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Effectiveness of diatomaceous earth for control of Sitophilus zeamais (Coleoptera: Curculionidae), Tribolium castaneum and Palorus subdepressus (Coleoptera: Tenebrionidae)
Journal of Stored Products Research 57 (2014) 1e5
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Effectiveness of diatomaceous earth for control of Sitophilus zeamais (Coleoptera: Curculionidae), Tribolium castaneum and Palorus subdepressus (Coleoptera: Tenebrionidae) Mamadou Doumbia a, *, Bleu Gondo Douan a, Koffi Eric Kwadjo a, Dagobert Kouadio Kra a, Véronique Martel b, Mamadou Dagnogo a a b
UFR SN, University Nangui Abrogoua, 02 PB 801 Abidjan 02, Cote d’Ivoire Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Center, 1055 du P.E.P.S., Quebec City, Quebec G1V4C7, Canada
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 29 November 2013
The effectiveness of diatomaceous earth (DE) or diatomite has been assessed against three major beetle pests of stored maize: Sitophilus zeamais (the maize weevil), Tribolium castaneum (the red flour beetle) and Palorus subdepressus (the depressed flour beetle). Maize has been treated with four doses of DE (1.5, 3, 4.5 and 6 g/kg) and four doses of Actellic SuperÔ Dust a chemical insecticide used as a reference (0.25, 0.5, 0.75 and 1 g/kg). The effective mortality was measured for each treatment after 1, 2, 4, 7 and 14 d of exposure. The corrected mortality rates were calculated by considering the mortality in the control group. Diatomaceous earth was as effective as Actellic SuperÔ Dust but required higher doses. Diatomaceous earth acted faster on S. zeamais and P. subdepressus compared to T. castaneum. The highest dose tested for DE caused the same mortality in T. castaneum as the recommended dose of Actellic SuperÔ Dust. Diatomaceous earth is a good alternative for the control of these three devastating insect pests of maize stocks and can readily be incorporated into integrated stored products pest management programs. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Efficacy Mortality Pests Stored maize Diatomaceous earth
1. Introduction Maize, with rice and sorghum, is one of the most consumed food products in Central and West Africa (Silou, 2003). Insects, mainly beetles and moths, play a significant role in the destruction of stored grain, causing losses from 20 to 100% in developing countries (Holst et al., 2000). The red flour beetle Tribolium castaneum (Herbst) is even able to attack cocoa and coffee stocks which are the two most significant export products in Ivory Coast (Lavabre, 1970). Although one of the first control strategies against stored grain pests has been the use of chemicals, the need for alternatives became apparent when problems associated with these products such as the development of insect resistance, environmental pollution, contamination of treated food as well as health risks during products handling, were encountered (Subramanyam and Hagstrum, 1995). Several alternatives have been investigated against stored product pests. Natural products have been tested such as palm oils (Elaeis guineensis L. (Arecaceae)), groundnut (Arachis hypogaea L. (Fabaceae)) and tobacco extract (Nicotiana tabacum L. (Solanaceae))
* Corresponding author. Tel.: þ225 0896 2029; fax: þ225 0113 2747. E-mail addresses: [email protected], [email protected] (M. Doumbia). 0022-474X/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jspr.2013.11.008
(Foua-Bi, 1993) or leaf essential oils extracted from Ageratum conyzoides (Asteraceae), Lantana camara (Verbenaceae), Chromolaena odorata (Asteraceae) and Ocimum viride (Lamiaceae) (Owusu, 2001). Similarly, leaf and seed extracts from Trigonella foenumgraecum L. (Fabaceae) have insecticidal effects against T. castaneum and Acanthoscelides obtectus (Say) (Pemonge et al., 1997). Dusts, such as diatomaceous earth, are also recognized for their insecticidal or repellant activity (Ebeling, 1971). Composed of amorphous silica, DE has low toxicity towards mammals, little potential for insect resistance as well as a good residual effect (Eldridge, 1964; Ebeling, 1971; Korunic, 1998), making it a promising natural alternative. Diatomaceous earth increases adult mortality while preventing the production of the offspring in the beetle pests Sitophilus zeamais Motshulski (Curculionidae), Sitophilus oryzae (L.) (Curculionidae), Callosobruchus maculatus (F.) (Bruchidae), A. obtectus (Say) (Bruchidae) and Prostephanus truncatus (Horn) (Bostrichidae) (Athanassiou et al., 2003; Stathers et al., 2004; Marsaro Junior et al., 2006; Ceruti et al., 2008). However the literature evaluating the effectiveness of DE against pests such as Palorus subdepressus Wollaston (Coleoptera: Tenebrionidae) is scarce. The use of DE to protect cereals is rare in Africa in general and Ivory Coast in particular. The only compound of natural origin used to control stored products pests in Ivory Coast is Spinosad, all other
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M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
products used being of synthetic derivation (Anon, 2013). The use of natural products such as DE is important to provide alternative methods to chemical control of stored pests. This approach will surely reduce the harmful effects of chemical insecticides on both consumers and the environment. The objective of this research was to evaluate and compare the efficiency of four different doses of DE, a new product for stored product pest control in Ivory Coast, with a chemical insecticide, Actellic SuperÔ Dust, against three important beetle pests of stored maize: S. zeamais, T. castaneum and P. subdepressus. 