Journal of Chemical Ecology, Vol. 13, No. 4, 1987
MALE-PRODUCED AGGREGATION PHEROMONE IN PEA A N D BEAN WEEVIL, Sitona lineatus (L.) 1
MARGARET M. BLIGHT and LESTER J. WADHAMS Rothamsted Experimental Station Harpenden, Herts., AL5 2JQ, U.K.
(Received February 12, 1986; accepted April 25, 1986) Abstract--The attraction of S. lineatus to live baits comprising S. lineatus
feeding on Vicia faba (L.) was studied in a field experiment in the early spring. There was clear evidence that male S. lineatus produced an aggregation pheromonewhich attracted approximatelyequal numbersof both sexes from overwintering sites. No evidence was obtained for the production, in the spring, of any semiochemicalby female weevils. Key Words--Sitona lineatus, pea and bean weevil, pea leaf weevil, Coleoptera, Curculionidae, aggregationpheromone. INTRODUCTION The pea and bean weevil, Sitona lineatus (L.), a pest of leguminous crops (Bardner et al., 1983; E1-Lafi, 1977), is widely distributed throughout Western Europe, the Middle East and the northwest region of North America. It has recently been found also in eastern North America (Hoebeke and Wheeler, 1985). The biology of this insect was first documented in detail in Britain by Jackson (1920), and it has since been studied intensively by several workers, including Andersen (1931) and Hans (1959) in Germany. Adult weevils overwinter in sheltered situations in long grass, clover, lucerne, or the stubble of pea and bean fields. They migrate to the preferred food plants, peas, beans, and vetches (Jackson, 1920; Hans, 1959), in the following spring when mating occurs and egg laying commences. Adult feeding damage, consisting of characteristic semicircular notches in the margins of leaves is most obvious, but more serious damage is caused by the larvae which live in the soil and feed on the root nodules. Coleoptera: Curculionidae. 733 0098-0331/87/0400-0733505.00/0
9 1987 Plenum Publishing Corporation
734
BLIGHT AND WADHAMS
The production of aggregation pheromones by several weevils, including
Anthonomus grandis, three Sitophilus spp., and three Pissodes spp., is welldocumented (Hardee et al., 1969; Tumlinson et al., 1969; Walgenbach et al., 1983; Fontaine and Foltz, 1982; Booth et al., 1983). We are therefore investigating the production by S. lineatus of pheromones which might be used to detect, monitor, and mass trap these insects or to time insecticide application. In this paper we present evidence for the presence of a male-produced aggregation pheromone in S. lineatus. The identification of and initial field studies on some components of this pheromone have been published elsewhere (Blight et al., 1984). METHODS AND MATERIALS
Insects. S. lineatus used in the experiments were adults which had overwintered in the field. Weevils were collected in early spring from cultured broad bean (Vicia faba) plants which had been placed out on Rothamsted farm in areas where field beans had grown in the preceding year. They were sexed by examination of the ventral posterior abdominal segments (Jackson, 1920). Males and females were maintained separately, until use, on broad bean plants, under a controlled 16:8 (light-dark) photoperiod with a temperature of 15-16~ in the light and 9-10~ in the dark period. Traps. The nonsticky cone traps (Figure 1) were similar in design to the Leggett trap (Leggett et al., 1975) used for capturing the cotton boll weevil, Anthonomus grandis. The base, A, consisted of an inverted yellow polythene bucket (26 cm diameter at lower edge, narrowing to 16 cm diameter x 25 cm high) from which the bottom had been removed. Surmounting the base was a cone, B, (24 cm diameter at lower edge, narrowing to ca. 5 cm diameter at upper edge x 27 cm high) made of woven stainless-steel square mesh wire cloth, aperture size 0.40 mm. The cone was held away from the base by three plastic spacers, G. A transparent polystyrene circular collecting pot, C, (7.5 cm diameter, narrowing to 6 cm diameter x 11 cm high) was held on the top of the cone with nylon shock cord. It contained a small (5 cm diameter x 8 cm high) wire cloth cone, D, which hindered the escape of live weevils. The assembled trap was held down on the soil by nylon shock cord guys, E, attached to tent pegs, F. Insects were able to gain access to the trap either by walking over the outside of the base and entering under the bottom edge of the large cone or by walking straight up the inside of the base from the ground. As the latter appeared to be the preferred route, six semicircular holes (3 cm radius) were cut out at the lower edge of the base to allow easier access. Live Baits. Each bait consisted of a 13-cm pot of five broad bean (Sutton variety) shoots enclosed in a fine mesh terylene bag. The bag was taped tightly to the pot, the weevils were added, and the bag was closed securely with a
735
A G G R E G A T I O N PHEROMONE IN WEEVILS
Dc
,.F FIG. 1. Diagram of cone trap. A, base; B, cone; C, collecting pot; D, small cone; E, shock cord guy; F, tent peg; G, spacer.
