Conventional synthetic insecticides have long played an important role in increasing agricultural production
(Popp et al., 2013). In the absence of practical and efficient alternatives, insecticides will continue to be a key component in pest management programmes and will remain essential for preventing food insecurity in meeting the needs of present and future generations
(Deravel et al., 2014). The extensive use of these insecticides has led to risks and hazards to human and environmental health as well as increasing resistance development in target pest insects through the exertion of selection pressure
(Helps et al., 2017; Jars et al., 2018; Ojha et al., 2018). The real challenge lies in the search for alternative control methods that reduce the risks associated with conventional synthetic insecticides (
Khater, 2012).The term biopesticides or natural pesticides is the result of this search, which are environmentally friendly and have low toxicity to non-target organisms (
Sharma and Gaur, 2019;
Morakchi et al., 2021; Tulashie et al., 2021).
Azadirachta indica is an important limonoid-producing plant from the Meliaceae family that has long been recognised as a source of environmentally friendly biopesticides (
Senthil-Nathan, 2013;
Dey et al., 2017). It has low toxicity to mammals and is effective even at low concentrations. Due to the complexity of its active compo-nents in
A.
indica, the likelihood of resistance development by these botanicals is considered low (
Vendramim and Castiglioni, 2000;
Roel et al., 2010). A.
indica has been reported to attack more than 300 insect pests (
Mordue and Blackwell, 1993). It can cause effects such as repellency, developmental arrest and retardation, deformations, ecdysis, reduction in fertility and fecundity, changes in behaviour and physiology of insect pests resulting in mortality. The extent of the effects and the reaction time depend on the dose and the duration of exposure (
Martinez 2002;
Roel et al., 2010). Melia azedarach L., which is closely related to
A.
indica, also contains several limonoids and shows excellent insecticidal activity
(Charleston et al., 2004). The most important active limonoid in both Meliaceae trees is azadirachtin, which acts as an antifeedant and growth regulator for insects (
Senthil-Nathan, 2013).
Toxicity of various botanicals
Neem seed oil and methanolic neem leaf extracts were effective insecticides against fall armyworm (
Spodoptera frugiperda), as per
Tulashie et al., (2021). Neem seed oil LC50 values were 1.7, 0.97 and 0.68% after 2, 6 and 12 hours respectively. Methanolic neem leaf extract LC50 values were 2.67, 2.62 and 1.64% for the same time periods. Concentrations of 3.0% and 5.0% resulted in 100% mortality after 6 and 12 hours.
Silva et al., (2015) found neem seed cake more toxic than neem leaf extract, with LC50 values of 0.13% and 0.25% respectively.
Duarte et al., (2019) observed reduced survival in
S.
frugiperda larvae with increasing neem oil concentrations. Mortality at 50% and 90% occurred at 9,500 and 17,230 ppm.
Roel et al., (2010) noted 100% mortality in
S.
frugiperda larvae at a 0.4% neem oil dose in the first instar stage.
Sisay et al., (2019) found higher mortality in
S.
frugiperda larvae with 5.0g of
A.
indica bio-insecticide in various conditions.
Lima et al., (2010) reported the highest larval mortality with commercial neem formulations (Natuneem® and Neemseto®) against
S.
frugiperda. Azadirachtin toxicity against coconut spike moth,
Tirathabarufivena, (Walker) (Lepidoptera: Pyralidae) was assessed for stomach and contact effects. Stomach toxicity ranged from 28.79 to 92.70 mg/L across instars, while contact toxicity ranged from 12.85 to 32.34 mg/L. LC50 values indicated first instars were 1.53 to 3.22 times more susceptible than subsequent instars
(Zhong et al., 2017).
Sharma and Singh (2014) examined neem leaf extracts in methanol and hexane for toxicity against the diamondback moth,
Plutellaxylostella. Tested at concentrations ranging from 0.5% to 3%, even the lowest concentration (0.5%) resulted in significantly higher larval mortality (61.67%) compared to the control (13.33%). Neem methanol extracts induced 100% mortality at 3% concentrations for first and second instar larvae. Mortality exceeded 50% at 2.5% and 2% NME concentrations during the first and second larval stages. Neem hexane extract (NHE) at 1.5% concentration showed notably higher lethal impact than the control, reaching 51.67% mortality at 3%. Higher neem leaf extract concentrations led to a maximum larval mortality of 52.5% for
P.
xylostella (Sow and Diarra 2013).
