The dual role of insects in parasitic plant reproduction solves a long-standing botanical mystery
In the dark and moist understories of the subtropical forests of Shimoshima Island in Japan grow parasitic plants that feed on the roots of other plants. They are called Balanophora, and for over a century, the mechanism of their seed dispersal has remained a mystery.
It has been suggested that the tiny seeds are carried away by the wind, but there is little to no wind in the understories of (sub)tropical forests. Some plant species among the Balanophora are bright red, resembling strawberries, and attract birds and rabbits to eat and thus disperse the seeds. However, others, like Balanophora subcupularis, have dull colors and a yeasty smell, making it unlikely that vertebrates are involved. The mechanism of the plant's pollination has similarly remained unclear.
The Kobe University botanist Suetsugu Kenji specializes in understanding the interactions between these parasitic plants and their surrounding ecosystems, including the often overlooked but crucial role of invertebrate pollinators and seed dispersers. To find out who aids B. subcupularis in its reproduction, he and his team watched the plants for more than 100 hours and took tens of thousands of automated night photographs while the flower was in bloom or bore fruit, identifying the visitors.
In addition, they conducted both animal exclusion experiments and seed feeding experiments to ascertain whether the animals on the photographs are actually effective pollinators and seed dispersers.
In two back-to-back papers published in the journal Ecology, the Kobe University team published that B. subcupularis is pollinated by ants and camel crickets, which visit the plants for their pollen and nectar. Remarkably, these same species also later feed on the fleshy leaves carrying the seeds, aiding in seed dispersal.
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Ants carry the bracts with the attached seeds to their nest, dropping some of the seeds on the way and disposing of others in "waste piles" outside their nests. Usually, seeds dispersed by ants are surrounded by nutrient-rich bodies called "elaiosomes" that serve as food for the ants. However, in the case of Balanophora subcupularis, the bracts seem to take over this function. Credit: Hashiwaki Hiromu -
Because camel crickets are small, it is very unusual that they can swallow the seeds together with their food. However, like for other parasitic plants, Balanophora subcupularis seeds are tiny and robust, and many survive the passage through the cricket's digestive tract unharmed. Pictured is a camel cricket's dropping containing Balanophora subcupularis seeds. Credit: Suetsugu Kenji
"It is well known that many plants rely on insects for pollination, although it's rare for ants and crickets. Also, many plants use birds and mammals to distribute their fruits, and again it's very unusual that crickets or other tiny arthropods take over this role. Even more striking, it is very rare for the same animal to perform both functions, and it is unique that the same invertebrates do so," says Suetsugu.
The Kobe University botanist suggests that this rare combination of pollination and seed distribution roles may be influenced by two factors. First, "B. subcupularis blooms late in the year when many typical pollinators, such as bees, are less active. In addition, our study site is a small island at the northern edge of the plant's distribution, which might contribute to the scarcity of pollinators and seed dispersers."
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A Balanophora subcupularis inflorescence (a cluster of flowers) is visited by a camel cricket seeking the plant's pollen and nectar. Similar to bee pollination, the cricket unwittingly transfers some pollen to female flowers on the same plant or on others. Pollination by camel crickets has so far been confirmed only in one other plant species, Mitrastemon yamamotoi, which is also a non-photosynthetic parasite. Credit: Hashiwaki Hiromu -
After pollination, the flowers of Balanophora subcupularis develop into seeds attached to fleshy leaves, called "bracts." Camel crickets and ants return to feed on the bracts but also take the seeds with them. Credit: Hashiwaki Hiromu
Suetsugu also highlights the broader implications of these findings, saying, "This underscores the importance of invertebrates in plant reproduction and encourages us to look deeper into how these relationships evolve and what environmental factors drive such unique adaptations.
"More practically, our findings also contribute to conservation strategies for rare and endangered plants like Balanophora subcupularis. Understanding their reliance on specific invertebrates for both pollination and seed dispersal helps inform habitat preservation efforts and the management of invertebrate populations, which are crucial for these plants' survival."
More information: Kenji Suetsugu et al. Beyond pollination: Ants and camel crickets as double mutualists in a non-photosynthetic plant, Ecology (2024). .
Kenji Suetsugu et al, Ants, camel crickets, and cockroaches as pollinators: The unsung heroes of a non鈥恜hotosynthetic plant, Ecology (2024).
Journal information: Ecology
Provided by Kobe University