rubber band. The five treatments (baits) were a blank control (pot containing soil only, enclosed in a bag), broad bean plant, and plants with, respectively, 40 females, 40 males, and 40 males plus 40 females. When the treatments were set out in the experiment, each pot was sunk into the ground so that the top of the pot was level with the soil surface, and a cone trap was then placed over the top. The plants were watered every day. When the experiment was terminated the numbers of live weevils of each sex present on the baits were recorded. Experimental Design. The experiment was carried out on Rothamsted Farm, Harpenden, Hertfordshire, April 12-26, 1984. Three blocks were set up, two of which were towards the edges o f fields where field beans had grown in 1983, and the third was on a field approx. 4 m from a wood. On each site, the treatments, 8 m apart, were placed in a row, parallel with the hedgeline. On two of the sites, the treatments were approx. 4 m out from the hedgerow and
736
BLIGHT AND WADHAMS
wood, respectively, but on the third, because of farming operations, they were 1 m in from the hedge. A randomized complete block design, with periodic rerandomization within the blocks, was used. Each treatment occurred once in each block, and each block was rerandomized when a minimum of 50 weevils had been caught. Weevils were removed from the traps each day and were stored alive at 6~ until sexed and counted. Total catch data were subjected to the transformation x = loge (t + 1.0) where x and t were the transformed and untransformed counts, respectively. Factorial analyses of variance were performed on these data and on the ratio of males to males-plus-females caught by each treatment. RESULTS AND DISCUSSION
The catch data, derived from 12 replicates, are shown in Table 1. Because of uneven weevil distribution among the three sites, eight of the replications were performed on one site, with the other two sites yielding two replicates each. Only low numbers of weevils were caught by either the blank control or the bean plant alone (5.4% and 5.6%, respectively, of the total catch). Although a few more weevils (7.3 % of the total caught) were trapped by treatment 2 containing females, the "female effect" was not significant (Table 2). However, treatments 1 and 3, containing males, were highly attractive to both sexes, which were trapped in approximately equal numbers ("male effect" significant at P < 0.001, Table 2). The presence of females with males had no effect on
TABLE 1. FIELD RESPONSE OF S. lineatus TO TRAPS BAITED WITH MALE AND/OR FEMALE S. lineatus FEEDING ON BEAN PLANTSa
Treatment
1. 2. 3. 4. 5.
Bean plant + 40 o" o" Bean plant + 40 9 9 Bean plant + 40 o'c~ + 40 9 9 Bean plant Blank control
Mean no. of weevils caught per replicate (range)
31.3 5.4 29.3 4.2 4.0
(13-78) (0-14) (8-72) (0-13) (0-10)
Sex Ratio (or : 9 )b
1.0:1 0.9 : 1 0.9:1 0.9:1 0.6:1
~The total number of weevils caught in 12 replicates was 891. At the end of the experiment, at least 85 % of each sex of the S. lineatus comprising the baits remained alive. bFactorial analysis of variance of the ratio of males to males plus females showed no significant differences between the five treatments.
