Journal of Chemical Ecology, Vol. 13, No. 5, 1987
Short Communication
EFFECTS OF NONHOST-PLANT ODORS ON ANEMOTACTIC RESPONSE TO HOST-PLANT ODOR IN FEMALE CABBAGE ROOT FLY, Delia radicum, AND CARROT RUST FLY, Psila rosae
S.F. N O T T I N G H A M Department of Applied Biology, University of Cambridge, Cambridge, U.K.
(Received January 28, 1986; accepted July 16, 1986) Abstract--An inflatablepolythene wind tunnel was used for behavioral assays of.female D. radicum and P. rosae in diffuse host- and non-host-plant odor, alone and in combination. Host-plant odor caused an upwind anemotactic response in both species. Changes in fly distribution, relative to wind direction, occurred when onion odor was combined with host odor for D. radicum and P. rosae, and when sage odor was combined with carrot ordor for P. rosae. The assay has potential for screening volatiles for their behavior-modifyingeffects, Key Words--Cabbage root fly, Delia radicum, carrot rust fly, Psila rosae, Diptera, Anthomyiidae,Psilidae,odor-inducedupwindanemotaxis,host-plant odor, non-host-plantodor.
INTRODUCTION The cabbage root fly, D e l i a r a d i c u m L. (Diptera; Anthomyiidae) and the carrot rust fly, P s i l a r o s a e Fab. (Diptera; Psilidae) have host plants within the Cruciferae and Umbelliferae, respectively. Each plant family has a distinctive plant chemistry (Kjaer, 1976; Harbourne, 1971) that is involved in the host-plant location and oviposition behavior of D. r a d i c u m (Finch, 1980; St/idler, 1978) and P. r o s a e (Guerin et al., 1983; St/idler and Buser, 1984). Gravid female D. r a d i c u m responded anemotactically to host-plant odor and allylisothiocyanate 1313 0098-0331/87/0500-1313505.00/0 Q 1987 Plenum Publishing Corporation
1314
NOTTINGHAM
(Hawkes et al., 1978; Nottingham and Coaker, 1985). Propyl-benzenes from Umbellifarae attracted female P. rosae (Guerin et al., 1983), but anemotactic responses have not been demonstrated. Both species were less exploitive of their host plants in diverse than simple plant plots in field experiments (Tukahirwa and Coaker, 1982; Uvah and Coaker, 1984), with onion odor being important in suppressing numbers of P. rosae. The objectives of this study were (1) to establish whether P. rosae responded anemotactically to host-plant odor and (2) to adapt the behavioral assay (Jones et al., 1981; Nottingham and Coaker, 1985) to observe any behaviormodifying effects of non-host-plant odors. METHODS AND MATERIALS
A series of behavioral assays presenting diffuse odor from host and nonhost plants, both singly and combined, were done with female D. radicum and P. rosae in an inflatable polythene wind tunnel (Jones et al., 1981). The wind tunnel, 0.5 m diameter, with a 2-m-long flight chamber, was constructed from layflat plastic tubing supported by two metal hoops placed at each end of the flight chamber and covered with metal honeycomb (1 cm diameter), wire mesh (0.1 mm), and muslin. The tube was inflated by fans connected at each end and adjusted to give a wind speed of 0.3 m/sec. The tunnel was erected in a controlled environment room maintained at 22 ~ 65 % relative humidity, and illuminated by overhead fluorescent tubes providing 1500 lux within the tunnel. Ammonium chloride smoke mixed thoroughly with the air in the treatment chamber and passed uniformly through the first screen into the flight chamber. The host plants used were cabbage (Brassica oleracea var. capitata cv. Primo) and carrot (Daucus carota cv. Danvers), for D. radicum and P. rosae, respectively. The non-host plants used were onions (Allium cepa var. Rhijneburger robusta) and sage (Salvia officialis). All the plants were grown under greenhouse donditions. Ten grams of 1 to 2-month-old cabbage plants or 75 g of carrot plants of similar age were presented alone and together with the same weight of non-host plants of the same age. Odorless control treatments were included. The plants were put into 100-ml glass beakers containing about 10 ml of water, with the foliage exposed above the rim of the beaker, and the beaker was placed on a tripod, within the treatment chamber, 20 cm from the first screen. In combined odor treatments, beakers containing host and non-host plants were arranged side-by-side on the tripod. In each of the three replicates of the assay treatments, approximately 15 six- to nine-day-old mated and gravid female D. radicum or P. rosae were released from the center of the flight chamber after preconditioning for 2 hr in the release cage within the tunnel in the absence of odor. The release cage
EFFECTS OF NON-HOST-PLANT ODORS ON FLIES
1315
consisted of a 15 x 5-cm glass tube enclosed at each end with muslin and suspended 20 cm from the tunnel floor. The flies were released 15 sec after the introduction of the treatment odor by gently removing the muslin from both ends of the tube. The flies' response was scored by counting the number of flies in the upwind, middle, and downwind thirds of the flight chamber 5 rain after their release. The data for the mean percentage of flies in each third of the flight chamber were analysed by chi-square contingency tables, done for paired treatments within each group of four treatments comprising odorless control, host odor and non-host odor alone, and host and non-host odor combined.
