102-1998 Role of fungi in freshwater ecosystems

Role of fungi in freshwater ecosystems

MICHELLE K.M. WONG, TEIK-KHIANG GOH, I. JOHN HODGKISS,KEVIN D. HYDE, V. MALA RANGHOO, CLEMENT K.M. TSUI,WAI-HONG HO, WILSON S.W. WONG and TSZ-KIT YUENDepartment of Ecology and Biodiversity, The University of Hong Kong, Pokfulam Road, Hong Kong

Received 15 December 1997; accepted 28 January 1998

There are more than 600 species of freshwater fungi with a greater number known from temperate,as compared to tropical, regions. Three main groups can be considered which include Ingoldianfungi, aquatic ascomycetes and non-Ingoldian hyphomycetes, chytrids and, oomycetes. The fungi

occurring in lentic habitats mostly di�er from those occurring in lotic habitats. Although there is nocomprehensive work dealing with the biogeography of all groups of freshwater fungi, their distri-bution probably follows that of Ingoldian fungi, which are either cosmopolitan, restricted to pan-

temperate or pantropical regions, or in a few cases, have a restricted distribution. Freshwater fungiare thought to have evolved from terrestrial ancestors. Many species are clearly adapted to life infreshwater as their propagules have specialised aquatic dispersal abilities. Freshwater fungi are

involved in the decay of wood and leafy material and also cause diseases of plants and animals.These areas are brie¯y reviewed. Gaps in our knowledge of freshwater fungi are discussed and areasin need of research are suggested.

Keywords: biodiversity; biogeography; ecology; freshwater; fungi; nutrient cycling

Introduction

This paper reviews the biology of fungi in freshwater sediments. We use the term sedi-ments in a broad sense to mean freshwater sand, gravel, silt, mud (Anon., 1989), wood,leaves and other organic matter that accumulates on the ¯oor of freshwater habitats. Wehave not treated lichen-forming fungi on rocks in or by lake or stream margins, whichmerit a modern separate review.

Biodiversity of freshwater fungi

There are more than 600 species of freshwater fungi and a greater number are known fromtemperate, as compared to tropical, regions. These include ca 300 ascomycetes, 300 mi-tosporic fungi and a number of chytrids and oomycetes (Goh and Hyde, 1996). Threemain groups can be considered:

1. The Ingoldian fungi which occur on decaying leaves in streams and lakes and whichare probably the most well studied. They have been documented in many countriesaround the world, although the tropics have received less attention.

2. The aquatic ascomycetes and hyphomycetes occurring on submerged woody ma-terial have received less attention. Studies on these fungi in temperate regions aremainly based in North America, around Chesapeake Bay (Shearer, 1993a) and

0960-3115 Ó 1998 Chapman & Hall

Biodiversity and Conservation 7, 1187±1206 (1998)

Hong Kong (Hyde et al., unpubl.). Less intensive collections have been made inAustralia, Brunei, England, Philippines, Seychelles and South Africa.

3. The chytrids and oomycetes, including those that cause diseases, are well-docu-mented (Laidlaw, 1985; Fuller and Jaworski, 1987; Barr, 1988; Bruning, 1991;Powell, 1993). These fungi generally lack the ability to degrade cellulose, and areprobably important in degrading noncellulosic entities entering the freshwaterecosystem (e.g. dead insects, keratin and pollen grains).

Ingoldian fungi are relatively well studied, although inventories in numerous tropicalcountries are lacking. Studies in tropical countries have resulted in the discovery of manynew species, e.g. the work carried out by Kuthubutheen and Nawawi in Malaysia. In thecase of ascomycetes and hyphomycetes on woody material, other than the work of Hydeand co-workers in Asia and that of Shearer and co-workers in North America, there islittle work being carried out. The task of documenting biodiversity is therefore prob-lematical. Hyde et al. (1997) concluded that in any new freshwater system studied in newcountry, more than 50% of the ascomycetes identi®ed may be new species. Although asmore species are being described, this is no longer likely, we can conclude that thefreshwater fungi are still relatively poorly studied.

During studies of the fungi occurring on submerged woody material in the tropics overthe last seven years, we have identi®ed numerous ascomycetes and hyphomycetes that arenew to science and have a large backlog of new species awaiting formal treatment. In onesmall river system, the Lam Tsuen River in Hong Kong, that we have now studiedextensively, we have identi®ed more than 200 fungi, which is more than the total numberof non-Ingoldian freshwater fungi presently known from the tropics. There is a great needfor such studies to be implemented on a global scale.

Habitats for freshwater fungi

Freshwater habitats that support fungi can be divided into: (1) lentic (lakes, ponds,swamps, pools); and (2) lotic (rivers, streams, creeks, brooks) (Thomas, 1996). In addition,many freshwater fungi have been reported from arti®cial habitats, such as water-coolingtowers (Jones and Eaton, 1969; Eaton and Jones, 1970, 1971a,b; Udaiyan, 1989; Udaiyanand Hosagoudar, 1991).

Lentic habitats

Lentic habitats comprise any natural aquatic environment lacking a continuous ¯ow ofwater. Lakes and ponds are typical lentic habitats (irrespective of their climatic zones)from which over 100 freshwater ascomycetes and their anamorphs are known (Shearer,1993a). Lakes and ponds may provide calm environments in which fungi can develop(Sparrow, 1968). Low wave action may allow undisturbed fungal growth. However, themild wave action may result in oxygen de®ciency and reduce the number of fungi present(BaÈ rlocher, 1992).

