in treatmentData analysisTreatments were arranged in a complete randomized design. Each treatmentwas replicated four times. Transformation of data was done using Arc Sine.Data were subjected to analysis of variance (ANOVA) and the means wereseparated using the least significant difference (LSD). The Probit analysiswas carried out to calculate regression equation (Finney, 1971), LT50, Lowerfiducial limit, upper fiducial limit, time responses and Chi Square for thethree test plants at a 10% concentration.ResultsEffects of Test Products on survival and developmentSignificant mortality of 40.54 and 43.39% was recorded, 7 days after

treatment, in insects treated with 10% concentration of neem and Jatropha

oils respectively compared to 15.19% in the control. Argel resulted in the

lowest mortality of 20.70% which was not significantly different from the

control (Fig. 1). Table 1 illustrates the results of probit analysis responses of

neem seed oil, Jatropha seed oil and argel extract. The results indicated that

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the neem and Jatropha oils were effective against 3rd instars nymph of S.

gregaria as shown by the lower LT50 value of 117.84, 135.95 respectively

compared to the value of argel 270.98. The responses of the two plants were

more or less homogenous as indicated by their close LT50 /LT90 ratio and the

slope. There was a significant difference between treatments for the time it

took surviving nymphs to moult to the next instar. Nymphs in the control

group took significantly less time (11.3 days) to develop from the 5th instar

to the 6th instar than those treated with neem and Jatropha oils which took

17.5 and 16.5 days respectively. Argel was not significantly different from

the control (Table 2). Jatropha and neem oils resulted in significant

malformation effect on the test insects while argel proved to have no

significant growth regulating effect (Fig. 2).

Phago-deterrent effect

The antifeedant effect of 5% concentration of neem oil, Jatropha oil and

argel extract on the 3rd instar nymphs of the desert locust is shown in Table

3. Argel induced a significantly less (56%) antifeedant effect on desert

locust nymphs compared with 79.62 and 78.92% for neem and Jatropha oils

respectively. The antifeedant effect of both neem and Jatropha oils was

similar and seems to last for at least 6 days after treatment.

Effect on fecundity and egg hatchability

The data presented in tables 4 and 5 demonstrate the effect of the test

products on fecundity and egg hatchability of females developed from

nymphs treated in the 3rd instar. Jatropha oil significantly reduced the

fecundity of females by 42.2% compared with 58.54% due to neem

treatment. Argel caused no significant effect on fecundity of treated insects.

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Discussion

Jatropha and neem oils have demonstrated a remarkable effect on the 3rd

instar nymphs of S. gregaria as toxic, antifeedant, and growth regulating

compounds. However, argel seems to have no significant biological effect

on the test insects, at least for the concentration tested. Many investigations

were carried out on the toxicity, antifeedant effects, growth inhibition and

abnormal development in various insects including S. gregaria due to neem

seed extracts and azadirachtin (Schmutterer, 1990; Nicol and Schmutterer,

1991). Their results were consistent with the findings reported in this study.

The antifeedant effect was manifested by differences in body weight of

nymphs offered food treated with neem and Jatropha oils. This was in

accordance with the earlier findings of Champagne et al. (1989), who

reported, in a laboratory feeding, that azadirachtin is a potent antifeedant

against the desert locust Schistocerca gregaria. Similar results were reported

by Mordue et al. (1998). Nasiruddin and Mordue (1993) reported that

spraying of azadirachtin at low dose of 2 ppm onto barley seedlings infested

by S. gregaria nymphs protected the plants. The

repellent and antifeedant activity showed by Jatropha against S. gregaria

during this study is in agreement with the results reported by Cobbinah and

Tuani (1992) who, in a laboratory studies, demonstrated that Jatropha seed

oil had a negative effect on survival and feeding rates of the variegated

grasshopper, Zonocerus variegatus L. They also reported that application of

Jatropha seed oil reduced the damage caused by Z. variegatus to cassava

foliage. Data concerning the biological effects of Jatropha oil on desert

locust is scant; however, good protection of cowpea seeds against C.

maculatus was achieved in storage by seed treatment with Jatropha seed oil

(Adebowale and Adedire, 2006). Singh and Sushilkumar (2008) showed

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antifeedant activity against the termite, Microcerotermes beesoni caused by

Jatropha oil at different dilutions ranged from 1%, to 20%. The maximum

wood protection and weight loss caused by termites were obtained at their

highest concentration i.e. 20%. This persistency can be exploited for barrier

treatment against hopper bands of the desert locust. The Jatropha oil can

also be integrated with the pheromone phenylacetonitrile (PAN) for the

integrated management of desert locust particularly in recession and before

plague formation. However, field studies on evaluation of Jatropha toxicity

to beneficial and non-target organisms are needed.

