In most aquatic habitats there is a submersion gradient from land to
water. The positions of such gradients may fluctuate seasonally and/or
episodically with weather events, thus it is difficult to establish
precise aquatic boundaries. Likewise, the degree of submergence of the
substrates of freshwater ascomycetes will vary with fluctuations in
water level. Thus if the definition of presence in water is used, the
same species may be considered terrestrial or freshwater depending on
the water level at the time that they are observed. As more
collections from freshwater habitats are made, our ability to define
this mycota more precisely will improve. The freshwater ascomycetes,
although monophyletic at the class level, comprise a diverse
assemblage of species with representatives in a variety of disparate
orders (e.g., Leotiales, Pezizales, Rhytismatales, Eurotiales,
Amphisphaeriales, Diaporthales, Hypocreales, Halosphaeriales,
Sordariales, Xylariales, Pleosporales and Melanommatales). Thus
definition by taxonomy is not useful. As a working definition, all
ascomycetes that occur on submerged or submerged parts of partially
submerged substrates are considered freshwater ascomycetes. Results
from past studies indicate that many freshwater ascomycetes are known
only from water and occur over broad geographic areas. Recently a new
order Jahnulales was established within the Dothideomycetes
(loculoascomycetes) for a monophyletic group of freshwater lignicolous
ascomycetes (Pang et al. 2002; Campbell et al. in review). Other
species are known only from water and occur at only a few sites but
occur in consecutive years at their respective sites. This suggests
that a distinctive freshwater ascomycota does exist. It is only
through detailed, extensive worldwide surveys and sequencing the fungi
found in these habitats, along with phylogenetic analyses that a
freshwater ascomycota can be confirmed and characterized.
Geographical Distribution.
There are so few comprehensive studies of freshwater ascomycetes of
different geographical areas that little can be said about their
worldwide geographical distribution patterns, except that they reflect
the geographical distribution of their collectors (Shearer 1993, Hyde
et al. 1997, Shearer 2001). In recent surveys conducted by the Shearer
Lab, the ranges of all the previously known species collected were
extended.
For example, Pseudoproboscispora caudae-suis was known from
only its type locality in the Lake District of England (Ingold
1951). We have collected this fungus 37 times in North America. It
occurs at latitudes ranging from 30°-55° N and longitudes
3°-124° W; however, it has not yet been reported from the
eastern or southern hemisphere.
The southern most distribution of Pseudoproboscispora
caudae-suis in North America is the Apalachicola National Forest
(29-30° N) in Florida.
Distinctive species distribution patterns for a number of frequently
occurring species were revealed as a result of our collections:
(1) Species which occur over a broad
latitudinal range, e.g.,
Aniptodera chesapeakensis,
Pseudoproboscispora caudae-suis,
Halosarpheia retorquens,
Kirschsteiniothelia elaterascus,
Lutrellia estuarina,
Massarina ingoldiana,
Nais inornata,
Pseudohalonectria lignicola,
Submersisphaeria aquatica and
Savoryella lignicola.
Not surprisingly, many of these species were among the first to be
described from freshwater habitats.
(2) Species restricted to latitudes of about 45° and above, e.g.,
most Discomycetes, Macrospora scirpicola;
(3) Species restricted to latitudes of about
45° and below, e.g., Cleistothecial sp. A-99, Boerlagiomyces
websteri, and
Zopfiella lundqvistii,
(4) Species that appear to occur only in the
tropics, e.g.,
Halosarpheia heteroguttulata,
Fluviatispora reticulata,
Phaeonectriella lignicola,
Aniptodera lignatilis,
Aniptodera palmicola,
Aniptodera inflatiascigera;
and (5) Species that appear to be limited to
their host distribution patterns, e.g.,
Massariosphaeria scirpina,
Ascovaginospora stellipala,
Phaeosphaeria typhae (Shearer 2001),
Discomycete species F-47 (Raja and Shearer unpublished).
For the vast majority of species, however, occurrences are too few in
number to elucidate distribution patterns at this time. Clearly much
more work is needed in this area. With respect to species richness
along latitudinal gradients, if all species reported worldwide are
considered, a pattern of greatest richness in mid-latitudes in both
the northern and southern hemispheres, with lower richness at low and
high latitudes is revealed (Shearer et al. 2003).
