Canopy cover and leaf age affect colonization by tropical fungal endophytes: Ecological pattern and process in Theobroma cacao (Malvaceae)

Abstract

Fungal endophytes inhabit healthy tissues of all terrestrial plant taxa studied to date and are diverse and abundant in leaves of tropical woody angiosperms. Studies have demonstrated that plant location and leaf age influence density of endophyte infection in leaves of tropical forest trees. However, ecological factors underlying these observations have not been explored in detail. Here, we establish that foliar endophytes of a tropical tree (Theobroma cacao, Malvaceae) are transmitted horizontally and that endophyte-free seedlings can be produced for experimental manipulation by protecting aerial tissues from surface wetting. At Barro Colorado Island, Panama, we used transects of endophyte-free seedlings to determine the importance of several factors (canopy cover, abundance of aerial and epiphytic propagules, leaf age, leaf chemistry, leaf toughness and duration of exposure to viable air spora) in shaping colonization by endophytic fungi. Endophytes colonized leaves of T. cacao more rapidly beneath the forest canopy than in cleared sites, reflecting local abundance of aerial and epiphytic propagules. The duration of exposure, rather than absolute leaf age, influenced endophyte infection, whereas leaf toughness and chemistry had no observed effect. Endophytes isolated from mature T. cacao grew more rapidly on media containing leaf extracts of T. cacao than on media containing extracts from other co-occurring tree species, suggesting that interspecific differences in leaf chemistry influence endophyte assemblages. Together, these data allow us to identify factors underlying patterns of endophyte colonization within healthy leaves of this tropical tree.

• Barro Colorado Island
• ecology
• endophytic fungi
• leaf chemistry
• leaf toughness
• Panama
• sporefall
• tropical forest

We thank L.A. McDade for insights, guidance and critically evaluating the manuscript; R. H. Robichaux, O. Petrini and an anonymous reviewer for improving the manuscript; Z. Maynard, E. Rojas, L. Mejía and J. Barnard for technical assistance; E. G. Leigh, Jr. for helpful discussion; J.L. Bronstein for guidance and support; and O. Acevedo, D. Millán, and the Smithsonian Tropical Research Institute for logistical support. We are grateful for financial support from a Smithsonian Short-term Fellowship (AEA, under E.G. Leigh, Jr., and E.A. Herre); the Research Training Grant in Biological Diversification at the University of Arizona (AEA); an NSF Graduate Research Fellowship (AEA); NSF-DEB 9902346 to L.A. McDade and AEA; the M&M/Mars Co. (EAH and AEA); and the American Cocoa Research Institute (EAH and AEA). Special thanks are given to L. Barnett for her support of cacao research at the Smithsonian Tropical Research Institute.