**4.1 Mineralisation**

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

Aquatic Fungi 243

et al., 2002), but studies of aquatic fungi show that diversity influences neither productivity (Baldy et al., 2002) nor decomposition rates (Bärlocher & Graça, 2002; Dang et al., 2005). It is likely that both functional redundancy and resource partitioning operate within aquatic ecosystems, but on different spatial and temporal scales, and with impacts at the level of

In many aquatic ecosystems, saprobic fungi are important decomposer organisms. While some species show a preference for substrates derived from a particular plant species or plant tissue (i.e. leaves or wood), many fungal species are generalist saprobes (Gulis, 2001). This suggests that a large degree of functional redundancy exists among saprobic aquatic

Aquatic fungi are microscopic organisms that interact with other species and "individuals" on a microscopic scale via enzymes and biochemical defences. Therefore, resource partitioning by fungi can be expected to occur at the molecular scale. This idea is supported by the well documented temporal succession (Garrett, 1951) that occurs as fungi colonise a submerged leaf, and the temporal partitioning of the resource that is implied. In order to exploit a substrate, fungi secrete extra-cellular enzymes that attack and degrade its chemical constituents. As separate and distinct enzymes or enzyme systems are required for the breakdown of starches, cellulose, hemicellulose, pectin, proteins, lipids and lignin, the fungal species, armed with the suite of enzymes able to efficiently degrade the most labile leaf components, become the initial colonisers. When labile resources are depleted, species able to efficiently degrade the remaining resources become dominant, and so on (Chamier, 1985). Complex plant components such as lignin may be degraded by a range of enzymes secreted by a number of fungal species (Evans et al., 1994), and this is an example of resource partitioning at the sub-molecular level (lignin moieties). It is thus likely that the biodiversity of aquatic fungi has inherent functional redundancy at larger spatial scales, but at the molecular scale, and through time there is inherent functional complementarity,

There are a number of studies from the past few decades that have established a strong role of fungi as important basal resources in aquatic ecosystems (Bärlocher, 1985; Albariño et al., 2008; Chung & Suberkropp, 2009), most notably in streams (Reid et al., 2008; Hladyz et al., 2009). For example, fungal biomass has been shown to be an important food source for aquatic invertebrates such as snails (McMahon et al., 1974; Newell & Bärlocher, 1993) and insect larvae (Bärlocher, 1981; 1982; 1985). Thereby, the fungal biomass is either removed

A synthesis of research from aquatic systems suggests that the functional role of aquatic heterotrophic fungi in moderating the food value of plant detritus may be more important than their role as organic matter producers (e.g. Thorp & Delong, 2002). Litter produced outside a water body may enter the water directly, as a result of abscission from riparian plants overhanging the water body, or may undergo a period of terrestrial aging before entering the water. These two pathways result in differences in litter chemistry (Baldwin, 1999) that influence their importance to the aquatic food-chain (Watkins et al., 2010). In general, fresh plant material has a higher protein content (lower C:N) and a higher proportion of readily available nutrients than aged material (Williams, 2010; Kerr et al., in prep.). However, fresh material also contains inhibitory substances such as tannins, polyphenols and aromatic oils, which function to deter microbial attack and herbivory in the

fungi at spatial scales ranging from submerged substrates to the whole ecosystem.

individuals, populations and communities (Loreau, 2004).

competitive exclusion and resource partitioning.

from the leaf surface, or the leaf itself is consumed.