RESULTS AND DISCUSSION
Response to Host-Plant Odor. The odorless control elicited similar percentages of D. radicum in the upwind and downwind sections (18 and 21%), respectively; whereas the distribution of flies in the cabbage treatment was different from the odorless control (P < 0.01), with more than twice the percentage of flies in the upwind than the downwind section (44 vs. 19%) (Table 1). This upwind anemotactic response supports previous findings that host odor stimulates upwind movement (e.g., Hawkes et al., 1978). The odorless control elicited similar percentages of P. rosae in the upwind and downwind sections (18 vs. 22%); whereas the distribution of flies in the carrot treatment was different from the odorless control (P < 0.01), with more flies in the upwind than the downwind section (45 vs. 5.5 %) (Table 1). Host-plant volatiles attracted female P. rosae in the laboratory and the field (Guefin et al., 1983), and the present results suggest that they also initiated an upwind anemotactic response, which may be important in its host-finding behavior. Effects of Non-Host-Plant Odor on Behavioural Response to Host-Plant Odor. The distribution of D. radicum in the onion and cabbage plus onion treatments was not different from the odorless control (P > 0.01). The distribution of flies in the cabbage treatment, however, was different from that in the cabbage plus onion odor treatment (P < 0.01), with the combined odor eliciting a lower percentage of flies in the upwind section (26 vs. 44%) and an increased percentage in the middle section (63 vs. 37 %) compared to cabbage odor alone (Table 1). The distribution of flies in the cabbage plus sage treatment, on the other hand, was not different from that in the cabbage treatment (P > 0.01) (Table 1). The presence of clover odor was not thought to be an important factor causing the decreased exploitiveness of D. radicum when it was grown with host plants (Tukahirwa and Coaker, 1982); however, the present results suggest
_+ 0.3 + 0.5 • 2.4 • 1.9 • 1.4 _+ 0.5
• 0.5 +_ 0.7 • 0.7 _+ 0.5 • 0.3 _+ 0.5
12.7 14.3 14.7 15.4 13.0 17.0
11.0 12.7 14.4 17.7 11.7 16.3
2.0 5.7 3.7 5.0 2.7 4.0
2.3 6.3 3.0 4.0 3.3 5.3 _+ 0.5 _+ 0.9 • 0.3 + 0.5 _+ 1.0 + 0.5
+_ 0.7 • 0.3 • 0.5 • 0.5 _+ 0.7 ___ 0.5
No. flies (•
18.2 44.8 25.7 28.2 23.1 24.5
18.1 44.1 20.4 26.0 25.4 31.2
Mean %
6.7 6.3 8.0 9.0 8.0 10.0
7.7 5.3 10.7 9.7 8.0 10.0 _+ 0.3 _+ 1.1 _+ 1.2 • 0.9 • 0.5 _+ 1.4
_+ 0.5 • 0.3 • 1.8 • 1.6 _+ 0.8 _+ 0.8
No. flies (_+SE)
61.9 49.6 55.5 51.8 68.4 61.3
60.6 37.0 72.8 63.0 61.5 58.8
Mean %
Middle third
2.3 0.7 2.7 3.7 1.0 2.3
2.7 2.7 1.0 1.7 1.7 1.7
• 0.3 • 0.3 + 0.7 _+ 0.7 • 0.8 _+ 0.5
_+ 0.3 -I- 0.5 • 0.5 _+ 0.3 + 0.3 + 0.3
21.9 5.5 18.8 20.0 8.5 14.1
21.3 18.9 6.8 11.0 13.1 10.0
Mean %
Downwind third No. flies (_+SE)
~Treatments with different letters have significantly different distributions of flies (P = 0.01 chi-square). (N = 3 for all treatments).