2. Material and methods 2.1. General method Infested maize was collected from Abobo market (5 250 0800 N, 4 0101400 W; Altitude: 76 m) cereal stores in September 2008 in Abidjan, Ivory Coast, in order to obtain the insects. The infested maize was kept in glass bottles under laboratory conditions (29 2 C and 75 5% r.h. in darkness). Adult S. zeamais, T. castaneum and P. subdepressus were collected from the bottle a month later, and identified using the descriptive key of Delobel and Tran (1993). Each species was thereafter bred separately in glass bottles under the same conditions for four generations before the study was conducted. The DE formulation used in this study was commercialized as InsectoÒ by Natural Insecto Products Inc. (CA, USA) and contains 90% of DE. The doses used were 0.5, 3, 4.5 and 6 g/kg. The chemical insecticide used, Actellic SuperÔ Dust (hereafter referred to as ASD), is distributed by STEPC, Abidjan, Ivory Coast, and contains 16 g/kg of pirimiphos-methyl and 3 g/kg of permethrin. The doses of the formulation used were 0.25, 0.5, 0.75 and 1 g/kg. 2.2. Maize treatment Each of the four doses of each insecticide was mixed with 100 g of maize. The distribution of the insecticide on maize grains was then homogenized by agitation for at least 5 min. Twenty grams of maize treated with one dose of an insecticide were placed in one glass bottle (7 cm height). Each bottle was infested with 20 individuals of one of the three pest species, for a total of five bottles per species per dose. An equal number of control bottles (one bottle per species per dose) were conducted, where no insecticide was applied on maize. The bottles were kept in a drying oven at 29 2 C and 75 5% r.h. in darkness. The number of dead individuals was observed after 1, 2, 4, 7 and 14 d. The corrected mortality was calculated, for each dose of each insecticide at each time interval, using Abbott’s formula (1925). From now on, the term mortality in the text indicates corrected cumulated mortality. The residual effect of each insecticide was also measured, but only for S. zeamais, as it was usually the first pest to colonize stored maize, in order to see the impact on offspring production. The production of offspring was thus observed every month for nine months after infestation. 2.3. Statistical analysis A Generalized Linear Model (GLM) was used to test the corrected mortality for each pest species. The different factors were time (with 5 levels), insecticide (with 2 levels) and doses of insecticides (with 4 levels for each insecticide). The principal effects as well as the interaction between factors were tested by post hoc Tukey test at P ¼ 0.05. All analyses were conducted using Statistica 7.1. (StatSoft, 2005). The logarithmic model: y ¼ a ln(x) þ b was used for evaluating mortality against exposure time to estimate the
necessary times to obtain 90 and 95% mortality. The adjusted coefficient (R2adj) was also evaluated using Excel 2007.
3. Results 3.1. Appearance of maize grains and insects after treatment After treatment with DE, the maize grains had a characteristic white color, more intense as the dose increased. In contrast to DE, the maize grains treated with ASD did not have any coloration, preventing its visual detection on grains. The insects on DE-treated maize were already covered with white powder at the first observation 1 day after infestation. The mobility of the three species decreased with time until death. On maize treated with ASD, S. zeamais was the only species showing a change in appearance, spreading its posterior wings before dying.
3.2. Insect mortality Mortality of all three beetle species was significantly affected by insecticide type, dose and exposure time (P < 0.001). Mortality increased with time of exposure, dosage, as well as with ASD compared to DE. All interactions were also significant (P < 0.001). For S. zeamais, all doses, except the lowest one (1.5 g/kg), gave 20% or more mortality on DE-treated maize from day 1 (Table 1, Fig. 1A). Mortality was similar for the three highest DE doses (3, 4.5 and 6 g/kg) (P ¼ 1.000), and reached 100% after 4 d of exposure. The adjusted coefficients (R2adj) were between 0.70 and 0.90 for all DE doses (Table 1). The lowest dose (0.25 g/kg) of ASD-treated maize caused significantly less mortality than the three highest ones (0.5, 0.75 and 1 g/kg) (P < 0.001). Mortality exceeded 80% after 4 d for all doses, reaching 100% for the two highest doses (Table 1, Fig. 1B). R2adj was superior to 0.90 for 0.25, 0.75 and 1 g/kg (Table 1). No offspring were produced in S. zeamais at all doses tested for both insecticides nine months after the experiment. Mortality of T. castaneum on DE-treated maize stayed below 50% for all doses for the first 4 d (Fig. 1C). Mortality after 14 d exceeded 90% for all doses except the lowest one, for which mortality stayed below 50%. Mortality after 7 d of treatment with 6 g/kg, the highest dose, was significantly higher than for other doses (P < 0.001). R2adj was superior to 0.90 for 6 g/kg only (Table 2). On ASD-treated maize mortality of T. castaneum increased with time for all doses, reaching just above 50% for 0.25 g/kg, but 100% for all other doses after 14 d (Table 2, Fig. 1D). The two highest doses reached 100% mortality after 7 days. R2adj was superior to 0.90 for 0.25 g/kg only (Table 2). For all DE doses tested, P. subdepressus mortality after 1 d of exposure to treated maize was less than 50%. Mortality increased with time, exceeding 90% for all doses after 4 days (Table 3, Fig. 1E). All insects were dead after 4 d at 3 and 4.5 g/kg, and after 2 d at 6 g/ kg. The mortality was similar for 3, 4.5 and 6 g/kg after 2 and 4 d (P ¼ 1.000). R2adj was superior to 0.90 for 1.5 g/kg only (Table 3). Mortality caused by ASD stayed below 50% for the lowest dose, 0.25 g/kg, up to 7 days and the difference between ASD and DE was less than for the other species (Table 3, Fig. 1E and F). Mortality increased with time and exceeded 80% after 7 days for the three highest doses, the lowest one being significantly different (P < 0.001). All insects died only in the highest dose after 7 d. R2adj was superior to 0.90 for 0.5 g/kg and 0.75 g/kg (Table 3). Interspecific comparisons showed that T. castaneum was significantly less susceptible to DE than either P. subdepressus or S. zeamais (P < 0.001).