Almost one-third of freshwater ascomycetes are reported from lakes and/or ponds.They colonize both wood and leaves of various plant species and are widely distributed.One of the ®rst freshwater fungi from lentic habitats was described in the pioneering workof Weston (1929). He described an interesting discomycete, Loramyces juncicola occurringon fallen culms of Juncus spp. from a small pond in America. Other collections of

1188 Wong et al.

freshwater ascomycetes in lakes and ponds include those of Ingold (1951, 1954, 1955),Ingold and Chapman (1952), Tubaki (1966), Cavaliere (1975), Minoura and Muroi (1978),Magnes and Hafellner (1991) and Hyde and Goh (1998) and these articles should beconsulted for further information. Discomycetes occur more commonly in temperate re-gions, especially in lentic habitats.

Lotic habitats

Lotic habitats comprise continuous ¯owing water bodies, such as rivers, streams, creeksand brooks. Numerous species of fungi have been reported from this dynamic system(Shearer, 1993a; Thomas, 1996; Hyde et al., 1997). Almost one-third of the freshwaterascomycetes have been reported from rivers and/or streams. Temperate species were re-ported by Shearer and co-workers (Kjùller, 1960; Shearer, 1972, 1984, 1989a, b, 1993a, b;Willoughby and Archer 1973; Shearer and Crane, 1978a, b, 1980a, b; Webster andDescals, 1979; Shearer and von Bodman, 1983; Shearer and Zare-Maivan, 1988; Re va yand GoÈ nczoÈ l, 1990) while tropical species were reported on by Hyde and co-workers(Goh, 1997; Hyde et al., 1997). Many of the tropical species found were new to science.

Biogeography of freshwater fungi

There is no comprehensive review dealing with the biogeography of all groups of fresh-water fungi. The Ingoldian fungi are probably better known than the other freshwaterfungi and have been reviewed by Wood-Eggenschwiler and BaÈ rlocher (1985). They con-clude that:

(1) Many species are cosmopolitan, although any single species may be more commonin tropical or temperate regions.

(2) Some species are restricted to temperate and cold, others to tropical and warm,regions.

(3) Some species are restricted to very small geographical areas.

Other freshwater fungi appear to follow similar distribution patterns.

Origin of freshwater fungi

Freshwater fungi are a diverse and heterogeneous group comprising species from di�erentorders. The dominant groups are the ascomycetes and hyphomycetes, depending ongeographical location and substrate. Shearer (1993a) stated that ``the presence of fungi inaquatic habitats alone may not be appropriate to de®ne an ascomycete as a freshwaterascomycete''. This is because the occurrence of a species may simply be fortuitous andpresence is therefore not conclusive evidence in assigning a particular fungus as ``fresh-water''. The fungus could have its origin in terrestrial habitats and may have entered thefreshwater system as spores. There are, however, numerous ascomycete (and hyphomy-cete) species which commonly occur in freshwater and have not been found in terrestrialhabitats. These can con®dently be categorized as freshwater fungi.

Certain genera, e.g. Jahnula and Proboscispora, are con®ned to freshwater habitats,while others have representatives in both terrestrial and marine habitats. Annulatascus hasterrestrial (mainly on bamboo and palms) as well as freshwater representatives. Savoryella

Role of fungi in freshwater ecosystems 1189

and Aniptodera has representatives in marine and freshwater habitats, while Ascotaiwaniawhich was ®rst reported as a freshwater genus, is now known from terrestrial palms (Hyde,1995). However, individual species are generally restricted to freshwater, marine or ter-restrial habitats. The main di�erences between species in a genus are found in the asco-spores, with sheaths or appendages often occurring in freshwater and marinerepresentatives, while other morphological characters vary little.

It has been suggested that some marine fungi have a fungal-algal ancestor, which gaverise to ancestral pyrenomycetes, and which were mainly parasites of algae (Kohlmeyerand Kohlmeyer, 1979). Terrestrial loculoascomycetes and pyrenomycetes are thought tohave originated from these parasitic pyrenomycetes. Subsequently these terrestrial asco-mycetes moved back into the marine environment and are known as secondary marinefungi. These secondary marine fungi include the intertidal loculoascomycetes Halotthia,Leptosphaeria, Mycosphaerella, Pontoporeia, and pyrenomycetes such as Chaetosphaeriaand Kallichroma.

Kohlmeyer and Kohlmeyer (1979) organised marine fungi in two groups: (1) primarymarine fungi (e.g. Ceriosporopsis, Corollospora, Halosphaeria) thought to have been de-rived from marine ancestors, that have not left their original marine environment; and (2)marine fungi which were thought to have evolved from terrestrial ancestors which havemigrated back into the sea. An analogy can be made between freshwater and marine fungi.The genus Aniptodera (Shearer and Miller, 1977) may be classi®ed as a primary freshwaterfungus as species occur in both freshwater and marine environments and no terrestrialrepresentatives have been found. Genera such as Annulatascus and Ascotaiwania may beclassi®ed as secondary freshwater fungi since they originate most probably from terrestrialhabitats, since they have terrestrial representatives.

Recent phylogenetic studies (Spatafora et al., 1995) have shown that many marineascomycetes are likely to have evolved from terrestrial ancestors (e.g.Microascales), whichhave lost many of their characters. Features such as active ascospore ejection are thoughtto be unnecessary in the sea. It is probably also true, that most, if not all, freshwaterascomycetes evolved from terrestrial ancestors.