Zada et al., (2018) assessed azadirachtin concentrations (0.31, 0.50, 0.60 and 1.0%) against third and fourth instar larvae of
P.
xylostella in choice and no-choice tests. LC50 values in the choice test were 0.66 to 0.37 µg/ml for third instar and 0.55 to 0.34 µg/ml for fourth instar larvae at 24 to 72 hours. No-choice test LC50 values were 0.63 to 0.29 µg/ml for third instar and 0.52 to 0.31 µg/ml for fourth instar larvae at 24 to 72 hours, showing descending toxicity. Paramita
et al. (2018) found
A.
indica seed extract 50 EC effective against
Spodoptera litura larvae, with mortality rates of 76.7, 86.7 and 93.3% at concentrations of 2, 3 and 4% respectively.
Sub-lethal influences of different botanicals on larvae, pupae and adults
The assessment of insecticides’ sub-lethal effects on insect biology is critical for integrated pest management programmers because while sub-lethal concentrations do not kill insects, they can reduce insect populations in subsequent generations by interfering with biological traits.
Sub-lethal influences on the growth and development stages of the
S.
frugiperda larvae, pupae and adults may also cause the malformation of adults, pupal-adult intermediates and larval-pupal intermediates.
Larval duration
Duarte et al., (2019) tested three
A.
indica oil concentrations (5000, 10000 and 15000 ppm) mixed with the artificial diet against
S.
frugiperda. At the highest concentration (15000 ppm), there was a significant 76% increase in the larval period of
S.
frugiperda compared to the control group.
Roel et al., (2010) observed sub-lethal effects of neem oil on
S.
frugiperda development, noting increased larval durations (23.47 days at 0.05%, 21.89 days at 0.006%) compared to the control (21.12 days).
Malik et al., (2017) found prolonged larval periods (15.47, 16.40, 17.23, 18.13 days) for
S.
litura fed on cauliflower leaves treated with neem oil concentrations (1000, 1500, 2000, 2500 ppm).
Azadirachtin’s impact on African cotton leafworm,
Spodopteralittoralis, (Boisduval)
(Lepidoptera: Noctuidae) was assessed in the laboratory. Third instar larvae on artificial diet with 0.3 and 0.6 ppm azadirachtin had a two-day longer instar duration compared to controls (
Martinez and Emden 2001).
Simmonds et al., (1990) noted insect mortality, especially during moulting, with higher azadirachtin concentrations in
S.
littoralis.
Abedi et al., (2014) reported a significant 21.3-day extension in larval duration for cotton bollworm,
Helicoverpaarmigera, (Hubner) (Lepidoptera: Noctuidae) exposed to azadirachtin (8.8 µg
a.
i./mL) in artificial diet.
Farias et al., (2019) observed prolonged larval periods (18.69 and 15.43 days) in
H.
armigera with neem-based formulations compared to the control’s 15.78 days.
Singh et al., (2006) found
Melia azedarach extracts increased larval durations (7.0-7.8 days) for second instar larvae of
P.
xylostella at concentrations of 1.47, 1.79 and 2.29% compared to the control (6.3-6.5 days). Sub-lethal concentrations led to a significant prolongation of development from second to fourth instar larvae.
Pupal duration
Duarte et al., (2019) studied sub-lethal effects on
S.
frugi-perda development, finding
A.
indica oil concentrations of 5000 and 15000 ppm increased pupal durations to 11.1 and 12.3 days, respectively, compared to 10.5 days in the control.
Merkey et al., (2011) noted reduced metamorphosis and pupal development with increased pupal duration in low-nutrition conditions for
S.
frugiperda.
S.
litura larvae exposed to neem oil concentrations (500-2500 ppm) by
Malik et al., (2017) showed increased pupal periods (7.10-9.23 days) compared to the control (6.80 days).
Roel et al., (2010) reported neem oil concentrations (0.006 and 0.05%) significantly increased
S.
frugiperda pupal duration (11.08-11.67 days).
Abedi et al., (2014) recorded a 23.1-day prolongation in
H.
armigera pupal duration with azadirachtin (8.8 µg a.i./ml).