References

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Lecoq, M. 2010. Integrated pest management for locusts and grasshoppers:are alternatives to chemical pesticides credible? Journal of OrthopteraResearch 19(1): 131-132.

Liu SY, Sporer F, Wink M, Jourdane J, Henning R Li YL, Ruppel, A. 1997.Anthraquinones in Rheum palmatum and Rumexdentatus(Polygonaceae), and phorbol esters in Jatropha curcas(Euphorbiaceae) with molluscicidal activity against the Schistosoma

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vector snails Oncomelania, Biomphalaria, and Bulinus. TM IH Trop.Med. Int. Health 2:179-188.

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Meinzingen, W., Kooyman, C. 1997. Results and recommendations of theworking group Control agents and methods. Pp. 263-264. In: Krall, S,Peveling R., Ba Diallo, D. (Eds.) New strategies in locust control.Birkhäuser, Basel, Switzerland

Mordue (Luntz), A.J.; Simmonds M.S.J..; Ley S.V.; Blaney, W.M.; mordue,W.; Nasiruddin, M. and Nisbet, A.J. (1998). Actions of azadirachtin, aplant allelochemical, against insects. Pestic. Sci. 54: 277-284.

Müller, P., 1988. Okotoxikologische Wirkungen von chloriertenKohlenwasserstoffen, Phosphorsäureestern, Carbamaten undPyrethroiden im nordöstlichen Sudan.Unpubl. Report to GTZ.Eschborn, Saarbrücken. 70 pp.

Nasiruddin, M. and Mordue (Luntz), A.J. (1993).The effect azadirachtin onthemidgut histology of the locusts, Schistocerca gregaria and Locustamigratoria. Tissue Cell 25: 875-884.

Nicol, V.C.M.Y. and Schmutterer, H. (1991). Cotact effects of seed oil fromthe neem tree, Azadirachta indica (A. Juss) on nymphs of thegregarious phase of the desert locust, Schistocerca gregaria. J. Appl.Entomol. 111(2):197-205.

Peveling, R., Weyrich, J. and Müller, P. (1994) Side-effects of botanicals,insect growth regulators and entomopathogenic fungi on epigeal non-target arthropods in locust control In: New Trends in Locust Control(eds. S. Krall, H. Wilps), GTZ, Eschborn, TZ-VerlagsgesellschaftRossdorf, p. 148-176.

Rembold, H. 1994. Controlling locusts with plant chemicals In: NewTrends in Locust Control (eds. S. Krall, H. Wilps), GTZ, Eschborn,TZ-Verlagsgesellschaft Rossdorf, p. 41-49.

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Wink M, Koschmieder C, Sauerwein M, Sporer, F. 1997. Phorbol esters ofJatropha curcas-biological activities and potential applications. In:Gübitz GM, Mittelbach M, Trabi M (eds) Bio-fuel and industrialproducts from Jatropha curcas. Dbv- Verlag Univ., Graz.

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Fig 1. Mean % mortality induced by10% concentration of Jatropha oil,neem oil and argel extract on the 3rd instar nymphs of S. gregaria

Fig. 2: Percentage of survival and deformed S. gregaria adults developedfrom 3rd instar nymphs treated with argel extract, Jatropha and neem oils

05

101520253035404550

1 2 3

Mor

talit

y %

13

Fig 1. Mean % mortality induced by10% concentration of Jatropha oil,neem oil and argel extract on the 3rd instar nymphs of S. gregaria

Fig. 2: Percentage of survival and deformed S. gregaria adults developedfrom 3rd instar nymphs treated with argel extract, Jatropha and neem oils

3 4 5 6 7

Days

Control

Hexane 10%

Argel 10%

Neem 10%

Jatropha 10%

13

Fig 1. Mean % mortality induced by10% concentration of Jatropha oil,neem oil and argel extract on the 3rd instar nymphs of S. gregaria

Fig. 2: Percentage of survival and deformed S. gregaria adults developedfrom 3rd instar nymphs treated with argel extract, Jatropha and neem oils

