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BIOMECHANICS of PERIDIOLE EJECTION and FUNCTION of the FUNICULAR CORD in BIRD's NEST FUNGI by Maribe

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BIOMECHANICS of PERIDIOLE EJECTION and FUNCTION of the FUNICULAR CORD in BIRD's NEST FUNGI by Maribe ABSTRACT SPLASH AND GRAB: BIOMECHANICS OF PERIDIOLE EJECTION AND FUNCTION OF THE FUNICULAR CORD IN BIRD’S NEST FUNGI by Maribeth Hassett The bird’s nest fungi (Agaricales, Nidulariaceae) package a millions spores into sporangia (referred to as peridioles) that are splashed from their basidiomata by the impact of raindrops. Peridioles are splashed from flute-shaped basidiomata at speeds of 1 to 5 meters per second (11 mph). This study examines the mechanism of peridiole ejection and funicular cord function in Cyathus and Crucibulum using high-speed video. The funicular cord is a highly-extensible bundle of hyphae whose tensile strength is maximized by the modification of clamp connections. The funicular cord remains in a condensed form during flight with an adhesive pad exposed on the projectile surface. The cord unravels when the pad sticks to surrounding vegetation and acts as a brake that quickly reduces the velocity of the projectile. This elaborate mechanism tethers peridioles in a perfect location for browsing by an herbivore and is viewed as a beautiful adaptation for a coprophilous fungus. SPLASH AND GRAB: BIOMECHANICS OF PERIDIOLE EJECTION AND FUNCTION OF THE FUNICULAR CORD IN BIRD’S NEST FUNGI A Thesis Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Master of Science Department of Botany by Maribeth Hassett Miami University Oxford, Ohio 2012 Advisor ____________________________________ (Dr. Nicholas Money) Reader_____________________________________ (Dr. Daniel Gladish) Reader_____________________________________ (Dr. Chun Liang) Table of Contents List of Tables………………………………………………..……………………………………iii List of Figures…………………………………………………………………………………….iv Acknowledgments…………………………………………………………………….…………..v Introduction…………………………………………………………….…………..……………...1 Materials and Methods……………………………………………………………...……………..3 Results and Discussion…………………………………….………………………………….…..6 Figures…………………………………….…………………………………………...…………14 References……………………….………………………………………………………..……...30 ii List of Tables Table 1. Measured biomechanical data of peridiole ejection based on high-speed video sequences. Table 2. Predicted biomechanical data based on modeled peridiole trajectories. Table 3. Measured mechanics of model peridiole discharge using model splash cups. iii List of Figures Figure 1: Cyathus fruiting body structure from Brodie (1975). Figure 2: Species within the Nidulariacae produce fruit bodies of varying shapes. Figure 3: Figure illustrating the four species used in this study: Cyathus olla, Cyathus stercoreus, Crucibulum laeve, and Cyathus striatus. Figure 4: Experimental design of splash experiments conducted on bird’s nest fungi. Figure 5: Splash experiments were performed on model splash for comparison with actual fruit bodies. Figure 6: Individual frames from video sequence of splash discharge in Cyathus olla at 3,000 fps. Figure 7: Still frame of Cyathus olla peridiole ejection taken from a high-speed video sequence. Figure 8: Predicted trajectories of peridioles of four species of bird’s nest fungi based on launch data obtained by high-speed video microscopy. Figure 9: Splash scenarios resulting from raindrops hitting a fruit body of Cyathus olla at two positions. Figure 10: Scanning electron micrographs of cross-sectioned peridiole of Cyathus olla. Figure 11: Scanning electron micrographs of the funicular cord. Figure 12: Scanning electron micrograph of strand of hyphae from the funicular cord showing a modified clamp connection. Figure 13: Scanning electron micrographs of clamp connections from the funicular cord showing extracellular bands around two septa iv Acknowledgments I would like to thank my advisor, Dr. Nicholas Money, for the opportunity to work on this project. I am thankful for his dedication, encouragement, and sense of humor that made this project rewarding and enabled me to grow professionally. I am also grateful for the insight and guidance given to me by Dr. Chun Liang and Dr. Daniel Gladish during the duration of this project. In addition, I am thankful that I had the opportunity to grow as educator under the tutelage of Dr. Susan Barnum. Thanks to Matt Duley for helping me with my scanning electron micrographs. A special thanks to Zachary Sugawara and Jessica Stolze-Rybczynski whose preliminary data made this project possible. Furthermore, I had the privilege of collaborating with Dr. Mark W. F. Fischer whom helped me develop my quantitative research skills. I am also especially grateful for the love and support from my family. v Introduction and historical context The bird’s nest fungi (Agaricales, Basidiomycota) produce basidiomata adapted for