Ecological adaptations of freshwater fungi

Adaptations of freshwater Ascomycetes

Many freshwater ascomycetes have ascospores with various sheaths, appendages or wallornamentations, which probably function in ascospore dispersal and/or attachment. Forexample the base of the ascospores of Loramyces species have a long, tapering ®liform,caudate and sinuous appendage or `tail' which may be involved in the entrapment andattachment. In addition, the head of the ascospore is surrounded by a gel-like stickymucilaginous sheath which may aid in adhesion to substrata (Weston, 1929; Ingold, 1954;Ingold and Chapman, 1952; Digby and Goos, 1987).

``Spores with sticky mucilaginous sheaths probably represent the most common typeencountered in fungi'' (Jones, 1994). This appears to be true in freshwater ascomycetes.Shearer (1993a) listed ascomycete species possessing ascospores surrounded by mucilagi-nous sheaths which included: Nimbomollisia sp., and Obtectodiscus aquaticus (discomy-cetes); Annulatascus velatispora, and Fluviatispora spp. (pyrenomycetes); and Caryosporacallicarpa, Kirschsteiniothelia elaterascus, Massarina spp., Phaeosphaeria spp., Pleosporascirpicola and Rebentischia sp. (loculoascomycetes). Some loculoascomycetes possess

1190 Wong et al.

mucilaginous appendages at their poles, e.g. Jahnula bipolaris, Lophiostoma spp., Reben-tischia sp. and Wettesteinina niesslii. In addition, ascospores with unfurling appendageswhich uncoil in water to form long viscous threads, are also common in freshwater as-comycetes, e.g. Aniptodera spp., Annulutascus bipolaris and Halosarpheia spp. (Shearerand Crane, 1980b; Hyde, 1992). Species of Aniptodera and Halosarpheia also occur in thesea, and it appears that the morphological adaptations in marine and freshwater species inthese genera are similar.

Shearer (1993a) concluded that the appendage ontogeny in freshwater ascomycetes issimply mucilaginous rather than involving fragmentation and/or extension of a spore wallas in many marine fungi. However, Jones (1994) predicted that as our knowledge of aascomycetes from freshwater habitat increases, ascospore appendages in marine fungi maynot prove to be unique. Several unique appendage types have now been shown to exist intropical freshwater ascomycetes (Wong and Hyde, 1998).

Asci of aquatic ascomycetes also appear to be adapted for dispersal in these habitats.Deliquescent asci are common in the marine Halosphaeriales and in some freshwaterspecies in the genera Halosarpheia and Nais. The nature of deliquescing asci allows lib-eration of ascospores without forcible discharge. The ascospores then accumulate aroundthe break or tip of the neck, and are dispersed by water movement. Shearer (1993a)suggested that the disappearance of the apical apparatus in the asci might be an adap-tation to life in water. In several freshwater ascomycetes, however, large and refractiveapical rings (to 7±8 lm long and 4±5 lm wide) have been reported in several commontropical genera, e.g. Annulatascus, Ascotaiwania and Submersisphaeria. Similarly, severalfreshwater loculoascomycete genera have species with well-developed apical dischargemechanisms in their asci (e.g. Jahnula spp., Massarina spp.). In Kirschsteiniothelia elate-rascus (Shearer, 1993b) the asci are ®ssitunicate, but a long and narrow posterior end ofthe endoascus becomes coiled within the ectoascus. The ectoascus ruptures in water andthe endoascus elongates to a length about 1.7 times of its original length (Shearer, 1993b)by the uncoiling of the basal structure. The posterior end of the endoascus remains con-nected to the endoascus or may be completely liberated. The need to eject ascosporestherefore appears to be important in freshwater.

In Ophioceras and Pseudohalonectria species (Shearer, 1989a) asci are liberated from theascomata into the surrounding water before the ascospores are probably ejected somedistance from the ascomata, but the advantages of this are unknown.

Adaptations of the anamorphs

Spore attachment and entrapment mechanisms in Ingoldian hyphomycetes, which com-monly have sigmoid or tetraradiate spores, are well-documented (Ingold, 1953, 1956, 1966,1975, 1984; Webster, 1981; Read, 1990). Sigmoid conidia often become attached at theirsticky poles, and then straighten in the direction of the water current so they are less likelyto be washed away. Tetraradiate and branched conidia act as an anchor and allow theirentrapment to the substrata or in surface foam (Ingold, 1942, 1953). Tetraradiate conidiacan also attach to the substratum, with three ``legs'' forming a strongly adhesive tripod(Webster and Descals, 1981). Adhesive mucilaginous material is also produced at each armof the conidium in contact with a surface (Read, 1990; Read et al., 1992) and attachesthem ®rmly to the substratum. Read (1990) indicated that substrate colonization byIngoldian hyphomycete may involve four factors: conidial entrapment and attachment;rapid germination; mucilage production on the spore surface and germ tubes; and the

Role of fungi in freshwater ecosystems 1191

formation of appressoria. These characters may confer an advantage for the Ingoldianhyphomycetes over other fungi.