737
AGGREGATION PHEROMONE IN WEEVILS
TABLE 2. ANALYSIS OF VARIANCE: FIELD RESPONSE OF S. Lineatus TO TRAPS BAITED WITH MALE AND/OR FEMALE S. Lineatus FEEDING ON BEAN PLANTS
[Variate = loge (catch + 1.0)]
Source of variation Replication Treatments, broken down into Blank control vs. other treatments Treatments with males vs without Treatments with females vs. without Interaction between males and females Residual Total Grand total
Degrees of freedom 11 1 1 1 l 42(2)a 46 57
Mean square ,
Variance ratio
0.6414
1.681
9.9472 41.1379 0.0026 0.2610 0.3816 1.4647
26.065b t07.794b 0.007 0.684
Missing values. ~ at P < 0.001.
this attraction (Table 2), and there were no significant differences between the sex ratios of weevils trapped by the five treatments. These results indicate clearly that S. lineatus produces an aggregation pheromone in the spring. In c o m m o n with most curculionids, it is male-produced (see references cited in the Introduction). However, in the experiment reported here, the possibility that some of the bean volatiles synergized the activity of the male-produced pheromone cannot be excluded. Indeed, we have independent evidence that the three synthetic bean volatiles, (Z)-3-hexen-l-ol, (Z)-3hexen-l-yl acetate, and linalool, synergize the male-produced attractant, 4methyl-3,5-heptanedione (Blight et al., 1984). There was no evidence that female S. lineatus produced any semiochemical, although they may do so at other times of the year. Females of some curculionids, viz., A. grandis and Cylasformicarius elegantulus (Coffelt et al., 1978) produce a sex pheromone. In the case of A. grandis, it has weak attractancy compared to the male-produced aggregation pheromone (McKibben et al., 1977). However, the aggregation pheromone apparently functions mainly as a sex attractant after the insects are established on the host plants (Lloyd et al., 1983). A similar situation could exist with S. lineatus (Blight and Wadhams, unpublished). The adaptive significance of an aggregation pheromone in these weevils is not clear. It has been suggested (Shorey, 1973) that coleopteran aggregation pheromones arose initially as mechanisms by which insects could cause others of the same species to aggregate at a suitable food source. The male-produced
738
BLIGHT AND WADHAMS
Sitona pheromone presumably does assist the aggregation of the weevils in legume fields for the purposes of both feeding and mating. However, in this artificial monoculture it must be of far less importance to survival than in an environment comprising widely scattered food resources. Acknowledgments--We thank J. McEwen and R. Moffitt for their help and cooperation with the field experiment, T. Dixon for statistical analyses, and J. Steinmann and M.C. Smith for technical assistance.
REFERENCES ANDERSEN, K.T. 1931. Der linierte Graufiissler oder Blattrandkfifer, Sitona lineata L. Monogr. Pflanzenschutz, 6:88 pp. Julius Springer, Berlin. BARDNER, R., FLETCHER, K.E., and GRIFFITHS, D.C. 1983. Chemical control of the pea and bean weevil, Sitona lineatus L. and subsequent effects on the yield of field beans Vicia faba L. J. Agric. Sci. Camb. 101:71-80. BOOTH, D.C., PHILLIPS,T.W., CLAESSON,A., SILVERSTEIN,R.M., LANIER,G.N., and WEST, J.R. 1983. Aggregation pheromone components of two species of Pissodes weevils (Coleoptera: Curculionidae): Isolation, identification and field activity. J. Chem. Ecol. 9:1-12. BLIGHT, M.M., PICKETT, J.A., SMITH, M.C., and WADHAMS,L.J. 1984. An aggregation pheromone of Sitona lineatus. Identification and initial field studies. Naturwissenschaften 71:480481. COFFELT, J.A., VICK, K.W., SOWER, L.L., and MCCLELLAN, W.T 1978. Sex pheromone of the sweet potato weevil, Cylas formicarius elegantulus: Laboratory bioassay and evidence for a multiple component system. Environ. Entomol. 7:756-758. EL-LAFI, A.M. 1977. The economic injury level of the pea leaf weevil Sitona lineatus (L.) in northern Idaho and eastern Washington. Ph.D. thesis. University of Idaho. FONTAINE, M.S., and FOLTZ, J.L. 1982. Field studies of a male-released aggregation pheromone in Pissodes nemorensis. Environ. Entomol. 11:881-883. HANS, H. 1959. Beitr/ige zur Biologie von Sitona lineatus L. Z. Angew. Entomol. 44:343-386. HARDEE, D.D., CROSS, W.H., and MITCHELL, E.B. 1969. Male boll weevils are more attractive than cotton plants to boll weevils. J. Econ. Entomol. 