Preliminary Beta diversity (variation in species composition among
sites in a geographic area) values between freshwater ascomycetes
collected in Wisconsin (46 °N latitude), and Florida (29-25 °N
latitude) were quite high (about 0.90) suggesting a complete
difference in species composition between the temperate and
subtropical fresh water sites within North America. These preliminary
beta diversity results provide important implications for
conservation of freshwater habitats, since high species turnover
reflects deterministic processes such as adaptations to climate,
substrate or habitat type and influences diversity. Knowledge of the
geographical distribution patterns of freshwater ascomycetes is
important since freshwater habitats are declining at an alarming rate
due to human activities and climate change (Dudgeon et
al. 2006). Perturbation of aquatic habitats can lead to loss of
species, which may further lead to alteration of ecological processes
and ecosystem function (Firth and Fisher 1991, Kareiva et al. 1993).
Substrate Distribution.
A variety of aquatic macrophytes, including species of Carex, Juncus,
Phragmites, Scirpus and Typha serve as substrates for freshwater
ascomycetes. Although species occurrences on aquatic macrophytes have
been reported sporadically in taxonomic treatises (Mueller 1950, Holm
1957, Munk 1957, Leuchtmann 1984), the first systematic efforts to
collect freshwater ascomycetes on aquatic macrophytes were by Ingold
(1951, 1954, 1955) and Ingold and Chapman (1952). These pioneering
studies were followed by those of Webster and Lucas (1961), Dudka
(1963), Pugh and Mulden (1971), Apinis et al. (1972a, b), Taligoola et
al. (1972), Magnes and Hafellner (1991) and Fallah and Shearer
(2000). Although Ingold (1955) predicted a rich pyrenomycetous mycota
on aquatic macrophytes, this substrate type has been largely
unstudied. Data from recent studies support Ingold's prediction and
amplifies it in that the ascomycota on aquatic macrophytes is not only
rich in pyrenomycetes but also in other groups such as the
loculoascomycetes and discomycetes (Magnes and Hafellner 1991, Fallah
and Shearer 1998a-c, Fallah et al. 1998, Fallah and Shearer
2000). Allochthonous woody debris as a substrate for freshwater fungi
has been studied more frequently (e.g., Dudka 1963, Shearer 1972,
Willoughby and Archer 1973, Lamore and Goos 1978, Minoura and Muroi
1978, Shearer and von Bodman 1983, Shearer and Crane 1986, Revay and
Gonczol 990, Shearer and Webster 1991, Hyde et al. 1998, Ho et
al. 2002, Raja and Shearer 2003; 2006a,b; Raja et al. 2005), and
numerous ascomycetes have been reported from these studies (Shearer
2001; Shearer et al. 2007). Ascomycetes have also been reported from
water-saturated wood in cooling towers, a sort of artifical tropical
habitat (Eaton and Jones 1971a, b, Eaton 1972, Udaiyan 1989, Udaiyan
and Hosagoudar 1991). In addition, many new taxa of ascomycetes have
been described from wood in freshwater (e.g., Webster 1959, Webster,
1965, Webster and Lucas 1961, Tubaki 1966, Jones and Eaton 1969, Iqbal
1972, Minoura and Muroi 1978, Shearer 1978, Shearer and Crane 1978,
Shearer and Crane 1980a, b, Abdullah and Webster 1981, Fisher and
Petrini 1983, Fisher and Webster 1983, Monod and Fisher 1983, Shearer
1984, Shearer 1989 a, b, Webster et al. 1991, Crane et al. 1992, Hyde
1992a-c, 1993, 1995a,b, 1996, Crane and Shearer 1995, Shearer and
Crane 1995, Hyde et al. 1996, Shearer and Hyde 1997, Hyde 1998,
Shearer and Crane 1998, Fallah et al. 1998, Shearer et al. 1999; Tsui
et al. 2002, 2003; Ho et al. 200; Dhanasekaran et al. 2005; see the
World Database for a complete summary). Although the fungi colonizing
allochthonous deciduous leaves have been studied more intensively than
those on wood, only a few meiosporic ascomycetes have been reported
from this substrate type (Shearer 1992). Allochthonous deciduous
leaves are colonized primarily by Ingoldian mitosporic ascomycetes and
a few basidiomycetes (Bäerlocher 1992).
Habitat Distribution.