Functional role of freshwater fungi

The main role of the freshwater ascomycete, basidiomycetes and mitosporic fungi infreshwater ecosystems is in the degradation of dead plant material (e.g. Juncus, leaves andwood) that ®nds its way into the water (Goh and Hyde, 1996). They may also be involvedin the degradation of animal parts such as insect exoskeletons, ®sh scales, and hair. Otherecological groups present are the plant pathogens and endophytes that may colonise livingplant tissues. The decay of dead plant tissues is a result of the fungi's ability to degradecelluloses and lignocelluloses (Zare-Maivan and Shearer, 1988a, b). Their success indegrading woody tissues lies in an ability to form soft-rot cavities (Shearer, 1993a; Yuenet al., pers. obs.). Basidiomycetes are rare and mainly absent in freshwater as they are notsoft-rotters, although they can degrade cellulose. It appears that the ability to degrade thelignocellulose from within the S2 layer of the cell wall is important in submerged water-logged wood. Several species have now been tested for their ability to cause soft-rot decayand although we have information for only a small proportion of known species, it isprobably representative.

Fungi on submerged wood

Knowledge of tropical fungi on submerged wood

The role of fungi, including freshwater fungi, in wood decay has been extensively exam-ined in cultural studies (Shigo, 1965, 1972; Shearer and von Bodman, 1983; Benner et al.,1986; Zare-Maivan and Shearer, 1988a). However, no similar work has been carried outusing tropical freshwater fungi. The growth parameters and woody plant species that thesetropical fungi colonise may be di�erent to similar fungi in temperate regions. Although,many new fungi have been found on submerged wood in tropical regions (Nawawi, 1985;Sridhar et al., 1992; Goh, 1997; Hyde et al., 1997), there has been little work carried out onthe roles of these fungi in nutrient cycling or in the degradation of lignocellulose.

Principal factors of the decay process

Woody tissues are distinguished from other plant tissues by their high lignocellulose andlow nitrogen content. The principal components of wood are cellulose, hemicellulose, andlignin. These components are degraded by di�erent organisms to various extents. Only alimited group of fungi possess enzymatic capabilities to digest wood (Tubaki, 1958; Singh,1982; Zare-Maivan and Shearer, 1988a; Abdullah and Taj-Aldeen, 1989), such as cellulaseand lignin degrading enzymes.

In the development of the decay process, colonisation, growth and survival of theorganism in wood are important. This depends on substrate conditions, which involve thepresence of a suitable substrate, a suitable temperature and also interaction betweenmicroorganisms. The growth rates are a�ected by temperature and substrate, and re¯ectthe di�erences in colonization ability among the component species (Ogawa et al., 1996).It is interesting to note that the optimum temperature for growth of most tropicalfreshwater fungi is between 20±25°C (Yuen et al., 1998), although several isolates exhibitoptimal growth at temperatures as low as 15°C or as high as 30°C. These results are similar

1192 Wong et al.

to those reported by Zare-Maivan and Shearer (1988a) and Koske and Duncan (1974) fortemperate species. They also showed that the optimal temperature for growth of mosttemperate aquatic fungi was 25°C, but that they could also grow relatively well at tem-peratures as low as 10°C. Tropical freshwater fungi do not grow well in low temperatures,and so are absent in streams in temperate regions. Although temperate species grow best at25°C, they are not able to grow as rapidly as tropical species and this probably accountsfor their absence in tropical streams (Yuen et al., 1998).

Interaction is an important factor in determining the organization, composition, andpattern of fungal colonization within freshwater ecosystems (Shearer, 1993a). The an-tagonistic activities of freshwater fungi on agar media have been investigated and it wasfound that some fungi can inhibit the growth of others by producing antibiotic substances(Khan, 1987; Zare-Maivan and Shearer, 1988a, b; Asthana and Shearer, 1990). Zare-Maivan and Shearer (1988a, b) showed that persistent and late colonizing fungi on long-lasting substrata (e.g. wood) are more likely to produce antagonistic substances than thoseon less persistent substrata (e.g. leaves).

Extent of decay

The extent of decay can be expressed by loss in weight, number of soft-rot cavities andreduction in crushing strength. Investigations so far carried out indicate that freshwaterfungi, with the exception of early succession species, cause signi®cant losses in weight(Jones, 1981; Zare-Maivan and Shearer, 1988b). Signi®cant weight loss and reduction instrength result from the formation of soft-rot cavities within the S2 layer of the cell wall(Wilcox, 1978).

Fungi on submerged wood in streams and water-saturated wood in cooling towers arealso able to degrade wood and produce soft-rot cavities on wood test blocks in thelaboratory (Eaton, 1976; Leightley and Eaton, 1977). Formation of cavities is closelyrelated to hyphal growth, and is explained by the limited di�usion of enzymes away fromhyphal surfaces (Hale and Eaton, 1985). However, some of the fungi cannot form soft-rotcavities in ligni®ed cell walls and it is thought that these fungi can only use dead cellcontents and the walls of parenchymatous ray cells (Mouzouras, 1986).