62:165-169. HOEBEKE, E.R., and WHEELER, A.G. 1985. Sitona lineatus (L.), the pea leaf weevil: First records in eastern North America (Coleoptera: Curculionidae), Proc. Entomol. Soc. Wash. 87:216220. JACKSON, D.J. 1920. Bionomics of weevils of the genus Sitones injurious to leguminous crops in Britain. Ann. Appl. Biol. 7:269-298. LEGGETT,J.E., CROSS,W.H., MITCHELL,H.C., JOHNSON, W.L., and McGOVERN,W.L. 1975. Improved traps for capturing boll weevils. J. G. Entomol. Soc. 10:52-61. LLOYD, E.P., MCKIBBEN, G.H., LEGGETT, J.E., and HARTSTACK, A.W. 1983. Pheromones for survey, detection, and control, p. 183, in R.L. Ridgway, E.P. Lloyd, and W.H. Cross (eds.). Cotton Insect Management with Special Reference to the Boll Weevil. U.S. Department of Agriculture, Agriculture Handbook, No. 589. McKIBBEN, G.H., HEDIN, P.A., McGOVERN, W.L., WILSON, N.M., and MITCHELL, E.B. 1977. A sex pheromone for male boll weevils from females. J. Chem. Ecol. 3:331-335. SHOREY, H.H. 1973. Behavioral responses to insect pheromones. Annu. Rev. Entomol. 18:349380.
AGGREGATION PHEROMONE 1N WEEVILS
739
TUMLINSON, J.H., HARDEE, D.D., GUELDNER, R.C., THOMPSON, A.C., HEDIN, P.A., and MINYARD, J.P. 1969. Sex pheromones produced by male boll weevil: isolation, identification and synthesis. Science 166:1010-1012. WALGENBACH,C.A., PHILLIPS,J.K., FAUSTINI, D.L., and BURKHOLDER, W,E. 1983. Male-produced aggregation pheromone of the maize weevil, Sitophilus zeamais, and interspecific attraction between three Sitophilus species. J. Chem. Ecol. 9:831-841.
MALE-PRODUCED AGGREGATION PHEROMONE IN PEA A N D BEAN WEEVIL, Sitona lineatus (L.) 1
MARGARET M. BLIGHT and LESTER J. WADHAMS Rothamsted Experimental Station Harpenden, Herts., AL5 2JQ, U.K.
(Received February 12, 1986; accepted April 25, 1986) Abstract--The attraction of S. lineatus to live baits comprising S. lineatus
feeding on Vicia faba (L.) was studied in a field experiment in the early spring. There was clear evidence that male S. lineatus produced an aggregation pheromonewhich attracted approximatelyequal numbersof both sexes from overwintering sites. No evidence was obtained for the production, in the spring, of any semiochemicalby female weevils. Key Words--Sitona lineatus, pea and bean weevil, pea leaf weevil, Coleoptera, Curculionidae, aggregationpheromone. INTRODUCTION The pea and bean weevil, Sitona lineatus (L.), a pest of leguminous crops (Bardner et al., 1983; E1-Lafi, 1977), is widely distributed throughout Western Europe, the Middle East and the northwest region of North America. It has recently been found also in eastern North America (Hoebeke and Wheeler, 1985). The biology of this insect was first documented in detail in Britain by Jackson (1920), and it has since been studied intensively by several workers, including Andersen (1931) and Hans (1959) in Germany. Adult weevils overwinter in sheltered situations in long grass, clover, lucerne, or the stubble of pea and bean fields. They migrate to the preferred food plants, peas, beans, and vetches (Jackson, 1920; Hans, 1959), in the following spring when mating occurs and egg laying commences. Adult feeding damage, consisting of characteristic semicircular notches in the margins of leaves is most obvious, but more serious damage is caused by the larvae which live in the soil and feed on the root nodules. Coleoptera: Curculionidae. 733 0098-0331/87/0400-0733505.00/0
9 1987 Plenum Publishing Corporation
734
BLIGHT AND WADHAMS
The production of aggregation pheromones by several weevils, including
Anthonomus grandis, three Sitophilus spp., and three Pissodes spp., is welldocumented (Hardee et al., 1969; Tumlinson et al., 1969; Walgenbach et al., 1983; Fontaine and Foltz, 1982; Booth et al., 1983). We are therefore investigating the production by S. lineatus of pheromones which might be used to detect, monitor, and mass trap these insects or to time insecticide application. In this paper we present evidence for the presence of a male-produced aggregation pheromone in S. lineatus. The identification of and initial field studies on some components of this pheromone have been published elsewhere (Blight et al., 1984). METHODS AND MATERIALS
