Journal of Chemical Ecology, Vol. 17, No. 3, 1991
FUMIGANT TOXICITY OF ESSENTIAL OILS AGAINST FOUR MAJOR STORED-PRODUCT INSECTS
E L I S H A A Y A , 1'* U Z I R A V I D , 2 N A C H M A N P A S T E R , l B E N J A M I N J U V E N , 3 U Z I Z I S M A N , t and V L A D I M I R P I S S A R E V 1Department of Stored Products, ARO :Newe Ya 'ar Experiment Station, ARO 3Department of Food Science, ARO Bet Dagan 50250, Israel
(Received August 29, 1990; accepted October 24, 1990) Abstract--The fumigant toxicity of 28 essential oils extracted from various spice and herb plants and some of their major constituents were assessed for adult coleopterans Rhyzopertha dominica, Oryzaephilus surinamensis, Tribolium castaneum, and Sitophilus oryzae. Three groups of active materials were distinguished: (1) The compounds terpinen 4-ol, 1,8-cineole, and the essential oils of three-lobed sage, sage, bay laurel, rosemary, and lavender were most active against R. dominica; (2) The compounds linalool, ee-terpineol, and carvacrol and the essential oils of oregano, basil, Syrian marjoram, and thyme were most active against O. surinamensis; and (3) the compound 1,8-cineole and the essential oils anise and peppermint were active against T. castaneum. Key Words--Sitophilus oryzae, Curculionidae, Rhyzopertha dominica, Bostrichidae, Oryzaephilus surinamensis, Cucujidae, Tribolium castaneum, Tenebrionidae, Coleoptera, essential oils, fumigant toxicity.
INTRODUCTION Insect control in stored-food products at present relies heavily u p o n the use o f gaseous f u m i g a n t s and residual insecticides, both of which pose serious hazards to w a r m - b l o o d e d a n i m a l s a n d the e n v i r o n m e n t . F u m i g a t i o n is still one o f the most effective methods for the p r e v e n t i o n o f storage losses. H o w e v e r , the availability o f f u m i g a n t s for insect control has d w i n d l e d drastically lately. As o f *To whom correspondence should be addressed. 499 0098-0331/91/0300-0499506.50/0 9 1991 Plenum Publishing Corporation
500
SHAAYA ET AL.
now, only two fumigants are still in use, namely, methyl bromide and phosphine. The former is suspected of leaving residues that are harmful to warmblooded animals (Dansi et al., 1984), while the latter, which is in wide use, has shown alarming indications of development of insect resistance to it (Mills, 1983; Tyler et al., 1983). Thus, it would be of marked benefit for the preservation of stored products to discover and develop new compounds that have the potential to replace the toxic fumigants, are less harmful, yet are easy, simple, and convenient to use. The present study was conducted to investigate further the potential use of essential oils, extracted from various spice and herb plants in Israel, and some of their major constituents as fumigants for the control of stored product insect pests. METHODS AND MATERIALS
The beetles were bred at 27~ and 70% relative humidity. Sitophilus oryzae (Curculionidae) and Rhyzopertha dominica (Bostrichidae) were reared on soft wheat, Oryzaephilus surinamensis (Cucujidae), on ground wheat with the addition of glycerin and yeast, and Tribolium castaneum (Tenebrionidae) on wheat flour. The essential oils were obtained from fresh plants by steam distillation (Marcus and Lichtenstein, 1979). Major oil constituents were purchased commercially. The English name of the essential oil is used; in case no English name was available, the Latin name is given. The fumigation chambers were 3.4-liter glass flasks with round bottoms, closed with a glass stopper fitted with a hook. The test materials were applied on a small square piece of filter paper, which was suspended by the hook, together with the insect cages, in the fumigation chamber. To obtain even distribution of the oil during the treatment, a magnetic stirrer was placed on the bottom of each flask. Twenty insects of each species, aged 5-10 days, were placed in each of the four cages (4 cm in length and 1.5 cm in diam), which were perforated with small holes enabling penetration of the gas. Small amounts of ground wheat were placed in each cage. Treatments were carried out for 24 hr, and percent mortality was recorded. RESULTS
