Underwater spore dispersal: a preliminary report of aquatic invertebrates associated with Psathyrella aquatica Jonathan L. Frank All images are courtesy and copyright of the article author, unless otherwise noted.

n 2005 Robert Coffan, a hydrologist in southern Oregon, species, Psathyrella aquatica, and the phenomenon was reported made what is believed to be the first discovery of an in Frank et al. (2010). However, while this report contained underwater mushroom. While several ascomycetes are abundant details and information, no spore dispersal mechanism Iknown to grow and was observed. fruit underwater, for Insects are known to example Vibrissea consume a wide range of truncorum, V. filisporia, basidiomycete fungi and Cudoniella clavus, no have been implicated gilled mushroom had as spore dispersal previously been known vectors (Fogel, 1975; to do so. Consequently, Lilleskov and Bruns, this report was met 2005). As with truffles with skepticism in that fruit underground the mycological and require animals community. Someone to dig them up and commented in an eat them to spread online forum that “it their spores, some makes about as much dispersal vector is likely sense as opening an required to counter umbrella underwater.” the constant flow of It took Coffan two years water downstream. of trying to contact Aquatic insects might mycologists to confirm be involved in this his observation, before process as underwater he convinced Darlene mycophagists and Southworth and me dispersal vectors. to take a look. Dr. To investigate this, Southworth and I had Figure 1. Mayfly collected on P. aquatica. I collected a few been studying truffles mushrooms to inspect and ectomycorrhizal for evidence of fungi associated with insects. Also, I used oaks and conifers in an underwater video Oregon; when Robert camera to capture contacted us, our field images that could be sites were bone dry, reviewed one frame and we enthusiastically at a time. Eventually, I welcomed the donned neoprene gloves opportunity to take a because the water is field trip in August. As cold (7-10o C), making unlikely as it may still it difficult to hold the sound (one reviewer camera underwater for this article felt for more than a few inclined to write, “I still seconds. Even so, it was have some reservation challenging to hold the on the phenomenon camera steady in the of the underwater current and to aim it mushroom”), we Figure 2. Caddisfly on P. aquatica with mirror reflection in situ. in focus at the elusive arrived at the site and little mushrooms. observed little brown mushrooms growing underwater. A few Despite these challenges, underwater videography enhanced my years later, based on morphological and molecular study, the ability to observe the mushrooms and minimized the need for underwater little brown mushroom was described as a new sporocarp collections.

38 FUNGI Volume 6:4 2013

Figure 4. Red spider mite among gills of P. aquatica. specimen, and a mayfly naiad from another. After visiting the Rogue River site six times in September and October of 2011, I obtained video images of Figure 3. Black fly larva on stipe of P. aquatica. aquatic invertebrates associating with Each year since 2007, I have revisited the underwater mushroom. These the main fruiting site and observed video data were first presented at the The Mushroom fruiting bodies (Table 1). The underwater Ashland Independent Film Festival in Identification Trilogy mushroom has been observed from early the short documentary, AQUATICA: The July to early October. I have also visited Underwater Mushroom (Frank, 2013). Now in wide-screen format streams and rivers in southern and central Mayflies, with their distinctive caudal Oregon, to look for new sites. However, filaments, were stationed on the upper • All of the original video clips have been lack of funding limits these surveys to stipe of several mushrooms (Figure 1). I reformatted and all images and illustrations also captured images of a caddisfly, replete have been upgraded and/or replaced. only a few days per year. The Rogue River upstream from Prospect, and Union Creek with casing, crawling along the upper stipe Oregon in Jackson Co. (approximately of one mushroom (Figure 2). I brought 20 km) as well as the Breitenbush specimens of the mayfly, caddisfly, black River and French Creek in Marion Co. fly larvae (Figure 3) and a red spider (approximately 20 km) have been surveyed mite (Figure 4), back to the laboratory repeatedly. The underwater mushroom to examine for the presence of any P. is now listed as a sensitive species by aquatica spores within or adhering to the the Oregon Biodiversity Information exterior of their bodies. I made slides of Center (ORBIC 2010), however survey the caddisfly and mayfly guts, and slides of protocols have yet to be established entire black flies and red spider mites, as or tested. My survey method included they were too small to dissect. Distinctive targeting sections of rivers and streams ellipsoid smooth brown spores of P. with Alnus rubra (red alder) growing aquatica were observed from slides made nearby. I have also responded to several of the guts of the caddisfly and the mayfly, reports of underwater mushrooms from and from mounts of the entire black flies amateurs, finding them to be either gilled (Figure 5). The red spider mite, though mushrooms that have been inundated by collected from spore-covered gills, did not rising waters or one of the ascomycetes have spores adhering to its exoskeleton. mentioned above. These observations suggest that aquatic I first observed aquatic insect larvae insects are involved in spore dispersal, associating with P. aquatica in 2009 either as mycophagists, grazers, or filter when I collected three fruiting bodies feeders collecting spores as they move www.mushroom.pro and later inspected them under a along the mushrooms underwater. While microscope. To my surprise, two black more data will be needed to confirm the fly larvae emerged from the cap of one roles of these invertebrates, aquatic insects 40 FUNGI Volume 6:4 2013 year # fb observed # stems # fb collected aquatic invertebrates Psathyrella and spores among the abundant stipe w/o caps spores fibrils. Not far from these undulating 2005 20 NA 8 NA NA structures, detached caps were lodged 2006 NA NA 0 NA NA in the vegetative debris and sediments 2007 28 NA 8 NA NA of the river bottom. This pattern of 2008 2 NA 0 NA NA caps detaching and the slow physical 2009 24 NA 3 black fly (Diptera) Y deterioration of stipes may provide a mayfly (Ephemeroptera) N redundant mechanism for maintaining 2010 18 3 3 NA NA inoculum in suitable habitats. Figure 6 2011 21 5 3 caddisfly (Tricoptera) Y illustrates the life cycle of P. aquatica. mayfly (Ephemeroptera) Y While these observations suggest viable red spider mite (Arthropoda) N mechanisms for spore dispersal for the 2012 16 4 0 NA NA new underwater mushroom, P. aquatica,