M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
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Table 1 Mean values and standard error of cumulated and corrected mortality (%) of Sitophilus zeamais as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
0 0a 20 7b 85 12b
20 11b 87 13c 100 0b
24 6b 94 4c 99 2b
33 9b 93 4c 100 0b
42 17c 83 9c 100 0b
33 10b 98 4c 100 0b
51 7c 89 4c 100 0b
0.25 61.3 7.5 0.914
3 57.7 29 0.868
0.5 54.1 34.83 0.799
4.5 48.3 41.83 0.827
0.75 41.83 46 0.946
6 48.3 43.5 0.772
1 35.34 55.5 0.908
Day 1 0 0a 2 1 2a 4 5 8a Parameters of the model Coefficient 1.5 a 3.6 b 0.5 2 0.892 R adj.
S. zeamais corrected mortality (%)
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
(A) DE 120
100
100
80
80 1.5 g/kg
60
3 g /kg
40 20
0.25 g/kg
60
0.5 g /kg
4.5 g/kg
40
0.75 g/kg
6 g/kg
20
1 g/kg
0
0 0
T. castaneum corrected mortality (%)
(B ) Ac t e l l i c S up e r Dus t
120
120
2
4
0
6
(C) DE
120
100
2
4
6
(D) Actellic Super Dust
100
80
80 1.5 g/kg
60
3 g /kg 40
4.5 g/kg
20
6 g/kg
0
0.25 g/kg
60
0.5 g /kg
40
0.75 g/kg 1 g/kg
20 0
0
5
10
15
0
5
10
15
P. subdepressus corrected mortality
-20
(E) DE
120
( F ) A c t e l l ic S upe r D u st
120
100
100
80
1.5 g/kg
80
0.25 g/kg
60
3 g /kg
60
0.5 g /kg
40
4.5 g/kg
40
0.75 g/kg
6 g/kg
20
1 g/kg
20
0
0 0
2
4
6
0
5
10
-20 Exposure time (days)
Exposure time (days)
Fig. 1. Comparison of adjusted model of four diatomaceous earth (DE) and Actellic SuperÔ dust (ASD) doses effectiveness on three beetle pests. Effects of: DE (A) and ASD (B) on Sitophilus zeamais; DE (C) and ASD (D) on Tribolium castaneum; DE (E) and ASD (F) on Palorus subdepressus.
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M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
Table 2 Mean values and standard error of cumulated and corrected mortality (%) of Tribolium castaneum as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ Dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
5 3a 16 8a 30 14b 39 9b 53 11a
0 0a 0 0a 10 7a 34 5b 94 6b
41 20b 78 12b 88 11c 97 2bc 100 0b
0 0a 5 6a 22 6b 74 31c 98 2b
67 7c 91 7b 97 2c 100 0bc 100 0b
0 0a 18 8a 48 10c 94 4bc 99 2b
66 10c 96 5b 100 0c 100 0bc 100 0b
0.25 18.22 4.306 0.998
3 33.75 17.39 0.774
0.5 21.12 52.63 0.838
4.5 40.12 13.67 0.896
0.75 12.24 74.47 0.722
6 41.67 3.75 0.945
1 11.21 77.45 0.607
Day 1 0 0a 2 0 0a 4 0 0a 7 3 4a 14 40 22a Parameters of the model Coefficient 1.5 a 12.66 b 8.28 R2adj. 0.552
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
4. Discussion The two insecticides tested in this study acted differently, as could be expected from the difference in their mode of action; ASD acting through a chemical action on the insects while DE causes a slow death due to a physical action (Golob, 1997; Korunic, 1998). ASD contains pirimiphos methyl which is an organophosphorus compound with anticholinesterasic action. The display of the posterior wings in S. zeamais in the presence of ASD could have been caused by a shock effect on the nervous system. For all pest species tested, one day was insufficient to obtain significant mortality with DE. Diatomaceous earth particles have abrasive properties but more importantly the absorption of cuticular lipids causes a deterioration of the cuticle and consequently, death by desiccation (Korunic, 1998; Subramanyam and Roelsi, 2000). Insects having a rough cuticle are more likely to carry the particles of DE in treated maize. Our results show that T. castaneum was less susceptible to DE compared to the two other species; 14 d were necessary before observing the mortality of all individuals. In S. oryzae and T. castaneum, all individuals died respectively after 5 and 14 d with a dose of 2 g/kg (Korunic, 1998). These results are similar to ours concerning T. castaneum. Korunic (1998) also showed that stored products pests of the genus Sitophilus and Cryptolestes are more sensitive to DE than species from the genera Tribolium, Rhyzopertha and Oryzaephilus. A mortality of 95% in S. zeamais populations on maize variety Hybrid BRS 1001 12 d after treatment with 0.2 g/kg of DE has been reported (Marsaro Junior et al., 2006). Diatomaceous earth at 0.75 and 1 g/kg
provided 90e100% control of S. zeamais after 7 and 14 d of exposure at 25 and 30 C (Ceruti et al., 2008). Arnaud et al. (2005) obtained over 95% mortality of T. castaneum after 21 d of exposure using 0.2 g/kg of DE. They also found differences in the effectiveness of DE due to the difference between the origin of the pest population and DE formulation. The DE formulation ProtectorÒ, a less effective formulation to that used in the current tests, failed to achieve 100% mortality in T. castaneum and Rhyzopertha dominica 14 d after treatment when applied at 0.5 g/kg (Baldassari et al., 2008). All S. zeamais were dead after 2 days of treatment with DE at 3 g/ kg, the dose recommended by the manufacturer, thus showing effectiveness of this dose against this pest species. According to Athanassiou et al. (2005) all