The fumigant toxicity of 28 essential oils and 10 of their principal components (Table 1) was tested against four major stored-product insect pests: S. oryzae, R. dominica, O. surinamensis, and T. castaneum. At a concentration of 5-15 /~l/liter of air, only 11 oils and five of their major components were found to be highly active (Table 1). Among the active materials, it was possible to distinguish three groups according to their activity: Group 1 compounds terpinen 4-ol, 1,8-cineole, and the essential oils of three-lobed sage, sage, bay
FUMIGANT TOXICITY OF ESSENTIAL OILS
501
TABLE 1. ESSENTIAL OILS AND SOME MAJOR CONSTITUENTS TESTED AS FUMIGANTS AGAINST FOUR MAJOR STORED-PRoDUCT INSECTS
Group A~ The essential oils of oregano, basil, Syrian marjoran, thyme, three-lobed sage, sage, bay laurel, rosemary, lavender, anise, peppermint. The compounds linalool, c~-terpineol,carvacrol, terpinen 4-ol, 1,8-cineote Group B The essential oils of celery, savory, lemon grass, rue, clary sage, cumin, caraway, lemon, grapefruit, orange, coriander, Salvia dominica, fennel, chamomile, Artemisia arboresence, parsley, Artemisiajudaica. The compounds ~3-caryophyUen,p-cymene, c~-terpinene, sabinene, myrcene aGroup A was found to be very active, and group B had low or no activity.
laurel, rosemary and lavender were found most active against R. dominica. All of them gave 100% mortality at a concentration of 15 /xl/liter of air. O. surinamensis was less susceptible than R. dominica and at a concentration of 15/zl/ liter of air, only terpinen 4-ol, 1,8-cineole, and rosemary gave 100% mortality (Figure 1). Group 2 compounds linalool, c~-terpineol, and carvacrol and the essential oils of oregano, basil, Syrian marjoram, and thyme were found most active against O. surinamensis. One hundred percent mortality was achieved by linalool, ot-terpineol, oregano, basil, and Syrian marjoram at a concentration of 15 #l/liter, and by linalool and oregano at 10/zl/liter (Figure 2). S. oryzae was much more resistant than O. surinamensis and R. dominica to all the tested essential oils and their major components. For S. oryzae, 100% mortality was obtained only with sage oil at a concentration of 15/xl/liter (Figure 1, see also Figures 2 and 3). In group 3 the compound 1,8-cineole and the essential oils of anise and peppermint were the only active fumigants against T. castaneum of all the materials tested. Anise and cineole gave 100% mortality at concentrations of 10 and 15 #l/liter, respectively. Among the other oils of low activity, Artemisia judaica, parsley, Salvia dominica, and clary sage were found to be active mainly against O. surinamensis; at a concentration of 15 #l/liter, mortalities of 80, 75, 55, and 45%, respectively, was recorded. On the other hand, fennel oil and the compound 3/-terpinene were active only against R. dominica, at a concentration of 15/xl/ liter with 83 % and 49 % mortality, respectively (data not shown). DISCUSSION
Three groups could be distinguished of the 28 essential oils and some of their major constituents as active fumigants against four major stored-product insects: group 1, most active against R. dominica, followed by O. surinamensis
502
SHAAYA ET AL.
rEPPINEN-4"OL
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ITHREE LOBED
100
n
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BAY LALAqEL
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FIG. 1. Essential oils and compounds most active against R. dominica. Percent mortality of R = R. dominica; 0 = O. surinamensis, and S = S. oryzae, using various concentrations (1 = 15, 2 = 10, 3 = 5 tzl/liter of air) of the test material. The results are the average of 5-10 replicates.
