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Biogeography of aquatic hyphomycetes: Current knowledge and future

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Article  in  Fungal Ecology · August 2015

DOI: 10.1016/j.funeco.2015.06.002

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Biogeography of aquatic hyphomycetes: Current

knowledge and future perspectives
€
Sofia DUARTEa,*, Felix BARLOCHER b
 udia PASCOALa, Fernanda
, Cla

CASSIO a

a
Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho Campus de
Gualtar, 4710-057 Braga, Portugal
b
Department of Biology, Mount Allison University, Sackville, New Brunswick E4L 1G7, Canada

article info abstract

Article history: Since Ingold’s (1942) initial description, mycologists have been interested in deciphering
Received 2 March 2015 global distribution patterns of aquatic hyphomycetes, a group of fungi that play a key role
Revision received 26 May 2015 in plant-litter decomposition in freshwaters. However, many questions remain largely
Accepted 5 June 2015 unanswered. In this review, we used distribution data of morphospecies from studies
Available online 1 August 2015 throughout the world in an attempt to better understand the magnitude of global species
Corresponding editor: richness, patterns of biodiversity and the extent of cosmopolitanism versus endemism.
Lynne Boddy Sampling efforts have varied among geographic regions, and correlate significantly with
species richness. Community similarity decreased with geographic or latitudinal distance.
Keywords: Species richness was highest at mid-latitudes (temperate streams), and high community
Aquatic hyphomycetes similarities were found between geographically distant locations in similar climatic zones.
Biogeography Studies relying on morphotypes have undoubtedly provided relevant information on the
Phylogeography geographic distribution of aquatic hyphomycetes. However, metagenomic approaches
Metagenomics combining taxonomic, phylogenetic and functional diversity in coordinated surveys will be
Morphospecies the best option to better decipher diversity patterns of these fungi and their functional
Genetic diversity roles at a global scale.
Next-generation sequencing ª 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction spanning more than 50 mm) of two predominant shapes:

Fungi are widely distributed across all biomes and play a
major role in the recycling of organic matter with more than
600 species reported from freshwaters (Wong et al., 1998;
Shearer et al., 2007). Ingoldian fungi or aquatic hyphomycetes
abound in well-aerated waters and are regarded as the dom-
inant microbial decomposers of leaves decaying in streams
€rlocher, 2016). Members of this ecologically defined group
(Ba
regularly sporulate under water, and have large conidia (often
branched and often tetraradiate or multiradiate (stauroid),
and sigmoid or worm-like (scolecoid) (Gulis et al., 2005;
Shearer et al., 2007) (Fig. 1). Much of our knowledge on aquatic
hyphomycete diversity in freshwaters emerges from species
classification based on their characteristic conidial shapes.
Though slightly heavier than water, conidia are readily trap-
ped in foam or scum, which accumulates in streams (Ingold,
1975). Conidia can also be sampled from the water column by
filtration or from naturally colonized submerged substrata

* Corresponding author.
E-mail address: sduarte@bio.uminho.pt (S. Duarte).
http://dx.doi.org/10.1016/j.funeco.2015.06.002
1754-5048/ª 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.
170 S. Duarte et al.

(e.g. leaves, twigs) and substrate baits after inducing spor-
ulation in the laboratory (Gulis et al., 2005).
De Wildeman (1893, 1894, 1895) was the first to recognize
some of the typical conidial forms of aquatic hyphomycetes
and described species of several genera (Clavariopsis, Lemon-
niera and Tetracladium) (Fig. 1). However, these fungi only
gained relevance nearly half a century later when Ingold
(1942) described 16 forms of conidia and traced them back to
mycelia on decaying alder leaves in a stream near Leicester, in
England. In the first of many papers devoted to aquatic
hyphomycetes, Ingold (1942) wrote: “My observations on
aquatic hyphomycetes have been limited, so far, to the
immediate neighbourhood of Cropston in Leicestershire, but it
is of interest to know if they are of wide occurrence”. In sub-
sequent years, he found identical or similar spores in samples
from many regions in Britain (Ingold, 1943a,b), and other parts
of the world, including Europe (e.g. Switzerland: Ingold, 1949),
Africa (Nigeria: Ingold, 1956, 1959; Uganda and Zimbabwe:
Ingold, 1958; Swaziland: Ingold, 1973), North America (Canada:
Ingold, 1960) and Caribbean Islands (e.g. Jamaica: Hudson and
Ingold, 1960), thus demonstrating the world-wide occurrence
of aquatic hyphomycetes. Studies by other researchers con-
firmed their global distribution (e.g. California: Ranzoni, 1953;
Japan: Tubaki, 1957; eastern USA: Petersen 1962, 1963a,b;
Scandinavia: Nilsson, 1958, 1964; South Africa: Greathead,
1961; Australia: Cowling and Waid, 1963; Cuba: Marvanova 

