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Fungal Ecology
journal homepage: www.elsevier.com/locate/funeco
Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho Campus de Gualtar, 4710-057 Braga, Portugal
Department of Biology, Mount Allison University, Sackville, New Brunswick E4L 1G7, Canada
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 2 March 2015
Received in revised form
26 May 2015
Accepted 5 June 2015
Available online xxx
Since Ingold's (1942) initial description, mycologists have been interested in deciphering global distribution patterns of aquatic hyphomycetes, a group of fungi that play a key role in plant-litter decomposition in freshwaters. However, many questions remain largely unanswered. In this review, we used
distribution data of morphospecies from studies throughout the world in an attempt to better understand the magnitude of global species richness, patterns of biodiversity and the extent of cosmopolitanism versus endemism. Sampling efforts have varied among geographic regions, and correlate
signicantly with species richness. Community similarity decreased with geographic or latitudinal distance. Species richness was highest at mid-latitudes (temperate streams), and high community similarities were found between geographically distant locations in similar climatic zones. Studies relying on
morphotypes have undoubtedly provided relevant information on the geographic distribution of aquatic
hyphomycetes. However, metagenomic approaches combining taxonomic, phylogenetic and functional
diversity in coordinated surveys will be the best option to better decipher diversity patterns of these
fungi and their functional roles at a global scale.
2015 Elsevier Ltd and The British Mycological Society. All rights reserved.
Keywords:
Aquatic hyphomycetes
Biogeography
Phylogeography
Metagenomics
Morphospecies
Genetic diversity
Next-generation sequencing
1. Introduction
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 dominant microbial decomposers
rlocher, in this issue). Members of
of leaves decaying in streams (Ba
this ecologically dened group regularly sporulate under water,
and have large conidia (often spanning more than 50 mm) of two
predominant shapes: 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 classication based on their characteristic conidial shapes.
Though slightly heavier than water, conidia are readily trapped in
foam or scum, which accumulates in streams (Ingold, 1975). Conidia can also be sampled from the water column by ltration or
from naturally colonized submerged substrata (e.g. leaves, twigs)
* Corresponding author.
E-mail address: sduarte@bio.uminho.pt (S. Duarte).
http://dx.doi.org/10.1016/j.funeco.2015.06.002
1754-5048/ 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Fig. 1. Conidia of aquatic hyphomycetes. A, Alatospora acuminata; B, Anguillospora liformis; 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.
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
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 tted 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 inuence 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 similarity are quite sensitive to sampling size,
especially for assemblages with numerous rare species, which was
the case of our dataset, Chao's abundance-based index was used in
all species turnover analyses (Chao et al., 2005).
2.1. Taxaearea and distanceedecay relationships
When assessing biodiversity, taxaearea and the distanceedecay
relationships are the most informative indicators of spatial turnover (Zinger et al., 2014). The former can be expressed as S k*Az,
where S corresponds to the number of species, k is a constant that is
empirically derived from the taxon and the specic location, A is the
sampled area and z the rate at which species increase with area or
the rate of species accumulation (Zinger et al., 2014). If everything
is everywhere, almost all species in a community would be expected within a very small area and few, if any new species, would
be discovered by sampling larger areas (Bell et al., 2005). For
example, Fenchel and Finlay (2004) found as many morphospecies
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
corresponded to different countries except for USA, Canada and
Russia where 3 regions were dened), we calculated a z of 0.6923
(Fig. 4A), which is quite similar to that found for communities 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 identiable to species at that time (e.g.
Ingold, 1956, 1958, 1973).
Recently, Sato et al. (2012) hypothesized that the biogeographic
distribution of microbial species depends on their colonization
ability and degree of isolation of suitable habitats; species that
experience negligible constraints for colonization 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 specicity) and habitat isolation (e.g.
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Eastern Hemisphere
400
sub-Arctic
Boreal
Temperate
300
Tropical
sub-Tropical
200
100
Oceania
Tropical Asia
Temperate Asia
Temperate Africa
Tropical Africa
Northern Africa
Mid East
Europe temperate
Boreal
sub-Arctic
Southern Temperate
Tropics
Northern Temperate
Boreal
sub-Arctic
Aquatic hyphomycete
species richness
Western Hemisphere
Fig. 2. Distribution of aquatic hyphomycetes (335 species) and species richness in 15 geographic regions in the western and eastern hemispheres (dened based on the geographic
location plus climate inuence; 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 inuences and bicolour dots are climatically intermediate locations. Details on the surveys are in Supplementary Appendix 1.
(Chandrashekar et al., 1991). Constraints due to substratum specicity 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 physicochemical conditions harbour different communities (e.g. Pascoal
et al., 2008; Duarte et al.,
et al., 2005; Castela et al., 2008; Sole
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
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Species richness S
400
300
200
100
SE)
r = 0.9252
0
0
50
100
150
200
Sampling effort SE
Fig. 3. 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 tted to
the MichaeliseMenten model in Prism 4.0 for Windows (GraphPad software Inc., San
Diego, CA, USA).
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Species richness S
(log)
Community similarity CS
2
logS = 0.6923*logSEf + 2.739
2
0.5514
1.0
0.8
0.6
0.4
0.2
0
Species richness S
200 S = 64.71/(1+((L-41.26)/
150
(-36.89)) )
r = 0.08394
100
50
1.0
0.8
CS = -2.042*10 *L + 0.4397
r = 0.06457
P<0.0001
0.6
0.4
0.2
0
-90-75-60-45-30-15 0 15 30 45 60 75 90
Latitude L ()
50
100
150
20
Endemic species
richness SE
25
Community similarity CS
Cosmopolitan species
richness SC
SE = 2.046*exp
r = 0.8112
40
15
10
0.02076*S
20
SC = (27.34*S)/(30.18+S)
r = 0.7555
0
0
50
100
150
200
0
0
50
100
150
200
Species richness S
Fig. 4. 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 ts for the relationships in (A), (B) and (D). Non-linear regression models gave best ts 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 Srensen 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).
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
1.5
2D Stress: 0.1
Tropical
sub-Tropical
Temperate
Boreal
sub-Arctic
1.0
0.5 15 12 14
1
7
-3.0
-2.0
6
-1.0
13
11
1.0
2.0
3.0
-0.5
10
-1.0
5
-1.5
Fig. 5. Non-metric multi-dimensional scaling (MDS) ordination diagram based on aquatic hyphomycete communities in each geographic region (dened by geographic location
plus climate inuence; Shearer et al., 2007). Similarities of aquatic hyphomycete communities were assessed with Chao's abundance-based Srensen 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 inuences and bicolour dots are climatically intermediate locations. MDS analysis was performed in Primer v6 for Windows (Plymouth, UK).
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002
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Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002