Underwater spore dispersal: a preliminary report
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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.
I
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
known 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
the short documentary, AQUATICA: The
mushroom has been observed from early
Identification Trilogy July to early October. I have also visited Underwater Mushroom (Frank, 2013).
streams and rivers in southern and central Mayflies, with their distinctive caudal
Now in wide-screen format
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 only a few days per year. The Rogue River also captured images of a caddisfly, replete
have been upgraded and/or replaced. with casing, crawling along the upper stipe
upstream from Prospect, and Union Creek
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
and later inspected them under a along the mushrooms underwater. While
www.mushroom.pro more data will be needed to confirm the
microscope. To my surprise, two black
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.
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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
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