S. oryzae are eliminated 14 d after treatment with doses of 0.75, 1 and 1.5 g/kg of DE on barley and wheat. The difference between our results and those of Athanassiou et al. (2005) could be explained by the different stored products treated, the different species tested even though they belong to the same genus, but most probably by the different doses used. We obtained the mortality of all insects after only 2 d at double the highest dose used by Athanassiou et al. (2005). Diatomaceous earth is highly affected by the type of treated grains and the insect species (Vayias and Stephou, 2009; Wakil et al., 2013). The DE dose (3 g/kg) was also effective against P. subdepressus within 2 d. The sensitivity of S. zeamais and P. subdepressus could be explained by their cuticle being rougher than that of T. castaneum, retaining more particles (Carlson and Ball, 1962). In addition, the cuticle of T. castaneum is thicker than that of S. zeamais and P. subdepressus, thus most likely delaying the absorption of cuticular
Table 3 Mean values and standard error of cumulated and corrected mortality (%) of Palorus subdepressus as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ Dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
0 0a 0 0a 19 8a 33 11a
14 11a 98 4b 100 0b e
4 5a 18 9a 75 9b 93 4b
23 7b 98 2b 100 0b e
5 5a 39 8a 85 10b 97 2b
35 11b 100 0b 100 0b e
24 15b 71 11b 97 2b 100 0b
0.25 17.87 4.992 0.883
3 62.03 27.66 0.767
0.5 15.52 6.833 0.905
4.5 55.68 35 0.769
0.75 49.66 6.517 0.974
6 46.88 45.83 0.75
1 39.48 33.26 0.898
Day 1 5 6a 2 58 5a 4 94 5b 7 100 0b Parameters of the model Coefficient 1.5 a 64.2 b 7.833 R2adj. 0.988
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
lipids or the reducing the chances of perforation by abrasive particles (Barlett, 1951). According to Ebeling (1971), the insects with a soft cuticle show a lower susceptibility to DE, which may be the case for S. zeamais and P. subdepressus compared to T. castaneum. Another factor that could reduce the susceptibility of T. castaneum would be its ability to replace water lost by desiccation by producing water by metabolism of the food products (Flanders, 1941). The highest dose tested for DE in this study was the most effective dose for the control of the tested insect pests of stored food products and caused the same mortality as the recommended dose of ASD (0.5 g/kg) for the control of T. castaneum, the least susceptible insect in this study. However, because a high amount of DE would give a dusty appearance to the grain, there is a need to take into account the level of susceptibility of the insect pests present, as well as the food product to be protected. A standard use of this insecticide would not be advised because the food products having coarser grains also tend to require higher amounts of DE. The residual effects of the DE differ according to the treated food products. Based on our results, DE ensures a good long-term protection of maize (at least 9 months) by preventing offspring production, and this for all four doses tested with S. zeamais. Athanassiou et al. (2005) noticed that DE killed more than 90% individuals of S. oryzae in treated wheat 270 days after treatment. Diatomaceous earth is a good alternative for the control of these three major pest insects of maize stocks in Ivory Coast. Increasing the amount, even though that could give a powdery aspect to the grains, could solve this problem. Consumer acceptance could be improved by knowing that this product is inert chemically and without any harmful effects on their health, in contrast to the chemical insecticides frequently used. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 256e257. Anon, 2013. List of Pesticides Approved and Authorized in Ivory Coast. Direction of Plant Protection and Quality Control. Ivory Coast Ministry of Agriculture (last accessed 02. 10. 13.). http://www.isysphyt.org/image/sw-documentation/ 18062013095720.pdf. Arnaud, L., Lan, H.T.T., Brostaux, Y., Haubruge, E., 2005. Efficacy of diatomaceous earth formulations admixed with grain against of Tribolium castaneum. J. Stored Prod. Res. 41, 121e130. Athanassiou, C.G., Kavalieratos, N.G., Economou, L.P., Dimizas, C.B., Vayias, B.J., Tomanovic, S., Milutinovic, M., 2005. Persistence of three diatomaceous earth (DE) formulations against Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J. Econ. Entomol. 98, 1404e1412. Athanassiou, C.G., Kavalieratos, N.G., Tsaganou, F.C., Vayias, B.J., Dimizas, C.B., Bouchelos, C.Th, 2003. Effect of grain type on the insecticidal efficacy of SilicoSec against Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Crop Prot. 22, 1141e1147. Baldassari, N., Prioli, C., Martini, A., Trotta, V., Baronio, P., 2008. Insecticidal efficacy of a diatomaceous earth formulation against a mixed age population of adults of Rhyzopertha dominica and Tribolium castaneum as function of different temperature and exposure time. Bull. Insectol. 61, 355e360.