Female D. radicum Odorless control (a) Cabbage (b) Onion (a) Cabbage + onion (a) Sage (a) Cabbage + sage (ab) Female P. rosae Odorless control (a) Carrot (b) Onion (a) Carrot + onion (a) Sage (a) Carrot + sage (a)
No. flies (+_SE)
Upwind third
DIFFUSE ODOR FROM HOST AND NoN-HOST PLANTS, PRESENTED SINGLY AND COMBINED.
TABLE I. NUMBER OF FLIES AND MEAN PERCENTAGE OF FLIES IN UPWIND, MIDDLE, AND DOWNWIND SECTIONS OF FLIGHT CHAMBER IN
EFFECTS OF NON-HOST-PLANT ODORS ON FLIES
1317
that certain non-host odors (e.g., onion) may be capable of modifying aspects of D. radicum's host-location behavior. The distribution of P. rosae in the onion, carrot plus onion, sage, and carrot plus sage treatments was not different from the odorless control (P > 0.01). However, the distributions of flies from both the carrot plus onion and the carrot plus sage treatments were different from the carrot treatment (P < 0.01), with lower percentages in the upwind section in the carrot plus onion (28%) and carrot plus sage (24.5%) than in the carrot treatment (45%) and higher percentages in the middle and downwind sections (Table 1). Onions intercropped with carrots were successful in reducing carrot fly damage only when they were young and actively growing (Uvah and Coaker, 1984) which, together with the present data, suggests that onion odor modifies aspects of P. rosae's host-plant-finding behavior. Sage also affected movement with respect to the wind, suggesting that other non-host odors might be effective at modifying the behavior of P. rosae in a similar way. Further Development of Assay. Further work should incorporate a wider selection of non-host-plant odors together with a range of host to non-host ratios. A larger number of replicates would also be desirable. The results of these preliminary experiments with non-host odors suggest that a behavioral assay of this type might provide a basis for screening odors for their effectiveness in modifying the behavior of insects that use host-plant odor to locate their host plants. This could not only provide a rationale for selecting intercrops to suppress certain insect pests, but, probably more importantly for future insect pest control, also identify non-host volatiles which could be used in the field to modify insect behavior. Acknowledgments--I would like to thank Dr. T.H. Coaker for advice and Mrs. M. Free for technical assistance. This work was supported by a Science and Engineering Research Council Studentship.
REFERENCES FINCH, S. 1980. Chemical attraction of plant-feeding insects to plants. Appl. Biol. 5:67-143. GUER~N, P.M., STADLER, E., and BUSER, H.R. 1983. Identification of host-plant attractants for the carrot fly Psila rosae. J. Chem. Ecol. 9:843-861. HARBOURNE, J.B. 1971. Flavenoid and phenylpropanoid patterns in the Umbelliferae, pp. 293314, in V.H. Heywood (ed.). The Biology and Chemistry of the Umbelliferae. Academic Press, London. HAWKES, C., PATTON, S., and COAKER, T.H. 1978. Mechanisms of host-plant finding in adult cabbage root fly, Delia brassicae. Entomol. Exp. Appl. 24:219-227. JONES, O.T., LOMER, R.A., and Howsz, P.E. 1981. Responses of male Mediterranean fruit flies, Ceratitis capitata, to trimedlure in a wind tunnel of novel design. Physiol. Entomol. 6:175181. KJAER, A. 1976. Glucosinolates in the Cruciferae, pp. 207-219, in J.G. Vaughan, A.J. MacLeod, and B.M.G. Jones (eds.). The Biology of the Cruciferae. Academic Press, London.
1318
NOTTINGHAM
NOTTINGHAM, S.F., and COAKER, T.H. 1985. The olfactory response of cabbage root fly Delia radicum to the host plant volatile altylisothiocyanate. Entomol. Exp. Appl. 39:307-316. STADLER, E. 1978. Chemoreception of host-plant chemicals by ovipositing females of Delia brassicae. Entomol. Exp. Appl. 24:511-520. ST~,DLER,E., and BusE~, H.R. 1984. Defense chemicals in leaf surface wax synergistically stimulate oviposition by a phytophagous insect. Experientia 40:1157-1159. TUnAHmWA, E.M., and COAKER, T.H. 1982. Effect of mixed cropping on some insect pests of brassicas; reduced Brevicoryne brassicae infestations and influences on epigeal predators and the disturbance of oviposition behavior in Delia brassicae. Entomol. Exp. Appl. 32:129-140. UVAH, I.I.I., and COAKE~, T.H. 1984. Effect of mixed cropping on some insect pests of carrots and onions. Entomol. Exp. Appl. 36:159-167.
