AbstractâThe ability of both male and female Prostephanus truncatus beetles to distinguish between the aggregation pheromone signals of two closely located ...
Journal of Chemical Ecology, Vol. 26, No. 6, 2000
FUNCTION OF AGGREGATION PHEROMONE IN THE LARGER GRAIN BORER Prostephanus truncatus: VARIATION IN RESPONSE TO INDIVIDUALS AS EVIDENCE FOR A ROLE IN SEXUAL SELECTION
L. A. BIRKINSHAW1,* and R. H. SMITH2 1Natural
Resources Institute, University of Greenwich Chatham Maritime, Kent ME4 4TB, UK 2Department of Biology, University of Leicester Leicester LE1 7RH, UK
(Received June 21, 1999; accepted January 22, 2000) Abstract—The ability of both male and female Prostephanus truncatus beetles to distinguish between the aggregation pheromone signals of two closely located conspecific male beetles was investigated by using an olfactometer. Beetles detected variation between male signalers and visited some signalers more than others. Beetles of both sexes were found to make the same choices. These patterns of preference were found to be mirrored in trap catches of dispersing beetles when single males were used to bait flight traps that were placed in pairs in a woodland habitat in Ghana. The results are discussed with reference to the hypothesis that males signal primarily to attract mates and, therefore, features of the aggregation-pheromone signal may be sexually selected. The implications of the results for current and possible future pest-management tools are also explored. Key Words—Prostephanus truncatus, Bostrichidae, aggregation pheromone, bioassay, individual variation, sexual selection.
INTRODUCTION
The larger grain borer (LGB), Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), has emerged in the last 20 years as a destructive pest of stored maize and cassava in the tropics (Hodges, 1986). LGB has the characteristics of a wood-boring beetle that has transferred from wood to stored products with *To whom correspondence should be addressed.
1325 0098-0331/ 00/ 0600-1325$18.00/ 0 2000 Plenum Publishing Corporation
1326
BIRKINSHAW
AND
SMITH
a low moisture content. Large aggregations may form in response to chemical communication from signaling individuals, in common with many wood borers and some other relatively long-lived storage pests, e.g., Rhyzopertha dominica (Coleoptera: Bostrichidae). Only males produce the chemical signal (referred to as aggregation pheromone) (Cork et al., 1991), although both males and females respond to the signal. Males produce aggregation pheromone when they find a host that is suitable for feeding (and for the most part breeding). The pheromone contains at least two components, known as truncall-1 and truncall-2 (Cork et al., 1991; Dendy et al., 1991), and pheromone production by individuals is phenotypically plastic. Pheromone production under laboratory conditions is low in recently emerged males, rises to a peak when beetles are around 3 weeks old, and then declines steadily until death (Smith et al., 1996). Males have been found to switch off pheromone signaling temporarily in response to a nonvolatile chemical signal (female factor) produced by adult females (Smith et al., 1996). LGB was accidentally introduced into East Africa about 20 years ago (Cross, 1985), where it has become a major pest and has spread to many parts of East and West Africa and most recently, South Africa. A synthetic aggregation pheromone has been developed and is used to bait flight traps to monitor the spread of LGB. The volatile pheromone can attract individuals from considerable distances provided the concentration of pheromone is sufficiently high (Farrell and Key, 1992), although it is not clear whether pheromone produced naturally by individual beetles attracts beetles in flight over long distances (hundreds of meters) or whether it is primarily effective at attracting crawling beetles over short distances ( 0.95). There was, therefore, no evidence that females discriminate in the field between signalers more than males do.