Fungi on leaves

Relative importance of fungi in leaf decay

Aquatic hyphomycetes are regarded as the dominant mycobiota associated with decayingleaves in streams (BaÈ rlocher and Kendrick, 1974; Butler and Suberkropp, 1986), althoughother fungal taxa have also been isolated from submerged decaying leaves (Kaushik andHynes, 1968; Godfrey, 1983). Zoosporic fungi and terrestrial fungi also occur on leavesthat are recovered from streams in addition to aquatic hyphomycetes. Oomycetes aregenerally early colonizers, but they decline rapidly (BaÈ rlocher and Kendrick, 1974; BaÈ rl-ocher, 1990). Terrestrial fungi (genera such as Alternaria, Aureobasidium, Cladosporium)that colonize the phyllosphere of senescent leaves often persist, but the aquatic hypho-mycetes usually outgrow these terrestrial fungi (BaÈ rlocher and Kendrick, 1974; Sub-erkropp and Krug, 1980). It has also been suggested that the predominance of aquatichyphomycetes on submerged leaves is based on their ability to remain active at lowtemperatures (BaÈ rlocher and Kendrick, 1974; Godfrey, 1983). There are some experi-mental data that suggest that di�erences in temperature alone do not explain such

Role of fungi in freshwater ecosystems 1193

di�erences in the ability to grow and degrade submerged leaves (Graca and Ferreira,1995). Such predominance is due to the ability of the aquatic hyphomycetes to degradesubmerged organic matter through a wide range of climatic conditions, and that terrestrialfungi are unable to macerate leaf material when submerged (Graca and Ferreira, 1995).Moreover, the tetraradiate or sigmoid conidia produced on submerged substrata provideaquatic hyphomycetes with an additional colonisation advantage over terrestrial fungi,which possess spores more suited to air dispersal (Webster and Descals, 1981).

Production of degrading enzymes in freshwater ecosystem

Aquatic fungi have been shown to produce a rich array of enzymes able to degrade themajor leaf polysaccharides (Suberkropp and Krug, 1980). These enzymes are able todegrade simple sugars, cellulose, and other plant polymers (Tubaki, 1957; Thornton, 1963,1965; Nilsson, 1964; Singh, 1982; Chandrashekar and Kaveriappa, 1988), and lead toskeletonization of leaves through maceration. Experimental evidence shows that aquatichyphomycetes have a pH-dependent degrading activity toward cellulose, xylan, and pectin(Chamier and Dixon, 1982; Suberkropp et al., 1983; Chandrashekar and Kaveriappa,1988). There is at least circumstantial evidence that some species can attack lignin andcause soft rot (Jones, 1981; Fisher et al., 1983; Zemek et al., 1985). Nitrogen content as apercentage of remaining leaf mass typically increases during decay (BaÈ rlocher, 1985;Webster and Ben®eld,1986). This is partly due to complex formation between leaf phe-nolics/lignins and proteins or other nitrogenous compounds, and partly due to the accu-mulation of microbial cells (Raviraja et al., 1996). Generally, it is assumed thatpronounced nitrogen increases indicate higher fungal activity. It has been shown that thedecay rates of leaves and fungal biomass are correlated (Maharning and BaÈ rlocher, 1996).A possible explanation is that increasing fungal colonization not only results in higherexoenzymatic activity, which contributes directly to mass loss and but eventually higherinvertebrate feeding, but also increases susceptibility to mechanical fragmentation (i.e.indirect e�ects) of the leaf (Raviraja et al., 1996).

Fungi on grasses

We are unaware of any work that has been carried out on the role of fungi on grasses infreshwater habitats. There have, however, been several studies on the role of fungi in thenutrient cycling of standing grasses, in salt marshes and estuaries with brackish water, e.g.Spartina alterni¯ora, Juncus sp. or Phragmites australis. Most litter and wood-decom-posing fungi, which have been tested, cannot grow at a water potential (w) lower than)6Mpa (Newell et al., 1991). Thus, freshwater habitats undoubtedly provide suitablephysical environments for an ecologically specialized group of fungi. Gallagher andPfei�er (1977) discovered that there is a metabolically active `dead-plant community' ofbacteria and/or fungi on submerged dead standing Spartina alterni¯ora leaves and leafsheathing bases. Padgett et al. (1985) showed that if both bacterial and fungal carbon-conversion e�ciencies were equal to 50%, then P70% of the carbon released as CO2

would be due to fungal respiratory activity. Newell et al. (1989) also provided evidencethat nearly all dead-leaf nitrogen was scavenged into fungal mass after the ®rst samplinginterval. Flux estimates for dead-leaf carbon indicated a ¯ow of 11±15% of the original tofungal biomass, 2% to bacterial biomass, 15±21% to carbondioxide, 10±12% to dissolvedleachate, and 34±36% to small particles; while 32±39% remained attached as shreds at the

1194 Wong et al.

end of the study period. Fungi therefore play an important role in the degradation ofstanding dead grass culms in brackish habitats.

A variety of aquatic macrophytes including Juncus, Phragmites, Scirpus and Typha,serve as substrata for freshwater fungi. Magnes and Hafellner (1991) collected ascomy-cetes on emergent plants from alpine lakes to determine relationships. Among the 52fungal species collected, one large group was considered unspecialized, occurring on avariety of plants hosts. Seventeen species were found to be substrate speci®c, but were notconsidered to be parasitic. There are several studies on the freshwater fungi occurring onliving macrophytes, which provide further information (Ingold and Chapman, 1952;Ingold, 1955; Webster and Lucas, 1961; Apinis et al., 1972a, b; Nannfeldt, 1985).

The succession of fungi on emergent macrophytes has also been investigated (Pugh andMulder, 1971; Apinis et al., 1972a, b; Taligoola et al., 1972). During the early stages of leafemergence in Typha latifolia, the mycobiota was dominated by species of yeasts anddematiaceous hyphomycetes. After the leaves died, species with ®ssitunicate asci (e.g.Leptosphaeria, Nodulosphaeria, Paraphaeosphaeria and Phaeosphaeria) became prominent(Pugh and Mulder, 1971). Ascomycetes were present in early (Massarina andWettsteinina)and late (Lasiosphaeria, Ophiobolus and Passeriniella) stages of succession on submergedculms of Phragmites australis (Apinis et al., 1972b).