Insects. S. lineatus used in the experiments were adults which had overwintered in the field. Weevils were collected in early spring from cultured broad bean (Vicia faba) plants which had been placed out on Rothamsted farm in areas where field beans had grown in the preceding year. They were sexed by examination of the ventral posterior abdominal segments (Jackson, 1920). Males and females were maintained separately, until use, on broad bean plants, under a controlled 16:8 (light-dark) photoperiod with a temperature of 15-16~ in the light and 9-10~ in the dark period. Traps. The nonsticky cone traps (Figure 1) were similar in design to the Leggett trap (Leggett et al., 1975) used for capturing the cotton boll weevil, Anthonomus grandis. The base, A, consisted of an inverted yellow polythene bucket (26 cm diameter at lower edge, narrowing to 16 cm diameter x 25 cm high) from which the bottom had been removed. Surmounting the base was a cone, B, (24 cm diameter at lower edge, narrowing to ca. 5 cm diameter at upper edge x 27 cm high) made of woven stainless-steel square mesh wire cloth, aperture size 0.40 mm. The cone was held away from the base by three plastic spacers, G. A transparent polystyrene circular collecting pot, C, (7.5 cm diameter, narrowing to 6 cm diameter x 11 cm high) was held on the top of the cone with nylon shock cord. It contained a small (5 cm diameter x 8 cm high) wire cloth cone, D, which hindered the escape of live weevils. The assembled trap was held down on the soil by nylon shock cord guys, E, attached to tent pegs, F. Insects were able to gain access to the trap either by walking over the outside of the base and entering under the bottom edge of the large cone or by walking straight up the inside of the base from the ground. As the latter appeared to be the preferred route, six semicircular holes (3 cm radius) were cut out at the lower edge of the base to allow easier access. Live Baits. Each bait consisted of a 13-cm pot of five broad bean (Sutton variety) shoots enclosed in a fine mesh terylene bag. The bag was taped tightly to the pot, the weevils were added, and the bag was closed securely with a
735
A G G R E G A T I O N PHEROMONE IN WEEVILS
Dc
,.F FIG. 1. Diagram of cone trap. A, base; B, cone; C, collecting pot; D, small cone; E, shock cord guy; F, tent peg; G, spacer.
rubber band. The five treatments (baits) were a blank control (pot containing soil only, enclosed in a bag), broad bean plant, and plants with, respectively, 40 females, 40 males, and 40 males plus 40 females. When the treatments were set out in the experiment, each pot was sunk into the ground so that the top of the pot was level with the soil surface, and a cone trap was then placed over the top. The plants were watered every day. When the experiment was terminated the numbers of live weevils of each sex present on the baits were recorded. Experimental Design. The experiment was carried out on Rothamsted Farm, Harpenden, Hertfordshire, April 12-26, 1984. Three blocks were set up, two of which were towards the edges o f fields where field beans had grown in 1983, and the third was on a field approx. 4 m from a wood. On each site, the treatments, 8 m apart, were placed in a row, parallel with the hedgeline. On two of the sites, the treatments were approx. 4 m out from the hedgerow and
736
BLIGHT AND WADHAMS
wood, respectively, but on the third, because of farming operations, they were 1 m in from the hedge. A randomized complete block design, with periodic rerandomization within the blocks, was used. Each treatment occurred once in each block, and each block was rerandomized when a minimum of 50 weevils had been caught. Weevils were removed from the traps each day and were stored alive at 6~ until sexed and counted. Total catch data were subjected to the transformation x = loge (t + 1.0) where x and t were the transformed and untransformed counts, respectively. Factorial analyses of variance were performed on these data and on the ratio of males to males-plus-females caught by each treatment. RESULTS AND DISCUSSION
The catch data, derived from 12 replicates, are shown in Table 1. Because of uneven weevil distribution among the three sites, eight of the replications were performed on one site, with the other two sites yielding two replicates each. Only low numbers of weevils were caught by either the blank control or the bean plant alone (5.4% and 5.6%, respectively, of the total catch). Although a few more weevils (7.3 % of the total caught) were trapped by treatment 2 containing females, the "female effect" was not significant (Table 2). However, treatments 1 and 3, containing males, were highly attractive to both sexes, which were trapped in approximately equal numbers ("male effect" significant at P < 0.001, Table 2). The presence of females with males had no effect on
TABLE 1. FIELD RESPONSE OF S. lineatus TO TRAPS BAITED WITH MALE AND/OR FEMALE S. lineatus FEEDING ON BEAN PLANTSa
Treatment
1. 2. 3. 4. 5.