Fig. 1 e Conidia of aquatic hyphomycetes. A, Alatospora acuminata; B, Anguillospora filiformis; C, Articulospora tetracladia; D,
Clavariopsis aquatica; E, Collembolispora barbata; F, Dimorphospora foliicola; G, Dendrospora erecta; H, Flagellospora penicillioides;
I, Heliscus lugdunensis; J, Heliscus submersus; K, Lemonniera aquatica; L, Lunulospora curvula; M, Tetracladium marchalianum; N,
Tetracladium setigerum; O, Tetrachaetum elegans; P, Tricladium attenuatum; Q, Tricladium chaetocladium; R, Tricladium
splendens; S, Varicosporium elodeae; and T, Ypsilina graminea.
Biogeography of aquatic hyphomycetes
and Marvan, 1969 and Malaysia: Nawawi, 1985). Compared to
other freshwater fungi, the distribution of aquatic hyphomy-
cetes is relatively well studied and several data compilations
exist based on morphospecies (taxonomy based on morpho-
logical differences of the conidia) (e.g. Ingold, 1975; Webster
and Descals, 1981; Marvanova  , 1997; Santos-Flores and
Betancourt-Lo  pez, 1997; Gulis et al., 2005), although studies in
tropical latitudes have been less common (e.g. Sridhar et al.,
1992; Goh, 1997; Marvanova  , 1997). Comparable communities
exist in temperate zones on both sides of the equator; streams
closer to the equator are represented by a characteristic
tropical mycoflora, which nevertheless contains many species
common to temperate zones (Wood-Eggenschwiler and
Ba€ rlocher, 1985). In fact, many species of aquatic hyphomy-
cetes have been found in stream foam collected in different
parts of the world (Ingold, 1975; Webster and Descals, 1981),
suggesting that the distribution of aquatic hyphomycetes
might follow the hypothesis of Baas Becking (1934). This
hypothesis postulates, with respect to microbes, that “every-
thing is everywhere” and that small organisms (<2 mm)
capable of dispersal have cosmopolitan distribution and are
found in suitable habitats with little or no evidence of his-
torical constraints, but with the important qualification that
“the environment selects” (Baas Becking, 1934). Consequently,
different contemporary environments should maintain dis-
tinctive microbial assemblages (Martiny et al., 2006).
However, questions regarding the magnitude of global
species richness, patterns of alpha (local) and beta (degree of
community differentiation) diversity and the extent of cos-
mopolitanism and endemism of aquatic hyphomycetes
remain largely unanswered. The most convincing approach to
answer these questions would be to perform coordinated and
systematic surveys in different geographic regions, however,
to our knowledge the largest study surveyed only 4 countries
over 5 latitudes and one stream per location (Jabiol et al., 2013).
Alternatively, species distribution data from the literature can
be used (e.g. Wood-Eggenschwiler and Ba €rlocher, 1985;
Shearer et al., 2007). In an attempt to improve our knowledge
on the geographic distribution of aquatic hyphomycetes, we
gathered data on species distribution in freshwater ecosys-
tems from different types of substrata (natural or artificial
foam, scum, water, and decaying plant litter). Studies that
surveyed aquatic hyphomycetes in terrestrial environments
or temporary aquatic ecosystems (e.g. tree holes, stem flow,
rain drops, rainwater from trees; see Chauvet et al., 2016)
were excluded. The selected data were published between
December 1942 and October 2014, and included those avail-
able in the “Web of Science” database, as well as others in
national journals, theses and taxonomic guides. The search
terms used in the Web of Science database were: “aquatic
hyphomycete” or “Ingoldian fungi” or “water borne spora” or
“water borne conidia” or “water borne fungal spores” or
“water borne fungal conidia” or “water borne fungi”. Aquatic
hyphomycete species names were validated using the Index
Fungorum (http://www.indexfungorum.org/), because names
of some species changed after their first description (up to 34
species) (Supplementary Appendix 2). In addition, we
attempted to assess to what extent DNA-based techniques
have helped to elucidate the phylogeography of aquatic
hyphomycetes, and we speculate how recently developed
171
molecular approaches may deepen our knowledge in deci-
phering biogeographic patterns of stream dwelling decom-
poser fungal communities.
Current knowledge of geographic distribution of
aquatic hyphomycetes
Based on data from 352 publications (Supplementary Appen-
dix 1) documenting 335 morphospecies (Supplementary
Appendix 2) on a wide range of substrata, we confirmed that
aquatic hyphomycetes are indeed very widely distributed
(Fig. 2), as stated previously (Ingold, 1975; Webster and Des-
cals, 1981; Wood-Eggenschwiler and Ba € rlocher, 1985). Not
surprisingly, the most intensively studied geographic regions
include temperate zones of the Northern hemisphere (mid-
latitudes), particularly in Europe (Fig. 2), where Ingold con-
ducted his first surveys (e.g. 1942, 1943a,b) followed by many
other authors (Supplementary Appendix 1). Other well-stud-
ied regions include North America (Northern Temperate e
USA and Canada), the Tropics (Venezuela, Brazil and Puerto
Rico) and Asia (Tropical Asia, in particular India) (Fig. 2). The
least studied regions are in Africa, with the exception of South
Africa, and the polar regions, where only a small number of
aquatic hyphomycetes has been reported (Fig. 2; regions
defined by the geographic location plus climate influence as in
Shearer et al., 2007). In fact, parts of Africa have been largely
neglected for many fungal groups (Crous et al., 2006). It has
been widely recognized that our perception of the geo-
graphical distribution of fungi is inherently biased due to
region-specific sampling efforts by mycologists (Wood-
Eggenschwiler and Ba € rlocher, 1985; Shearer et al., 2007; Raja
et al., 2009; Ba€ rlocher, 2010). A fundamental pattern in eco-
logical studies is an increase in the number of observed spe-
cies as the sampled area increases (Zinger et al., 2014, see next
sub-section). Ecologists often use such speciesearea curves to
estimate the minimum size of a sampled area necessary to
adequately characterize a community, by plotting a curve and
estimating the area after which more sampling adds only “a
few more species” e the minimum area (Scheiner, 2003). We
plotted a curve with our data (Fig. 2), and used the number of
studies, which is related to the sampling effort, as a proxy of
the sampled area. The data were fitted to a rectangular
hyperbola (analogous to the MichaeliseMenten equation).
Based on this model, at least ca. 29 papers per region would be
necessary to document 50% of the actual number of species,
and 275 papers to achieve 90% (Fig. 3). Of the 15 geographic
regions surveyed, only Northern temperate and tropics
(western hemisphere) and Europe temperate and tropical Asia
(eastern hemisphere) meet the 50% and none meets the 90%
target. Other speciesearea curves yield lower estimates
(Zinger et al., 2014), but Fig. 3 clearly suggests that for most
regions, there is only preliminary information on the true
diversity of aquatic hyphomycetes. Nevertheless, the large
dataset created in the current review allowed us to test several
ecological concepts on aquatic hyphomycetes: taxaearea and
distanceedecay relationships; the influence of latitude on
species richness and of the geographic region/climate in
structuring aquatic hyphomycete communities in world
freshwaters. Since the classic indices of compositional
172 S. Duarte et al.