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Journal of Stored Products Research journal homepage: www.elsevier.com/locate/jspr
Effectiveness of diatomaceous earth for control of Sitophilus zeamais (Coleoptera: Curculionidae), Tribolium castaneum and Palorus subdepressus (Coleoptera: Tenebrionidae) Mamadou Doumbia a, *, Bleu Gondo Douan a, Koffi Eric Kwadjo a, Dagobert Kouadio Kra a, Véronique Martel b, Mamadou Dagnogo a a b
UFR SN, University Nangui Abrogoua, 02 PB 801 Abidjan 02, Cote d’Ivoire Natural Resources Canada, Canadian Forest Service, Laurentian Forestry Center, 1055 du P.E.P.S., Quebec City, Quebec G1V4C7, Canada
a r t i c l e i n f o
a b s t r a c t
Article history: Accepted 29 November 2013
The effectiveness of diatomaceous earth (DE) or diatomite has been assessed against three major beetle pests of stored maize: Sitophilus zeamais (the maize weevil), Tribolium castaneum (the red flour beetle) and Palorus subdepressus (the depressed flour beetle). Maize has been treated with four doses of DE (1.5, 3, 4.5 and 6 g/kg) and four doses of Actellic SuperÔ Dust a chemical insecticide used as a reference (0.25, 0.5, 0.75 and 1 g/kg). The effective mortality was measured for each treatment after 1, 2, 4, 7 and 14 d of exposure. The corrected mortality rates were calculated by considering the mortality in the control group. Diatomaceous earth was as effective as Actellic SuperÔ Dust but required higher doses. Diatomaceous earth acted faster on S. zeamais and P. subdepressus compared to T. castaneum. The highest dose tested for DE caused the same mortality in T. castaneum as the recommended dose of Actellic SuperÔ Dust. Diatomaceous earth is a good alternative for the control of these three devastating insect pests of maize stocks and can readily be incorporated into integrated stored products pest management programs. Ó 2013 Elsevier Ltd. All rights reserved.
Keywords: Efficacy Mortality Pests Stored maize Diatomaceous earth
1. Introduction Maize, with rice and sorghum, is one of the most consumed food products in Central and West Africa (Silou, 2003). Insects, mainly beetles and moths, play a significant role in the destruction of stored grain, causing losses from 20 to 100% in developing countries (Holst et al., 2000). The red flour beetle Tribolium castaneum (Herbst) is even able to attack cocoa and coffee stocks which are the two most significant export products in Ivory Coast (Lavabre, 1970). Although one of the first control strategies against stored grain pests has been the use of chemicals, the need for alternatives became apparent when problems associated with these products such as the development of insect resistance, environmental pollution, contamination of treated food as well as health risks during products handling, were encountered (Subramanyam and Hagstrum, 1995). Several alternatives have been investigated against stored product pests. Natural products have been tested such as palm oils (Elaeis guineensis L. (Arecaceae)), groundnut (Arachis hypogaea L. (Fabaceae)) and tobacco extract (Nicotiana tabacum L. (Solanaceae))
* Corresponding author. Tel.: þ225 0896 2029; fax: þ225 0113 2747. E-mail addresses: [email protected], [email protected] (M. Doumbia). 0022-474X/$ e see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jspr.2013.11.008
(Foua-Bi, 1993) or leaf essential oils extracted from Ageratum conyzoides (Asteraceae), Lantana camara (Verbenaceae), Chromolaena odorata (Asteraceae) and Ocimum viride (Lamiaceae) (Owusu, 2001). Similarly, leaf and seed extracts from Trigonella foenumgraecum L. (Fabaceae) have insecticidal effects against T. castaneum and Acanthoscelides obtectus (Say) (Pemonge et al., 1997). Dusts, such as diatomaceous earth, are also recognized for their insecticidal or repellant activity (Ebeling, 1971). Composed of amorphous silica, DE has low toxicity towards mammals, little potential for insect resistance as well as a good residual effect (Eldridge, 1964; Ebeling, 1971; Korunic, 1998), making it a promising natural alternative. Diatomaceous earth increases adult mortality while preventing the production of the offspring in the beetle pests Sitophilus zeamais Motshulski (Curculionidae), Sitophilus oryzae (L.) (Curculionidae), Callosobruchus maculatus (F.) (Bruchidae), A. obtectus (Say) (Bruchidae) and Prostephanus truncatus (Horn) (Bostrichidae) (Athanassiou et al., 2003; Stathers et al., 2004; Marsaro Junior et al., 2006; Ceruti et al., 2008). However the literature evaluating the effectiveness of DE against pests such as Palorus subdepressus Wollaston (Coleoptera: Tenebrionidae) is scarce. The use of DE to protect cereals is rare in Africa in general and Ivory Coast in particular. The only compound of natural origin used to control stored products pests in Ivory Coast is Spinosad, all other
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M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
products used being of synthetic derivation (Anon, 2013). The use of natural products such as DE is important to provide alternative methods to chemical control of stored pests. This approach will surely reduce the harmful effects of chemical insecticides on both consumers and the environment. The objective of this research was to evaluate and compare the efficiency of four different doses of DE, a new product for stored product pest control in Ivory Coast, with a chemical insecticide, Actellic SuperÔ Dust, against three important beetle pests of stored maize: S. zeamais, T. castaneum and P. subdepressus. 