Gulzar et al., (2018) found
A.
indica methanolic extract affected
Earias vittella (Fabr.) (Lepidoptera: Noctuidae) pupal duration significantly at sub-lethal concentrations (1.59 and 5.50%), with durations of 15.61 and 12.51 days, respectively, compared to the control (9.42 days).
Schmidt et al., (1997) observed an extension in
Agrotisipsilon (Hufn.) (Lepidoptera: Noctuidae) pupal period, averaging 20.3 days at 50 ppm extract concentration, compared to 14.6 days in the control. Concentrations of 15, 25 and 50 ppm showed no significant differences in pupal period.
Pupal weight
Singh et al., (2006) found
M.
azedarach concentrations (1.47, 1.79, 2.29%) significantly reduced pupal weight (36.0-38.4 mg/10 pupae) compared to the control (54.4-56.0 mg/10 pupae) in
P.
xylostella. In
A.
ipsilon,
Melia extract concentrations (10, 15, 25, 50 ppm) reduced pupal weight (165-327 mg) compared to control (400 mg).
S.
littoralispupal weight decreased at 15, 25 and 50 ppm of
Melia extract (267-343 mg) compared to control (397 mg). Higher concentrations prevented larvae from reaching pupal stage
(Schmidt et al., 1997).
S.
littoralis larvae treated with azadirachtin (0.5, 0.1, 0.05 ppm) showed reduced pupal weight (
Martinez and Emden, 2001).
Abedi et al., (2014) found azadirachtin (8.8 µg a.i./ml) reduced pupal weight in
H.
armigera (205.1 mg) compared to untreated groups (298.3 mg).
Ma et al., (2000) reported sub-lethal effects of azadirachtin on
H.
armigera pupal weight.
A.
indica extract significantly decreased pupa weight of
E.
vittella (50.21 and 39.25 mg) compared to control (63.25 mg)
(Gulzar et al., 2018). Neem oil concentrations (0.006% and 0.05%) in S.
frugiperda reduced pupal weight (0.156-0.191 g) compared to control (0.194 g)
(Roel et al., 2010). Duarte et al., (2019) exposed
S.
frugiperda larvae to neem oil concentrations (5000, 10000, 15000 ppm) resulting in decreased pupal weight (151.4-182.7 mg) compared to control (214.0 mg).
Lima et al., (2010) observed a 19% lower pupal weight in
S.
frugiperda larvae exposed to
A.
indica oil (500 ppm) compared to untreated insects.
Malik et al., (2017) noted pupal weight reduction in
S.
litura at neem oil concentrations (500-2500 ppm).
Ahmad et al., (2015) evaluated neem-based insecticides on
H.
armigera, observing decreased pupal weight with neem oil (255.3 mg) compared to the control (278.6 mg).
Adult emergence
Abdel-Aziz et al. (2013) studied sub-lethal effects of bitter and neem oils on
S.
littoralis. Second and fourth instar larvae were exposed to sub-lethal concentrations of bitter oil (0.116, 0.184%) and neem oil (0.153, 0.21%). Adult emergence decreased to 12.29% for neem oil in pretreated fourth instars and 25% for bitter oil compared to 84% in the control.
Bakr et al., (2012) noted increased overall adult deformities in
S.
littoralis with neem treatment (66.1%) in second instars and bitter treatment (50, 43.34%) in fourth and second instars, respectively, compared to the 8% control. Neem-based formulations (Neemarin, Neemazal, Neemix, Neem oil) significantly reduced
H.
armigera adult emergence (53.7%) compared to the control (90%)
(Ahmad et al., 2015). Singh et al., (2006) found
M.
azedarach extracts from different regions of India significantly reduced adult emergence in
P.
xylostella compared to the untreated group.
Adult size
Duarte et al., (2019) noted a 13and 63% reduction in wing length in
S.
frugiperda larvae treated with the highest neem oil concentrations (10,000 and 15,000 ppm) via artificial diet. The percentage of deformed adults increased with higher neem oil concentrations.
Jones (2014) observed reduced forewing length, wing shape, body size and diminished flight in
S.
frugiperda.
Singh et al., (2006) found
P.
xylostela adults emerging from
M.
azedarach extract treatments exhibited reduced size, highly twisted and fringed wings, hindering normal flight and mating.