similarity are quite sensitive to sampling size, especially for indicators of spatial turnover (Zinger et al., 2014). The former
assemblages with numerous rare species, which was the case can be expressed as S ¼ k*Az, where S corresponds to the
of our dataset, Chao’s abundance-based index was used in all number of species, k is a constant that is empirically derived
species turnover analyses (Chao et al., 2005). from the taxon and the specific location, A is the sampled area
and z the rate at which species increase with area or the rate of
Taxaearea and distanceedecay relationships species accumulation (Zinger et al., 2014). If “everything is
everywhere”, almost all species in a community would be
When assessing biodiversity, taxaearea and the dis- expected within a very small area and few, if any new species,
tanceedecay relationships are the most informative would be discovered by sampling larger areas (Bell et al., 2005).

Western Hemisphere Eastern Hemisphere

Aquatic hyphomycete

400 sub-Arctic Tropical

species richness

Boreal sub-Tropical
Temperate
300

200

100

0
sub-Arctic

Boreal

Boreal
Tropics
Northern Temperate

sub-Arctic
Southern Temperate

Europe temperate

Northern Africa

Tropical Africa

Temperate Africa

Tropical Asia

Oceania
Temperate Asia
Mid East

Fig. 2 e Distribution of aquatic hyphomycetes (335 species) and species richness in 15 geographic regions in the western
and eastern hemispheres (defined based on the geographic location plus climate influence; Shearer et al., 2007). Data were
retrieved from 352 diversity surveys based on morphospecies (i.e., morphological differences in fungal conidia). Different
colours depict different climatic influences and bicolour dots are climatically intermediate locations. Details on the surveys
are in Supplementary Appendix 1.
Biogeography of aquatic hyphomycetes
400
Species richness S
300
200
100
E SE)
r = 0.9252
0 reaching 36.5  C (Chandrashekar et al., 1991). Constraints due
0 50 100 150 200
Sampling effort SE
Fig. 3 e Relationship between aquatic hyphomycete
species richness and the sampled area. The number of
studies, which is related to the sampling effort, was used
as a proxy of the sampled area for each geographic region
(see Fig. 2). Data were fitted to the MichaeliseMenten
model in Prism 4.0 for Windows (GraphPad software Inc.,
San Diego, CA, USA).
For example, Fenchel and Finlay (2004) found as many mor-
phospecies of protists in a single lake as previously described
from the entire world. Earlier studies suggested that z for
microbial taxa (ca. 0.002e0.07) falls well below that observed
for taxonomic groups of larger organisms (ca. 0.1e0.6) (Bell
et al., 2005; Zinger et al., 2014). However, more recent evidence
suggests that the rate of species increase observed for plants
and animals may also be found for certain microbes (ca.
0.3e0.6) (e.g. ectomycorrhizal fungi, Peay et al., 2007; marine
bacteria, Zinger et al., 2014). By using the number of studies,
which is related to the sampling effort, as a proxy of the
sampled area, at a regional scale (70 regions that corre-
sponded to different countries except for USA, Canada and
Russia where 3 regions were defined), we calculated a z of
0.6923 (Fig. 4A), which is quite similar to that found for com-
munities of larger organisms (e.g. Bell et al., 2005). However,
we are not able to conclude that some aquatic hyphomycetes
have a restricted geographic distribution, due in part to the
uneven number of studies conducted in different regions. In
addition, some of these studies were conducted many years or
decades apart, which may bias our analysis. For instance,
most of the data obtained for the African continent rely on
very old studies and many aquatic hyphomycetes were not
identifiable to species at that time (e.g. Ingold, 1956, 1958,
1973).
Recently, Sato et al. (2012) hypothesized that the biogeo-
graphic distribution of microbial species depends on their
colonization ability and degree of isolation of suitable hab-
itats; species that experience negligible constraints for colo-
nization may have broader distribution (e.g. root-inhabiting
fungi with low host specialization) (Queloz et al., 2011) than
those with strong colonization constraints (e.g. host specific-
ity) and habitat isolation (e.g. ectomycorrhizal fungi: Sato
et al., 2012; Tedersoo et al., 2014a,b; hot-spring cyanobacteria:
Papke et al., 2003; Whitaker et al., 2003). The wide geographic
173
distribution of aquatic hyphomycetes suggests excellent dis-
persal abilities (Ba € rlocher, 2009), which would tend to flatten
the relationship between species richness and sampled area
(Ba€ rlocher, 2010). Although the diversity of aquatic hypho-
mycetes is high in pristine habitats (Krauss et al., 2011), some
species are remarkably resilient and can occur in harsh
environments, such as in streams with high levels of metals
(Krauss et al., 2001; Sole  et al., 2008), and/or high nutrient