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Table 1: Log time response of S. gregaria 3rd instar nymphs exposed to 10%concentration of argel extract, Jatropha and neem oils

Source oftreatment

Lethal Time%

Fiducial limit Chi-squire

LT90/LT50ratio

Slope df. Sensitivitylower upper

Argelextract

LT10

161.00 142.87 185.39 1.034 1.68 0.176 2 2.29

LT50

270.98 224.29 394.50

LT90 456.10 332.47 889.07

Jatrophaoil

LT10

80.77 57.21 95.36 1.034 1.68 0.176 1.15

LT50

135.95 124.09 146.87

LT90 228.82 198.04 307.45

Neem oilLT10

70.01 45.98 85.50 1.034 1.68 0.176 1

LT50

117.84 102.30 128.37

LT90 198.34 176.68 248.31

LT10: lethal time that kills 10% of the exposed nymphsLT50: lethal time that kills 50% of the exposed nymphsLT90: lethal time that kills 90% of the exposed nymphsdf: degrees of freedom

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Table 2: Effect of argel extract, neem and Jatropha oils on nymphaldevelopment of the desert locust, Schistocerca gregaria

TreatmentDevelopment duration (days)

3rd – 4th instar 4th – 5th instar 5th – 6th instarControl 8.76a 10.16a 11.33aHexane 8.78a 10.50a 12.00aArgel extract (10%) 8.78a 11.66a 11.50aNeem oil (10%) 16.44a 15.33b 17.50bJatropha oil (10%) 16.41a 14.00b 16.50cLSD 12.54 1.99 0.84SE+ 6.89 1.09 0.45

Third instar nymphs were treated and development was followedThe means followed by the same letter in the same column are notsignificantly different at (P=0.05) according to LSD.LSD= Least Significant DifferentSE+ = Standard Error

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Table 3: Antifeedant % induced by argel, neem and Jatropha oils on the 3rd

nymphal instar of S.gregariaTreatment After 3 days After 6 daysControl - -

Hexane (54.72)a42.30

(64.9)a36.33

Argel extract 5% (52.96)a43.57

(56)a41.54

Neem oil 5% (76.45)b29.06

(79.62)b26.85

Jatropha oil 5% (72.64)b31.56

(78.92)b27.83

LSD 14.59 12.24

SE± 8.02 6.73

The means followed by the same letter(s) in the same column are notsignificantly different at (P=0.05) according to LSD.The numbers between parentheses represent arc sine transformation dataLSD= Least Significant DifferentSE+ = Standard Error

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Table 4: Fecundity of S. gregaria developed from 3rd nymphal instar treatedwith 10% argel extract, neem, and Jatropha oils

Treatment Average number of egg- pods/10 females1st count 2nd count 3rd count 4th count

Control (1.86)a7.92

(5.04)a12.92

(9.05)a17.56

(10.95)a19.23

Hexane 10% (0.57)a0.1

(3.15)a10.31

(7.30)a15.68

(10.24)a18.72

Argelextract10%

(1.86)a7.92

(5.04)a12.92

(7.16)a15.56

(10.69)a19.09

Neem oil 10% (0.57)a0.1

(0.57)a0.1

(3.15)a10.31

(4.54)b12.25

Jatropha oil10%

(0.57)a0.1

(0.57)a0.1

(3.15)a10.31

(6.33)b14.54

LSD 2.24 3.64 5.55 4.31SE+ 1.63 2.41 3.68 2.99The means followed by the same letter in the same column are notsignificantly different at (P=0.05) according to LSD.The numbers between parentheses represent arc sine transformation data.LSD= Least Significant DifferentSE+ = Standard Error

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Table 5: Per cent hatchability of eggs laid by S. gregaria developed from 3rd

nymphal instar treated with argel extract, neem, and Jatropha oilsTreatment Days

1 2 3Control 47.50a 59.00a 34.52aHexane 10% 44.75a 58.75a 36.00a

Argel extract 10% 50.75a 60.00a 42.50aNeem oil 10% 16.30b 2.52b 0.10bJatropha oil 10% 12.55b 5.50b 0.10bLSD 19.16 14.63 13.74SE+ 12.71 9.70 9.11

The means followed by the same letter in the same column are notsignificantly different at (P=0.05) according to LSD.L.S.D. = Least significant difference.SE+ = Standard Error