BIRKINSHAW
1336
AND
SMITH
DISCUSSION
Are Some Signals Consistently More Attractive to Conspecifics? By using the olfactometer apparatus, we have shown that both males and females detect differences in aggregation pheromone signals and vary their response accordingly. Neither males nor females were found to make an absolute choice between two signals. Instead, responders bias their response away from a random one to a degree that is related to the difference between the signals. The outcome as given by one responder is correlated to relative ranking of the two signals as determined by other responders of the same sex. This shows that within each sex there is some consistency in the pattern of preferences shown between signals. In the field trapping trials, there was a significant skew in trap catch between two traps of a pair. Identity of the signaler was found to be the most significant determinant of trap catch. The large influence of male identity on trap catch implies that variation exists between male signals, that this variation influences the response of conspecifics, and that some signals are consistently more successful at attracting conspecifics than others. Comparison Between Male and Female Preferences Males and females exhibited similar patterns of preference when given the choice between two male signalers. This is in contrast to some studies of birdsong where the song signal may serve a dual role of mate attraction and competitor repulsion (see Fisher, 1930, quoted in Andersson, 1994). The results of this study suggest that nonsignaling males have been selected to gain an advantage in reproduction from the effects of signalling by other males. Are Males and Females Equally Choosy? Data from the trapping trials in the field showed no sex difference in the level of discrimination between two male signalers presented side by side. This indicates that males and females invest equally in the assessment of signals, and there may be no special sex-specific adaptations to choose between aggregation pheromone signals of different quality. One sex-specific difference in choice between signals has been described: this is the significant increase in female bias in catches in traps baited with synthetically produced T1 and T2 (1 mg of each) compared to traps baited with each component alone (1 mg total) (Scholz, 1997). Scholz proposes that this could arise if males land at a lower threshold of response to a concentration of pheromone. This could be the case if males follow pheromone primarily to locate new hosts and females locate the point of highest concentration to locate
AGGREGATION PHEROMONE IN
P. truncatus
1337
the signaling male as well as a host. Indeed, males may actively avoid landing exactly where another male competitor has tunneled. It is difficult, however, to extrapolate results obtained by using synthetic pheromones, at abnormally high concentrations, to the natural situation. Implications of Findings to Possible Male Reproductive Strategies The maximum number of LGB adults attracted to a trap baited with a single male in the field was 31 beetles in 24 hr. Mean trap catch was approximately 4 beetles/ trap/ day (median c 2). The overall sex ratio of beetles attracted in this study was 64% females. Variation in aggregation pheromone signaling in the field will, therefore, translate into considerable differences in the number of females that male signalers will attract at any one time. The reasons for femalebiased trap catches are unclear but mostly are likely due to a greater number of females than males in the dispersing population, arising from a greater propensity for females to take flight (Scholz, 1997). The sex ratio of emerging F1 is reported to be 1 : 1 males to females (Vowotor et al., 1999). In cases where a sex difference in response to pheromone signals has been recorded, there has been the possibility that males have become habituated/ desensitised to pheromone from exposure to their own signal, whereas females have been removed from such an influence (see discussion in Birkinshaw, 1998). Whatever the reason for a female bias in insects attracted to aggregation pheromone signals, since access to females is one determinant of mating success, characteristics of the aggregation pheromone signal are likely to be sexually selected. It would be interesting to establish if different female responders vary in their level of discrimination between signals. This being the case, the quality of mates attracted by males may, in part, also be determined by signal characteristics. Males can increase their reproductive success by employing one of two strategies. They can signal for mates by emitting aggregation pheromone, or they can follow other males’ signals. In this study, males caught from a field population that used a synthetic aggregation pheromone lure were subsequently successfully used to provide a pheromone signal. This shows that males cannot be divided into mutually exclusive categories of signalers or responders, but that they often use both strategies. Implications for Possible Future Control Strategies Beetle perception and choice within the natural variation in aggregation pheromone signals are important considerations for any proposed program of mass trapping or mating disruption (through influence on dispersal) where synthetic sources are presented as point sources. The greater the extent to which beetles invest in choosing between signals, the more efficient trapping could be, provided the synthetic lure is engineered to be more effective than the natural
BIRKINSHAW
1338
AND
SMITH
signal. Care may need to be taken not simply to use high-dose lures without considering that beetles may land some distance from a high concentration of pheromone in order to avoid the high levels of intraspecific competition that a high concentration could indicate. In summary, all three categories of evidence required to demonstrate a primary role of aggregation pheromone in sexual selection in LGB have been demonstrated here. The evidence is from a controlled study of the ability of responders to detect variation in pheromone signals. Causes of variation in signaling were not investigated. Smith et al. (1996) investigated several aspects of behavioral plasticity in the emission of pheromone signals in LGB. Establishing whether characteristics of signaling are heritable in LGB would be difficult to investigate. Prostephanus truncatus is a relatively long-lived, iteroparous beetle, and sexual selection may have led to complex and sophisticated strategies of pheromone signaling in individual males. The new bioassay described here provides one means of investigating signaling strategies. Acknowledgments—This research was supported by the Crop Post-Harvest Programme, funded by the UK government Department for International Development. The authors thank Dr. Rick Hodges, who was involved at all stages of the work. We thank the Post-Harvest Management Division of the Ministry of Agriculture in Ho, Ghana, for support during the field work.
