Date Published: January 30, 2019
Publisher: Public Library of Science
Author(s): Atsushi Kawakita, Akira A. Wong Sato, Juana R. Llacsahuanga Salazar, Makoto Kato, Adrien Sicard.
In the Old World tropics, several hundred species of leafflowers (Phyllanthus sensu lato; Phyllanthaceae) are engaged in obligate mutualisms with species-specific leafflower moths (Epicephala; Gracillariidae) whose adults actively pollinate flowers and larvae consume the resulting seeds. Considerable diversity of Phyllanthus also exists in the New World, but whether any New World Phyllanthus is pollinated by Epicephala is unknown. We studied the pollination biology of four woody Phyllanthus species occurring in Peru over a period of four years, and found that each species is associated with a species-specific, seed-eating Epicephala moth, here described as new species. Another Epicephala species found associated with herbaceous Phyllanthus is also described. This is the first description of Epicephala from the New World. Field-collected female moths of the four Epicephala species associated with woody Phyllanthus all carried pollen on the proboscises, and active pollination behavior was observed in at least two species. Thus, Epicephala moths also pollinate New World Phyllanthus. However, not all of these Epicephala species may be mutualistic with their hosts, because we occasionally observed females laying eggs in developing fruits without pollinating. Also, the flowers of some Phyllanthus species were visited by pollen-bearing thrips or gall midges, which potentially acted as co-pollinators or primary pollinators. Phylogenetic analysis showed that the New World Epicephala associated with woody Phyllanthus are nested within lineages of Old World active pollinators. Thus, actively-pollinating Epicephala moths, which originated in the Old World, successfully colonized the New World probably across the Pacific and established mutualisms with resident Phyllanthus species, although whether any of the relationships are obligate requires further study. There is likely a major radiation of Epicephala still to be found in the New World.
Obligate pollination mutualism between plants and actively pollinating, seed parasitic pollinators represent some of the most sophisticated examples of plant–pollinator coevolution . Examples include the fig–fig wasp [2,3], yucca–yucca moth , and leafflower–leafflower moth mutualisms [5,6], wherein the plants sacrifice a subset of the seeds as nourishment of pollinator larvae in return for pollination services. The pollinating insects have evolved to actively pollinate host flowers to ensure food (developing seeds) for their larvae, and have morphological features that enhance active pollination, such as the coxal comb and pollen pockets in fig wasps , maxillary tentacles in yucca moths , and hairy proboscis in leafflower moths . Usually a subset of the seeds is left uneaten by the pollinator larvae, providing net benefit of the mutualism for the plants. Plant specializations to these pollinators have led to highly restrictive floral structures and/or loss of nectar reward, making their flowers hardly attractive to ordinary flower visitors.
Although the presence of Epicephala in the New World has been implicated based on the presence of Epicephala-like larvae and pupal cocoons on herbarium specimens of Neotropical Phyllanthus , this is the first report of any Epicephala from the New World. The diversity of Phyllanthus in Peru is not high as compared to other regions in the Neotropics; however, we found species-specific Epicephala species from each of four woody Phyllanthus that were studied and one Epicephala species associated with three herbaceous Phyllanthus. Considering that there are ca. 250 Phyllanthus species throughout the New World, there is probably a considerable diversity of Epicephala remaining to be found. Epicephala chancapiedra was associated with herbaceous Phyllanthus species belonging to two distantly related subgenera (Conami and Swartziani). This species is thus likely capable of attacking various herbaceous Phyllanthus species and may be found from other herbaceous Phyllanthus in other parts of the Neotropics.