**3.1 Hidden diversity**

Several aquatic microhabitats – well studied for bacteria - have not yet been well incorporated in biodiversity studies on fungi (Wurzbacher et al., 2010). These microhabitats include biofilms (periphyton, benthic algae), floating algae, and submerged/floating macrophytes, which contribute substantially to lake primary productivity. Detrital aggregates (lake and riverine snow) are also known hotspots of bacterial activity in the pelagic zone of lakes and large rivers, but fungal contribution to these aggregates has not been evaluated. Although remineralisation processes have been well studied for bacteria, fungi have been largely excluded from these studies. The riparian/littoral zone of aquatic

sampling programs using consistent methodology to evaluate fungal biodiversity in

Gessner & Van Ryckegem (2003) estimated the total number of aquatic fungal species to a maximum of 20 000 different species based on the assumption that only 5% have been described so far. Whereas only a few newly described fungal species have been added in recent years, an increasing number of genetically distant environmental DNA sequences have been found (Hibbett et al., 2011). For example, biodiversity of basal fungal lineages, which bear numerous aquatic species, seems to be much higher than expected. In addition, biodiversity of these basal phyla is elevated in aquatic sediments when compared to terrestrial soil (Mohamed & Martiny, 2011). The highest estimates of global fungal diversity reach up to 5 million species (Blackwell, 2011). The above mentioned "lower fungi" belonging to *Eumycota*, excluding

Currently, the species ratio of terrestrial fungi to land plants is approximately 10.6:1. Most likely, this ratio will increase in the future since mycologists have largely increased their efforts to find new fungal species. Freshwater ecosystems can be considered as rather unexplored fungal habitats whereby the few, presently available molecular studies point to a high species diversity. Blackwell (2011) gives helpful suggestions on where to search for these hidden species and highlights insects and other animals as potential fungal habitats. For example, in a single pilot-study in 2005, Suh et al. have isolated 196 new yeast species from guts of mushroom eating beetles and thereby increased the total number of worldwide described yeast species by more than 30%. Next to fungi residing in arthropod guts, endophytes in freshwater ecosystems are another budding source of high fungal biodiversity. For example, when applying molecular tools Neubert et al. (2006) found >600 fungal operational taxonomic units (a measurement of environmental DNA sequence diversity) in single plants (*Phragmites australis*) of a single lake (Lake Constance). This remarkably high diversity of endo- and ectophytic fungi points to a so far largely hidden

As already mentioned, fungal parasites in pelagic systems can greatly add to global fungal diversity, which should by far exceed even that of saprophytic fungi. This is due to the following features of parasitic fungi: (1) the presence of a specialised attack-defence coevolution based on the red queen hypothesis and (2) a high specificity to host species of various eukaryotes. A precise estimation of their diversity is difficult since parasites can be either host strain specific (De Bruin et al., 2008) or cover a wider spectrum of hosts such as *B. dendrobatidis.* In addition to parasitic fungi, many opportunistic saprophytic fungi are hostspecific (Sparrow, 1960). Nevertheless, variability in host and substrate specificity is high

Several aquatic microhabitats – well studied for bacteria - have not yet been well incorporated in biodiversity studies on fungi (Wurzbacher et al., 2010). These microhabitats include biofilms (periphyton, benthic algae), floating algae, and submerged/floating macrophytes, which contribute substantially to lake primary productivity. Detrital aggregates (lake and riverine snow) are also known hotspots of bacterial activity in the pelagic zone of lakes and large rivers, but fungal contribution to these aggregates has not been evaluated. Although remineralisation processes have been well studied for bacteria, fungi have been largely excluded from these studies. The riparian/littoral zone of aquatic

various aquatic systems around the globe.

congruously *Oomycetes* and *Thaustrochytrids*, are listed in table 1.

fungal diversity associated with higher aquatic organisms.

among aquatic fungi and it is difficult to generalise.

**3.1 Hidden diversity** 


Table 1. Lower fungal phyla of *Eumycota* in accordance to Hibbett et al. (2007) and Lara et al. (2010). Detailed information was obtained mainly from Sparrow (1960), Hywel-Jones & Webster (1986), Ebert (1995), Keeling & Fast (2002), Lichtwardt (2004) and Benny (2009). Asterisks mark not yet confirmed phyla.

systems is an ideal habitat for fungi and hence should be the focus of future fungal biodiversity research. Littoral food webs are very complex and a wealth of invertebrates, vertebrates and progeny suggest close interaction with a diverse community of fungi including parasitic, symbiotic and endophytic fungi. Littoral zones are highly structured by large emerged macrophytes, floating macrophytes and submerged macrophytes, which can

