The Phyllantheae–Epicephala mutualism

 

natural history of the mutualism

Glochidion acuminatum in full bloom, Amami-Oshima Island, May 2004

   The mutualism between Phyllantheae plants and Epicephala moths was discovered in 2002 by Prof. Makoto Kato at Kyoto University (Kato et al. 2003). The first observation was made in Glochidion acuminatum, a tree species occurring in subtropical forests in southern Japan. Below, I will first focus on G. acuminatum to illustrate the natural history of the mutualism. Most of the details given below are shared among other Epicephala-pollinated Phyllantheae plants.


   Glochidion acuminatum (Phyllanthaceae; tribe Phyllantheae) is a medium to tall tree occurring widely from India to Thailand, extending as far north as the southern islands of Japan. The plant is light demanding and are often found along forest edges and roadsides. Flowers are produced massively in May, but due to the small size of individual flowers, flowering is usually overlooked. Glochidion acuminatum produces separete male and female flowers, the former situated towards the base of branches and the latter near the apex. Male flowers possess six tepals that spread outwardly, which gives the flower an overall “flower-like” appearance. Female flowers, however, only have reminiscent tepals and three erect styles forming a columnar structure, hardly looking like an insect-pollinated flower. The flowers are small; the diameter of male flowers is about 5mm, and the length of female flowers only about 4mm. Both male and female flowers do not produce nectar and do not attract insects during daytime.

   In the evening, G. acuminatum flowers emit pleasant odor and are visited by moths of a species of Epicephala (Gracillariidae). This Epicephala species is a seed feeder of this Glochidion tree – they feed on young developing seeds as their larval food. However, female moths do not lay eggs in fruits but instead oviposit in flowers before they start developing into fruits. This means that if a moth lays its egg in a flower and that flower does not get pollinated, the flower will drop and the moth will waste her egg. What is intriguing about this moth is that an ovipositing female uses her proboscis to collect pollen on male flowers and use that to pollinate female flowers in which she lays her eggs. By doing so, she ensures that the flowers will mature into fruits.


   Upon visiting male flowers, a female moth stretches her proboscis and pushes it against anthers to collect pollen; in doing so, she repeatedly coils up the stretched proboscis, presumably to transfer pollen grains collected at proboscis tip to a more basal part of proboscis. Pollen collection on male flowers typically lasts more than one minute. Under a microscope, pollen collected on moth proboscis can be seen as massive yellow clump on moth’s mouthpart.

Male (left) and female (right) flowers of Glochidion acuminatum.

   Female Epicephala then visits a female flower and pollinates the stigma by pushing her proboscis tip against the apical pit of the stylar column. During pollination, a female moth stretches and coils up the proboscis repeatedly, just as she did during pollen collection, although this time she uses pollen grains stored at proboscis base for pollination (see below video). As she finishes pollinating, she bends her abdomen to insert the long ovipositor into the stylar tissue and lays a single egg in the flower that she just pollinated. After oviposition, she looks out for another female flower and repeats the same stereotypic behavior on the next flower. Because there is still ample pollen left on the proboscis, female moths do not go back to male flowers every time they pollinate female flowers.

(Left) A female Epicephala moth stretching her proboscis on a male flower (note that the anthers of this male flower have not dehisced, so this moth was probably unable to collect pollen on this flower). (Right) A femle Epicephala moth with her proboscis coated with Glochidion pollen.

   Adaptation for pollination is not limited to this remarkable behavior but is also manifested in moth’s morphology. Proboscis of female moth bears numerous hairs, which likely increase the amount of pollen to be held on the proboscis. These hairs are completely absent on male proboscis, suggesting that they are a morphological adaptation associated with pollination behavior.

A female Epicephala moth pollinates the stigma wtih pollen collected on her proboscis (left) and inserts her ovipositor into the style to lay an egg (right).

   Pollinated flowers of G. acuminatum begin to develop in October, and mature seeds are produced during late November to December. Epicephala egg hatches as the flower starts to develop. A larva then consumes the developing ovules and complete its larval development before the seeds mature. Each G. acuminatum fruit is about 1cm in diameter and contains six seeds. Because a single Epicephala larva only needs 2 or 3 seeds to complete its development, there are usually some seeds left intact in each fruit.


   A fully grown larva emerges the fruit by boring a hole through the fruit wall and pupates on the ground. In G. acuminatum, Epicephala overwinters as pre-pupa. In the next spring, they undergo a pupal stage, and the adults emerge when the flowers start to bloom again.

Proboscis of female (left) and male (right) Epicephala moths.

   Epicephala moths have evolved sophisticated behavioral and morphological adaptations to pollinate Glochidion flowers. This was followed by reciprocal floral specialization in Glochidion plants, which virtually excluded all other insects from being pollinators of Glochidion flowers. Although Epicephala larvae feeds on Glochidion ovules, many seeds are left viable for plant reprocution. This balance between the number of seeds produced/consumed is critical for this interaction to be a mutualism.


   Since the discovery of this mutualism, pollination systems have been studied for many other Phyllantheae plants, providing a broader picture of the origin and evolutionary history of this mutualism. In the following sections, I will describe what is currrently known about pollination systems in Phyllantheae and their evolutionary history.



Global Diversity of Phyllantheae Plants and Their Pollination Systems (under construction)


The Evolution of Mutualism between Phyllantheae and Epicephala (under construction)



References:


  1. (1)Kato, M., A. Takimura & A. Kawakita (2003) An obligate pollination mutualism and reciprocal diversification in the tree genus Glochidion (Euphorbiaceae). Proceedings of the National Academy of Sciences, USA 100: 5264-5267.

  2. (2)Kawakita, A. (2010) Evolution of obligate pollination mutualism in the tribe Phyllantheae (Phyllanthaceae). Plant Species Biology 25: 3-19.



Back to Kawakita Lab website

(Left) Fruits of Glochidion acuminatum. (Right) Horizontal section of G. acuminatum fruit. One of the six developing seeds has been destroyed by an immature Epicephala larva.

Video showing female Epicephala moth pollinating and ovipostiting in Glochidion acuminatum female flower.