2. Material and methods 2.1. General method Infested maize was collected from Abobo market (5 250 0800 N, 4 0101400 W; Altitude: 76 m) cereal stores in September 2008 in Abidjan, Ivory Coast, in order to obtain the insects. The infested maize was kept in glass bottles under laboratory conditions (29 2 C and 75 5% r.h. in darkness). Adult S. zeamais, T. castaneum and P. subdepressus were collected from the bottle a month later, and identified using the descriptive key of Delobel and Tran (1993). Each species was thereafter bred separately in glass bottles under the same conditions for four generations before the study was conducted. The DE formulation used in this study was commercialized as InsectoÒ by Natural Insecto Products Inc. (CA, USA) and contains 90% of DE. The doses used were 0.5, 3, 4.5 and 6 g/kg. The chemical insecticide used, Actellic SuperÔ Dust (hereafter referred to as ASD), is distributed by STEPC, Abidjan, Ivory Coast, and contains 16 g/kg of pirimiphos-methyl and 3 g/kg of permethrin. The doses of the formulation used were 0.25, 0.5, 0.75 and 1 g/kg. 2.2. Maize treatment Each of the four doses of each insecticide was mixed with 100 g of maize. The distribution of the insecticide on maize grains was then homogenized by agitation for at least 5 min. Twenty grams of maize treated with one dose of an insecticide were placed in one glass bottle (7 cm height). Each bottle was infested with 20 individuals of one of the three pest species, for a total of five bottles per species per dose. An equal number of control bottles (one bottle per species per dose) were conducted, where no insecticide was applied on maize. The bottles were kept in a drying oven at 29 2 C and 75 5% r.h. in darkness. The number of dead individuals was observed after 1, 2, 4, 7 and 14 d. The corrected mortality was calculated, for each dose of each insecticide at each time interval, using Abbott’s formula (1925). From now on, the term mortality in the text indicates corrected cumulated mortality. The residual effect of each insecticide was also measured, but only for S. zeamais, as it was usually the first pest to colonize stored maize, in order to see the impact on offspring production. The production of offspring was thus observed every month for nine months after infestation. 2.3. Statistical analysis A Generalized Linear Model (GLM) was used to test the corrected mortality for each pest species. The different factors were time (with 5 levels), insecticide (with 2 levels) and doses of insecticides (with 4 levels for each insecticide). The principal effects as well as the interaction between factors were tested by post hoc Tukey test at P ¼ 0.05. All analyses were conducted using Statistica 7.1. (StatSoft, 2005). The logarithmic model: y ¼ a ln(x) þ b was used for evaluating mortality against exposure time to estimate the
necessary times to obtain 90 and 95% mortality. The adjusted coefficient (R2adj) was also evaluated using Excel 2007.
3. Results 3.1. Appearance of maize grains and insects after treatment After treatment with DE, the maize grains had a characteristic white color, more intense as the dose increased. In contrast to DE, the maize grains treated with ASD did not have any coloration, preventing its visual detection on grains. The insects on DE-treated maize were already covered with white powder at the first observation 1 day after infestation. The mobility of the three species decreased with time until death. On maize treated with ASD, S. zeamais was the only species showing a change in appearance, spreading its posterior wings before dying.
3.2. Insect mortality Mortality of all three beetle species was significantly affected by insecticide type, dose and exposure time (P < 0.001). Mortality increased with time of exposure, dosage, as well as with ASD compared to DE. All interactions were also significant (P < 0.001). For S. zeamais, all doses, except the lowest one (1.5 g/kg), gave 20% or more mortality on DE-treated maize from day 1 (Table 1, Fig. 1A). Mortality was similar for the three highest DE doses (3, 4.5 and 6 g/kg) (P ¼ 1.000), and reached 100% after 4 d of exposure. The adjusted coefficients (R2adj) were between 0.70 and 0.90 for all DE doses (Table 1). The lowest dose (0.25 g/kg) of ASD-treated maize caused significantly less mortality than the three highest ones (0.5, 0.75 and 1 g/kg) (P < 0.001). Mortality exceeded 80% after 4 d for all doses, reaching 100% for the two highest doses (Table 1, Fig. 1B). R2adj was superior to 0.90 for 0.25, 0.75 and 1 g/kg (Table 1). No offspring were produced in S. zeamais at all doses tested for both insecticides nine months after the experiment. Mortality of T. castaneum on DE-treated maize stayed below 50% for all doses for the first 4 d (Fig. 1C). Mortality after 14 d exceeded 90% for all doses except the lowest one, for which mortality stayed below 50%. Mortality after 7 d of treatment with 6 g/kg, the highest dose, was significantly higher than for other doses (P < 0.001). R2adj was superior to 0.90 for 6 g/kg only (Table 2). On ASD-treated maize mortality of T. castaneum increased with time for all doses, reaching just above 50% for 0.25 g/kg, but 100% for all other doses after 14 d (Table 2, Fig. 1D). The two highest doses reached 100% mortality after 7 days. R2adj was superior to 0.90 for 0.25 g/kg only (Table 2). For all DE doses tested, P. subdepressus mortality after 1 d of exposure to treated maize was less than 50%. Mortality increased with time, exceeding 90% for all doses after 4 days (Table 3, Fig. 1E). All insects were dead after 4 d at 3 and 4.5 g/kg, and after 2 d at 6 g/ kg. The mortality was similar for 3, 4.5 and 6 g/kg after 2 and 4 d (P ¼ 1.000). R2adj was superior to 0.90 for 1.5 g/kg only (Table 3). Mortality caused by ASD stayed below 50% for the lowest dose, 0.25 g/kg, up to 7 days and the difference between ASD and DE was less than for the other species (Table 3, Fig. 1E and F). Mortality increased with time and exceeded 80% after 7 days for the three highest doses, the lowest one being significantly different (P < 0.001). All insects died only in the highest dose after 7 d. R2adj was superior to 0.90 for 0.5 g/kg and 0.75 g/kg (Table 3). Interspecific comparisons showed that T. castaneum was significantly less susceptible to DE than either P. subdepressus or S. zeamais (P < 0.001).