Zanuncio et al., (2016) studied sub-lethal effects of neem oil concentrations (0.5-50%) on the stink bug
Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) adults. Abnormalities ranged from 2.5 to 30.8%, increasing with higher neem oil concentrations. Main deformations included reduced hemelytra size, fewer veins, decreased membranous wing area, asymmetric scutellum and leg extension and folding.
Adult longevity
Duarte et al., (2019) observed reduced adult longevity in
A.
indica oil-exposed
S.
frugiperda, with males and females living 5.1 and 6.7 days at 5000 ppm neem oil compared to the control (9.4 and 11.9 days).
Lima et al., (2010) reported decreased longevity in
S.
frugiperda adults fed on neem oil-treated corn leaves.
Bruce et al., (2004) found neem oil reduced adult longevity in African pink stem borer,
Sesamia calamistis (Hampson) (Lepidoptera: Noctuidae).
Malik et al., (2017) noted reduced adult longevity in
S.
litura at neem oil concentrations (500-2500 ppm), with the longest lifespan at 11.83 days in the control.
Pineda et al., (2009) reported decreased longevity in
S.
littoralis adults exposed to azadirachtin (1-100 ppm).Neem-based formulations (Neenmax, Emulzinim, Nim-I-go) reduced longevity in
H.
armigeraadults, with males and females living shorter lives than the control
(Farias et al., 2019). Abedi et al., (2014) found azadirachtin reduced adult longevity in
H.
armigera by 18.1% and
Pineda et al., (2007) reported a similar effect in
S.
littoralis.
Singh et al., (2006) observed reduced adult longevity in
P.
xylostella treated with
M.
azedarach extract.
Schmidt et al., (1997) found
Melia extract decreased male and female longevity in
S.
littoralis and
A.
ipsilon was similarly affected, with significant reductions at higher concentrations.
Sub-lethal influences of different botanicals on various reproductive parameters
Sub-lethal effects are defined as biological, physiological, demographic or behavioural effects on individuals or populations that survive exposure to a toxicant at lethal or sub-lethal concentration. A sub-lethal concentration causes no apparent mortality in the test group (
Inbar and Gerling 2008). Insecticide concentrations below the median lethal (LC50) are called sub-lethal in general. Life expectancy, development rates, population expansion, fertility, fecundity, changes in sex ratio, malformations and changes in behaviour, feeding, searching and oviposition are all examples of sub-lethal consequences (
Lee 2000). Toxicants can have both subtle and overt effects, which must be taken into information when assessing their overall impact.
Oviposition period
Bernardi et al., (2011) assessed NeemAzal-T/S® on bollworm,
Bonagota salubricola (Meyrick) (Lepidoptera: Noctuidae) finding a 7.0-day reduction in oviposition period at 0.18% concentration compared to the 10.8-day control.
Farias et al., (2019) reported Emulzinim® (0.12% azadirachtin) decreased oviposition period in
H.
armigera to 3.9 days from the 5.5-day control.
Ahmad et al., (2015) observed a three-day reduction in
H.
armigera pre-oviposition period with neem-based products.
Ghosh et al., (1999) found azadirachtin negatively impacted Asturias,
Heteracris littoralis (Ramb.) (Orthoptera: Acrididae) development, oogenesis and spermatogenesis.
Ghazawi et al., (2007) reported a significant 36.10 to 33.60-day decline in oviposition period in
H.
littoralis nymphs treated at 25 to 75 ppm azadirachtin concentrations compared to the 70.21-day control.
Schmidt et al., (1997) observed
Melia extract (10, 15, 25 ppm) reducing the oviposition period by 5.6 days for
S.
litoralis and 6.4 days for
A.
ipsilon.
Fecundity
Duarte et al., (2019) noted
A.
indica oil at 5000, 10000 and 15000 ppm reduced
S.
frugiperda fecundity to 827.4, 729.2 and 223.5 compared to 1216.1 in the control.
Malik et al., (2017) found neem oil concentrations (500-2500 ppm) significantly reduced
S.
litura fecundity (505.00-631.67) compared to the control (1178.00).
Pineda et al., (2009) reported
S.
littoralis fecundity reduction to 250.8 at 100 mg azadirachtin concentration compared to the 1753.6 control.The reduced fecundity effects might be caused by azadirachtin interfering with the production of vitellogenin in developing oocytes (
Kanost et al., 1990,
Pineda et al., 2007).