and S. oryzae, group 2, most active against O. surinamensis, followed by R. dominica and S. oryzae; and group 3, against T. castaneum, followed by R. dominica, 0 . surinamensis and S. oryzae. From the activity of the various essential oils and their major constituents, it can be seen that alcohol and phenol, such as linalool and carvacrol, show greater activity against O. surinamensis. In the case of R. dominica, alcohol and ether, e.g., terpinen 4-ol and 1,8-cineole, are the most active, and ethers, such as 1,8-cineole, against T. castaneum. These differences in activity of the various compounds were used in the search for more potent compounds for the control of these insects. Recently, we were able to select a compound, ZP51, with much higher potency than all the essential oils and the various compounds tested. A concentration of 3 /zl/liter was enough to obtain 100% mortality of the four test insects (Shaaya et al., in preparation). This should be compared with 20-30 mg/liter of methyl bromide recommended for control in the field of stored-product insects. In addition, this compound was most active against S. oryzae, a concentration of 1,5/d/liter being enough to obtain 100% mortality. The fumigant toxicity of a number of essential oils was also tested against Sitotroga cerealella and Acanthoscelides obtectus (Klingauf et al., 1983) and
FUMIGANT
TOXICITY
OF ESSENTIAL
503
OILS
8~SIL
INALOOL O
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o
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123
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~ ' ~
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{THYME
tl
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FIG. 2. Essential oils and compounds most active against O. s u r i n a m e n s i s . Percent mortality of R = R. d o m i n i c a ; 0 = O. s u r i n a m e n s i s , and S = S. or y z ae , using various concentrations (1 = 15, 2 = 10, 3 = 5/xl/liter of air) of the test material. The results are the average of 5 - 1 0 replicates.
100"
b
~"
ANISE T
'PEPPERMINT
:I,8-C~NEOLE T R
T
0
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0
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l
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123
123
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FIG. 3. Essential oils and compounds active against T. c a s t e n a u m . Percent mortality of R = R. d o m i n i c a ; 0 = O. s u r i n a m e n s i s ; S = S. oryzae, and T = T. c a s t e n a u m , using
various concentrations (1 = 15, 2 = 10, 3 = 5/~l/liter of air) of the test material, The results are the average of 5 - 1 0 replicates.
504
SHAAYA ET AL.
o f M e n t h a p i p e r i t a against T. c a s t a n e u m (Misra and Jitender, 1983). The various studies were done using different fumigation methods and exposure times, so it is not possible to correlate our results with those reported in the literature. The existence o f naturally occurring insecticidal plant components has been known for centuries. However, relatively few of these compounds are actually used in crop protection today (Marcus and Lichtenstein, 1979). Increasing problems concerning the use o f m o d e m synthetic insecticides, such as persistence o f residues, resistance, and damage to the environment and human health have generated interest in naturally occurring compounds. It should be noted that biologically active compounds o f food plants are assumed to be environmentally more acceptable and less hazardous than others to humans. The results presented in this study suggest that some oils or their major constituents could be efficient fumigants and also could be integrated with other pest management procedures.
REFERENCES DANSI, L., VAN VELSEN,F.L., and VANDERHEUDEN, C.A. 1984. Methyl bromide: carcinogenic effects in the rat fore stomach. Toxicol. Appl. Pharmacol. 72:262-27t. KLINGAUF,F., BESTMANN,H.J., VOSTROWSKY,O. and MICHAELIS,K. 1983. Wirkung yon titherischen ()len auf Schadinsekten. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 4:123-126. MARCUS, C., and LICHTENSTEIN, P. 1979. Biologically active components of anise: Toxicity and interaction with insecticides in insects. J. Agric. Food Chem. 27:1217-1223. MILLS, K.M. 1983. Resistance to the fumigant hydrogen phosphide in some stored-product species associated with repeated inadequate treatments. Mitt. Dtsch. Ges. AIlg. Angew. Entomol. 4:98101. MISHRA,R.C., and JITENDER, K. 1983. Evaluation of Mentha piperita L. oil as fumigant against the red flour beetle Tribolium castaneum (Herbst.). Indian Performer 27:73-76. TYLER, P.M., TAYLOR,R.W., and REES, D.P. 1983. Insect resistance to phosphine fumigation in food warehouses in Bangladesh. Int. Pest Control 25:10-13, 21.