loads (Pascoal and Cassio, 2004; Pascoal et al., 2005; Duarte
et al., 2009), and even in sulphur springs with temperatures
to substratum specificity should also be less stringent, since
most aquatic hyphomycetes are capable of colonizing a wide
range of deciduous leaves (Webster and Descals, 1981), though
substrata such as wood and grass appear to be more selective
(Gulis, 2001). On the other hand, streams within the same
region but with different physico-chemical conditions har-
bour different communities (e.g. Pascoal et al., 2005; Castela
et al., 2008; Sole et al., 2008; Duarte et al., 2009). This suggests a
degree of selective colonization and niche differentiation by
aquatic hyphomycetes.
The distanceedecay relationship indicates how similarity
in community composition changes with geographic distance
between sites, and represents the compositional turnover rate
(Green et al., 2004), and any effect of richness (e.g. Legendre,
2014). We found that aquatic hyphomycete community sim-
ilarity based on morphospecies negatively correlated with
increasing geographic distance (Fig. 4B). However, the dis-
persion of our data was high (r2 ¼ 0.065), in part because
conidial abundance in streams is strongly affected by natural
or anthropogenic factors, which can fluctuate on a daily or
seasonal scale. These factors include temperature (e.g.
Chauvet, 1991; Ba € rlocher et al., 2011), pH (e.g. Ba € rlocher and
Rosset, 1981; Casas and Descals, 1997), conductivity (e.g.
Wood-Eggenschwiler and Ba € rlocher, 1983), altitude (e.g.
Chauvet, 1991; Ba € rlocher et al., 2011), differences in riparian
vegetation (Ba € rlocher and Graça, 2002), and presence of vari-
ous pollutants (e.g. metals, Sole  et al., 2008; high nutrient
loads, Pascoal et al., 2005; Castela et al., 2008; Duarte et al.,
2009; Schoenlein-Crusius et al., 2009). These confounding
factors might blur overall patterns of aquatic hyphomycete
diversity distribution. In bacteria, the relative influence of
historical (natural barriers) versus environmental factors
seems to be related to the scale of sampling (Martiny et al.,
2006). Communities separated by only a few kilometres (up to
10 km) were structured by environmental factors (Kuske et al.,
2002; Horner-Devine et al., 2004), while at intermediate scales
(10e3000 km), significant effects of distance were detected
(Green et al., 2004; Reche et al., 2005; Yannarell and Triplett,
2005). On the other hand, at an intercontinental scale, bacte-
rial assemblages in hot springs were differentiated by distance
but did not correlate with any environmental variable (Papke
et al., 2003; Whitaker et al., 2003). A similar pattern was found
for fungi from wetland sediments in China; variation in fungal
diversity was driven by natural barriers at a regional sale
(1000e4000 km) and by environmental factors at a smaller
scale (<1000 km) (Wu et al., 2013). In fact, environmental
factors influence the composition of aquatic hyphomycete
communities at small spatial scales (2.9e100 km) (Pascoal
et al., 2005; Castela et al., 2008; Sole  et al., 2008; Duarte et al.,
174 S. Duarte et al.

Community similarity CS
6 1.0
A B CS = -1.183*10 *GD + 0.4687
r = 0.06530

Species richness S
0.8 P<0.0001

4
0.6

(log) 0.4
2
logS = 0.6923*logSEf + 2.739 0.2
2
0.5514

0 0
0 1 2 3 4 0 5000 10000 15000 20000 25000
Sampling effort SEf (log) Geographic distance (km) GD
200 S = 64.71/(1+((L-41.26)/ 1.0 CS = -2.042*10 *L + 0.4397
C D

Community similarity CS
(-36.89)) ) r = 0.06457
P<0.0001
Species richness S

r = 0.08394 0.8
150
0.6
100
0.4
50
0.2

0
-90-75-60-45-30-15 0 15 30 45 60 75 90 0 50 100 150
Latitude L (º) Pairwise latitudinal difference L (º)

