Journal of Chemical Ecology, Vol. 7, No. 3, 1981



R. M I L L E R


K. H A A R E R

Department of Entomology and Pesticide Research Center Michigan State University East Lansing, Michigan 48824 (Received June 23, 1980; revised August 21, 1980) The attractancy of enzymatic yeast hydrolysate, a corn hydrolysate, brewers' yeast, boney, ammonia, n-dipropyl disulfide, and several combinations of these treatments was tested in an onion field containing onion flies, Hylemya antiqua (Meigen) and seedcorn flies, H. platura (Meigen). Enzymatic yeast hydrolysate (concentrated powder) proved to be highly attractive to both fly species; females were more responsive than males. Brewers' yeast and corn hydrolysate were intermediately attractive, while all other treatments were only slightly or not at all attractive. Although no steps were taken to prolong release of volatiles, some of the nutritious materials remained highly attractive even after 11 days. The yeast products may, at certain times, be even more attractive than specific host volatiles. However, their activity was not constant over time and may be influenced by the stage of reproductive development of female flies. Abstract

Key Words--Onion fly, ttylernya antiqua, seedcorn fly, ttylemya platura, Diptera, Anthomyiidae, yeast hydrolysates, brewers' yeast, food attractants.

INTRODUCTION Investigations into the chemical stimuli which mediate host finding by the o n i o n fly, H y l e m y a antiqua ( D i n d o n i s a n d M i l l e r , 1980, 1 9 8 1 a - c ) , h a v e s h o w n t h a t flies o f b o t h s e x e s a r e a t t r a c t e d b y d a m a g e d a n d d e c o m p o s i n g

IDiptera: Anthomyiidae 2Paper No. 9511 of the Michigan State University Agricultural Experiment Station. 555 0098-0331/81/0500-0555503.00/09 1981PlenumPublishingCorporation



onions as well as high release rates (mg/hr) of certain synthetic constituents of onions. Moreover, upon arriving at sources of damaged and decomposing onions, onion flies were observed to feed for extended periods (Dindonis and Miller, 1981a). The question arose as to how various food attractants which were not host-related might compare to specific host odors as potential baits for H. antiqua monitoring traps. We report here results of field tests on the comparative attractiveness of various foodstuffs to H. antiqua as well as to the seedcorn fly, H. platura, which coinhabited the onion field under study. M E T H O D S AND M A T E R I A L S

Experimental Design. Materials to be evaluated for attractiveness to flies were placed under acetate cone traps (Dindonis and Miller, 1980) deployed along the edges of an H. antiqua-infested commercial onion field in Stockbridge, Michigan. Either 30% aqueous ethylene glycol or 0.5% Triton X solutions was used as an ensnarement medium in the traps. A linearly arranged randomized complete-block design (see Dindonis and Miller, 1980 for justification) with a 3- to 4-m intertrap spacing was used with four replicates in each experiment. Experiment 1. The treatments, dispensed in 60-ram plastic petri dishes covered with 30 rnesh/cm cotton fabric, were: (1) EYH, enzymatic yeast hydrolysate (NBC, Cleveland, Ohio) (10 g of solid concentrate); (2) BY, brewers' yeast (Bio-Serv, Inc., Frenchtown, New Jersey) (10 g solid concentrate); (3) MB, Miller 3787 Insecticide Bait (10 ml of liquid concentrate) which is an acid-catalyzed hydrolysis product derived from corn (Miller Chemical and Fertilizer Corporation, Hanover, Pennsylvania); (4) H, honey (Michigan Harvest Honey, Lowell, Michigan) (10 ml concentrate liquid); (5-8) EYHS, BYS~ MBS, and HS which were 10 ml of 10% solutions of each respective substance above in 5% aqueous sucrose; (9) n-Pr2S2, n-dipropyl disulfide (>99% pure by GLC) (Eastman Organic Chemicals, Rochester, New York) dispensed from a saturated size 3 BEEM TM polyethylene enclosure (Dindonis and Miller, 1981b); (10) C1, a control, 10 ml of 5% aqueous sucrose solution; and (11) C2, a control consisting of an empty dispenser dish. EYH, BY, and H were selected because they elicited significant aggregation of H. antiqua at feeding dishes in laboratory studies (Niemczyk, 1965; McLeod, 1964); moreover, yeast products are known to be attractive to other fly species, e.g., the Caribbean fruit fly, Anastrepha suspensa (Lopez et al., 1971), and the apple maggot fly, Rhagoletispomonella (Neilson, 1960). Likewise, corn and other plant hydrolysates have been known to attract insects. The sucrose solutions of each of the treatments were meant to: (I) lower the release rate of volatiles from each substance, and (2) promote