FUMIGANT TOXICITY OF ESSENTIAL OILS AGAINST FOUR MAJOR STORED-PRODUCT INSECTS
E L I S H A A Y A , 1'* U Z I R A V I D , 2 N A C H M A N P A S T E R , l B E N J A M I N J U V E N , 3 U Z I Z I S M A N , t and V L A D I M I R P I S S A R E V 1Department of Stored Products, ARO :Newe Ya 'ar Experiment Station, ARO 3Department of Food Science, ARO Bet Dagan 50250, Israel
(Received August 29, 1990; accepted October 24, 1990) Abstract--The fumigant toxicity of 28 essential oils extracted from various spice and herb plants and some of their major constituents were assessed for adult coleopterans Rhyzopertha dominica, Oryzaephilus surinamensis, Tribolium castaneum, and Sitophilus oryzae. Three groups of active materials were distinguished: (1) The compounds terpinen 4-ol, 1,8-cineole, and the essential oils of three-lobed sage, sage, bay laurel, rosemary, and lavender were most active against R. dominica; (2) The compounds linalool, ee-terpineol, and carvacrol and the essential oils of oregano, basil, Syrian marjoram, and thyme were most active against O. surinamensis; and (3) the compound 1,8-cineole and the essential oils anise and peppermint were active against T. castaneum. Key Words--Sitophilus oryzae, Curculionidae, Rhyzopertha dominica, Bostrichidae, Oryzaephilus surinamensis, Cucujidae, Tribolium castaneum, Tenebrionidae, Coleoptera, essential oils, fumigant toxicity.
INTRODUCTION Insect control in stored-food products at present relies heavily u p o n the use o f gaseous f u m i g a n t s and residual insecticides, both of which pose serious hazards to w a r m - b l o o d e d a n i m a l s a n d the e n v i r o n m e n t . F u m i g a t i o n is still one o f the most effective methods for the p r e v e n t i o n o f storage losses. H o w e v e r , the availability o f f u m i g a n t s for insect control has d w i n d l e d drastically lately. As o f *To whom correspondence should be addressed. 499 0098-0331/91/0300-0499506.50/0 9 1991 Plenum Publishing Corporation
500
SHAAYA ET AL.
now, only two fumigants are still in use, namely, methyl bromide and phosphine. The former is suspected of leaving residues that are harmful to warmblooded animals (Dansi et al., 1984), while the latter, which is in wide use, has shown alarming indications of development of insect resistance to it (Mills, 1983; Tyler et al., 1983). Thus, it would be of marked benefit for the preservation of stored products to discover and develop new compounds that have the potential to replace the toxic fumigants, are less harmful, yet are easy, simple, and convenient to use. The present study was conducted to investigate further the potential use of essential oils, extracted from various spice and herb plants in Israel, and some of their major constituents as fumigants for the control of stored product insect pests. METHODS AND MATERIALS
The beetles were bred at 27~ and 70% relative humidity. Sitophilus oryzae (Curculionidae) and Rhyzopertha dominica (Bostrichidae) were reared on soft wheat, Oryzaephilus surinamensis (Cucujidae), on ground wheat with the addition of glycerin and yeast, and Tribolium castaneum (Tenebrionidae) on wheat flour. The essential oils were obtained from fresh plants by steam distillation (Marcus and Lichtenstein, 1979). Major oil constituents were purchased commercially. The English name of the essential oil is used; in case no English name was available, the Latin name is given. The fumigation chambers were 3.4-liter glass flasks with round bottoms, closed with a glass stopper fitted with a hook. The test materials were applied on a small square piece of filter paper, which was suspended by the hook, together with the insect cages, in the fumigation chamber. To obtain even distribution of the oil during the treatment, a magnetic stirrer was placed on the bottom of each flask. Twenty insects of each species, aged 5-10 days, were placed in each of the four cages (4 cm in length and 1.5 cm in diam), which were perforated with small holes enabling penetration of the gas. Small amounts of ground wheat were placed in each cage. Treatments were carried out for 24 hr, and percent mortality was recorded. RESULTS