25 60
E F
Cosmopolitan species

Endemic species

20 0.02076*S
SE = 2.046*exp
richness SC

richness SE

40 r = 0.8112
15

10
20
5 SC = (27.34*S)/(30.18+S)
r = 0.7555
0 0
0 50 100 150 200 0 50 100 150 200
Species richness S

Fig. 4 e Relationships between: sampling effort (SEf ) (number of studies) and species richness (S ) (in 70 regions) (A),
geographic distance (GD) and community similarity (CS ) (B), latitude (L) and species richness (C), pairwise latitudinal
difference and community similarity (D), species richness and cosmopolitan species (SC ) (E), and species richness and
endemic species (SE ) (F). Linear regression models gave best fits for the relationships in (A), (B) and (D). Non-linear
regression models gave best fits for the relationships in (C) (Lorentzian model), (E) (MichaeliseMenten model), and (F)
(exponential model). Similarity analysis of aquatic hyphomycete communities in (B) and (D) were assessed with Chao’s
abundance-based Sørensen index in EstimateS 9.0 for Windows (Colwell, 2013). The incidence of each species was based on
the number of times it appeared in the 352 publications surveyed. Regression analyses were performed in Prism 4.0 for
Windows (GraphPad software Inc., San Diego, CA, USA).

2009). In 16 streams distributed by 4 geographic areas in
France, Germany and Switzerland, community similarity was
highest within each region and clear differences between
regions were found (Wood-Eggenschwiler and Ba € rlocher,
1983). But in Australian streams, separated by up to 175.7 km,
the distance between streams accounted for a small portion of
the variability, while altitude, followed by temperature had
the most pronounced impact (Ba € rlocher et al., 2011). Thus,
previous studies suggested that there are few geographical
barriers limiting the dispersal of aquatic fungi (there are sev-
eral species with cosmopolitan distribution, i.e. identical
species occur in different continents and in geologically young
islands), but that their community structure is strongly
influenced by complex biotic and abiotic factors determined
on a regional basis (Wood-Eggenschwiler and Ba € rlocher, 1983).
Therefore, a global scale analysis with substantial sampling
effort is needed to elucidate the relative influence of con-
temporary and seasonally fluctuating environmental factors
Biogeography of aquatic hyphomycetes 175

versus the legacies of historical events/natural barriers on
present-day distribution patterns of aquatic hyphomycetes.
Latitude and climatic influence
An increase in species richness from higher (polar zones)
towards lower latitudes (equatorial zones) is the oldest and
most fundamental pattern of the distribution of life on earth
and a widely documented macroecological pattern, in partic-
ular in terrestrial ecosystems (e.g. Rosenzweig, 1995). In our
study, aquatic hyphomycete diversity was lowest at lat-
itudinal extremes and peaked at mid-latitude regions (tem-
perate streams) (Figs. 2 and 4C), as found in previous surveys
(Wood-Eggenschwiler and Ba € rlocher, 1985; Shearer et al., 2007;
Jabiol et al., 2013), but diverging from the conventional mac-
roecological pattern with higher diversity in the tropics. The
latter was confirmed in a recent study on freshwater lig-
nicolous fungi (Hyde et al., 2015). Shearer et al. (2015) exam-
ined the distribution of freshwater ascomycetes along an
elevational gradient (as analogue of latitudinal gradient) in
Peru from the Andes to the Amazon lowlands. They found a
slight peak at mid-elevations, however, in addition to altitude,
pH had a strong effect on fungal communities. Shearer et al.
(2015) did not specify the stream order of their collection sites;
regardless of altitude, many physico-chemical and biotic
properties change in a more or less predictable manner as one
moves downstream (Vannote et al., 1980).
If real, the greater diversity of aquatic hyphomycetes in
temperate streams may be explained by season due to more
diversified ecological niches (Shearer et al., 2007; Jabiol et al.,
2013). Graça et al. (2015) hypothesized that lower turbulence
and nutrient concentrations in many of the examined trop-
ical/subtropical streams and the presence of more highly
defended leaves may have contributed to the lower diversity
of aquatic hyphomycetes.
Kennedy et al. (2012) recently hypothesized that diversifi-
cation of ectomycorrhizal fungi may be more rapid in tem-
perate than tropical habitats, but at a global scale the
latitudinal patterns of diversity of soil fungi were similar to
those of plants and animals e a decrease was found towards
the poles (Meiser et al., 2014; Tedersoo et al., 2014b).
Aquatic hyphomycete community similarity decreased
with the increase of latitudinal difference (Fig. 4D). This lends
some credence to Ingold’s (1966) statement “I think I could tell
my latitude with an error of 15 by examining the aquatic
spores in a sample of stream foam”, and emphasizes the
impact of latitude on the distribution of aquatic hyphomy-
cetes. Non-metric multi-dimensional scaling analysis (MDS)
based on the occurrence of the 335 aquatic hyphomycete
species in 15 geographic regions (definition based on the
geographic location plus climate influence; Shearer et al.,
2007) (Figs. 2 and 5, Supplementary Appendix 2) suggests
higher similarities between geographically distant locations
with similar climate (e.g. Tropical Asia and South America or
Temperate Europe and North America or Temperate Asia and
Temperate Africa). Wood-Eggenschwiler and Ba € rlocher (1985)
reached similar conclusions based on the distribution of over
150 aquatic hyphomycete species.
In our study, 4 species occurred in all 15 geographic regions
(Alatospora acuminata, Anguillospora longissima, Articulospora