Bean plant + 40 o" o" Bean plant + 40 9 9 Bean plant + 40 o'c~ + 40 9 9 Bean plant Blank control
Mean no. of weevils caught per replicate (range)
31.3 5.4 29.3 4.2 4.0
(13-78) (0-14) (8-72) (0-13) (0-10)
Sex Ratio (or : 9 )b
1.0:1 0.9 : 1 0.9:1 0.9:1 0.6:1
~The total number of weevils caught in 12 replicates was 891. At the end of the experiment, at least 85 % of each sex of the S. lineatus comprising the baits remained alive. bFactorial analysis of variance of the ratio of males to males plus females showed no significant differences between the five treatments.
737
AGGREGATION PHEROMONE IN WEEVILS
TABLE 2. ANALYSIS OF VARIANCE: FIELD RESPONSE OF S. Lineatus TO TRAPS BAITED WITH MALE AND/OR FEMALE S. Lineatus FEEDING ON BEAN PLANTS
[Variate = loge (catch + 1.0)]
Source of variation Replication Treatments, broken down into Blank control vs. other treatments Treatments with males vs without Treatments with females vs. without Interaction between males and females Residual Total Grand total
Degrees of freedom 11 1 1 1 l 42(2)a 46 57
Mean square ,
Variance ratio
0.6414
1.681
9.9472 41.1379 0.0026 0.2610 0.3816 1.4647
26.065b t07.794b 0.007 0.684
Missing values. ~ at P < 0.001.
this attraction (Table 2), and there were no significant differences between the sex ratios of weevils trapped by the five treatments. These results indicate clearly that S. lineatus produces an aggregation pheromone in the spring. In c o m m o n with most curculionids, it is male-produced (see references cited in the Introduction). However, in the experiment reported here, the possibility that some of the bean volatiles synergized the activity of the male-produced pheromone cannot be excluded. Indeed, we have independent evidence that the three synthetic bean volatiles, (Z)-3-hexen-l-ol, (Z)-3hexen-l-yl acetate, and linalool, synergize the male-produced attractant, 4methyl-3,5-heptanedione (Blight et al., 1984). There was no evidence that female S. lineatus produced any semiochemical, although they may do so at other times of the year. Females of some curculionids, viz., A. grandis and Cylasformicarius elegantulus (Coffelt et al., 1978) produce a sex pheromone. In the case of A. grandis, it has weak attractancy compared to the male-produced aggregation pheromone (McKibben et al., 1977). However, the aggregation pheromone apparently functions mainly as a sex attractant after the insects are established on the host plants (Lloyd et al., 1983). A similar situation could exist with S. lineatus (Blight and Wadhams, unpublished). The adaptive significance of an aggregation pheromone in these weevils is not clear. It has been suggested (Shorey, 1973) that coleopteran aggregation pheromones arose initially as mechanisms by which insects could cause others of the same species to aggregate at a suitable food source. The male-produced
738
BLIGHT AND WADHAMS
Sitona pheromone presumably does assist the aggregation of the weevils in legume fields for the purposes of both feeding and mating. However, in this artificial monoculture it must be of far less importance to survival than in an environment comprising widely scattered food resources. Acknowledgments--We thank J. McEwen and R. Moffitt for their help and cooperation with the field experiment, T. Dixon for statistical analyses, and J. Steinmann and M.C. Smith for technical assistance.