Fungi in muddy sediments

As far as the role and occurrence of fungi in muddy sediments is concerned we know verylittle. If sediments are extracted and plated onto agar, then a range of fungal species areisolated. However, we have no knowledge if these fungi are functional in muddy sedimentsor if the isolates are from dormant fungal spores.

Pathogens

The majority of freshwater fungi have been reported as saprotrophs on dead plant sub-strata (Shearer, 1993a; Goh and Hyde, 1996; Thomas, 1996), but whether this re¯ects areal dominance of saprotrophs over parasites, or is due to collector bias, is unknown.Certainly, in contrast to the well-studied Ingoldian fungi or less well documented aquaticascomycetes, there have been few studies on the pathogens of aquatic organisms, and thereis no comprehensive account of them. The roles of these fungi have been brie¯y discussedin review by Shearer (1993a), Goh and Hyde (1996) and Thomas (1996).

The extent of mycoparasitism in freshwater ecosystems is unknown. Several hypho-mycete genera, chytrids and oomycetes associated with other fungi, have been reportedfrom freshwater ecosystems (e.g. Crucella, Janetia, Nectria), but interactions betweenfungi are poorly documented (Thomas, 1996). Janetia curviapicis was described as ``as-sociated with or growing on other hyphomycetes on submerged wood'' from a stream innorth Queensland, Australia (Goh and Hyde, 1996), while the Crucella subtilis anamorphof Camptobasidium hydrophilum is apparently a mycoparasite of several aquatic hypho-mycetes (Marvanova and Suberkropp, 1990). Nectria species are also regularly observeddeveloping on old fruiting bodies of various ascomycetes on submerged wood, and thesemay be mycoparasites (Hyde, pers. obs.).

Parasitism of plants and animals in water have been documented in Australia (Thomas,1996). Aquatic plant pathogens have representatives in the oomycete, chytridiomycete,

Role of fungi in freshwater ecosystems 1195

ascomycete, basidiomycete, and mitosporic fungi, and are commonplace. Most of thesefungi cause diseases of the aerial parts of aquatic plants. Rusts (basidiomycetes) are oftenassociated with the leaves of aquatic macrophytes, while smuts often develop in aerialin¯orescences (Thomas, 1996). Species of Phyllachora (ascomycetes) are often present as tarspots on the aerial leaves of aquatic grasses (Hyde, pers. obs), and the popular Asian leafywater spinach (Kang Kong, Ipomea aquatica) is often parasitised by the oomycete Albugoipomoeae-aquaticae (Shivas et al., 1996). Infection of submerged plant parts is less welldocumented, however, the staple Taro (Colocasia esculenta) which grows along river banks,may be severely a�ected by Taro Blight. This blight is caused by Phytophthora colocasiae(oomycete) which may cause devastating losses, as the underground rhizomes become softand are attacked by a watery rot (Hyde et al., 1991). Semisubmerged leaves of water liliesmay also be infected by the chytridiomycete Physoderma limnanthemi (Thomas, 1996).

Infection of aquatic animals by fungi is better documented (Thomas, 1996). Achlya,Aphanomyces, Pythium and Saprolegnia species (oomycetes) are regularly reportedgrowing in association with diseased ®sh (Thomas, 1996), and can also parasitise captiveaquatic fauna such as turtles, tadpoles and ®sh. In many cases these infections result as theorganisms are under stress from environmental conditions. The role of oomycetes aspossible biocontrol agents of mosquitoes has also received attention. Several oomycetes,trichomycetes and mitosporic fungi are pathogens of mosquitoes or other aquaticarthropods and their potential for biocontrol is discussed by Thomas (1996). Mucoramphibiorum is an interesting fungal/animal association noted in Australia, as it is para-sitic on Platypus spp. in Tasmania, and Cane Toads in Queensland and the NorthernTerritory (Thomas, 1996).

Linkages to other organisms

Plant material produced in the riparian zone has been regarded as a major energy sourcefor low order streams (Vannote et al., 1980). Such material consists mainly of leaves and,to a lesser extent twigs, barks, seeds and ¯owers. Senescent leaves are rich in high-energystructural compounds, but this energy is not easily accessible to aquatic detritivores. Thereis evidence that aquatic fungi can macerate the leaf matrix and make the energy availableto feeding animals in freshwater habitats (Kaushik and Hynes, 1971; Suberkropp andKrug, 1980; Singh, 1982; Suberkropp et al., 1983). There is considerable experimentalevidence that detritivores selectively feed on conditioned leaves, i.e. those previouslycolonized by fungi (Suberkropp, 1992; Graca, 1993). Fungi can alter the food quality andpalatability of leaf detritus, a�ecting shredder growth rates. Animals that feed on a dietrich in fungi have higher growth rates and fecundity than those fed on poorly colonizedleaves (Graca et al., 1993).

Interactions between invertebrates and aquatic hyphomycetes have been demonstrated(Rossi, 1985; Graca et al., 1993). Some shredders prefer to feed on leaves that are colo-nized by fungi, whereas others consume fungal mycelium selectively (Graca et al., 1993).At the same time, the palatability of detritus is a�ected by a number of factors, includingleaf softness, nitrogen content and fungal biomass (Suberkropp, 1992).

The situation with wood is less well known, although mycophagy of lignicolous fungihas been observed (Tsui et al., pers. obs.). Woody substrata are more bulky and hard todecompose and consume, and therefore little data are available on the relationshipsbetween other wood inhabitants and fungi.