A number of studies on freshwater ascomycetes have been conducted at
spatially limited sites in either lotic (Lamore and Goos 1978, Shearer
and Von Bodman 1983, Hyde and Goh, 1997; Hyde et al. 1998, Hyde and
Goh 1998b, Hyde and Goh 1999, Sivichai et al. 2000, 2002, Tsui et
al. 2001, 2003, 2003, Tsui and Hyde 2004, Kane et al. 2002, Ho et
al. 2001, 2002, Cai et al. 2003, Fryar et al. 2004) or lentic habitats
(Shearer and Crane 1986, Hyde and Goh 1998a, Goh and Hyde 1999, Fallah
et al. 1999, Cai et al. 2002, Luo et al. 2004). However, there have
been no studies that target both habitat types within a small
relatively homogenous geographical area. To better understand the
distribution of organisms, it is important to understand their
associations with different habitat types. More studies have been
carried out in lotic waters than in lentic waters, therefore, basic
knowledge of freshwater ascomycetes exists but at present, it is not
yet clear whether there is a unique group of ascomycetes in lentic
habitats. Fallah (1999) conducted a study of freshwater ascomycetes on
submerged wood and herbaceous material in lentic habitats in Northern
Wisconsin and reported 10 new species and two new genera of
ascomycetes with little species overlap in species composition among
the lakes and bogs studied. Goh and Hyde (1999) conducted a study of
freshwater fungi from a single reservoir in Hong Kong and found eight
new species of ascomycetes. More recently, several species of
ascomycetes were described from peat swamps in Thailand (Pinruan et
al. 2002, Pinruan et al. 2004a, b, Pinnoi et al. 2003, Pinnoi et
al. 2004). A number of these fungi appear to be unique to lentic
habitats and have not been previously reported from lotic
waters. Additional studies comparing lentic and lotic habitats are
needed to determine whether lentic habitats contain species of
freshwater ascomycetes that are restricted to these habitat
types. Studies from our lab thus far suggest that the composition of
the freshwater ascomycota differs between lentic and lotic habitats,
but that some geographically broadly distributed species occur in both
habitats but numerous species occur in either lotic or lentic
habitats. Lentic habitats might support more unique communities of
freshwater ascomycetes, but we need additional comparative collections
in different geographical locations to support this initial
observation.
Systematics.
The systematics of ascomycetes in general is at present controversial
and taxonomic schemes abound (Hawksworth, et al. 1995). The
classification system of Barr (1987, 1990) as modified by new
molecular based information
(Myconet,
http://www.fieldmuseum.org/myconet/
)
is used in World Monograph. Based on Barr's classification scheme, ~
500 species of ascomycetes in 20 orders have been reported from
freshwater habitats. Of the known species, 111 are Discomycetes, 257
are Pyrenomycetes and 162 are Loculoascomycetes. Orders with 10 or
more representatives from fresh water are Sordariales (82 spp.),
Leotiales (101 spp.), Pleosporales (106 spp.), Melanommatales (30
spp), Eurotiales (25 spp.), Halosphaeriales (25 spp.), Hypocreales (14
spp.), Jahnulales (18 spp). These orders represent distinctly
different evolutionary lines, indicating that adaptation to the
freshwater habitat has occurred numerous times. At the same time, it
appears that certain evolutionary lines (Leotiales, Pleosporales,
Sordariales) have been more successful than others in the freshwater
habitat. Numerous newly described freshwater ascomycetes are incertae
sedis above the generic level. Hopefully molecular phylogenetic
studies of freshwater ascomycetes will help resolve the phylogenetic
relationships and taxonomic placement of these taxa.
The mitosporic ascomycetes found in fresh water can be divided into
several groups: the Ingoldian hyphomycetes, the aeroaquatic
hyphomycetes, the dematiaceous hyphomycetes, and the coelomycetous
hyphomycetes or the (miscellaneous mitosporic fungi) Shearer et
al. (2007). These taxa are somewhat easy to identify because of their
morphologically distinctive spores. Their phylogenetic relationships,
for the most part, are unknown except for a few studies (see Belliveau
and Bärlocher 2005; Baschein et al. 2006; Campbell et
al. 2006). Isolations of freshwater ascomycetes and phylogenetic
analyses of molecular sequences should help to identify the
phylogenetic relationships of freshwater mitosporic ascomycetes.