**4.1.2 Fungi as producers of organic matter** 

recycled. Microbial mineralisation of plant litter supports a complex food-web including all kinds of microbes (*Archaea*, *Bacteria*, fungi, protozoans) and invertebrates (nematodes, trematodes, gammarids, insects, snails). As a consequence plant litter even supplies top predators such as crayfishs, amphibians, birds, fishes and bats with organic matter and energy via the microbial food web. The main basis of the microbial food web consists of fungi and bacteria growing in and on the plant debris. Microorganisms, in particular fungi, possess enzymes capable of degrading even highly polymeric substances, and filamentous fungi are capable of degrading the plant material from the inside, driving the break down of high molecular weight polymers to smaller molecules of medium molecular weight (Fischer et al., 2006). These small fragments and oligomers, e.g. sugar residues, can be readily utilized by bacteria and the so called "sugar fungi" (a sloppy term for the lower fungal phyla consisting of *Chytridiomycota, Blastocladiomycota, Mucoromycotina, Zoopagomycotina, Oomycetes*). Freshwater hyphomycetes of temperate waters are usually well adapted to lower temperatures prevailing during leaf litter input and senescence of aquatic macrophytes. During the cold season (autumn, winter and spring), filamentous fungi account for over 90 to 99% of total microbial biomass in emergent macrophytes and riparian leaf litter and their secondary production is one to two orders of magnitude higher than the bacterial production (Gulis et al., 2009). Therefore, fungal decomposition of this important POM pool seems to be of primary importance during several months in the cold season. Surprisingly, decomposition of submerged aquatic plants has not been well examined, although it is likely that filamentous fungi are of secondary importance (Mille-Lindblom et al., 2006). Thereby, other fungal taxa potentially substitute the filamentous forms, but may vary in time. For example, lower fungi are able to degrade small plant debris and particles. Foremost, *Chytridiomycetes* are suitable candidates since they are able to degrade a wide range of substrates (Sparrow, 1960). However, their saprophytic capabilities and related carbon turnover rates have not been quantified, yet. Some *Chytridiomycetes* can utilise a range of organic polymers such as glucose, starch, sucrose, cellobiose, chitin and cellulose (Gleason et al., 2011; Reisert & Fuller, 1962) whereas others possess incomplete enzymatic degradation pathways suggesting a possible complementation through other microbes. Many active *Chytridiomycetes* often occur sporadically in flooded mud of the riparian zone and submerged sediments and form a very different *Chytridiomycetes* flora compared to that of soils of the catchment area (Willoughby, 1961). This suggests that aquatic *Chytridiomycetes* include indigenous species well adapted to the prevailing environmental factors.

#### **4.1.1 Functional redundancy of saprobes**

Lawton and Brown (1993) introduced the concept of functional redundancy as a means of exploring the importance of biodiversity for ecosystem functioning. Functional redundancy is the idea that multiple species can perform the same function within an ecosystem, therefore, a reduction in number of species will not affect ecosystem functioning until all species performing a particular function are lost. However, functional redundancy is at odds with the concept of resource partitioning (Schoener, 1974), which proposes that competition between species drives them to specialise in exploiting discrete resources or ecological niches. Recent research has shown that biodiversity influences aquatic ecosystem processes such as productivity (Smith, 2007; Gustafsson & Boström, 2011) and heterotrophy (Cardinale

recycled. Microbial mineralisation of plant litter supports a complex food-web including all kinds of microbes (*Archaea*, *Bacteria*, fungi, protozoans) and invertebrates (nematodes, trematodes, gammarids, insects, snails). As a consequence plant litter even supplies top predators such as crayfishs, amphibians, birds, fishes and bats with organic matter and energy via the microbial food web. The main basis of the microbial food web consists of fungi and bacteria growing in and on the plant debris. Microorganisms, in particular fungi, possess enzymes capable of degrading even highly polymeric substances, and filamentous fungi are capable of degrading the plant material from the inside, driving the break down of high molecular weight polymers to smaller molecules of medium molecular weight (Fischer et al., 2006). These small fragments and oligomers, e.g. sugar residues, can be readily utilized by bacteria and the so called "sugar fungi" (a sloppy term for the lower fungal phyla consisting of *Chytridiomycota, Blastocladiomycota, Mucoromycotina, Zoopagomycotina, Oomycetes*). Freshwater hyphomycetes of temperate waters are usually well adapted to lower temperatures prevailing during leaf litter input and senescence of aquatic macrophytes. During the cold season (autumn, winter and spring), filamentous fungi account for over 90 to 99% of total microbial biomass in emergent macrophytes and riparian leaf litter and their secondary production is one to two orders of magnitude higher than the bacterial production (Gulis et al., 2009). Therefore, fungal decomposition of this important POM pool seems to be of primary importance during several months in the cold season. Surprisingly, decomposition of submerged aquatic plants has not been well examined, although it is likely that filamentous fungi are of secondary importance (Mille-Lindblom et al., 2006). Thereby, other fungal taxa potentially substitute the filamentous forms, but may vary in time. For example, lower fungi are able to degrade small plant debris and particles. Foremost, *Chytridiomycetes* are suitable candidates since they are able to degrade a wide range of substrates (Sparrow, 1960). However, their saprophytic capabilities and related carbon turnover rates have not been quantified, yet. Some *Chytridiomycetes* can utilise a range of organic polymers such as glucose, starch, sucrose, cellobiose, chitin and cellulose (Gleason et al., 2011; Reisert & Fuller, 1962) whereas others possess incomplete enzymatic degradation pathways suggesting a possible complementation through other microbes. Many active *Chytridiomycetes* often occur sporadically in flooded mud of the riparian zone and submerged sediments and form a very different *Chytridiomycetes* flora compared to that of soils of the catchment area (Willoughby, 1961). This suggests that aquatic *Chytridiomycetes* include indigenous species well adapted to the prevailing environmental

Lawton and Brown (1993) introduced the concept of functional redundancy as a means of exploring the importance of biodiversity for ecosystem functioning. Functional redundancy is the idea that multiple species can perform the same function within an ecosystem, therefore, a reduction in number of species will not affect ecosystem functioning until all species performing a particular function are lost. However, functional redundancy is at odds with the concept of resource partitioning (Schoener, 1974), which proposes that competition between species drives them to specialise in exploiting discrete resources or ecological niches. Recent research has shown that biodiversity influences aquatic ecosystem processes such as productivity (Smith, 2007; Gustafsson & Boström, 2011) and heterotrophy (Cardinale

factors.

