Circadian mating activity and effect of pheromone pre-exposure on pheromone response rhythms in the moth Spodoptera littoralis

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Abstract

Mating in moths is generally mediated by female-produced sex pheromones. Mating activity, female pheromone production/release and male pheromone responsiveness all show diurnal variations in many species. We found that the response of the male Egyptian cotton leafworm, Spodoptera littoralis, to sex pheromone gland extracts showed a diel rhythm in olfactometer tests, and the variation was persistent for at least 1 day in constant darkness. High male response to sex pheromone was correlated in time with high mating and locomotor activity. Male S. littoralis, maintained in constant darkness and exposed to pheromone gland extracts on a daily basis, showed an induced temporal variation in response after several days, in contrast to unexposed males. This suggests that in the absence of other external zeitgebers, exposure to sex pheromone may function to synchronise circadian behavioural rhythms in male moths. The daily rhythm in mating activity in S. littoralis is also shown to be persistent for at least 2 days in constant darkness. Pairs mated significantly less when either the male or female had been raised in a light:dark cycle 10 h out of phase, indicating that the proposed circadian rhythm in mating activity is composed of rhythmic mating preference/ability in both sexes.

Introduction

Finding a female to mate with is a key event in the life of an adult male moth. For this purpose, many moth species rely on long-range species-specific sex pheromones. These are in most species released by the female, with the release correlated in time with high male responsiveness and locomotor activity (Raina and Menn, 1987). Previous studies have revealed circadian regulation of male responses to sex pheromone in several moth species. Males of both the codling moth, Cydia pomonella (L.), and the turnip moth, Agrotis segetum (Schiff.), show persistent rhythms in attraction to pheromone in the absence of external zeitgebers (Castrovillo and Cardé, 1979; Rosén et al., 2003). Such studies of male rhythms in sex pheromone communication are complemented by corresponding clock-controlled rhythms in females, primarily rhythmic pheromone biosynthesis (Rosén, 2002) and calling behaviour (i.e. the exposure of the pheromone gland to facilitate pheromone release) (Delisle and McNeil, 1987). However, sex pheromone communication restricted to certain hours of the day requires temporal synchronisation between males and females. This synchronisation may arise from both sexes relying on the same environmental zeitgebers, such as the light:dark (L:D) cycle. It has also been shown that social cues may affect circadian rhythmicity in at least some species. Social, likely olfactory cues synchronise locomotor activity in fruit flies (Levine et al., 2002; Levine, 2004) and studies of some mammals show similar results (Refs. in Davidson and Menaker, 2003; Mistlberger and Skene, 2004). Since calling behaviour in most moth species coincides with peaks in mating frequency (Dreisig, 1986, and refs. therein), the female sex pheromone is not only a long-range indication of a female's location, but also a sign that she is physiologically ready to mate. The pheromone plume, released by a female, therefore constitutes a powerful external stimulus to a male moth, and could hypothetically function to synchronise rhythms in reproductive behaviours. The present study aims to characterise the circadian nature of mating behaviours in Spodoptera littoralis (Boisduval) (Noctuidae) and to investigate the effects of previous pheromone exposures on the behavioural rhythm in male pheromone response.

Section snippets

Insects

A laboratory culture of S. littoralis, originating from Egypt, was maintained in a reversed 17:7 L:D cycle with lights-off at 12:00, lights-on at 19:00 (50% R.H., 23 °C). Larvae were reared on an artificial bean-based diet (Zhu et al., 1996). To prevent mating and pre-exposure of males to the female sex pheromone, male and female pupae were separated by morphological traits and maintained in separate climate chambers. Newly emerged moths were transferred to a new box 1–2 h before each scotophase,

Mating experiments

In the mating experiments (Sections 3.1.1–3.1.4), temporal variation in proportions of females ovipositing fertilised eggs (larvae emerged) did not differ from observed variations/rhythms in mating frequency. Only variations in mating frequencies are therefore discussed below.

Discussion

Most moth species prefer to mate during the scotophase, more often during the latter part than at dusk (Dreisig, 1986). Pairs of S. littoralis preferably mate during a few hours before dawn (17:7 L:D cycle; pers obs.). We here show that this diel rhythm in mating preference likely involves a circadian component, as males and females do not mate at hours corresponding to the daytime when maintained in constant darkness. Furthermore, the observed rhythm in mating activity is composed of temporal

Acknowledgements

This project received financial support from the Swedish Science Foundation Vetenskapsrådet (VR) and the Crafoord Foundation. Male and female S. littoralis to start the culture were gratefully obtained from Dr. Peter Anderson (Swedish Agricultural University, Alnarp, Sweden). The authors would also like to thank Dr. Peter Anderson, Prof. How-Jing Lee (National Taiwan University, Taipei, Taiwan) and two anonymous reviewers for useful comments on the preliminary manuscript.

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