A flower in fruit's clothing: Pollination of jackfruit Artocarpus heterophyllus, Moraceae) by a new species of gall midge, Clinodiplosis ultracrepidata sp. nov. (Diptera: Cecidomyiidae)

Authors: GARDNER, ELLIOT - Northwestern University; Gagne, Raymond; Kendra, Paul; Montgomery, Wayne; RAGUSO, ROBERT - Cornell University; MCNEIL, TASHINA - Lake Forest College; ZEREGA, NYREE - Northwestern University

Submitted to: International Journal of Plant Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/15/2018
Publication Date: 6/1/2018
Citation: Gardner, E., Gagne, R., Kendra, P.E., Montgomery, W.S., Raguso, R.A., Mcneil, T.T., Zerega, N.J. 2018. A flower in fruit's clothing: Pollination of jackfruit Artocarpus heterophyllus, Moraceae) by a new species of gall midge, Clinodiplosis ultracrepidata sp. nov. (Diptera: Cecidomyiidae). International Journal of Plant Sciences. 179(5):350-367.

Interpretive Summary: Jackfruit (Artocarpus heterophyllus) has been categorized as a priority underutilized crop that should be targeted for improvement and expanded use. However, this tropical/subtropical fruit has been poorly studied, and little is known about its pollination. In a collaborative effort involving scientists from Northwestern University, Cornell University, the Smithsonian Institution, and USDA-ARS (Miami, FL), research was initiated to investigate the reproductive biology and chemical ecology of jackfruit, including pollination. This seminal study identified a new species of midge (Clinodiplosis ultracrepidata sp. nov.) that pollinates jackfruit and breeds in a fungus that grows on male jackfruit flowers. The midges are able to detect (smell) three key chemicals (aliphatic esters) emitted by jackfruit flowers, and those chemicals attract the minute flies to both male and female flowers, facilitating transfer of pollen. These results increase our understanding of the biology of jackfruit and its complex interactions with a unique fungus and a newly-described midge pollinator. This information will aid in developing sound cultural practices necessary for improving and expanding production of this underutilized food crop.

Technical Abstract: Premise of the Research: Jackfruit (Artocarpus heterophyllus, Moraceae) is an emerging but underutilized crop whose pollination is poorly understood. We present a multidimensional investigation of the reproductive biology and chemical ecology of jackfruit and a putative pollinator, Clinodiplosis ultracrepidata sp. nov. (Diptera:Cecidomyiidae), which likely originated in Asia. Methodology: We employed observations, insect trapping, GC-MS analysis of floral volatiles, behavioral bioassays, and quantitative electroantennography to investigate the relationship between jackfruit and C. ultracrepidata in Miami, Florida, USA. Pivotal Results: Results indicated that C. ultracrepidata females visit both male and female jackfruit inflorescences. They oviposit in fungus-infected male inflorescences, and their larvae feed on the fungus; female inflorescences provide no reward. Behavioral assays indicated that the midges are attracted to inflorescences by scent. The main components of jackfruit floral volatiles are aliphatic esters, primarily methyl 2-methylbutyrate, methyl isovalerate, and methyl tiglate, all three of which elicited strong olfactory responses in C. ultracrepidata females. Most of the esters in jackfruit floral volatiles also exist in jackfruit fruit volatiles, suggesting a link between adaptation to pollinators and adaptation to seed-dispersing mammals, which are sensitive to aliphatic esters. Conclusions: We have documented a tripartite pollination mutualism involving midges and a fungus in an understudied crop, a result that may inform proper pollinator management. While male inflorescences provide a brood site and nutrition, attraction of midges to female inflorescences is the result of deceit by scent. Our results support the existence of insect pollination in jackfruit but do not negate the possibility of wind pollination, which warrants further study.