Male animals usually raise their sperm allocation after detecting sperm competition risk. To date, only a few studies have investigated the cues used by males to sense and respond to rivals. Yet, it is still largely unknown whether males respond to single or combined cues and whether they can increase their lifetime spermatozoal investment after a perception of rival cue(s). Here we postulate that males increase ejaculation and production of sperm after detecting combined cues from rivals, but such response quickly diminishes after the cues are removed. We exposed newly emerged and virgin focal males of the moth Ephestia kuehniella to various rival cues and then permanently removed the cues. We introduced a virgin female to an exposed focal male and an unexposed focal male, respectively, per day and counted the number of sperm transferred by the focal males in each mating and recovered in their body after death. We demonstrate that males significantly increased their lifetime sperm allocation and production after premating detection of either single (acoustic or chemical) or combined cues (acoustic + chemical or acoustic + chemical + tactile) from their rivals with combined cues (acoustic + chemical + tactile) somewhat strengthening such response in eupyrene production. The number of sperm ejaculated by males significantly decreased over successive matings in their lifetime regardless of whether they were exposed to rival cues, but the decline was significantly faster in rival‐cue‐exposed males than in unexposed ones. This suggests that the increase in spermatogenesis cannot fully compensate for that of sperm expenditure in response to rival cues. We show that 10‐hr premating rival exposure was sufficient to maximize males' response in sperm ejaculation and production. The impact of the rival perception on sperm transfer persisted for most of males' reproductive life, suggesting that the moth males have a long‐term memory of sperm competition risk experienced in the early adulthood. A free Plain Language Summary can be found within the Supporting Information of this article.

Endoclita signifer is a major wood-boring pest of eucalyptus trees in China, and its third instar larvae can accurately find and infest eucalyptus trees in mixed-species forests, although it can also feed on another 51 tree species in the same planted area. A total of 34 volatile compounds were identified from eucalyptus trunks, including non-infested and infested trunks with single or multiple (more than three) larval entrance cover packets, and forest floor humus. Of these, o-cymene showed a strong gas chromatography-electroantennographic detection (GC-EAD) activity and significant attraction of the third instar E. signifer larvae. Higher abundance of alpha-phellandrene, o-cymene, and the unique 2-phenyl-2-propanol in the volatile profile from infested eucalyptus trunks indicated that they were herbivore-induced plant volatiles (HIPVs). The larvae showed significantly higher attraction to volatile blends, especially those from infested eucalyptus trunks, than to single volatiles. A blend of the three HIPVs, α-pinene, D-limonene, and n-butyl ether may serve as an attractant for the control of E. signifer larvae in eucalyptus plantations. Further, exposure of third instar E. signifer larvae to some of these volatiles which also elicited electroantennogram and behavioral responses, influenced expressions of some olfactory proteins. Our results show that third instar E. signifer larvae can recognize o-cymene from host eucalyptus trunks and are attracted to the trunk by the three HIPVs when they shift their habitats from the forest floor humus to the tree trunks.