**4.1.1 Functional redundancy of saprobes** 

et al., 2002), but studies of aquatic fungi show that diversity influences neither productivity (Baldy et al., 2002) nor decomposition rates (Bärlocher & Graça, 2002; Dang et al., 2005). It is likely that both functional redundancy and resource partitioning operate within aquatic ecosystems, but on different spatial and temporal scales, and with impacts at the level of individuals, populations and communities (Loreau, 2004).

In many aquatic ecosystems, saprobic fungi are important decomposer organisms. While some species show a preference for substrates derived from a particular plant species or plant tissue (i.e. leaves or wood), many fungal species are generalist saprobes (Gulis, 2001). This suggests that a large degree of functional redundancy exists among saprobic aquatic fungi at spatial scales ranging from submerged substrates to the whole ecosystem.

Aquatic fungi are microscopic organisms that interact with other species and "individuals" on a microscopic scale via enzymes and biochemical defences. Therefore, resource partitioning by fungi can be expected to occur at the molecular scale. This idea is supported by the well documented temporal succession (Garrett, 1951) that occurs as fungi colonise a submerged leaf, and the temporal partitioning of the resource that is implied. In order to exploit a substrate, fungi secrete extra-cellular enzymes that attack and degrade its chemical constituents. As separate and distinct enzymes or enzyme systems are required for the breakdown of starches, cellulose, hemicellulose, pectin, proteins, lipids and lignin, the fungal species, armed with the suite of enzymes able to efficiently degrade the most labile leaf components, become the initial colonisers. When labile resources are depleted, species able to efficiently degrade the remaining resources become dominant, and so on (Chamier, 1985). Complex plant components such as lignin may be degraded by a range of enzymes secreted by a number of fungal species (Evans et al., 1994), and this is an example of resource partitioning at the sub-molecular level (lignin moieties). It is thus likely that the biodiversity of aquatic fungi has inherent functional redundancy at larger spatial scales, but at the molecular scale, and through time there is inherent functional complementarity, competitive exclusion and resource partitioning.

#### **4.1.2 Fungi as producers of organic matter**

There are a number of studies from the past few decades that have established a strong role of fungi as important basal resources in aquatic ecosystems (Bärlocher, 1985; Albariño et al., 2008; Chung & Suberkropp, 2009), most notably in streams (Reid et al., 2008; Hladyz et al., 2009). For example, fungal biomass has been shown to be an important food source for aquatic invertebrates such as snails (McMahon et al., 1974; Newell & Bärlocher, 1993) and insect larvae (Bärlocher, 1981; 1982; 1985). Thereby, the fungal biomass is either removed from the leaf surface, or the leaf itself is consumed.

A synthesis of research from aquatic systems suggests that the functional role of aquatic heterotrophic fungi in moderating the food value of plant detritus may be more important than their role as organic matter producers (e.g. Thorp & Delong, 2002). Litter produced outside a water body may enter the water directly, as a result of abscission from riparian plants overhanging the water body, or may undergo a period of terrestrial aging before entering the water. These two pathways result in differences in litter chemistry (Baldwin, 1999) that influence their importance to the aquatic food-chain (Watkins et al., 2010). In general, fresh plant material has a higher protein content (lower C:N) and a higher proportion of readily available nutrients than aged material (Williams, 2010; Kerr et al., in prep.). However, fresh material also contains inhibitory substances such as tannins, polyphenols and aromatic oils, which function to deter microbial attack and herbivory in the

Aquatic Fungi 245

hyperparasites belong to the genus *Rozella.* This genus was formerly assigned to the *Chytridiomycetes* and is now proposed to be part of the unique fungal phylum of the Rozellida (Lara et al., 2010). All members of *Rozella* are considered to be parasites of lower fungi (*Chytridiomycetes, Blastocladiomycetes, Oomycetes*). It is intriguing to think about the minimum population size of parasitic/saprobic fungi needed to sustain an obligate mycoparasitic fungal population. This suggests that a very common and stable mycoplankton population must exist in aquatic systems. Therefore, parasitism can be