REFERENCES ANDERSSON, M. 1994. Sexual Selection. Princeton University Press, Princeton, New Jersey. BIRKINSHAW, L. A. 1998. Mate choice in Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae): The Role of Male-Produced Aggregation Pheromone. PhD thesis. University of Leicester, Leicester, UK. BOAKE, C. R. B., SHELLY, T. E., KANESHIRO, K. Y. 1996. Sexual selection in relation to pest management strategies. Annu. Rev. Entomol. 41:211–229. CADE, W. H. 1984. Genetic variation underlying sexual behavior and reproduction. Am. Zool. 24:355–366. CORK, A., HALL, D. R., HODGES, R. J., and PICKETT, J. A. 1991. Identification of major component of male produced aggregation pheromone of larger grain borer Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). J. Chem. Ecol. 17:789–803. CROSS, M. 1985. Boring into Africa’s grain. New Sci. 1456:10–11. DENDY, J., DOBIE, P., SAIDI, J. A., SMITH, J., and URONU, B. 1991. Trials to assess the effectiveness of new synthetic pheromone mixtures for trapping Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) in maize stores. J. Stored Prod. Res. 27:69–74. FADAMIRO, H. Y., WYATT, T. D., and HALL, D. R. 1996. Behavioural response of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) to the individual components of its pheromone in a flight tunnel: Discrimination between two odour sources. J. Stored Prod. Res. 32:163–170. FARRELL, G., and KEY, G. E. 1992. Flight behaviour of the larger grain borer Prostephanus truncatus in response to synthetic pheromone. Trop. Sci. 32:163–170. HODGES, R. J. 1986. The biology and control of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae)—a destructive storage pest with an increasing range. J. Stored Prod. Res. 22:1–14. HODGES, R. J. 1994. Recent advances in the biology and control of Prostephanus truncatus
AGGREGATION PHEROMONE IN
P. truncatus
1339
(Coleoptera: Bostrichidae), pp. 929–934, in E. Highley, E. J. Wright, H. J. Banks, and B. R. Champ (eds.). Stored Product Protection, Vol. 2, Proceedings of the 6th International Working Conference on Stored-Product Protection, April 17–23, 1994, Canberra, Australia. CAB International, Wallingford, UK. HODGES, R. J., and DOBSON, C. C. 1998. Laboratory studies on behavioural interactions of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae) with conspecifics, synthetic pheromone and the predator Teretrius nigrescens (Lewis) (Coleoptera: Histeridae). J. Stored Prod. Res. 34:297–305. KEY, G. E., TIGAR, B. J., FLORES-SANCHEZ, E., and VAZQUEZ-ARISTA, M. 1994. Response of Prostephanus truncatus and Teretrius nigrescens to pheromone-baited flight traps, pp. 410–415, in E. Highley, E. J. Wright, H. J. Banks and B. R. Champ (eds.), Stored Product Protection, Vol. 1, Proceedings of the 6th International Working Conference on Stored Product Protection, April 17–23 1994, Canberra, Australia. CAB International, Wallingford, UK. LEWIS, S. M., and AUSTAD, S. N. 1994. Sexual selection in flour beetles: the relationship between sperm precedence and male olfactory attractiveness. Behav. Ecol. 5:219–224. MOORE, A. J., REAGAN, N. L., and HAYNES, K. F. 1995. Conditional signalling strategies: Effects on ontogeny, social experience and social status on the pheromonal signal of male cockroaches. Anim. Behav. 50:191–202. SCHOLZ, D. 1997. Dispersal and host finding behaviour of Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae). PhD thesis. Hannover University, Hannover, Germany. SCHOLZ, D., BORGEMEISTER, C., MEIKLE, W. E., MARKHAM, R. H., and POEHLING, H. M. 1997a. Infestation of maize by Prostephanus truncatus initiated by male-produced pheromone. Entomol. Exp. Appl. 83:53–61. SCHOLZ, D., TCHABI, A., BORGEMEISTER, C., MARKHAM, R. H., POEHLING, H. M., and LAWSON, A. 1997b. Host finding behaviour of Prostephanus truncatus (Horn) (Col., Bostrichidae): Primary attraction or random attack? J. Appl. Entomol. 121:261–269. SMITH, J. L., CORK, A., HALL, D. R., and HODGES, R. J. 1996. Investigation of the effect of female Larger Grain Borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrichidae), and their residues on the production of aggregation pheromone by males. J. Stored Prod. Res. 32:171–181. SOKAL, R. R., and ROHL, F. J. 1981. Biometry. 2nd ed. W. H. Freeman and Company, San Francisco. TEALE, S. A., HAGER, B. J., and WEBSTER, F. X. 1994. Pheromone based assortative mating in a bark beetle. Anim. Behav. 48:569–578. VOWOTOR, K. A., MEIKLE, W. G., AYERTEY, J. N., BORGEMEISTER, C., and MARKHAM, R. H. 1999. Intraspecific competition in larvae of the larger grain borer, Prostephanus truncatus (Horn) within maize grains. Insect Sci. Appl. 18:171–175.