microbial activity, e.g., ethanol release by the live yeasts, n-Pr2S2 was included because it could be released at a steady rate (Dindonis and Miller, 1980b), and hence this treatment (as well as the controls) served as a reference point for fly activity over time. Experiment l, was conducted July 30 to August 10, 1979. Flies were collected after 1, 2, 3, 4, 7, and 11 days and traps were rerandomized within blocks on day 3. Experiment 2. If microorganisms were to colonize the proteinaceous foodstuffs, one of the likely end products of amino acid catabolism would be ammonia, which is itself attractive to certain flies, e.g., the apple maggot fly (Hodson, 1943; Oatman, 1964; Moore, 1969). In a second experiment, 5% household a m m o n i a (NH3) was evaluated for attractancy to H. antiqua and H. platura. Also, trap catches elicited by the combinations o f E Y H + n-PrzS: and n-Pr2S: + NH3 were compared to those of each material tested separately. Combinations were achieved by placing separate dispensers for each material under one trap. Experimental procedures were similar to those of experiment 1. This test was conducted August 17-24, 1979, during which time baits were replenished as necessary. RESULTS

Experiment 1. The average catches of onion and seedcorn flies over the 11 days of this test are presented in Table 1. Overall, the patterns in catch were very similar for the two species. The most highly attractive material for females of both fly species was EYH; catches were more than double those of any other treatments and were 17 and 27 times the control catches for H. antiqua and H. platura females, respectively. BY, MB, and the diluted yeast products (BYS and EYHS) were all similarly attractive to onion fly females, producing catches ca. 6 times the control. In this test, H, MBS, HS, and surprisingly, n-Pr2S2, did not catch significantly more female H. antiqua than the control 5% sucrose solution. Likewise, BY, BYS, EYHS, as well as MB and MBS, were intermediately to slightly attractive to H. platura females while H, HS, and n-Pr2S2 were not attractive. The materials most attractive to onion fly males were BYS and BY, followed by EYH. However, these treatments did not, on the average, elicit stronger responses from males than females (Table 1). Few H. platura males were caught; however, the yeast products and MB did catch numbers distinguishable from controls. Judging from catches by the controls and unattractive treatments, the male-female ratios for H. antiqua and H.platura in this field were ca. 1 : 1 and 6 : 1, respectively. EYH was clearly more attractive to the females than males, while EYHS and MB also caught significantly more 11. antiqua females than



Mean number of flies caught per treatment b

Hylemya antiqua Treatments ~ 1. Enzymatic yeast hydrolysate (EYH) 2. Brewers' yeast (BY) 3. Miller insecticide bait (MB) (corn hydrolysate) 4. Honey (H) 5. Dilution of 1 (EYHS) 6. Dilution of 2 (BYS) 7. Dilution of 3 (MBS) 8. Dilution of 4 (HS) 9. n-Dipropyl disulfide (n-Pr2S2) 10. 5% sucrose solution (control 1) 11. Empty dispenser (control 2)