The fumigant toxicity of 28 essential oils and 10 of their principal components (Table 1) was tested against four major stored-product insect pests: S. oryzae, R. dominica, O. surinamensis, and T. castaneum. At a concentration of 5-15 /~l/liter of air, only 11 oils and five of their major components were found to be highly active (Table 1). Among the active materials, it was possible to distinguish three groups according to their activity: Group 1 compounds terpinen 4-ol, 1,8-cineole, and the essential oils of three-lobed sage, sage, bay
FUMIGANT TOXICITY OF ESSENTIAL OILS
501
TABLE 1. ESSENTIAL OILS AND SOME MAJOR CONSTITUENTS TESTED AS FUMIGANTS AGAINST FOUR MAJOR STORED-PRoDUCT INSECTS
Group A~ The essential oils of oregano, basil, Syrian marjoran, thyme, three-lobed sage, sage, bay laurel, rosemary, lavender, anise, peppermint. The compounds linalool, c~-terpineol,carvacrol, terpinen 4-ol, 1,8-cineote Group B The essential oils of celery, savory, lemon grass, rue, clary sage, cumin, caraway, lemon, grapefruit, orange, coriander, Salvia dominica, fennel, chamomile, Artemisia arboresence, parsley, Artemisiajudaica. The compounds ~3-caryophyUen,p-cymene, c~-terpinene, sabinene, myrcene aGroup A was found to be very active, and group B had low or no activity.
laurel, rosemary and lavender were found most active against R. dominica. All of them gave 100% mortality at a concentration of 15 /xl/liter of air. O. surinamensis was less susceptible than R. dominica and at a concentration of 15/zl/ liter of air, only terpinen 4-ol, 1,8-cineole, and rosemary gave 100% mortality (Figure 1). Group 2 compounds linalool, c~-terpineol, and carvacrol and the essential oils of oregano, basil, Syrian marjoram, and thyme were found most active against O. surinamensis. One hundred percent mortality was achieved by linalool, ot-terpineol, oregano, basil, and Syrian marjoram at a concentration of 15 #l/liter, and by linalool and oregano at 10/zl/liter (Figure 2). S. oryzae was much more resistant than O. surinamensis and R. dominica to all the tested essential oils and their major components. For S. oryzae, 100% mortality was obtained only with sage oil at a concentration of 15/xl/liter (Figure 1, see also Figures 2 and 3). In group 3 the compound 1,8-cineole and the essential oils of anise and peppermint were the only active fumigants against T. castaneum of all the materials tested. Anise and cineole gave 100% mortality at concentrations of 10 and 15 #l/liter, respectively. Among the other oils of low activity, Artemisia judaica, parsley, Salvia dominica, and clary sage were found to be active mainly against O. surinamensis; at a concentration of 15 #l/liter, mortalities of 80, 75, 55, and 45%, respectively, was recorded. On the other hand, fennel oil and the compound 3/-terpinene were active only against R. dominica, at a concentration of 15/xl/ liter with 83 % and 49 % mortality, respectively (data not shown). DISCUSSION
Three groups could be distinguished of the 28 essential oils and some of their major constituents as active fumigants against four major stored-product insects: group 1, most active against R. dominica, followed by O. surinamensis
502
SHAAYA ET AL.
rEPPINEN-4"OL
~I,8-CINEOLE
ITHREE LOBED
100
n
11i".l!- '! l "itlll
12:
:~
121
~
R
0
0
123
ROSEMARY
BAY LALAqEL
tu
123
1;~3
Cone 125
.AVENDER leo
Te-
0 Co~c. 23
23
2
1
FIG. 1. Essential oils and compounds most active against R. dominica. Percent mortality of R = R. dominica; 0 = O. surinamensis, and S = S. oryzae, using various concentrations (1 = 15, 2 = 10, 3 = 5 tzl/liter of air) of the test material. The results are the average of 5-10 replicates.