The taxonomic diversity of freshwater ascomycetes and the absence of
taxonomic keys for their identification make them difficult to
identify. There are several general works on ascomycetes that have
proved to be useful (Dennis 1978, Kohlmeyer and Kohlmeyer 1979,
Kohlmeyer and Volkmann-Kohlmeyer 1991, Korf 1973, Luttrell 1973,
Mueller and v. Arx 1973, Sivanesan 1984) and monographs of specific
groups (Mueller 1950; Holm 1957; Munk 1957; Eriksson 1967; Hedjaroude
1969; Lundqvist 1972; Barr 1978, 1987, 1990; Leuchtmann 1984,
Shoemaker and Babcock 1989). More recently two books on Freshwater
ascomycetes have been published by Tsui and Hyde (2003), and Cai et
al. (2006), which can be used for the identification of some tropical
freshwater ascomycetes. Some descriptions and illustrations are now
available on this site in the Species Monograph Database.
Evolution.
It is likely that most freshwater ascomycetes have evolved from
terrestrial ancestors via a variety of evolutionary pathways. A recent
study by Dhanasekaran et al. (2006) on origins of freshwater
ascomycetes supports the above hypothesis. One such pathway is that of
pathogens, endophytes and saprophytes of wetland and aquatic
plants. As these plants invaded freshwater habitats, they no doubt
brought their associated microorganisms with them. Fungal species able
to survive and adapt to aquatic habitats may have been ancestral to
present-day species that occur on freshwater macrophytes. Included in
this group are primarily Discomycetes and Loculoascomycetes. A second
route to freshwater habitats may have been on riparian vegetation in
the form of tree and shrub litter. This debris carries with it a large
variety of fungi capable of adapting to freshwater. Included in this
assemblage are Discomycetes, Hypocreales, Sordariales, and
Loculoascomycetes. A third route to freshwater habitats may have been
through the run-off of rainwater and sediments that carry propagules
of species in the Eurotiales, Sordariales and Hypocreales. One way to
test these hypotheses is by collecting and isolating freshwater
ascomycetes for use in molecular phylogenetic analyses of ascomycetes
from terrestrial and freshwater habitats. Kohlmeyer and Kohlmeyer
(1979) suggested that extant marine fungi could be divided into two
groups based on their origins. Primary ascomycetes (e.g.,
Halosphaeriales) evolved directly from a marine ancestor, probably one
common to both marine fungi and red algae. Secondary marine
ascomycetes originated from terrestrial ancestors and are mostly
saprophytic.
Kohlmeyer and Kohlmeyer (1979) agreed with Savile (1968) that
parasites are more ancient than saprophytes and they suggested that
the most ancient types of marine ascomycetes are Spathulosporales and
some parasitic Xylariales (sub Sphaeriales) on marine
Rhodophyta. Molecular data now available do not support the red algal
ancestry of marine ascomycetes (Spatafora et al. 1998). Based on 18s
rDNA, the scolecosporus freshwater ascomycetes do not appear to be
closely related to species in the marine scolecosporous ascomycete
genus, Lulworthia (Spatafora et al. 1998; Chen et al. 1999).
A large number of freshwater ascomycete taxa, ~70, are considered
inc. sed. and cannot be accommodated in any existing orders or
families. There are a number of single taxa (belonging to about 17
genera) that differ in morphology from known taxa of Ascomycetes and
likely represent new evolutionary lineages. New, rare or unusual taxa
found during the surveys need to be sequenced for18S small-subunit,
SSU and 28S large-subunit LSU ribosomal genes to estimate their
appropriate taxonomic placement at the generic and ordinal
levels. These genes are appriopriate based upon the availability of
pre-existing data in GenBank, which have been used successfully in
previous phylogenetic studies of freshwater ascomycetes and in
accordance with the AFTOL project, which is a broad-scale phylogenetic
study of fungi.
Adaptations.
Freshwater ascomycetes appear to have adapted morphologically to
aquatic habitats in a variety of ways. One type of modification
involves the presence on ascospores of viscous, sticky appendages that
may enable the ascospores to stick onto substrates in moving
water. Species of freshwater ascomycetes in
Aniptodera,
Aquadiscula,
Pseudoproboscispora,
Ceriosporopsis,
Halosarpheia and Nais have ascospores equipped with
viscous appendages.
The appendages of
Aniptodera and
Halosarpheia spp. unwind to form extremely long, sticky threads
which may help to entangle the ascospores with substrates (Shearer and
Crane 1980b). The ascospores of several loculoascomycetes are equipped
with sticky gelatinous sheaths
(Aliquandostipite,
Jahnula,
Leptosphaeria,
Luttrellia,
Massarina,
Phaeosphaeria,
Pleospora,
Trematosphaeria)
or apical gelatinous appendages
(Flammispora,
Jahnula,
Lophiostoma,
Rebentischia,
Wettsteininia).