REFERENCES ANDERSEN, K.T. 1931. Der linierte Graufiissler oder Blattrandkfifer, Sitona lineata L. Monogr. Pflanzenschutz, 6:88 pp. Julius Springer, Berlin. BARDNER, R., FLETCHER, K.E., and GRIFFITHS, D.C. 1983. Chemical control of the pea and bean weevil, Sitona lineatus L. and subsequent effects on the yield of field beans Vicia faba L. J. Agric. Sci. Camb. 101:71-80. BOOTH, D.C., PHILLIPS,T.W., CLAESSON,A., SILVERSTEIN,R.M., LANIER,G.N., and WEST, J.R. 1983. Aggregation pheromone components of two species of Pissodes weevils (Coleoptera: Curculionidae): Isolation, identification and field activity. J. Chem. Ecol. 9:1-12. BLIGHT, M.M., PICKETT, J.A., SMITH, M.C., and WADHAMS,L.J. 1984. An aggregation pheromone of Sitona lineatus. Identification and initial field studies. Naturwissenschaften 71:480481. COFFELT, J.A., VICK, K.W., SOWER, L.L., and MCCLELLAN, W.T 1978. Sex pheromone of the sweet potato weevil, Cylas formicarius elegantulus: Laboratory bioassay and evidence for a multiple component system. Environ. Entomol. 7:756-758. EL-LAFI, A.M. 1977. The economic injury level of the pea leaf weevil Sitona lineatus (L.) in northern Idaho and eastern Washington. Ph.D. thesis. University of Idaho. FONTAINE, M.S., and FOLTZ, J.L. 1982. Field studies of a male-released aggregation pheromone in Pissodes nemorensis. Environ. Entomol. 11:881-883. HANS, H. 1959. Beitr/ige zur Biologie von Sitona lineatus L. Z. Angew. Entomol. 44:343-386. HARDEE, D.D., CROSS, W.H., and MITCHELL, E.B. 1969. Male boll weevils are more attractive than cotton plants to boll weevils. J. Econ. Entomol. 62:165-169. HOEBEKE, E.R., and WHEELER, A.G. 1985. Sitona lineatus (L.), the pea leaf weevil: First records in eastern North America (Coleoptera: Curculionidae), Proc. Entomol. Soc. Wash. 87:216220. JACKSON, D.J. 1920. Bionomics of weevils of the genus Sitones injurious to leguminous crops in Britain. Ann. Appl. Biol. 7:269-298. LEGGETT,J.E., CROSS,W.H., MITCHELL,H.C., JOHNSON, W.L., and McGOVERN,W.L. 1975. Improved traps for capturing boll weevils. J. G. Entomol. Soc. 10:52-61. LLOYD, E.P., MCKIBBEN, G.H., LEGGETT, J.E., and HARTSTACK, A.W. 1983. Pheromones for survey, detection, and control, p. 183, in R.L. Ridgway, E.P. Lloyd, and W.H. Cross (eds.). Cotton Insect Management with Special Reference to the Boll Weevil. U.S. Department of Agriculture, Agriculture Handbook, No. 589. McKIBBEN, G.H., HEDIN, P.A., McGOVERN, W.L., WILSON, N.M., and MITCHELL, E.B. 1977. A sex pheromone for male boll weevils from females. J. Chem. Ecol. 3:331-335. SHOREY, H.H. 1973. Behavioral responses to insect pheromones. Annu. Rev. Entomol. 18:349380.
AGGREGATION PHEROMONE 1N WEEVILS
739
TUMLINSON, J.H., HARDEE, D.D., GUELDNER, R.C., THOMPSON, A.C., HEDIN, P.A., and MINYARD, J.P. 1969. Sex pheromones produced by male boll weevil: isolation, identification and synthesis. Science 166:1010-1012. WALGENBACH,C.A., PHILLIPS,J.K., FAUSTINI, D.L., and BURKHOLDER, W,E. 1983. Male-produced aggregation pheromone of the maize weevil, Sitophilus zeamais, and interspecific attraction between three Sitophilus species. J. Chem. Ecol. 9:831-841.