Aquatic Fungi 241

Fig. 5. *Zoophagus tentaclum* captures rotifers and grows epiphytic on *Nitella* (Figure from

The importance of fungi as secondary producers of biomass has been well described for headwater streams with leaf litter (Suberkropp, 1992) and for reed stands in littoral zones of lakes and in marshlands. The foregut content of 109 different aquatic insects collected on submerged wood showed that in 66% of all studied insect species fungi were part of their diet (Pereira et al., 1982) and many conidia of aquatic fungi were found in faeces of fish (Sridhar & Sudheep, 2011). Furthermore, it has been shown that food web manipulations greatly alter the fungal biomass in lakes (Mancinelli et al., 2002). This suggests that saprophytic fungi transfer organic matter directly to the higher trophic levels of aquatic food webs. It is therefore likely that environmental change can have severe consequences for

In addition, fungi can be important parasites of primary producers, e.g. phytoplankton, which fuel the aquatic food web with organic matter and energy. Lysis of aquatic organisms by fungal and protozoan parasites increases organic matter and energy cycling. These processes are often solely attributed to *Bacteria* and *Archaea*, however, aquatic fungi actively

Aquatic systems typically lack effective herbivores meaning that most of the biomass of aquatic macrophytes and riparian plant litter enters the detrital organic matter pool and is subsequently metabolised and transformed into microbial biomass, making it available for higher trophic levels. Generally, a major fraction of carbon will be respired (as CO2) during degradation, whereas nutrients such as phosphorus and nitrogen are efficiently

Karling (1936) with permission)*.* 

contribute as mineralisers and parasites.

**4.1 Mineralisation** 

**4. Importance of fungi for aquatic food webs** 

overall food web topology, and hence nutrient and energy cycling.

form a dense meadow and are suitable habitats for fungal proliferation. The high diversity of algae, pelagic and benthic species, and their function as an accumulation zone for dissolved nutrients and terrigenous detritus from the catchment, renders the littoral zone an ideal fungal habitat. Littoral sediments are often well aerated by the roots of emergent and submerged macrophytes and form microenvironments with strong physico-chemical gradients frequently altered by water movement and bioturbation by invertebrates such as mussels or chironomids. Therefore, it is not surprising that Willoughby (1961) found a high diversity and activity of fungi in soils on lake margins. Monchy et al. (2011) observed a high biodiversity in littoral water, and Mohamed & Martiny (2011) found a positive relation of fungal biodiversity to abundance of macrophytes. Nevertheless, fungi are often difficult to recognize due to methodological and morphological considerations: a single observed hypha of one species is visually indistinguishable from a thousand other fungal species. Fungi are highly variable in size and many tend to grow hidden inside their substrates, all factors which make them difficult to study and easy to overlook. The recent and on-going development of modern molecular tools, however, enables ecologists to better resolve biodiversity and ecology of aquatic fungi (e.g. Neubert et al., 2006, Baar et al., 2011). Still, most aquatic plants are only superficially examined for fungi (Orlowska et al., 2004) and many unexplored aquatic microhabitats potentially serve as niches for specialists. Examples include a mutualistic relationship of a predatory *Oomycete* living inside a mussel and protecting the mussel from parasite infections, e.g. nematodes (DeVay, 1956). Another predatory fungus uses the surface structure of macroalgae and grows epiphytically on *Characea* meadows (see figure 5). The most impressive example for interspecies relationships with high impact for general fungal biodiversity considerations stems from members of *Arthropoda.* Theoretically, one single animal can simultaneously provide microhabitats for several aquatic fungi (not including saprophytic or coprophagous fungi): host muscle cells as habitat for intracellular parasites of Microsporidia (Ebert, 1995; Messick et al., 2004); in the host tissue yeasts can be found (Ebert et al., 2004); and in the haemocoel occasionally detrimental *Chytridiomycetes* occur (Johnson et al., 2006). Moreover, an obligate endoparasite of *Entomophthorales* (Sparrow, 1960) and likely a represantative of *Coelomomycetes* (Whisler et al., 1975) can be found and the animal's gut hosts yeasts and symbiotic species of *Harpellales*  (trichomycetes; Strongman & White, 2008). Lastly, obligate ectoparasites belonging to an order of higher fungi called *Laboulbeniales* (*Ascomycota)* grow well on the chitinous integument. These fungi are not really aquatic, but more or less specific for arthropods, independent of habitat and are visible on their exoskeletons (Weir, 2004). Interestingly, almost all parasites and symbionts (with the exception of yeasts) are more or less host specific and *Laboulbeniales* are even sex-host specific. If we assume host specificity, a ratio of 6:1 between fungi and their arthropod host species, then a tremendous, yet hidden, fungal biodiversity is implied.