Hylemya platura









191a 74b

27bc 38ab

218a l12b

7.1a 2.0bcd

54a 22b

5a 3ab

59a 25b

10.8c 7.3

19cde t0ef 2led 45a 14def 12def

76c 23e 81c 126b 44d 27de

3.0b 1.2d 2,9bc 1,8cd 2.1bcd 1.3d

1lc 4d 24b 21b 10c 2d

2b lbc 2b 3ab 0.5bc 0.3c

13c 5d 26b 24b llc 2d

5.5 4.0 12.0 7.0 20.0 6.7

57c 12cd 60b 81b 30c 15cd 23c
























~See Methods section for a complete description of treatments. bMeans followed by the same letters within columns are not statistically different at the 5% level as determined by a planned F test for mean separation of data transformed to (X + 0.5) 1/2 for trap catches and log (X + 0.5) for sex ratios. CThe large number of zero catches for H.platura males precluded accurate statistical analysis of sex ratios.

males. A l t h o u g h t h e l o w c a t c h e s o f m a l e 11. platura p r e c l u d e d a c c u r a t e analysis o f sex r a t i o s for this species, t h e r e was a t r e n d t o w a r d e l e v a t e d f e m a l e catches for EYH, EYHS, and possibly MBS. T h e p a t t e r n s in f e m a l e H. antiqua c a t c h o v e r t i m e are p r e s e n t e d in F i g u r e 1. O n d a y 1, b o t h E Y H a n d BY w e r e h i g h l y a t t r a c t i v e . By d a y 2, the a t t r a c t i v e n e s s o f BY r e l a t i v e to t h e o t h e r t r e a t m e n t s was g r e a t l y r e d u c e d w h i l e t h e r e l a t i v e a t t r a c t i v e n e s s o f B Y S b e g a n to i n c r e a s e significantly, p e a k i n g at d a y 3 for b o t h f e m a l e s a n d males. A t this time, yeasts w e r e a c t i v e a n d e t h a n o l c o u l d be d e t e c t e d by t h e h u m a n nose. T h e c a t c h o f o n i o n fly f e m a l e s by E Y H d e c l i n e d o v e r the first 4 days b u t t h e n stabilized. It c a n n o t be c o n c l u d e d t h a t this decline r e p r e s e n t e d r e d u c e d a t t r a c t i v e n e s s only; as j u d g e d f r o m c a t c h e s by the c o n t r o l s a n d u n a t t r a c t i v e t r e a t m e n t s , fly a c t i v i t y also d e c l i n e d initially a n d s u b s e q u e n t l y r o s e slightly.



At all times, EYH caught significantly more flies than any other treatment, and after 11 days, it was still catching at the rate of tO times the control. For H. platura, attractive materials maintained activity over the l 1 days with only slight declines. There were no clear increases in the attractiveness of any treatments with respect to the others. Experiment 2. Five percent NH3 proved to be unattractive to H. antiqua females and males (Table 2). In this experiment, n-PrzS2 was significantly attractive to H. antiqua females but not males. Addition of NH3 to n-Pr2S2 did not increase catch significantly for females but did so for males. During experiment 2, EYH was not significantly more attractive to female H. antiqua than n-PrzS2; trap catches by EYH were only 8 times the control rather than 17 as in experiment 1. Also, the sex ratio for the EYH catch did not highly favor females; however, fewer females than males were caught in the control traps. Addition of n-Pr2S2 to EYH did not increase catch over EYH alone. For H. platura, NH3 proved to be significantly repellent. However, this effect was not apparent when n-Pr2S2 and NH3 were combined. EYH trap


5O tm

.~ 2c Z U.l












FIG. 1. Patterns in female onion fly trap catch as elicited by various nutritious materials over time. Points between 5 and 7 and 8 and 11 days are averages for those periods.