As shown above, fungi possess multiple ecological functions in aquatic food webs. They often have a dual role which is on the one hand consumption of organic matter and on the other hand transmission of energy and genetic information (Amundsen et al., 2009; Rasconi et al., 2011). Parasitic fungi, for example, can selectively alter food web topology and thereby increase interactions and nestedness of ecosystems. Parasites including fungi, for example, interlink organisms of all trophic levels (resulting in twice as many links as without parasites) and thus increase food chain length and number of trophic levels. Amundsen et al. (2009) show that 50% of all parasites are trophically transmitted and thereby exploit different trophic levels and largely increase omnivory in the trophic web. They also show that the number of trophically transmitted parasite-host links is positively correlated with the linkage density of the host species, i.e. highly connected species have a higher rate of infection, in particular those with complex life cycles. Therefore, parasites play a prominent role in ecological networks, significantly increasing interaction strength and hence

Parasites are ubiquitous in the aquatic environment and have subtle, sublethal or even lethal impacts. Their impacts on hosts are propagated up and down food webs and thus are manifested throughout the entire community. Environmental changes, however, greatly affect their dynamics and hence parasites can be seen as indicators of many aspects of host physiology. Parasites are uniquely situated within food webs, and following their transmission process could serve management and ecosystem conservation (Marcogliese, 2004; Lafferty et al., 2006). In general, the diversity of parasites reflects the overall diversity within the ecosystem (see Rasconi et al., 2011). In many pelagic systems, fungal parasites are 1) a driver of phytoplankton community structure, 2) crucial for organic matter and energy transfer, 3) important for food web dynamics by affecting fitness and reproduction of many aquatic organisms and 4) causes of intra-specific variability and even increased speciation. Since fungal parasites largely increase the number of trophic levels and often lower the dominance of a few species they also increase ecosystem stability and most likely even functional diversity. Fungi are also potential vectors of genetic elements and hence may also transfer genetic information between organisms of different trophic levels. In any case, they lead to a higher biodiversity by affecting key evolutionary parameters and also functional diversity, e.g. by transferring terrestrial material including leaves and pollen - otherwise unavailable for aquatic organisms - to higher trophic levels (e.g. Masclaux et al. 2011). Hence, aquatic fungi should be seen as key variables for food web structure and genetic as well functional diversity of the aquatic community rendering it less susceptible to changes

regarded as a key driver of food-web stability and POM transfer.

**4.3 Stabilisation of ecosystems** 

selectively changing food web links.

in environmental variables.

living plant (Campbell & Fuchshuber, 1995; Canhoto et al., 2002; Graça et al., 2002). In contrast to fresh material, aged organic matter has a higher C:N (low C:N is correlated with higher nutritional value; Boyd & Goodyear, 1971; Hladyz et al., 2009), but a lower content of inhibitory substances.

When fungi colonise submerged plant material that has undergone terrestrial aging, the C:N ratio of the detritus declines (Bärlocher, 1985) as fungi utilise nitrogen from the water column to synthesise proteins for their own growth (Stelzer et al., 2003). They also produce lipids essential for growth (Chung & Suberkropp, 2009) and reproduction (Cargill et al., 1985) in some aquatic invertebrates. In addition to this, the activity of fungal enzymes releases sugars from structural carbohydrates (Chamier, 1985), breaks down lignins reducing leaf toughness (Leonowicz et al., 2001; Medeiros et al., 2009) and neutralises inhibitory substances such as tannins (Mahadevan & Muthukumar, 1980; Abdullah & Taj-Aldeen, 1989). Moreover, where plant detritus undergoes a period of terrestrial or standing dead aging, a more diverse consortium of fungi is able to actively degrade refractory plant components such as lignin (Bergbauer et al., 1992; Abdel-Raheem & Ali, 2004; Schulz & Thormann, 2005). Consequently, the sequential activity of terrestrial and aquatic fungi on plant detritus potentially leads to improved food value for members of the aquatic biota extending from other microorganisms to fish (Williams, 2010).

As aquatic fungi serve as a basal resource in many aquatic ecosystems, it is important to consider factors influencing their productivity. Fungal biomass increases with increasing concentration of nitrogen and phosphorus in the water column (Sridhar & Bärlocher, 1997) and decreases with lower dissolved oxygen concentrations (Medeiros et al., 2009). Thus the productivity of fungi and their importance as organic matter producers vary with climate and the availability of nutrients and organic substrates (Ferreira & Chauvet, 2010), and in some instances fungal production will not be a significant resource for the aquatic community (Bunn & Boon, 1993; Hadwen et al., 2010). Additionally, productivity will also be limited by ecological interactions such as competition (Mille-Lindblom et al., 2006) and mycotrophy (Newell & Bärlocher, 1993; Kagami et al., 2004; Lepere et al., 2007), and physical changes such as burial (Janssen & Walker, 1999; Cornut et al., 2010).