In aquatic microhabitats oxygen conditions can be extremely variable and hence it is important for fungi to be capable of survival or even growth under such conditions. Anoxic conditions are prevalent in aquatic sediments, in animal guts, in biofilms, on decomposing particles or, at a larger scale, in di- to polymictic lakes with seasonally anoxic water masses. Several fungi can withstand anoxic conditions or even grow fermentatively (Held et al., 1969). For example, archaic anoxic environments seem to be predominant habitats for lower fungi and yeasts (Stock et al., 2009; Mohamed & Martiny, 2011) but are awaiting mycologists to explore them.

form a dense meadow and are suitable habitats for fungal proliferation. The high diversity of algae, pelagic and benthic species, and their function as an accumulation zone for dissolved nutrients and terrigenous detritus from the catchment, renders the littoral zone an ideal fungal habitat. Littoral sediments are often well aerated by the roots of emergent and submerged macrophytes and form microenvironments with strong physico-chemical gradients frequently altered by water movement and bioturbation by invertebrates such as mussels or chironomids. Therefore, it is not surprising that Willoughby (1961) found a high diversity and activity of fungi in soils on lake margins. Monchy et al. (2011) observed a high biodiversity in littoral water, and Mohamed & Martiny (2011) found a positive relation of fungal biodiversity to abundance of macrophytes. Nevertheless, fungi are often difficult to recognize due to methodological and morphological considerations: a single observed hypha of one species is visually indistinguishable from a thousand other fungal species. Fungi are highly variable in size and many tend to grow hidden inside their substrates, all factors which make them difficult to study and easy to overlook. The recent and on-going development of modern molecular tools, however, enables ecologists to better resolve biodiversity and ecology of aquatic fungi (e.g. Neubert et al., 2006, Baar et al., 2011). Still, most aquatic plants are only superficially examined for fungi (Orlowska et al., 2004) and many unexplored aquatic microhabitats potentially serve as niches for specialists. Examples include a mutualistic relationship of a predatory *Oomycete* living inside a mussel and protecting the mussel from parasite infections, e.g. nematodes (DeVay, 1956). Another predatory fungus uses the surface structure of macroalgae and grows epiphytically on *Characea* meadows (see figure 5). The most impressive example for interspecies relationships with high impact for general fungal biodiversity considerations stems from members of *Arthropoda.* Theoretically, one single animal can simultaneously provide microhabitats for several aquatic fungi (not including saprophytic or coprophagous fungi): host muscle cells as habitat for intracellular parasites of Microsporidia (Ebert, 1995; Messick et al., 2004); in the host tissue yeasts can be found (Ebert et al., 2004); and in the haemocoel occasionally detrimental *Chytridiomycetes* occur (Johnson et al., 2006). Moreover, an obligate endoparasite of *Entomophthorales* (Sparrow, 1960) and likely a represantative of *Coelomomycetes* (Whisler et al., 1975) can be found and the animal's gut hosts yeasts and symbiotic species of *Harpellales*  (trichomycetes; Strongman & White, 2008). Lastly, obligate ectoparasites belonging to an order of higher fungi called *Laboulbeniales* (*Ascomycota)* grow well on the chitinous integument. These fungi are not really aquatic, but more or less specific for arthropods, independent of habitat and are visible on their exoskeletons (Weir, 2004). Interestingly, almost all parasites and symbionts (with the exception of yeasts) are more or less host specific and *Laboulbeniales* are even sex-host specific. If we assume host specificity, a ratio of 6:1 between fungi and their arthropod host species, then a tremendous, yet hidden, fungal

In aquatic microhabitats oxygen conditions can be extremely variable and hence it is important for fungi to be capable of survival or even growth under such conditions. Anoxic conditions are prevalent in aquatic sediments, in animal guts, in biofilms, on decomposing particles or, at a larger scale, in di- to polymictic lakes with seasonally anoxic water masses. Several fungi can withstand anoxic conditions or even grow fermentatively (Held et al., 1969). For example, archaic anoxic environments seem to be predominant habitats for lower fungi and yeasts (Stock et al., 2009; Mohamed & Martiny, 2011) but are awaiting mycologists

biodiversity is implied.

to explore them.

Fig. 5. *Zoophagus tentaclum* captures rotifers and grows epiphytic on *Nitella* (Figure from Karling (1936) with permission)*.* 