Ahmad et al., (2015) observed
H.
armigera fecundity reductions with Neemazal (378 eggs/female/generation) and other neem-based products.
Pratibha (2018) found reduced
E.
vittella fecundity with neem derivatives (169.50-177.80 at 20% LC50).
Gulzar et al., (2018) reported
E.
vittella fecundity reduction (96.83-140.89) with
A.
indica extract.
Schmidt et al., (1997) observed reduced
S.
littoralis and
A.
ipsilon fecundity with
Melia extract.
Irigaray et al., (2010) reported European grape berry moth,
Lobesia botrana Denis and Schiffermüller (Lepidoptera: Tortricidae) fecundity reduction with azadirachtin-based formulation (117.9 at 1 mg/L). Eggs laid by treated females showed embriocidal effects, which indicated azadirachtin trans-ference through the gravid female (
Mordue and Blackwell 1993,
Mordue 2004,
Seljasen and Meadow 2006).
Hatchability of the eggs
Schmidt et al., (1997) reported reduced hatchability in
S.
litoralis and
A.
ipsilon larvae treated with
M.
azedarach concentrations of 10, 15 and 25 ppm. Hatchability rates were 78.7, 28.6 and 0% for
S.
litoralis and 74.1, 52.9 and 16.7% for
A.
ipsilon, compared to 87.1% in the control.
Tirathaba rufivena (Lepidoptera: Pyralidae) eggs were treated for 24, 48 and 72 hours respectively after deposition, with the LC25 (11.35 mg AI/L), LC50 (28.79 mg AI/L) and LC90 (169.00 mg AI/L) concentrations of azadirachtin solution based on stomach toxicity to first instars. The significantly reduced eggs hatchability
i.
e. 88.5, 88.3 and 62.6 % after 24 hours, 85.3, 85.0 and 61.7% after 48 hours and 82.0, 88.3 and 56.6% after 72 hours were reported
(Zhong et al., 2017). The residual effects of azadirachtin on the egg hatchability of
T.
rufivena were tested. When applied directly to the eggs on different days after deposition, the LC25 and LC50 concentrations did not affect larval hatch, whereas the LC90 treatment delayed hatch from eggs treated by 1 to 3 days after deposition (
Ghatak and Bhusan 1995).
Pratibha (2018) compared three bio-formulations on
E.
vittella egg hatchability: NeemGold (NG), aqueous neem leaf extract (AEN) and aqueous garlic bulb extract (AEG). NG was the most effective, followed by AEN and AEG, with 90.75% hatchability in control. The two commercial neem-based formulations (Nimbicidine and Neemazal) have the potential to be part of
E.
vittella management strategies as they significantly reduce the hatchability of eggs (25-50 %) (
Bhardwaj and Ansari 2015).
Schneider et al., (2017) observed that neem oil extract increased the number of undeveloped eggs in American sugarcane borer,
Diatraea saccharalis (Fabricius) (Lepidoptera: Crambidae) at concentrations of 0.3, 0.5, 1.0 and 2.0%, with undeveloped eggs at 19.07, 28.18, 45.90 and 95.95%, compared to 9.54% in control.
Oliveira et al., (2013) also noted a prolonged embryonic period and 42.4% hatch rate with neem oil treatment in
D.
saccharalis.
Survival of the larvae
Martinez and Emden (2001) found that azadirachtin, had sub-lethal effects on the survival and development of
S.
litura. Neonate larvae exhibited moulting disruptions, morphological anomalies and increased mortality when fed an artificial diet with 0.1 to 1.0 ppm azadirachtin. Higher concentrations reduced survivability and affected developmental stages of
S.
littoralis. In fruit fly,
Drosophila melanogaster (Frederick) (Diptera: Drosophilidae), azadirachtin significantly decreased the numbers of eggs, larvae, pupae and adults in the F1 generation at concentrations of 0.1 to 1.2 µg
(Oulhaci et al., 2018). Seljasen and Meadow (2006) observed that neem treatment did not affect egg hatch rates in cabbage moth,
Mamestra brassicae (Linnaeus) (Lepidopstera: Noctuidae) but reduced larval survival after one week. Larvae on neem-treated plants remained in the first instar stage and all died within two weeks, unlike control plants with an average of 15.6 surviving larvae. All larval instars of
T.
rufivena were susceptible to azadirachtin, with higher concentrations reducing neonate larvae survival, especially those emerging from treated eggs. Survival rates dropped significantly after 24, 48 and 72 hours with LC25, LC50 and LC90 concentrations
(Zhong et al., 2017).