and S. oryzae, group 2, most active against O. surinamensis, followed by R. dominica and S. oryzae; and group 3, against T. castaneum, followed by R. dominica, 0 . surinamensis and S. oryzae. From the activity of the various essential oils and their major constituents, it can be seen that alcohol and phenol, such as linalool and carvacrol, show greater activity against O. surinamensis. In the case of R. dominica, alcohol and ether, e.g., terpinen 4-ol and 1,8-cineole, are the most active, and ethers, such as 1,8-cineole, against T. castaneum. These differences in activity of the various compounds were used in the search for more potent compounds for the control of these insects. Recently, we were able to select a compound, ZP51, with much higher potency than all the essential oils and the various compounds tested. A concentration of 3 /zl/liter was enough to obtain 100% mortality of the four test insects (Shaaya et al., in preparation). This should be compared with 20-30 mg/liter of methyl bromide recommended for control in the field of stored-product insects. In addition, this compound was most active against S. oryzae, a concentration of 1,5/d/liter being enough to obtain 100% mortality. The fumigant toxicity of a number of essential oils was also tested against Sitotroga cerealella and Acanthoscelides obtectus (Klingauf et al., 1983) and
FUMIGANT
TOXICITY
OF ESSENTIAL
503
OILS
8~SIL
INALOOL O
III~-
F
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R
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r
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o
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123
$
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FIG. 2. Essential oils and compounds most active against O. s u r i n a m e n s i s . Percent mortality of R = R. d o m i n i c a ; 0 = O. s u r i n a m e n s i s , and S = S. or y z ae , using various concentrations (1 = 15, 2 = 10, 3 = 5/xl/liter of air) of the test material. The results are the average of 5 - 1 0 replicates.
100"
b
~"
ANISE T
'PEPPERMINT
:I,8-C~NEOLE T R
T
0
$
0
s 1tl-
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123
123
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FIG. 3. Essential oils and compounds active against T. c a s t e n a u m . Percent mortality of R = R. d o m i n i c a ; 0 = O. s u r i n a m e n s i s ; S = S. oryzae, and T = T. c a s t e n a u m , using
various concentrations (1 = 15, 2 = 10, 3 = 5/~l/liter of air) of the test material, The results are the average of 5 - 1 0 replicates.
504
SHAAYA ET AL.
o f M e n t h a p i p e r i t a against T. c a s t a n e u m (Misra and Jitender, 1983). The various studies were done using different fumigation methods and exposure times, so it is not possible to correlate our results with those reported in the literature. The existence o f naturally occurring insecticidal plant components has been known for centuries. However, relatively few of these compounds are actually used in crop protection today (Marcus and Lichtenstein, 1979). Increasing problems concerning the use o f m o d e m synthetic insecticides, such as persistence o f residues, resistance, and damage to the environment and human health have generated interest in naturally occurring compounds. It should be noted that biologically active compounds o f food plants are assumed to be environmentally more acceptable and less hazardous than others to humans. The results presented in this study suggest that some oils or their major constituents could be efficient fumigants and also could be integrated with other pest management procedures.
REFERENCES DANSI, L., VAN VELSEN,F.L., and VANDERHEUDEN, C.A. 1984. Methyl bromide: carcinogenic effects in the rat fore stomach. Toxicol. Appl. Pharmacol. 72:262-27t. KLINGAUF,F., BESTMANN,H.J., VOSTROWSKY,O. and MICHAELIS,K. 1983. Wirkung yon titherischen ()len auf Schadinsekten. Mitt. Dtsch. Ges. Allg. Angew. Entomol. 4:123-126. MARCUS, C., and LICHTENSTEIN, P. 1979. Biologically active components of anise: Toxicity and interaction with insecticides in insects. J. Agric. Food Chem. 27:1217-1223. MILLS, K.M. 1983. Resistance to the fumigant hydrogen phosphide in some stored-product species associated with repeated inadequate treatments. Mitt. Dtsch. Ges. AIlg. Angew. Entomol. 4:98101. MISHRA,R.C., and JITENDER, K. 1983. Evaluation of Mentha piperita L. oil as fumigant against the red flour beetle Tribolium castaneum (Herbst.). Indian Performer 27:73-76. TYLER, P.M., TAYLOR,R.W., and REES, D.P. 1983. Insect resistance to phosphine fumigation in food warehouses in Bangladesh. Int. Pest Control 25:10-13, 21.