M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
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Table 1 Mean values and standard error of cumulated and corrected mortality (%) of Sitophilus zeamais as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
0 0a 20 7b 85 12b
20 11b 87 13c 100 0b
24 6b 94 4c 99 2b
33 9b 93 4c 100 0b
42 17c 83 9c 100 0b
33 10b 98 4c 100 0b
51 7c 89 4c 100 0b
0.25 61.3 7.5 0.914
3 57.7 29 0.868
0.5 54.1 34.83 0.799
4.5 48.3 41.83 0.827
0.75 41.83 46 0.946
6 48.3 43.5 0.772
1 35.34 55.5 0.908
Day 1 0 0a 2 1 2a 4 5 8a Parameters of the model Coefficient 1.5 a 3.6 b 0.5 2 0.892 R adj.
S. zeamais corrected mortality (%)
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
(A) DE 120
100
100
80
80 1.5 g/kg
60
3 g /kg
40 20
0.25 g/kg
60
0.5 g /kg
4.5 g/kg
40
0.75 g/kg
6 g/kg
20
1 g/kg
0
0 0
T. castaneum corrected mortality (%)
(B ) Ac t e l l i c S up e r Dus t
120
120
2
4
0
6
(C) DE
120
100
2
4
6
(D) Actellic Super Dust
100
80
80 1.5 g/kg
60
3 g /kg 40
4.5 g/kg
20
6 g/kg
0
0.25 g/kg
60
0.5 g /kg
40
0.75 g/kg 1 g/kg
20 0
0
5
10
15
0
5
10
15
P. subdepressus corrected mortality
-20
(E) DE
120
( F ) A c t e l l ic S upe r D u st
120
100
100
80
1.5 g/kg
80
0.25 g/kg
60
3 g /kg
60
0.5 g /kg
40
4.5 g/kg
40
0.75 g/kg
6 g/kg
20
1 g/kg
20
0
0 0
2
4
6
0
5
10
-20 Exposure time (days)
Exposure time (days)
Fig. 1. Comparison of adjusted model of four diatomaceous earth (DE) and Actellic SuperÔ dust (ASD) doses effectiveness on three beetle pests. Effects of: DE (A) and ASD (B) on Sitophilus zeamais; DE (C) and ASD (D) on Tribolium castaneum; DE (E) and ASD (F) on Palorus subdepressus.
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M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
Table 2 Mean values and standard error of cumulated and corrected mortality (%) of Tribolium castaneum as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ Dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
5 3a 16 8a 30 14b 39 9b 53 11a
0 0a 0 0a 10 7a 34 5b 94 6b
41 20b 78 12b 88 11c 97 2bc 100 0b
0 0a 5 6a 22 6b 74 31c 98 2b
67 7c 91 7b 97 2c 100 0bc 100 0b
0 0a 18 8a 48 10c 94 4bc 99 2b
66 10c 96 5b 100 0c 100 0bc 100 0b
0.25 18.22 4.306 0.998
3 33.75 17.39 0.774
0.5 21.12 52.63 0.838
4.5 40.12 13.67 0.896
0.75 12.24 74.47 0.722
6 41.67 3.75 0.945
1 11.21 77.45 0.607
Day 1 0 0a 2 0 0a 4 0 0a 7 3 4a 14 40 22a Parameters of the model Coefficient 1.5 a 12.66 b 8.28 R2adj. 0.552
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
4. Discussion The two insecticides tested in this study acted differently, as could be expected from the difference in their mode of action; ASD acting through a chemical action on the insects while DE causes a slow death due to a physical action (Golob, 1997; Korunic, 1998). ASD contains pirimiphos methyl which is an organophosphorus compound with anticholinesterasic action. The display of the posterior wings in S. zeamais in the presence of ASD could have been caused by a shock effect on the nervous system. For all pest species tested, one day was insufficient to obtain significant mortality with DE. Diatomaceous earth particles have abrasive properties but more importantly the absorption of cuticular lipids causes a deterioration of the cuticle and consequently, death by desiccation (Korunic, 1998; Subramanyam and Roelsi, 2000). Insects having a rough cuticle are more likely to carry the particles of DE in treated maize. Our results show that T. castaneum was less susceptible to DE compared to the two other species; 14 d were necessary before observing the mortality of all individuals. In S. oryzae and T. castaneum, all individuals died respectively after 5 and 14 d with a dose of 2 g/kg (Korunic, 1998). These results are similar to ours concerning T. castaneum. Korunic (1998) also showed that stored products pests of the genus Sitophilus and Cryptolestes are more sensitive to DE than species from the genera Tribolium, Rhyzopertha and Oryzaephilus. A mortality of 95% in S. zeamais populations on maize variety Hybrid BRS 1001 12 d after treatment with 0.2 g/kg of DE has been reported (Marsaro Junior et al., 2006). Diatomaceous earth at 0.75 and 1 g/kg
provided 90e100% control of S. zeamais after 7 and 14 d of exposure at 25 and 30 C (Ceruti et al., 2008). Arnaud et al. (2005) obtained over 95% mortality of T. castaneum after 21 d of exposure using 0.2 g/kg of DE. They also found differences in the effectiveness of DE due to the difference between the origin of the pest population and DE formulation. The DE formulation ProtectorÒ, a less effective formulation to that used in the current tests, failed to achieve 100% mortality in T. castaneum and Rhyzopertha dominica 14 d after treatment when applied at 0.5 g/kg (Baldassari et al., 2008). All S. zeamais were dead after 2 days of treatment with DE at 3 g/ kg, the dose recommended by the manufacturer, thus showing effectiveness of this dose against this pest species. According to Athanassiou et al. (2005) all S. oryzae are eliminated 14 d after treatment with doses of 0.75, 1 and 1.5 g/kg of DE on barley and wheat. The difference between our results and