Do the tropical freshwater fishes feed on aquatic fungi?

Abstract

Consumption and processing of allochthonous plant litter by fishes is more common in tropical than temperate streams and rivers. Therefore, aquatic hyphomycetes in water (filtration), leaf litter (bubble chamber incubation), and fecal pellets (direct observation and inoculation to sterile leaf litter) of three dominant fishes belonging to the family Cyprinidae (BoldItalic, BoldItalic, and BoldItalic) in two locations of the River Kali of the Western Ghats, India, were evaluated during postmonsoon season. Spores of 14 and 9 species of aquatic hyphomycetes were recovered on filtering water samples of Kaiga stream and Kadra dam with equal number of spores (32 spores·100 mL^-1) and high Shannon diversity in Kaiga stream. In a bubble chamber incubation of leaf litter, 16 and 9 species were recovered from Kaiga stream and Kadra dam with high spore output (1122 versus 324 spores per mg dry mass) and high Shannon diversity in Kaiga stream. Both direct and indirect methods of examination of fecal pellets of fishes revealed more species in Kaiga stream than Kadra dam (4–7 versus 1–4 species). The spore release in leaf litter incubated with fecal pellets ranged from 2.3 to 98 spores·mg^-1·day^-1 with the highest BoldItalic in Kaiga stream; while in Kadra dam, it was from 0.02 to 22.9 spores·mg^-1·day^-1 with the highest in BoldItalic. The Shannon diversity of aquatic hyphomycetes was high in fecal pellets of BoldItalic of Kaiga stream and BoldItalic of Kadra dam. The top-ranked five species of aquatic hyphomycetes differed in water, leaf litter, and fish fecal pellets; however, BoldItalic was common for all. All five top-ranked species of aquatic hyphomycetes in feces produced multicelled spores; thus, they were likely to have a better chance of viability through gut passage than single-celled spores. Preferential feeding, fungi in gut and feces, and survival and dissemination of spores by invertebrates and fishes with reference to aquatic hyphomycetes were discussed.

Key words： Western Ghats; freshwater fishes; feces; drift spores; leaf litter; aquatic hyphomycetes

Acknowledgements

The authors are grateful to Mangalore University for permission to carry out this study at the Department of Biosciences and Nuclear Power Corporation of India, Ltd. (NPCIL), Mumbai, for funding. NMS is indebted to the NPCIL for the award of research fellowship. Authors are thankful to Dr. H.M. Somashekarappa, University Science Instrumentation Centre, Mangalore University, Drs. S G Ghadge, M Kansal, P M Ravi, B N Dileep and S K Singh, NPCIL, Kaiga, Karnataka for support.

References

1 APHA (1995). Standard Methods in Examination of Water and Waste Water. Washington DC: American Public Health Association

2 Baldy V, Chauvet E, Charcosset J Y, Gessner M O (2002). Microbial dynamics associated with leaves decomposing in the mainstem and a floodplain pond of a large river. Aquat Microb Ecol, 28: 25–36

3 Bärlocher F (1981). Fungi on the food and in the faeces of Gammarus pulex. Trans Br Mycol Soc, 76(1): 160–165

4 Bärlocher F (1992). Recent developments in stream ecology and their relevance in aquatic mycology. In: Bärlocher F, ed. The Ecology of Aquatic Hyphomycetes. Berlin: Springer-Verlag, 16–37

5 Bärlocher F (2009). Reproduction and dispersal in aquatic hyphomycetes. Mycoscience, 50(1): 3–8

6 Bärlocher F, Brendelberger H (2004). Clearance of aquatic hyphomycete spores by a benthic suspension feeder. Limnol Oceanogr, 49(6): 2292–2296

7 Bärlocher F, Kendrick B (1976). Hyphomycetes as intermediaries of energy flow in streams. In: Jones E B G, ed. Recent Advances in Aquatic Mycology. London: Elek Science, 435–445

