Survival trade-off in cycad-insect interactions: cycad volatiles known to attract mutualists are the same luring harmful insects

Unlike pollinators, which visit both male and female cones of Encephalartos spp., the larvae of the sexually dimorphic non-pollinators Antliarhinus zamiae. develop in and feed on female cones, causing significant cone damages. However, we do not know whether the volatile organic compounds (VOCs) that attract the pollinators are the same that attract the non-pollinating Antliarhinus zamiae. We hypothesized that the VOCs attracting pollinators would rather repel the antagonistic Antliarhinus spp. Using Y-maze olfactometer assays, we monitored 800 behavioral responses of Antliarhinus zamiae to single and blends of VOCs well-known to attract pollinators to Encephalartos spp. We found that both male and female A. zamiae are attracted not by single but a blend of VOCs, with more positive responses observed for female A. zamiae. Notably, the ternary blend of (3E)-1,3-octadiene, linalool, and benzaldehyde, previously identified as a potent attractant for pollinators, showed the highest attraction of A. zamiae. These findings suggest that non-pollinators exploit pollinator-attracting chemical cues to locate female cones, potentially through associative learning. Our results underscore the ecological complexity of cycad-insect interactions and raise an important paradox: the same volatile cues that promote mutualistic cycad-insect interactions also attract antagonistic insects that cause significant damages to cycad female cones.