**4.2 Parasites**

Fungal pelagic parasites are often host-specific, but their evolution didn't stop at the species level and several fungal species developed dependencies on (1) certain algal cell types, e.g. heterocysts and akinetes (Sparrow, 1960); (2) certain cell entry sites of the host cell (Powell, 1993); and (3) certain algal strains (De Bruin et al., 2008). The latter study targets a prominent freshwater diatom called *Asterionella formosa* because it often harbours a obligatory, host-specific, very virulent fungal parasite called *Zygorhizidium planktonicum*. Infection by this fungus is often epidemic and can rapidly reach up to 90% of the host population with fatal consequences for the host. Interestingly, the authors could show that a genetically diverse host population maintains an evolutionary equilibrium between the parasite and the host population. A diminished host diversity, which is promoted, e.g. by disturbance or algal monoculture, would allow a rapid adaptive evolution of the parasite with a serious aftermath.

The occurrence of hyperparasites is really amazing since such fungi represent parasites of the algae's fungal parasites. Examples of these hyperparasites of fungal parasites on *Cyclotella, Cosmarium and Asterionella* are given by Canter-Lund & Lund (1995). Fungal

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

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

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

Fungal pelagic parasites are often host-specific, but their evolution didn't stop at the species level and several fungal species developed dependencies on (1) certain algal cell types, e.g. heterocysts and akinetes (Sparrow, 1960); (2) certain cell entry sites of the host cell (Powell, 1993); and (3) certain algal strains (De Bruin et al., 2008). The latter study targets a prominent freshwater diatom called *Asterionella formosa* because it often harbours a obligatory, host-specific, very virulent fungal parasite called *Zygorhizidium planktonicum*. Infection by this fungus is often epidemic and can rapidly reach up to 90% of the host population with fatal consequences for the host. Interestingly, the authors could show that a genetically diverse host population maintains an evolutionary equilibrium between the parasite and the host population. A diminished host diversity, which is promoted, e.g. by disturbance or algal monoculture, would allow a rapid adaptive evolution of the parasite

The occurrence of hyperparasites is really amazing since such fungi represent parasites of the algae's fungal parasites. Examples of these hyperparasites of fungal parasites on *Cyclotella, Cosmarium and Asterionella* are given by Canter-Lund & Lund (1995). Fungal

extending from other microorganisms to fish (Williams, 2010).

changes such as burial (Janssen & Walker, 1999; Cornut et al., 2010).

inhibitory substances.

**4.2 Parasites** 

with a serious aftermath.

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

### **4.3 Stabilisation of ecosystems**

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 selectively changing food web links.

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 in environmental variables.

Aquatic Fungi 247

functioning (Lafferty et al., 2008). Hypothetical scenarios resulting from the loss of fungal diversity include: aggradation of aquatic ecosystems via the accumulation of CPOM and polymers, a decline in macroinvertebrate food sources, a reduction in the rate and range of decontamination of industrial toxins, diminished total diversity in planktonic communities and the development of fungal monocultures that would potentially impact on total biodiversity. Since fungal biodiversity is representative of ecosystem functioning and thus of ecosystem health, it is in the interests of human society to explore the fungal biodiversity

We would like to thank A. Grossherr for illustrations and helpful comments and the Leibniz society and the German Science foundation (DFG GR1540/15-1) for funding. Janice Kerr would like to thank the Murray-Darling Freshwater Research Centre (Wodonga, Australia)

Abdel-Raheem, A. M. & Ali, E. H. (2004). Lignocellulolytic enzyme production by aquatic

Abdullah, S. K. & Taj-Aldeen, S. J. (1989). Extracellular enzymatic activity of aquatic and

Adl, S. M., Simpson A. G. B., et al. (2005). The new higher level classification of eukaryotes

Ali, E. H. & Abdel–Raheem, A. (2003). Distribution of zoosporic fungi in the mud of major

Amundsen, P.A. and Lafferty, K.D. and Knudsen, R. and Primicerio, R. and Klemetsen, A.

Ananda, K. & Sridhar, K. R. (2002). Diversity of endophytic fungi in the roots of mangrove species on the west coast of India. *Canadian Journal of Microbiology, 48*(10), 871-878. Albariño, R., Villanueva, V. D., et al. (2008). The effect of sunlight on leaf litter quality

Ali-Shtayeh, M. S., Khaleel, T. K. M., & Jamous, R. M. (2002). Ecology of dermatophytes and

Baar, J., Paradi, I., Lucassen, E. C. H. E. T., Hudson-Edwards, K. a, Redecker, D., Roelofs, J.

hyphomycetes species isolated from the Nile's delta region. *Mycopathologia, 157*(3),

with emphasis on the taxonomy of protists. *The Journal of Eukaryotic Microbiology,* 

and Kuris, A.M. (2009). Food web topology and parasites in the pelagic zone of a subarctic lake. *Journal of Animal Ecology*, *78*(3), 566-572. doi: 10.1111/j.1365-

reduces growth of the shredder *Klapopteryx kuscheli*. *Freshwater Biology, 53*(9), 1881-

other keratinophilic fungi in swimming pools and polluted and unpolluted

G. M., et al. (2011). Molecular analysis of AMF diversity in aquatic macrophytes: A comparison of oligotrophic and utra-oligotrophic lakes. *Aquatic Botany*, *94*(2), 53-61.

present in natural environments, especially aquatic habitats.

and its staff for their support in production of the manuscript.

aero-aquatic conidial fungi. *Hydrobiologia, 174*, 217-223

Egyptian lakes. *Journal of Basic Microbiology, 43*(3), 175-184

**7. Acknowledgment** 

**8. References** 

277-286

*52*(5), 399-451

2656.2008.01518.x

streams. *Mycopathologia*, *156*(3), 193-205

doi: 10.1016/j.aquabot.2010.09.006

1889