Since most of the foregoing loculoascomycete genera also contain
terrestrial species with ascospore sheaths or apical appendages,
aquatic representatives may have been pre-adapted. When introduced
into water, terrestrial ancestors with ascospore sheaths or appendages
may have been better able than species lacking these features to
attach to substrates in water and thus were more likely to
succeed. The cells at the base of the ascomata of all species of
Jahnulales produce broad, brown, thick-walled hyphae that spread
across the substrate and often connect adjacent ascomata. Initially
these broad hyphae were considered to be algal associates (Hyde and
Wong 1999), but more recently Pinruan et al (2002) considered this
unlikely. These thick filaments are connected to and/or develop from
peridial cells, and hence, are fungal (Raja and Shearer 2006). These
large, brown hyphae are produced in cultures derived from single
ascospores of Jahnulales species. It is hypothesized that these
repent, connecting hyphae may play an important role in colonizing and
holding fungi onto softened wood in wet or aquatic habitats, which may
represent another adaptative feature for an aquatic existence (Raja
and Shearer 2006; Dhanashekaran et al. 2006). However, unlike other
adaptive characters, which are homoplastic due to convergent
evolution, the thick walled hyphae developing from the ascomata of
members of the Jahnulales is an evolutionarily informative character
(Pang et al. 2002; Campbell et al. in review).
Many marine ascomycetes have evolved a fascinating array of ascospore
appendages formed by the fragmentation and/or extension of outer
ascospore walls (Jones and Moss 1978). None of the appendages reported
thus far for freshwater ascomycetes appear to result from these
mechanisms. The sigmoid spore form as an adaptation to freshwater and
marine habitats has been discussed frequently (Webster and Davey 1984,
Webster, 1987; Jones, 2006). The sigmoid shape increases the area of
orthogonal projection and the long filamentous structure enhances
entanglement with substrates. Sigmoid ascospores are found in numerous
freshwater Discomycetes
(Apostemidium,
Loramyces,
Niptera,
Obtectodiscus,
Vibrissea)
and Pyrenomycetes (Ophioceras,
Plagiosphaeria,
Pseudohalonectria).
Ascomal and ascus structure and function do not seem to be modified
for aquatic habitats. There is little difference in these structures
between aquatic and terrestrial counterparts. Deliquescent asci are
present in some genera
(Aniptodera,
Fluviatispora,
Halosarpheia,
Nais).
It is thought that this is an adaptation to water, as ascospores can
be washed from ascomata and forcible discharge is not necessary. An
interesting situation exists in Pseudohalonectria (Shearer
1989b) and Ophioceras (Conway and Kimbrough 1978) in which asci
separate from ascogenous hyphae, are discharged, and assume a
sigmoidal shape in water. Ascospores and asci are released
simultaneously in submerged culture. The larger size of the ascus,
compared to a single ascospore may improve the chances of impaction on
substrates.
Numerous freshwater ascomycetes have adapted to freshwater via their
anamorphs (Shearer 1993, Sivichai and Jones 2003; this site
Anamorph/Teleomorph Database). Anamorphs with
branched, tetraradiate, sigmoid, helicosporous and multicellular
air-trapping conidia have been reported for freshwater
ascomycetes. The functional significance of helical spore forms in
aquatic habitats has been discussed by Ingold (1975) and Webster
(1987, 1992). The sigmoidal conidial form appears to have evolved in
several different evolutionary lines. It occurs in discomycetes,
pyrenomycetes, and loculoascomycetes. Comparable adaptation through
modification of anamorphs has not occurred as frequently in marine
ascomycetes. Only three similar teleomorph-anamorph connections have
been made for marine ascomycetes (Shearer and Crane 1971, Nakagiri and
Tubaki 1983; Kohlmeyer et al. 1998). This is not surprising given that
seawater apparently selects against conidial forms (Shearer
1972). Connections between freshwater ascomycete teleomorphic states
and aquatic hyphomycete anamorphic states are relatively
rare. Continued efforts to connect anamorphs and teleomorphs of
freshwater ascomycetes are needed to shed light on evolutionary
relationships in both the freshwater ascomycetes and Ingoldian,
aeroaquatic and the miscellaneous mitosporic fungi.
© Carol Shearer & The University of Illinois at Urbana-Champaign
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