1.5 2D Stress: 0.1

Tropical
1.0 sub-Tropical
Temperate
Boreal
sub-Arctic
1 0.5 15 12 14
4
7 3 13
11
6
-3.0 -2.0 -1.0 2 1.0 2.0 3.0
8
-0.5

10 9
-1.0

5
-1.5

Fig. 5 e Non-metric multi-dimensional scaling (MDS) ordination diagram based on aquatic hyphomycete communities in
each geographic region (defined by geographic location plus climate influence; Shearer et al., 2007). Similarities of aquatic
hyphomycete communities were assessed with Chao’s abundance-based Sørensen index in EstimateS 9.0 for Windows
(Colwell, 2013). The incidence of each species was based on the number of times it appeared in the 352 publications
surveyed. Western hemisphere: 1, sub-Arctic; 2, Boreal; 3, Northern temperate; 4, Tropics; 5, Southern temperate; Eastern
hemisphere: 6, sub-Arctic; 7, Boreal; 8, Europe temperate; 9, Mid East; 10, Northern Africa; 11, Tropical Africa; 12, Temperate
Africa; 13, Temperate Asia; 14, Tropical Asia and 15, Oceania. Different colours depict different climatic influences and
bicolour dots are climatically intermediate locations. MDS analysis was performed in Primer v6 for Windows (Plymouth,
UK).
176
tetracladia and Lemonniera aquatica), 36 species occurred in 10
of the geographic regions (Appendix 2), and 67 species were
restricted to 1 geographic region. Aquatic hyphomycetes may
follow a biogeographical model of restricted moderate
endemism, as suggested by Foissner (1999) for small eukar-
yotes; some species are cosmopolitan whereas others are
biogeographically and ecologically limited. Jabiol et al. (2013)
in a recent survey across a broad latitudinal gradient also
found many species with cosmopolitan distribution from the
arctic to the tropics (e.g. A. tetracladia, Flagellospora curvula),
while others were restricted to single locations (e.g. Triscelo-
phorus acuminatus and Triscelophorus monosporus were only
observed in the tropical location). One of the major con-
straints of aquatic hyphomycete diversity analysis based on
morphospecies is that the probability of finding rare species
depends on the approach used to document the occurrence of
conidia. The simultaneous use of several methods e collection
of natural foam and plant substrata, and the use of artificial
foam and substratum baits e will increase the probability of
finding rare species (e.g. Shearer and Webster, 1985; Pascoal
et al., 2005). In fact, while the number of cosmopolitan species
(found in more than 50% of the regions) increased asymp-
totically with the total number of species found at a regional
scale (Fig. 4E), the number of endemic or rare (found in less
than 10% of the regions) species increased exponentially
(Fig. 4F). Species that are present but not captured lead to
undersampling or unequal sampling and are one of the major
sources of error when estimating microbial diversity (Torsvik
et al., 2002; Sato et al., 2012). Our understanding of the geo-
graphical distribution of aquatic hyphomycete species would
clearly benefit from more comprehensive sampling strategies
that can capture a higher diversity.
Contribution of DNA-based studies to reveal
phylogeographic patterns
Since most aquatic hyphomycete species are believed to be
readily identifiable by their conidial morphology, ecological
studies continue to rely on this straightforward approach to
measure fungal diversity (Gulis et al., 2005) (Fig. 1). Partly for
this reason, DNA based techniques were applied later to
aquatic hyphomycetes than to other morphologically less
diverse fungal groups (e.g. Nikolcheva et al., 2003; Manerkar
et al., 2008; Seena et al., 2008; Clivot et al., 2013). Using the
reproductive ability of a fungus as a proxy for its contribution
to ecological functions or overall diversity, presents a clear
bias in favour of prolific spore producers (e.g. Duarte et al.,
2009). In addition, accurate identification is often difficult or
impossible in species producing less differentiated conidia
(e.g. scolecoid conidia). Many aquatic hyphomycete species
appear to be cosmopolitan, but conclusions based on mor-
phospecies overlook cryptic species and may blur global-scale
biogeographical patterns. Indeed, DNA-based studies in other
fungal groups are providing increasing evidence that not
“everything is everywhere” and that fungi do have a bio-
geography (Hibbet, 2001; Dettman et al., 2006; Taylor et al.,
2006; Meiser et al., 2014).
At present, molecular studies on the phylogeography of
aquatic hyphomycetes do not allow any well-supported con-
clusions, since very few attempts have been made to analyse
S. Duarte et al.
biogeographic patterns based on DNA data. Two studies using
internal transcribed spacer region (ITS) barcodes from cos-
mopolitan species with isolates from different geographic
regions, have somewhat contradictory conclusions (Duarte
et al., 2012; Seena et al., 2012). Several ITS genotypes of A.
tetracladia were geographically widespread (Iberian Peninsula,
Central Europe, United Kingdom, Canada, and Japan) irre-
spective of sampling time, substratum or location (Seena
et al., 2012), but Malaysian genotypes grouped in a different
phylogenetic clade and were not shared by other countries
(Seena et al., 2012). Duarte et al. (2012) studied ITS genotypes
of 130 strains from 6 species isolated from plant litter or foam
in streams in Europe and Australia. Distribution patterns were
species-specific: European and Australian genotypes of
Anguillospora filiformis, Flagellospora penicillioides, Geniculospora