Short Communication
EFFECTS OF NONHOST-PLANT ODORS ON ANEMOTACTIC RESPONSE TO HOST-PLANT ODOR IN FEMALE CABBAGE ROOT FLY, Delia radicum, AND CARROT RUST FLY, Psila rosae
S.F. N O T T I N G H A M Department of Applied Biology, University of Cambridge, Cambridge, U.K.
(Received January 28, 1986; accepted July 16, 1986) Abstract--An inflatablepolythene wind tunnel was used for behavioral assays of.female D. radicum and P. rosae in diffuse host- and non-host-plant odor, alone and in combination. Host-plant odor caused an upwind anemotactic response in both species. Changes in fly distribution, relative to wind direction, occurred when onion odor was combined with host odor for D. radicum and P. rosae, and when sage odor was combined with carrot ordor for P. rosae. The assay has potential for screening volatiles for their behavior-modifyingeffects, Key Words--Cabbage root fly, Delia radicum, carrot rust fly, Psila rosae, Diptera, Anthomyiidae,Psilidae,odor-inducedupwindanemotaxis,host-plant odor, non-host-plantodor.
INTRODUCTION The cabbage root fly, D e l i a r a d i c u m L. (Diptera; Anthomyiidae) and the carrot rust fly, P s i l a r o s a e Fab. (Diptera; Psilidae) have host plants within the Cruciferae and Umbelliferae, respectively. Each plant family has a distinctive plant chemistry (Kjaer, 1976; Harbourne, 1971) that is involved in the host-plant location and oviposition behavior of D. r a d i c u m (Finch, 1980; St/idler, 1978) and P. r o s a e (Guerin et al., 1983; St/idler and Buser, 1984). Gravid female D. r a d i c u m responded anemotactically to host-plant odor and allylisothiocyanate 1313 0098-0331/87/0500-1313505.00/0 Q 1987 Plenum Publishing Corporation
1314
NOTTINGHAM
(Hawkes et al., 1978; Nottingham and Coaker, 1985). Propyl-benzenes from Umbellifarae attracted female P. rosae (Guerin et al., 1983), but anemotactic responses have not been demonstrated. Both species were less exploitive of their host plants in diverse than simple plant plots in field experiments (Tukahirwa and Coaker, 1982; Uvah and Coaker, 1984), with onion odor being important in suppressing numbers of P. rosae. The objectives of this study were (1) to establish whether P. rosae responded anemotactically to host-plant odor and (2) to adapt the behavioral assay (Jones et al., 1981; Nottingham and Coaker, 1985) to observe any behaviormodifying effects of non-host-plant odors. METHODS AND MATERIALS
A series of behavioral assays presenting diffuse odor from host and nonhost plants, both singly and combined, were done with female D. radicum and P. rosae in an inflatable polythene wind tunnel (Jones et al., 1981). The wind tunnel, 0.5 m diameter, with a 2-m-long flight chamber, was constructed from layflat plastic tubing supported by two metal hoops placed at each end of the flight chamber and covered with metal honeycomb (1 cm diameter), wire mesh (0.1 mm), and muslin. The tube was inflated by fans connected at each end and adjusted to give a wind speed of 0.3 m/sec. The tunnel was erected in a controlled environment room maintained at 22 ~ 65 % relative humidity, and illuminated by overhead fluorescent tubes providing 1500 lux within the tunnel. Ammonium chloride smoke mixed thoroughly with the air in the treatment chamber and passed uniformly through the first screen into the flight chamber. The host plants used were cabbage (Brassica oleracea var. capitata cv. Primo) and carrot (Daucus carota cv. Danvers), for D. radicum and P. rosae, respectively. The non-host plants used were onions (Allium cepa var. Rhijneburger robusta) and sage (Salvia officialis). All the plants were grown under greenhouse donditions. Ten grams of 1 to 2-month-old cabbage plants or 75 g of carrot plants of similar age were presented alone and together with the same weight of non-host plants of the same age. Odorless control treatments were included. The plants were put into 100-ml glass beakers containing about 10 ml of water, with the foliage exposed above the rim of the beaker, and the beaker was placed on a tripod, within the treatment chamber, 20 cm from the first screen. In combined odor treatments, beakers containing host and non-host plants were arranged side-by-side on the tripod. In each of the three replicates of the assay treatments, approximately 15 six- to nine-day-old mated and gravid female D. radicum or P. rosae were released from the center of the flight chamber after preconditioning for 2 hr in the release cage within the tunnel in the absence of odor. The release cage
EFFECTS OF NON-HOST-PLANT ODORS ON FLIES
1315
consisted of a 15 x 5-cm glass tube enclosed at each end with muslin and suspended 20 cm from the tunnel floor. The flies were released 15 sec after the introduction of the treatment odor by gently removing the muslin from both ends of the tube. The flies' response was scored by counting the number of flies in the upwind, middle, and downwind thirds of the flight chamber 5 rain after their release. The data for the mean percentage of flies in each third of the flight chamber were analysed by chi-square contingency tables, done for paired treatments within each group of four treatments comprising odorless control, host odor and non-host odor alone, and host and non-host odor combined.