the functional roles of this underwater Table 1. Number of fruiting bodies observed in situ in upper Rogue River mushroom in aquatic ecosystems remain to be more thoroughly investigated. 2005-2012. Stems without caps were first observed in 2010. Aquatic insects Since P. aquatica has thus far only been were observed in 2009 and 2011. Data from 2005 were reported by R. A. observed in the upper Rogue River, Coffan. No data were collected in 2006. this underwater fruiting ability may be have the ability to counter the flow of another physical phenomenon that obligately associated with the cold, clear water downstream and potentially move may pertain to the ability of this oxygenated section of the upper Rogue spores upstream to new suitable habitats. underwater mushroom to stay in one River with its volcanic sediments and Additionally, the insects can be consumed place. These mushrooms did not fall over small diameter alder debris or with river by fish or birds and these may distribute and decompose quickly. Near mature systems with similar conditions. Further spores even further. fruiting bodies, older mushrooms had surveys to establish the range of this In addition to collecting and lost their caps, and the mushrooms species will be essential for determining videographing aquatic invertebrates had been reduced to softening stipes the relevant conditions for this unusual associated with P. aquatica, I observed undulating in the current, trapping debris fruiting phenomenon.

Taylor Lockwood presents another collection of beautiful mushrooms from America and around the world. 11” x 8.5”. 11” x 17” hanging. Saddle-stitched. Thirteen months including Jan. ‘15 and mini-months. Printed in the USA. Price $14.95

To order, visit: www.Mushroom.pro

FUNGI Volume 6:4 2013 41 Acknowledgements I thank Carol Ferguson, Peter Schroeder and Michael Parker for help with identification of invertebrates and for useful editorial comments, and Darlene Southworth for reviewing drafts of this manuscript. References Cited Fogel, R. 1975. Insect mycophagy: a preliminary bibliography. USDA Forest Service General Technical Report PNW-36. Frank, J.L., R.A. Coffan, and D. Southworth. 2010. Aquatic gilled mushrooms: Psathyrella fruiting in the Rogue River in southern Oregon. Mycologia 102(1): 93-107. doi: 10.3852/07-190 Frank, J.L. 2013. AQUATICA: The Underwater Mushroom. Video Documentary. Ashland Independent Film Festival, Ashland, OR. 15 mins. Lilleskov, E.A., and T.D. Bruns. 2005. Spore dispersal of a resupinate ectomycorrhizal fungus, Tomentella sublilacina, via soil food webs. Mycologia 97(4): 762-769. ORBIC: Oregon Biodiversity Information Center. 2010. Rare, Threatened and Endangered Species of Oregon. Portland, OR. Institute for Natural Resources, Portland State University. 105 p. Figure 6 (lower left). Basidiocarp development in Psathyrella Figure 5. Spores of P. aquatica a) from gut of caddisfly, b) from gut of mayfly aquatica: a-b) young basidiocarp and c) from fruiting body. with pileus slightly wider than stipe and cottony evanescent partial veil, c) veil is lost; cap is incurved and narrowly convex; gas collects beneath pileus; small gas bubbles adhere to hyphae, d) pileus enlarges, convex to campanulate; gas bubble beneath pileus enlarges and undulates in current; smaller gas bubbles continue to adhere to pileus and stipe; fibrils of lower stipe trap suspended sediments, e) cap broadens; spores mature; aquatic insect larvae and naiads present, some in the gills and on upper stipe f) stipe standing in current after cap detaches and falls into tangle of vegetation and debris below, g) stipe softens and undulates in current and h) falls back into substrate.

42 FUNGI Volume 6:4 2013