grandis and Tetrachaetum elegans were consistently different,
while those of Lunulospora curvula and Tricladium chaetocladium
were intermixed in the phylogenetic trees. Similar genotypes
were found in both continents for T. chaetocladium, suggesting
intercontinental gene flow in this species (Duarte et al., 2012).
On the other hand, a study with 97 isolates of T. elegans
from 9 streams within a 1450 km2 area in Southwestern
France showed that only 20% of molecular variance, assessed
by amplified fragment length polymorphism (AFLP), was
explained by stream location (Laitung et al., 2004). Although a
high genotypic diversity based on polymorphic microsatellite
loci was found for 391 isolates of Tetracladium marchalianum
from rivers in Illinois and Wisconsin (Anderson and Shearer,
2011), stable genetic differentiation was only observed
between the most distant rivers (ca. 450 km) (Anderson and
Shearer, 2011). These studies suggest that environmental
barriers to dispersal may play a role in the genetic structure of
aquatic hyphomycete species, but patterns were not con-
sistent and biogeography within aquatic hyphomycetes may
be species-specific. In addition, the analysis of 96 strains of
T. elegans from a single site yielded 13 random amplified pol-
ymorphic DNA (RAPD) profiles and some genotypes were more
abundant on particular leaf species and rare or absent in
others (Charcosset and Gardes, 1999). Thus, the resource
quality (substrate type) may constrain aquatic hyphomycete
colonization.
Unfortunately, the sample size of most studies was small
(number of isolates or spatial scale) and relied on DNA from
pure cultures. This conventional approach is time-consuming
and its success is greatly affected by the probability of getting
isolates from different geographic areas belonging to the same
morphospecies (Duarte et al., 2012). Phylogenetic information
for many lineages, their abundances and geographical
occurrence, and the associated environmental data are clearly
needed to elucidate why populations of a given aquatic
hyphomycete (morpho)species occur and persist in a geo-
graphic region, but not in others (Ba € rlocher, 2010).
Do molecular tools promise a deeper knowledge
in deciphering the biogeography of aquatic
hyphomycetes?
Molecular tools have dramatically increased our knowledge of
Fungi in less than 20 years (Persoh, 2015), but many fungal
Biogeography of aquatic hyphomycetes
species remain to be discovered (Blackwell, 2011). There is no
doubt that molecular techniques provide powerful tools to
reveal stream-dwelling fungal diversity more deeply and
widely than ever before (Ba € rlocher, 2010, 2016). Understanding
the biogeography of aquatic fungi will continue to benefit
from these methodological advances.
Different molecular tools have been applied to assess
stream-dwelling decomposer fungal communities (DGGE: 5
streams in Northwestern Portugal, Duarte et al., 2009; 5
streams in Northeastern France, Clivot et al., 2013; 9 streams
in South-central Sweden, Bergfur and Sundberg, 2014; clone
libraries: 5 streams in Northeastern France, Clivot et al., 2013;
and 454 pyrosequencing: 30 streams in North-western and
-eastern Finland, Tolkkinen et al., 2013; Heino et al., 2014; 5
streams in Northwestern Portugal, Duarte et al., 2015). In these
studies, aquatic hyphomycete communities were structured
by similar environmental drivers, regardless of whether they
were evaluated by conidium identification or genetic diversity
(e.g. pH, nutrients, fluvial geomorphology) (Duarte et al., 2009;
Clivot et al., 2013; Bergfur and Sundberg, 2014; Duarte et al.,
2015). But studies relying on 454 pyrosequencing detected
differences at the genetic level; for instance, A. tetracladia
operational taxonomic units (OTUs) on decomposing oak
leaves differed among streams along a gradient of eutrophi-
cation (Duarte et al., 2015). In fact, intraspecific traits of
A. tetracladia modulated the effects of biodiversity on eco-
logical processes (e.g. plant litter decomposition) under stress
conditions (Fernandes et al., 2011). Next generation sequenc-
ing technology promises a higher resolution for testing the
degree of differentiation between communities.
An additional advantage of pyrosequencing is its sensi-
tivity to detect very rare species recovered as “singletons” i.e.,
unique sequences that may be informative of exclusive line-
ages in “rare biospheres” (Zhan et al., 2013). Rare taxa may
contribute disproportionally to overall metabolic activities
(Jones and Lennon, 2010; Campbell et al., 2011), carry out
unusual metabolic functions (Galand et al., 2009) and show
distinct spatial distribution patterns. Applying Next Gen-
eration Sequencing (NGS) to cDNA (the synthesis of cDNA
from RNA is only possible in metabolically active species) (e.g.
Kuramae et al., 2013) will provide greater insights into meta-
bolically active species.
To disentangle the relative importance of local versus
regional factors in structuring aquatic hyphomycete com-
munities in world freshwaters, repeated, multi-scale sam-
pling is crucial (Heino et al., 2014). In fact, the pyrosequencing
of soil samples from 365 globally distributed sites allowed, for
the first time, integrating fungi into a general macroecological
framework (Tedersoo et al., 2014b). Environmental parame-
ters weakly explained community composition of plant-
associated fungi (endophytic, root-associated and soil), and