RESULTS AND DISCUSSION
Response to Host-Plant Odor. The odorless control elicited similar percentages of D. radicum in the upwind and downwind sections (18 and 21%), respectively; whereas the distribution of flies in the cabbage treatment was different from the odorless control (P < 0.01), with more than twice the percentage of flies in the upwind than the downwind section (44 vs. 19%) (Table 1). This upwind anemotactic response supports previous findings that host odor stimulates upwind movement (e.g., Hawkes et al., 1978). The odorless control elicited similar percentages of P. rosae in the upwind and downwind sections (18 vs. 22%); whereas the distribution of flies in the carrot treatment was different from the odorless control (P < 0.01), with more flies in the upwind than the downwind section (45 vs. 5.5 %) (Table 1). Host-plant volatiles attracted female P. rosae in the laboratory and the field (Guefin et al., 1983), and the present results suggest that they also initiated an upwind anemotactic response, which may be important in its host-finding behavior. Effects of Non-Host-Plant Odor on Behavioural Response to Host-Plant Odor. The distribution of D. radicum in the onion and cabbage plus onion treatments was not different from the odorless control (P > 0.01). The distribution of flies in the cabbage treatment, however, was different from that in the cabbage plus onion odor treatment (P < 0.01), with the combined odor eliciting a lower percentage of flies in the upwind section (26 vs. 44%) and an increased percentage in the middle section (63 vs. 37 %) compared to cabbage odor alone (Table 1). The distribution of flies in the cabbage plus sage treatment, on the other hand, was not different from that in the cabbage treatment (P > 0.01) (Table 1). The presence of clover odor was not thought to be an important factor causing the decreased exploitiveness of D. radicum when it was grown with host plants (Tukahirwa and Coaker, 1982); however, the present results suggest
_+ 0.3 + 0.5 • 2.4 • 1.9 • 1.4 _+ 0.5
• 0.5 +_ 0.7 • 0.7 _+ 0.5 • 0.3 _+ 0.5
12.7 14.3 14.7 15.4 13.0 17.0
11.0 12.7 14.4 17.7 11.7 16.3
2.0 5.7 3.7 5.0 2.7 4.0
2.3 6.3 3.0 4.0 3.3 5.3 _+ 0.5 _+ 0.9 • 0.3 + 0.5 _+ 1.0 + 0.5
+_ 0.7 • 0.3 • 0.5 • 0.5 _+ 0.7 ___ 0.5
No. flies (•
18.2 44.8 25.7 28.2 23.1 24.5
18.1 44.1 20.4 26.0 25.4 31.2
Mean %
6.7 6.3 8.0 9.0 8.0 10.0
7.7 5.3 10.7 9.7 8.0 10.0 _+ 0.3 _+ 1.1 _+ 1.2 • 0.9 • 0.5 _+ 1.4
_+ 0.5 • 0.3 • 1.8 • 1.6 _+ 0.8 _+ 0.8
No. flies (_+SE)
61.9 49.6 55.5 51.8 68.4 61.3
60.6 37.0 72.8 63.0 61.5 58.8
Mean %
Middle third
2.3 0.7 2.7 3.7 1.0 2.3
2.7 2.7 1.0 1.7 1.7 1.7
• 0.3 • 0.3 + 0.7 _+ 0.7 • 0.8 _+ 0.5
_+ 0.3 -I- 0.5 • 0.5 _+ 0.3 + 0.3 + 0.3
21.9 5.5 18.8 20.0 8.5 14.1
21.3 18.9 6.8 11.0 13.1 10.0
Mean %
Downwind third No. flies (_+SE)
~Treatments with different letters have significantly different distributions of flies (P = 0.01 chi-square). (N = 3 for all treatments).
