Japanese red elder plants safeguard their own survival when they drop fruits infested by Heterhelus beetle larvae, as well as the survival of these larvae. The Kobe University study changes the narrative on how a plant and its pollinator can keep benefits balanced.
When an insect pollinates a plant and then uses the fruit as a nursery for its young, biologists speak of "nursery pollination mutualism." Kobe University botanist SUETSUGU Kenji says, "These interactions are fascinating because they sit on the boundary between cooperation and conflict." Famous examples include figs and fig wasps as well as yuccas and yucca moths, where the plants keep the insects in check by prematurely dropping fruits infested by too many larvae, which is fatal for the young insects. This punishment mechanism is often seen as critical in keeping the relationship balanced. "I once observed Japanese red elder flowers full of Heterhelus beetles mating and feeding, and I also saw fruits infested by the beetles' larvae dropping in large numbers. With such seemingly great losses to both sides, I wondered whether this was really punishment and how the insects keep their losses contained," says Suetsugu, voicing suspicion that there is something missing in the current narrative of the sanction-driven balance in nursery pollination mutualisms.
Together with his team, Suetsugu therefore set out to answer two questions. First, are Heterhelus beetles essential pollinators for the Japanese red elder Sambucus sieboldiana? And second, what is the mechanism that keeps the relationship beneficial for both parties? KAWASHIMA Suzu, a master's student at Suetsugu's lab, says: "To tackle this issue, one requires an unusual combination of careful field observation of pollination events, exclusion and hand pollination experiments, as well as developmental tracking of the insects even after the fruit drop. Many studies stop at one of these steps, simply because doing all of them takes time, patience and logistical commitment."
In the journal Plants, People, Planet, the team now reports on the fruits of their efforts. They showed that while the plant requires the beetles for pollination, it also aborts almost all fruits that contain larvae, hedging its resource losses. Importantly, however, the larvae don't die as a consequence, but emerge from the fruit and burrow into the soil where they complete their development. "What our finding shows is a different route to a stable balance, where fruit abortion can function as a compromise that both sides can tolerate. This finding shifts the narrative from dropping fruit as punishment to it being a shared benefit — without denying the underlying conflict that defines nursery pollination mutualisms in the first place," says Kawashima, who was the first author of the study.
The Kobe University team was even able to quantify the cost-to-benefit ratio of the plant-beetle relationship. They found that the balance varies among different locations and therefore likely depends on the environment. Kawashima explains: "While all Heterhelus beetle species depend on elder plants for reproduction, the same is not true in reverse, and there is considerable variation in pollinator dependence across elder plant species. In future work, mapping where Heterhelus dominates versus where alternative pollinators are more important should clarify the ecological drivers behind when the 'fallen-fruit compromise' is favored and when it is not."
Suetsugu adds: "On a personal level, this study makes me feel that we are only beginning to appreciate how much cooperation in nature is maintained by mechanisms that look, at first glance, like failure. A fallen fruit looks like a loss. Realizing that it can instead be the very structure that keeps a mutualism stable is exactly the kind of insight that makes me want to keep following these interactions year after year."
This research was funded by the Japan Science and Technology Agency (grant JPMJPR21D6). It was conducted in collaboration with a researcher from the University of Human Environments.
Kobe University is a national university with roots dating back to the Kobe Higher Commercial School founded in 1902. It is now one of Japan's leading comprehensive research universities with over 16,000 students and over 1,700 faculty in 11 faculties and schools and 15 graduate schools. Combining the social and natural sciences to cultivate leaders with an interdisciplinary perspective, Kobe University creates knowledge and fosters innovation to address society's challenges.