effects were inconsistent at local and regional scales in met-
a’omics studies (Persoh, 2015). But decreased community
similarity with increasing distance from local to global scales
seems to be due to the inability of fungi to establish them-
selves at a particular locality (i.e. via environmental filtering or
competitive exclusion), rather than to spatially limited dis-
persal (Per soh, 2015). This is in accordance with a meta-
analysis of fungal communities from phyllosphere and soils
based on 454 pyrosequencing suggesting that globally
177
distributed OTUs may be rare in fungi (Meiser et al., 2014). In
fact, only 14% of the fungal species overlapped in soil samples
collected at a distance of 1 m (Taylor et al., 2010). Similar
results were found in pyrosequencing studies of other
microbial eukaryotic communities from the deep-sea (fungi,
nematodes, protists) (Bik et al., 2012; Creer and Sinniger, 2012)
and protozoa from soil, freshwater and marine sediments
(Bass et al., 2007). A few taxa were cosmopolitan, but the
majority showed restricted and/or patchy distribution.
NGS technologies will continue to improve both accuracy
and throughput and, in the near future, benchtop sequencers
will become standard equipment in individual labs. Amplicon
analyses are expected to become a rapid screening technique
in preparation for more detailed metagenomic studies, rather
than representing the final stage in ecological analysis
(Nikolaki and Tsiamis, 2013). While NGS technologies may
inform us that different geographic regions harbour different
aquatic fungal communities, they will not reveal much about
their function. This will require the application of functional
metagenomics, i.e. analysis of the complete genetic informa-
tion including the relative abundance of all genes, allowing a
description of the functional potential of each community
(Chistoserdova, 2014). Coupling metagenomic analyses with
extensive cross-site sampling efforts led to a more compre-
hensive picture of biogeographical patterns in diversity,
community composition and functional attributes of soil
fungal communities (Fierer et al., 2012). New approaches
exploiting NGS technologies and single cell genomics (char-
acterizing genomes of uncultured phyla from single cells
obtained directly from the environment; Lasken, 2007) may
target genomes and associate them with quantitative meas-
urements in particular geographic regions. This approach
potentially targets all active members (abundant and rare) of a
given ecosystem, quantifies the transcribed genes, and
obtains complete genomes (Nikolaki and Tsiamis, 2013). Sin-
gle cell genomics have been employed to investigate the bio-
geographic distribution of uncultured marine Flavobacteria
and marine bacterioplankton (Mason et al., 2012; Woyke et al.,
2009). The application of this methodology to stream-dwelling
decomposer fungi seems feasible because a single spore can
be used as a source of DNA (Ba € rlocher et al., 2010).
Outlook and perspectives
A central question in ecological research is how biodiversity is
structured by spatial processes and environmental factors.
The conventional view in microbial ecology emphasized that
“everything is everywhere, but the environment selects” (Baas
Becking, 1934), implying that microbial species occur at sites
of suitable conditions instead of occurring at specific geo-
graphic locations. It has been assumed that aquatic hypho-
mycetes have a world-wide distribution (e.g. Ingold, 1975;
Sridhar et al., 1992; Marvanova  , 1997), but relevant informa-
tion is still scarce partly due to uneven sampling efforts in
different geographic regions (Jabiol et al., 2013). In addition,
most surveys have been based on the morphology of detached
conidia, which can be ineffective or misleading when dealing
with closely related or morphologically convergent species.
DNA-based studies might avoid the pitfalls presented by
studies based on morphospecies. Recent sequencing efforts
178
are revealing a large amount of hidden microbial diversity (e.g.
Meiser et al., 2014). However, many ecosystems, among them
streams, where aquatic hyphomycetes play a key role in
organic matter turnover, remain largely unexplored (but see
Duarte et al., 2015) and are promising targets for discovering
new fungal taxa and revealing diversity patterns. High-
throughput studies have barely scratched the surface of the
vast information that remains to be explored concerning
stream-dwelling decomposer fungi. As more locations are
scrutinized and sequencing efforts become more extensive
with new technology, more endemic species may be dis-
covered. More studies, incorporating different habitats and
environmental conditions, are needed to decipher global
trends of fungal biodiversity in world freshwaters, and met-
agenomic approaches that use a combination of taxonomic,
phylogenetic and functional diversity applied in coordinated
surveys at a global scale will be indispensable for revealing
these patterns.
Acknowledgements
This work was supported by FCT I.P. through the strategic
funding UID/BIA/04050/2013. Financial support granted by the
FCT to S. Duarte (postdoctoral fellowship SFRH/BPD/47574/
2008) is also gratefully acknowledged.
Supplementary data
Supplementary data related to this article can be found at
http://dx.doi.org/10.1016/j.funeco.2015.06.002.
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