Mean number of flies caught per treatment a

Hylemya antiqua

Hylemya platura b






1. Ammonia (NH3) 2. n-Dipropyl disulfide (n-PrzS2) 3. 1 + 2 4. Enzymatic yeast hydrolysate (EYH) 5. 4 + 2 6. Unbaited





28b 37ab

20b 36a

1.4a 1.0ab

3d 4cd

4lab 53a 5c

33ab 32ab 12be

1.2a 1.7a 0.4c

24a 1lb 4cd

Means followed by the same letters within columns are not statistically different at the 5% level as determined by a planned Ftest for mean separation of data transformed to (X + 0.5) 1/2for trap catches and to log (X + 0.5) for sex ratios. bA total of four male H. platura were caught, precluding both statistical analyses for males and establishment of sex ratios. catch was only 8 times the c o n t r o l c o m p a r e d to 27 in e x p e r i m e n t 1. A d d i t i o n of n-Pr2S2 to E Y H caused a significant r e d u c t i o n in catch for H. platura.


Several of the n u t r i t i o u s materials included in these e x p e r i m e n t s yielded large catches of o n i o n a n d seedcorn flies in the field; hence, they d o offer p o t e n t i a l as baits for m o n i t o r i n g traps. P r e l i m i n a r y o b s e r v a t i o n s in the field suggest t h a t volatiles f r o m the nutritious m a t e r i a l s elicited fly b e h a v i o r s very similar to those elicited by c h o p p e d onions, i.e., a series o f positive taxes (most likely a n e m o t a x e s ) p u n c t u a t e d by p e r i o d s of resting on the substrate ( D i n d o n i s a n d Miller, 1981a). Hence, volatiles f r o m these m a t e r i a l s such as E Y H p r o b a b l y serve as long-range a t t r a c t a n t s in the field as well as arrestants a n d s h o r t - r a n g e a t t r a c t a n t s as d o c u m e n t e d by the l a b o r a t o r y cage experiments of N i e m c z y k (1965). The r e a s o n for o n i o n fly responsiveness to these materials is m o s t certainly n u t r i t i o n a l . In the lab, vitellogenesis c a n n o t occur w i t h o u t an e x o g e n o u s source o f p r o t e i n ( M c L e o d , 1964). F u r t h e r m o r e , certain p r o t e i n sources ( m i c r o n u t r i e n t s might also be involved) are clearly s u p e r i o r to others in p r o m o t i n g oogenesis. F o r H. antiqua, brewers' yeast a n d yeast h y d r o l y s a t e ( a p p a r e n t l y n o t enzymatic) were s u p e r i o r to soya flour or a m i x t u r e of



brewers' yeast and soya flour (McLeod, 1964). Moreover, in the lab, the foodstuffs most adaptive for egg production seemed to elicit the largest aggregations in feeding dishes and the most prolonged feeding (McLeod, 1964; Niemczyk, 1963). In the field, female onion flies must likewise secure exogenous protein. The strong selection pressure to do so should, over time, lead to the development of finely tuned physiologic mechanisms for efficient finding of optimal protein sources. The pattern in attractiveness of the various nutritious materials that emerged from the present field experiments with H. antiqua is essentially consistent with the pattern in feeding preferences found in the lab (Niemczyk, 1965). In both cases EYH was the most stimulatory material, especially for females. Materials such as BY and acid corn hydrolysates promoted significantly less feeding in the lab and less long-range orientation in the field. While honey appeared to be a fairly good short-range "attractant" in the lab, it was totally inactive in our field experiment. Although more tests need to be conducted to determine which materials are most effective at promoting oogenesis (EYH should be compared to BY), it appears that H. antiqua is most attracted to the odors from protein sources that would be maximally adaptive reproductively. The work of Niemczyk (1965) would further suggest that the attractiveness of EYH to H. antiqua females might vary with time. In the lab, newly eclosed flies do not aggregate on EYH dishes; however, by ca. day 3, strong aggregation on this material is noticed and it lasts until ca. day 12, peaking at day 8. Males are fairly uniformly responsive to EYH. Hence, as age structure within a fly population changes, responsiveness to EYH could rise or fall. Possibly, this happened between experiments 1 and 2 of this study, for identical EYH sources were comparatively less attractive to females during experiment 2. The variability in attractiveness of n-Pr2S2 is harder to explai_n. In all our previous experiments (Dindonis and Miller, 1981c, and references therein), one capsule filled with this compound was significantly attractive to both male and female onion flies. The field in which the present experiments were conducted contained large numbers of damaged and maggot-infested onions, especially during experiment 1. Possibly, a high background of host volatiles masked the n-Pr2S2 plumes in a manner equivalent to the disruption of pheromone communication by the atmospheric permeation technique. Since certain foodstuffs like EYH seem to be as attractive to H. antiqua (if not more so) as any of the host cues so far investigated, the chemistry of their volatiles should be explored. Perhaps, as suggested for the case of green lacewing, Chrysopa carnea, attraction to protein hydrolysates (Hagen et al., 1976; van Emden and Hagen, 1976), the active constituents, may be volatile degradation products of certain amino acids like tryptophan. Syn-