Female D. radicum Odorless control (a) Cabbage (b) Onion (a) Cabbage + onion (a) Sage (a) Cabbage + sage (ab) Female P. rosae Odorless control (a) Carrot (b) Onion (a) Carrot + onion (a) Sage (a) Carrot + sage (a)
No. flies (+_SE)
Upwind third
DIFFUSE ODOR FROM HOST AND NoN-HOST PLANTS, PRESENTED SINGLY AND COMBINED.
TABLE I. NUMBER OF FLIES AND MEAN PERCENTAGE OF FLIES IN UPWIND, MIDDLE, AND DOWNWIND SECTIONS OF FLIGHT CHAMBER IN
EFFECTS OF NON-HOST-PLANT ODORS ON FLIES
1317
that certain non-host odors (e.g., onion) may be capable of modifying aspects of D. radicum's host-location behavior. The distribution of P. rosae in the onion, carrot plus onion, sage, and carrot plus sage treatments was not different from the odorless control (P > 0.01). However, the distributions of flies from both the carrot plus onion and the carrot plus sage treatments were different from the carrot treatment (P < 0.01), with lower percentages in the upwind section in the carrot plus onion (28%) and carrot plus sage (24.5%) than in the carrot treatment (45%) and higher percentages in the middle and downwind sections (Table 1). Onions intercropped with carrots were successful in reducing carrot fly damage only when they were young and actively growing (Uvah and Coaker, 1984) which, together with the present data, suggests that onion odor modifies aspects of P. rosae's host-plant-finding behavior. Sage also affected movement with respect to the wind, suggesting that other non-host odors might be effective at modifying the behavior of P. rosae in a similar way. Further Development of Assay. Further work should incorporate a wider selection of non-host-plant odors together with a range of host to non-host ratios. A larger number of replicates would also be desirable. The results of these preliminary experiments with non-host odors suggest that a behavioral assay of this type might provide a basis for screening odors for their effectiveness in modifying the behavior of insects that use host-plant odor to locate their host plants. This could not only provide a rationale for selecting intercrops to suppress certain insect pests, but, probably more importantly for future insect pest control, also identify non-host volatiles which could be used in the field to modify insect behavior. Acknowledgments--I would like to thank Dr. T.H. Coaker for advice and Mrs. M. Free for technical assistance. This work was supported by a Science and Engineering Research Council Studentship.
REFERENCES FINCH, S. 1980. Chemical attraction of plant-feeding insects to plants. Appl. Biol. 5:67-143. GUER~N, P.M., STADLER, E., and BUSER, H.R. 1983. Identification of host-plant attractants for the carrot fly Psila rosae. J. Chem. Ecol. 9:843-861. HARBOURNE, J.B. 1971. Flavenoid and phenylpropanoid patterns in the Umbelliferae, pp. 293314, in V.H. Heywood (ed.). The Biology and Chemistry of the Umbelliferae. Academic Press, London. HAWKES, C., PATTON, S., and COAKER, T.H. 1978. Mechanisms of host-plant finding in adult cabbage root fly, Delia brassicae. Entomol. Exp. Appl. 24:219-227. JONES, O.T., LOMER, R.A., and Howsz, P.E. 1981. Responses of male Mediterranean fruit flies, Ceratitis capitata, to trimedlure in a wind tunnel of novel design. Physiol. Entomol. 6:175181. KJAER, A. 1976. Glucosinolates in the Cruciferae, pp. 207-219, in J.G. Vaughan, A.J. MacLeod, and B.M.G. Jones (eds.). The Biology of the Cruciferae. Academic Press, London.
1318
NOTTINGHAM
NOTTINGHAM, S.F., and COAKER, T.H. 1985. The olfactory response of cabbage root fly Delia radicum to the host plant volatile altylisothiocyanate. Entomol. Exp. Appl. 39:307-316. STADLER, E. 1978. Chemoreception of host-plant chemicals by ovipositing females of Delia brassicae. Entomol. Exp. Appl. 24:511-520. ST~,DLER,E., and BusE~, H.R. 1984. Defense chemicals in leaf surface wax synergistically stimulate oviposition by a phytophagous insect. Experientia 40:1157-1159. TUnAHmWA, E.M., and COAKER, T.H. 1982. Effect of mixed cropping on some insect pests of brassicas; reduced Brevicoryne brassicae infestations and influences on epigeal predators and the disturbance of oviposition behavior in Delia brassicae. Entomol. Exp. Appl. 32:129-140. UVAH, I.I.I., and COAKE~, T.H. 1984. Effect of mixed cropping on some insect pests of carrots and onions. Entomol. Exp. Appl. 36:159-167.