1196 Wong et al.

Human disturbance to aquatic fungal communities

Most freshwater habitats are vulnerable to disturbance. Any perturbation within thedrainage basin will a�ect in-stream communities through wash-o� or run-o� processesand, owing to the downhill ¯ow of water, any change in headstream areas will alter thedownstream reaches (Dudgeon, 1992). Human in¯uence, such as the discharge of indus-trial and domestic e�uents, indiscriminate use of pesticides and fertilizers, and clearanceof riparian vegetation, all have deleterious e�ects on the fungal community and arediscussed by BaÈ rlocher (1992).

Pollution

With the exception of Ingoldian fungi, there is no information on the e�ect of disturbanceon freshwater fungi. Bermingham (1996) has reviewed the e�ects of pollution on Ingoldianfungi. Because macroinvertebrates (shredders) have feeding preferences for leaf materialcolonized by a particular species of fungi, any perturbation of the fungal community coulddirectly a�ect the rate of incorporation of leaf material into the detrital food web.

The e�ects of organic pollution on aquatic fungi are apparent, and this subject will notbe treated in detail as they are reviewed elsewhere (Cooke, 1976; van der Merve andJooste, 1988; Au et al., 1992a, b). In general, the diversity of organisms, usually aquatichyphomycetes and occasionally sediment fungi, in polluted and unpolluted freshwatersystems are compared. The results indicate that species richness and conidial production ishigher in unpolluted streams, whereas fungi that are the inhabitants of organic substrata(e.g. Cercophora spp.) are more common in polluted streams. The fungal diversity andrates of the decomposition of leaf baits was also suppressed in polluted streams (Au et al.,1992b).

Human activities often increase the concentration of toxic metals in streams, andstudies have reviewed the sensitivity of fungi to certain chemicals (Duddridge andWainwright, 1980; Abel and BaÈ rlocher, 1984). Both Pb2+ and Cd2+ have been shown toinhibit the growth of the fungi studied, with Cd2+ a�ecting aquatic hyphomycetes (Abeland BaÈ rlocher, 1984). Apart from industrial and domestic wastes, agrochemicals andfertilizers from farms may leach into streams during heavy monsoonal rains and maya�ect the fungal community. Pesticides and herbicides, such as PCP, paraquat and DDT,inhibit the growth and sporulation of fungi at low concentrations (Dalton et al., 1970;BaÈ rlocher and Premdas, 1988; Chandrashekar and Kaveriappa, 1989). However, most ofthese studies were carried out in temperate regions, and whether this impact of pollution isparalleled in tropical communities is unknown.

The e�ect of acid mine drainage and pH on temperate Ingoldian fungi has been studied.Low pH (<5.5) results in lower biodiversity, which corresponds to a lower rate of leafdecomposition (Chamier, 1987). Mine drainage, acidic and with heavy metals, has alsobeen shown to reduce biodiversity, with the aquatic hyphomycete community being themost sensitive of the groups of fungi investigated (Maltby and Booth, 1991). It thereforeseems that Ingoldian fungi are sensitive to low pH and metals, but few studies have beencarried out.

Deforestation and stream regulation

As mentioned before, allochthonous organic matter accounts for a major energy input instream ecosystems, as they are vital for providing substrates and in sustaining the aquatic

Role of fungi in freshwater ecosystems 1197

fungal community (Shearer, 1993a). Removal of the vegetation along the streams due toroad building or stream regulation will a�ect the fungal community. Metwalli and Shearer(1989) found that the mean number of conidia per litre and the degree of colonization ofleaf discs found in streams in wooded areas was greater than those in streams with clear-cut riparian vegetation. The richness of riparian vegetation was also positively correlatedwith fungal species richness (Fabre, 1996).

Major gaps in knowledge in the functional role of fungi in freshwater ecosystems

There are numerous gaps in our knowledge of the biodiversity, ecology and role offreshwater fungi. Although the Ingoldian fungi are relatively well documented, othergroups, such as ascomycetes on submerged wood and fungi in muddy sediments are poorlystudied. This is particularly true of tropical regions where few studies have been carried out.

Dematiaceous hyphomycetes are regularly collected on submerged wood (e.g. Acro-genospora spp., Beltrania rhombica, Sporoschisma spp.). However, we are not sure whetherthese fungi originate from freshwater or terrestrial habitats. Studies need to be imple-mented to establish the requirements or adaptations for a species to be truly aquatic.

Very little work has also been carried out on interactions between freshwater fungi. Ourknowledge of whether fungi can compete for substrata by inhibiting the growth of com-petitors is rudimentary. We also lack knowledge of the importance of fungi relative toother freshwater organisms in nutrient cycling. Fungi appear to be the dominant organ-isms involved in the decay of leaves, wood and probably dead animals and animal parts,but we are unclear of their role in the decay of particulate detritus in sediments. It is alsounclear if single species can degrade tissues or if a suite of fungi complement each other inthe decay of organic matter.

Several studies have shown that fungi alter dead submerged leaves in such a way thatthey become palatable to small invertebrates, and also that some of these invertebrates canfeed directly on fungal mycelium. However, the extent to which this occurs in nature isspeculative, and no such studies have been carried out in the tropics.

Although we have some idea of which fungi occur in freshwater ecosystems, we havelittle idea how biodiversity is linked to ecosystem functioning. Apart from the e�ects ofpollution on Ingoldian fungi and its e�ect on leaf palatability, we are unaware of any otherexperiments attempting to link biodiversity with ecosystem functioning.