t h e t i c E Y H v o l a t i l e s s h o u l d b e u s e f u l t o o l s in m o n i t o r i n g H . a n t i q u a a n d H. p l a t u r a as well as o t h e r i n s e c t p o p u l a t i o n s . I n t h e i n t e r i m , t h e p o w d e r e d concentrates may be useful baits. Acknowledgments--We wish to thank J. Behm for technical assistance and the Michigan Onion Committee for funding. This work was also supported by a USDA Competitive Grant, Agreement No. 5901-0410-9-0229-0.

REFERENCES DINDONIS, L.L., and MILLER,J.R. 1980. Host-finding responses of onion and seedcorn flies to healthy and decomposing onions and several synthetic constituents of onion. Environ. Entomol. 9:467-472. DINDONIS, L.L., and MILLER, J.R. 1980a. Host-finding behavior of onion flies. Environ. Entomol. In press. DINDONIS, L.L., and MILLER, J.R. 1980b. Onion fly trap catch as affected by release rate of n-dipropyl disulfide from polyethylene Enclosures. J. Chem. Ecol. 7:413-420. DINDONIS, L.L., and MILLER, J.R. 1980c. Onion fly and little house fly host finding selectively mediated by decomposing onion and microbial volatiles. J. Chem. Ecol. 7:421-428. EMDEN, J.F. VAN, and HACEN, K.S. 1976. Olfactory reactions of the green lacewing, Chrysopa carnea, to tryptophan and certain breakdown products. Environ. Entomol. 5:469-473. HAGEN, K.S., GREANY, P., SAWALL, E.F., Jr., and TASSAN, R.L. 1976. Tryptophan in artificial honeydews as a source of an attractant for adult Chrysopa carnea. Environ. Entomol. 5:458-468. HODSON, A.C. 1943. Lures attractive to the apple maggot. J. Econ. Entomol. 36:545-548. LoPEZ-D., F., STEINER, L.F., and HOLBROOK, F.R. 1971. A new yeast hydrolysate-borax bait for trapping the Caribbean fruit fly. J. Econ. Entomol. 64:1541-1543. McLEoD, D.G.R. 1964. Nutrition and feeding behavior of the adult onion maggot, Hylemya antiqua. J. Econ. EntomoL 57:845-847. MOORE, R.C. 1969. Attractiveness of baited and unbaited lures to apple maggot and beneficial flies. J. Econ. Entomol. 62:1076-1078. NEILSON, WIT.A. 1960. Field tests of some hydrolyzed proteins as lures for the apple maggot, Rhagoletis pomonella (Walsh). Can. EntomoL 92:464-467. N1EMCZYK, H.D. 1965. The response of Hylemya antiqua adults to hydrolyzed proteins and other materials: A laboratory study. J. Econ. Entomol. 58:425-428. OATMAN, E.R. 1964. Apple maggot trap and attractant studies. Z Econ. Entomol. 57:529-531.

Yeast and corn hydrolysates and other nutritious materials as attractants for onion and seed flies.

The attractancy of enzymatic yeast hydrolysate, a corn hydrolysate, brewers' yeast, honey, ammonia,n-dipropyl disulfide, and several combinations of t...
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