splash dispersal, utilizing the force of a raindrop to launch their spore containing peridioles to remarkable heights. Species within this family package hundreds of thousands of basidiospores inside spore dispersing packets known as peridioles. Ejected peridioles become tethered to vegetation, placing them in a perfect position to be eaten by grazing herbivores, a perfect location for grazing herbivores. Peridioles are tethered by a specialized structural organ known as the funicular cord, an extendible bundle of hyphae that is twisted together to form a strengthened cord-like structure. Brodie illustrates the structural anatomy of the fruit body of Cyathus in detail (1) (Figure 1). Structural adaptations for splash dispersal and attachment of peridiole vary among the five genera of bird’s nest fungi. Species of Cyathus and Nidula produce a flute-shaped fruit body. Species of Crucibulum produce a shallow, saucer-shaped fruit body. Species of Nidularia and Mycocalia produce sac-like fruit bodies that split open upon maturity to reveal peridioles embedded in a gelatinous pad. Peridioles of Nidularia, Mycocalia, and Nidula lack a funiculus but are covered in an adhesive coat, while Cyathus and Crucibulum produce peridioles with funiculus (Figure 2). Species that produce a flute-shaped fruit body with a funiculus are believed to be most effective at launching peridioles long distances via splash dispersal (1). The first mention of the bird’s nest fungi in literature was by Clusius in 1601 (8), followed by several classic works including Tulasne (18), Sachs (17), Eidam (11), and Brefeld (2). These works inspired several descriptive monographs including White (20) and C.J. Lloyd (13). These monographs detailed the morphology of the fruit bodies but lacked information on the splash mechanism. Researchers at this time were puzzled by the function of the unusual anatomical structures found in this family and what role these structures might play in spore dispersal. The mechanics of splash dispersal of the bird’s nest fungi was misunderstood by early investigators. The Tulasne brothers wrote detailed descriptions of the morphology of Cyathus species including a description of the funiculus. The brothers were unable however, to determine the function of the funiculus and the relationship between the structure of the fruit body and its function (3). In 1927 Martin (14) was first to suggest that raindrops might splash peridioles from 1 the fruit bodies into the air and onto vegetation. He conducted simple splash experiments by holding a pipette containing water a meter above the fruit bodies and observed that the force of a raindrop was able to eject the peridioles. Interest in the bird’s nest fungi was renewed again in the 1940s when several researchers learned that bird’s nest fruit bodies’ function as spectacular splash cups. In 1941, Zenker (21) published a paper describing a parasitic fungus that he named Leptostroma camelliae adhering on Camellia leaves. William Diehl (9) corrected this mistake and discovered that this purported parasitic fungus was Cyathus. Zenker had mistaken Cyathus peridioles for the hyphae of a parasitic fungus. Diehl marveled at how high he found the peridioles on foliage and wondered how they were launched vertically to such great heights. Also in 1941, Dodge (10) received several inquiries describing bird’s nest peridioles found four meters above ground. Dodge (10) speculated that the funiculus might function as an attachment organ for peridioles but his work made no mention of splash dispersal. He estimated what force would be strong enough to propel the peridioles three to five meters in the air. It was not until 1941 that Buller (7) revealed the relationship between the vase- shape fruit body and peridiole ejection. Buller combined previous knowledge of morphology of fruit bodies, and work done by Diehl (9), to solve the puzzle of splash dispersal. He was the first to describe splash dispersal of peridioles and the correct function of the funiculus. Buller’s student, Harold Brodie (3,4,5,6) continued his work and dedicated his career and many publications to the study of the bird’s nest fungi. Brodie (5) conducted simple splash experiments on several species of bird’s nest fungi, however was limited to ambiguous measurements of peridiole ejection because he had was unable to visualize peridiole launch. He hypothesized about the events that occurred during peridiole ejection and was left with many unanswered questions about the biomechanics of splash dispersal in the bird’s nest fungi. He was puzzled by the mechanics of the funicular cord, and without high-speed video, was unable to describe in detail the events that occurred during splash dispersal (1). Since peridiole ejection occurs at great speeds, tools such as high-speed video can enable visualization and analysis of splash dispersal
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