those of Athanassiou et al. (2005) could be explained by the different stored products treated, the different species tested even though they belong to the same genus, but most probably by the different doses used. We obtained the mortality of all insects after only 2 d at double the highest dose used by Athanassiou et al. (2005). Diatomaceous earth is highly affected by the type of treated grains and the insect species (Vayias and Stephou, 2009; Wakil et al., 2013). The DE dose (3 g/kg) was also effective against P. subdepressus within 2 d. The sensitivity of S. zeamais and P. subdepressus could be explained by their cuticle being rougher than that of T. castaneum, retaining more particles (Carlson and Ball, 1962). In addition, the cuticle of T. castaneum is thicker than that of S. zeamais and P. subdepressus, thus most likely delaying the absorption of cuticular
Table 3 Mean values and standard error of cumulated and corrected mortality (%) of Palorus subdepressus as a function of the exposure time to different doses of diatomaceous earth (DE) and Actellic SuperÔ Dust (ASD) and parameters of the model. Doses (g/kg) DE
ASD
DE
ASD
DE
ASD
DE
ASD
1.5
0.25
3
0.5
4.5
0.75
6
1
0 0a 0 0a 19 8a 33 11a
14 11a 98 4b 100 0b e
4 5a 18 9a 75 9b 93 4b
23 7b 98 2b 100 0b e
5 5a 39 8a 85 10b 97 2b
35 11b 100 0b 100 0b e
24 15b 71 11b 97 2b 100 0b
0.25 17.87 4.992 0.883
3 62.03 27.66 0.767
0.5 15.52 6.833 0.905
4.5 55.68 35 0.769
0.75 49.66 6.517 0.974
6 46.88 45.83 0.75
1 39.48 33.26 0.898
Day 1 5 6a 2 58 5a 4 94 5b 7 100 0b Parameters of the model Coefficient 1.5 a 64.2 b 7.833 R2adj. 0.988
Within a row, different letters denote a significant difference between mortality (HSD Tukey test (P ¼ 0.05)).
M. Doumbia et al. / Journal of Stored Products Research 57 (2014) 1e5
lipids or the reducing the chances of perforation by abrasive particles (Barlett, 1951). According to Ebeling (1971), the insects with a soft cuticle show a lower susceptibility to DE, which may be the case for S. zeamais and P. subdepressus compared to T. castaneum. Another factor that could reduce the susceptibility of T. castaneum would be its ability to replace water lost by desiccation by producing water by metabolism of the food products (Flanders, 1941). The highest dose tested for DE in this study was the most effective dose for the control of the tested insect pests of stored food products and caused the same mortality as the recommended dose of ASD (0.5 g/kg) for the control of T. castaneum, the least susceptible insect in this study. However, because a high amount of DE would give a dusty appearance to the grain, there is a need to take into account the level of susceptibility of the insect pests present, as well as the food product to be protected. A standard use of this insecticide would not be advised because the food products having coarser grains also tend to require higher amounts of DE. The residual effects of the DE differ according to the treated food products. Based on our results, DE ensures a good long-term protection of maize (at least 9 months) by preventing offspring production, and this for all four doses tested with S. zeamais. Athanassiou et al. (2005) noticed that DE killed more than 90% individuals of S. oryzae in treated wheat 270 days after treatment. Diatomaceous earth is a good alternative for the control of these three major pest insects of maize stocks in Ivory Coast. Increasing the amount, even though that could give a powdery aspect to the grains, could solve this problem. Consumer acceptance could be improved by knowing that this product is inert chemically and without any harmful effects on their health, in contrast to the chemical insecticides frequently used. References Abbott, W.S., 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 256e257. Anon, 2013. List of Pesticides Approved and Authorized in Ivory Coast. Direction of Plant Protection and Quality Control. Ivory Coast Ministry of Agriculture (last accessed 02. 10. 13.). http://www.isysphyt.org/image/sw-documentation/ 18062013095720.pdf. Arnaud, L., Lan, H.T.T., Brostaux, Y., Haubruge, E., 2005. Efficacy of diatomaceous earth formulations admixed with grain against of Tribolium castaneum. J. Stored Prod. Res. 41, 121e130. Athanassiou, C.G., Kavalieratos, N.G., Economou, L.P., Dimizas, C.B., Vayias, B.J., Tomanovic, S., Milutinovic, M., 2005. Persistence of three diatomaceous earth (DE) formulations against Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J. Econ. Entomol. 98, 1404e1412. Athanassiou, C.G., Kavalieratos, N.G., Tsaganou, F.C., Vayias, B.J., Dimizas, C.B., Bouchelos, C.Th, 2003. Effect of grain type on the insecticidal efficacy of SilicoSec against Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Crop Prot. 22, 1141e1147. Baldassari, N., Prioli, C., Martini, A., Trotta, V., Baronio, P., 2008. Insecticidal efficacy of a diatomaceous earth formulation against a mixed age population of adults of Rhyzopertha dominica and Tribolium castaneum as function of different temperature and exposure time. Bull. Insectol. 61, 355e360.
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