Antifeedant effects of different botanicals
Azadirachtin is usually associated with marked antifeedant activity and even behavioural avoidance in a large number of insect species including hemipterans (
Kumar and Poehling 2007), lepidopterans
(Charleston et al., 2004, Shannag et al., 2015), orthopterans (
Capinera and Froeba 2007), coleopterans (
Baumler and Potter 2007) and dipterans
(Kilani-Morakchi et al., 2017).
Prasoona et al. (2022) evaluated the antifeedant effect of several plant extracts against
S.
frugiperda under laboratory conditions. The results showed that one % neem seed kernel extract was the strongest antifeedant as compared to one % lantana leaf extract. It was found that one % neem seed kernel extract in ethyl acetate had the highest antifeedant activity (60.95 to 75.17%) against third instar larvae of
S.
frugiperda in comparison to one% lantana leaf extract in ethyl acetate (42.25 to 46.98%) after 24, 48, 72-hour treatment.
The study was conducted to evaluate the different concentrations of azadirachtin against third and fourth-instar larvae of
P.
xylostella. The choice and no-choice test methods were implied for the four different concentrations,
i.
e. 0.31, 0.50, 0.60 and 1.0% of azadirachtin. It was revealed that maximum antifeedant activity was 95% and 90% for third instar larvae at 1.0 and 0.6% concentrations and similarly, antifeedant activity in the case of fourth instar larvae was 85 and 75 % at the 0.6 and 0.5% concentrations of azadirachtin, respectively
(Zada et al., 2018). The primary antifeedant effect of azadirachtin seems to be mediated by gustatory chemosensillas and connected to inhibition of the rate of firing of sugar-sensitive cells of the gustatory chemoreceptors by activating bitter sensitive gustatory cells
(Lee et al., 2010, Weiss et al., 2011, Delventhal and Carlson 2016,
Morakchi et al.,2021). The sensitivity to the primary antifeedant, azadirachtin was reported in different species. The insects avoided the ingestion of this biopesticide and preferred starving to death (
Mordue and Nisbet, 2000). The internal response of a mechanism called secondary antifeedant, including a long-term reduction in food intake and toxic effects on different insect tissues (muscles, fat body and gut epithelial cells) was also reported
(Mordue et al., 2004; Khosravi and Sendi, 2013;
Shannag et al., 2015).
The study on the antifeedant effect of
A.
indica leaf extract was carried out using the no-choice leaf disc test, with different extract concentrations of 0.5, 1, 5 and 10 % against the mealworms,
Tenebrio molitor (Linnaeus) (Coleoptera: Tenebrionidae). The feeding was inhibited in the case of all three
A.
indica leaf extracts. It was observed that ethyl acetate extract possessed more antifeedant activity than methanol extract and n-hexane extract of
A.
indica (
Saidi and Nasution, 2018).
Third-instar larvae of
S.
littoralis orally treated with sub-lethal concentrations of azadirachtin display a reduction in food intake, conversion efficiency and feeding behaviour (
Martinez and van Emden, 1999). In second instar larvae of
Spodoptera eridania (Lepidoptera: Noctuidae), short-term consumption (2 days) of food treated with Azatrol, a commercial formulation of azadirachtin, reduced relative consumption rate, the efficiency of conversion of ingested food, relative growth rate, approximate digestibility and assimilation rate of food during the entire larval developmental period
(Shannag et al., 2015).
The biological activity of neem on the red pumpkin beetle,
Aulacophora foveicollis (Lucas) (Coleoptera: Chrysomelidae), was studied. The effective concentration for 50% antifeedant activity was 0.01% methanolic neem seed kernel extract (NSKE) and 0.4% neem oil, using leaves of muskmelon as feeding substrate. The antifeedant activity of NSKE was found to vary with cucurbitaceous hosts. These results show that methanolic NSKE was approximately 40 times more effective than neem oil (
Gujar and Mehrotra 1988). Similar studies using choice and no-choice test conditions were reported for
S.
litura by
Shin and Zhang (1984).