Some metals are toxic to fungi (Abel and BaÈ rlocher, 1984). However, the causal rela-tionship between the speci®c metal and their e�ects to natural communities are not wellestablished (Bermingham, 1996). In addition to the fact that a species may be present inboth polluted and unpolluted habitats, the question as to whether the fungus is a�ected bypollutants is unknown. Ergosterol has been recognized as a marker to quantify fungalbiomass (Newell, 1992), but the method cannot be used to determine the biomass ofindividual fungal species. The e�ect of elevated carbon dioxide, rainfall and land use hasnot been investigated. These various disturbances may a�ect species composition, andlosses of keystone species (Box 1) may even occur.

Methods available to answer these problems

Most work on freshwater fungi has been of either the inventory type, or physiologicalstudies that have been carried out on arti®cial media or wood blocks and have largelyconcentrated on the early stages of decay. It is important that inventory is carried out

1198 Wong et al.

globally and in as many types of freshwater habitats as possible, as information is lackingfor most countries and aquatic ecosystems. Although in vitro studies are important, the®ndings of studies on arti®cial media, need to be tested in vivo, in order to establish howfungi interact on submerged material. Less is known of the extent to which competitiveinteractions occur in fungal communities and of the extent of degradation of wood thatoccurs in nature. An attempt must be made to ascertain what events may occur undernatural conditions. Wood blocks can be inoculated with fungi and then placed in thenatural environment in order to establish competitiveness against the inhabitant myco-biota. Preliminary ®eld studies placing uncolonized and precolonized wood blocks instreams have been carried out (Yuen et al., pers. obs.). Precolonized wood blocks wereinoculated with one or two isolates of tropical fungi, while no fungi were inoculated ontothe uncolonized controls. After three months, wood blocks were collected and the numberof fungi, the rate of decay and interaction activities between di�erent fungal colonies wereestablished. More fungi were found on uncolonized wood blocks, presumably as there isless competition compared to precolonized wood blocks. Other in vitro experiments canalso be devised in order to study these competitive interactions. By developing an ex-perimental system in which individual fungi and mixtures of fungi are inoculated ontosterile wood blocks or leaf samples, the functional role of individual and groups of fungican be established.

It is thought that some fungi may pre-condition the wood so as to allow settlement andcolonization of the wood by other organisms. The e�ect of prior infection of wood by afungus, or in combination with di�erent types of microorganisms, should be investigated.As in the case of leaves, the conditioned leaves are consumed in preference to non-conditioned leaves by invertebrates (Arsu� and Suberkropp, 1985), and it is known thatleaves colonized by certain fungal species are more attractive than others (Suberkropp,1992). This also needs to be investigated in the tropics and with woody material.

As wood is very resistant to decay, it takes a long time for the decay process to becompleted and for the nutrients to be released and recycled. The later stages of decay canbe traced by placing wood blocks in streams for a longer time before collection.

Although we can isolate fungi from sediments, we cannot be sure that these fungi areinvolved in the nutrient cycling of particulate matter. Methods are needed in which we canmeasure fungal and not other organism activity. One possible method could be to measureergosterol activity, but this method has been criticized. Alternatively, it may be possible todevelop a way to measure fungal biomass in a sediment or water column. The relativeamounts of fungi and bacteria could also be investigated in this way.

Further experiments with feeding detritivores should also be carried out. This shouldinclude mixtures of fungi, and the role of tropical fungi particularly is in need ofinvestigation.

Acknowledgements

We thank The University of Hong Kong for the provision of University Studentships,Postdoctoral Fellowships, and Part-Time Demonstratorships to allow this work to bepossible.

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Role of fungi in freshwater ecosystems 1205

Box 1. Are there keystone species of fungi in freshwater?

Large quantities of woody material containing lignocellulose ®nds it ways into streamsand rivers and is rapidly colonized by aquatic fungi, the main organisms responsible forthe decomposition process. These fungi are mostly ascomycetes or their asexual stagesand appear to be a unique group adapted for this aquatic lifestyle (Shearer, 1993a; Gohand Hyde, 1996). In recent studies in Australia, in which we have collected submergedwood and placed it in a moist incubation chambers, we have identi®ed 37±42 fungi instream and lake systems, as being potential decomposers of lignocellulose (Hyde andGoh, 1997, 1998). Most of the species identi®ed are rare and a small `core group' of lessthan 6±10 form the dominant species. The success of these aquatic fungi in their role aslignocellulose degraders probably lies in their ability to form penetration hyphae andsoft rot cavities within the S2 of the xylem cell wall. This is thought to prevent dilutionor removal of enzymes in the waterlogged wood, as would probably occur in the whiteor brown rotting fungi, which enter the wood and decompose it via the cell lumen.

We have tested several of the `core species' for their ability to degrade lignocellulose,and we have found that some of them are unable to produce enzymes capable ofdegrading lignocellulose, nor are they able to form soft-rot cavities. It is also thoughtthat no single species is capable of producing all of the necessary enzymes to degradewoody tissue and in nature it is likely that a consortium of fungi work together in thedecomposition process. It is therefore, probable that the `core species' play a pivotalrole in the degradation of woody tissue in a local stream system and can be regarded askeystone species. Therefore, the loss of these keystone species due to environmentalchange or human disturbance could have a consequential e�ect on woody tissue de-composition in streams.

1206 Wong et al.