8 Bhat A (2003). Diversity and composition of freshwater fishes in river systems of Central Western Ghats, India. Environ Biol Fishes, 68(1): 25–38

9 Boulton A J, Boyero L, Covich A P, Dobson M, Lake P S, Pearson R G (2008). Are tropical streams ecologically different from temperate streams? In: Dudgeon D, ed. Aquatic Ecosystems: Tropical Stream Ecology. London: Elsevier Science, 257–284

10 Bowen S H (1983). Detritivory in Neotropical fish communities. Environ Biol Fishes, 9(2): 137–144

11 Bowen S H, Bonetto A A, Ahlgren M O (1984). Microorganisms and detritus in the diet of a typical neotropical reverine detritivore, Prochilodus platensis (Pisces: Prochilodontidae). Limnol Oceanogr, 29(5): 1120–1122

12 Boyero L, Ramírez A, Dudgeon D, Pearson R G (2009). Are tropical streams really different? J N Am Benthol Soc, 28(2): 397–403

13 Chandrashekar K R, Sridhar K R, Kaveriappa K M (1989). Palatability of rubber leaves colonized by aquatic hyphomycetes. Arch Hydrobiol, 115: 361–369

14 Chauvet E, Suberkropp K (1998). Temperature and sporulation of aquatic hyphomycetes. Appl Environ Microbiol, 64(4): 1522–1525

PMID

15 Chergui H, Pattee E (1990). The processing of leaves of trees and aquatic macrophytes in the network of the River Rhone. Int Rev Gesamten Hydrobiol Hydrograph, 75(3): 281–302

16 Cheshire K, Boyero L, Pearson R G (2005). Food webs in tropical Australian streams: shredders are not scarce. Freshwat Biol, 50(5): 748–769

17 Cross W F, Covic A P, Crowl T A, Benstead J P, Ramirez A (2008). Secondary production, longevity and resource consumption rates of freshwater shrimps in two tropical streams with contrasting geomorphology and food web structure. Freshwat Biol, 53(12): 2504–2519

18 Crowl T A, Mcdowell W H, Covic A P, Johnson S L (2001). Freshwater shrimp effects on detrital processing and nutrients in a tropical headwater stream. Ecology, 82(3): 775–783

19 Cummins K W (1973). Trophic relations of aquatic insects. Ann Rev Entomol, 18(1): 183–206

20 Cummins K W, Coffman W P, Roff P A (1966). Trophic relations in a small woodland stream. Ver Int Verein Theor Angew Limnol, 16: 627–638

21 Cummins K W, Wilzbach M A (1985). Field Procedures for Analysis of Functional Feeding Groups of Stream Invertebrates. University of Maryland, Frostburg: Appalachian Environmental Laboratory Contribution # 1611

22 Cummins K W, Wilzbach M A, Gates D M, Perry J B, Taliaferro W B (1989). Shredders and riparian vegetation. BioScience, 39(1): 24–30

23 Dobson M (2004). Freshwater crabs in Africa. Freshwat Forum, 21: 3–26

24 Dobson M, Magna A, Mathooko J, Ndegwa F (2002). Detritivores in Kenyan highland streams: more evidence for the paucity of shredders in the tropics? Freshwat Biol, 47(5): 909–919

25 Dudgeon D (1999). Tropical Asian Streams: Zoobenthos, Ecology and Conservation. Hong Kong: Hong Kong University Press

26 Findlay S E G, Arsuffi T L (1989). Microbial growth and detritus transformation during decomposition of leaf litter in a stream. Freshwat Biol, 21(2): 261–269

27 Fisher S G, Likens G E (1972). Stream ecosystem: organic energy budget. BioScience, 22(1): 33–35

28 Gessner M O (1997). Fungal biomass, production and sporulation associated with particulate organic matter in streams. Limnetica, 13: 33–44

29 Gessner M O, Gulis V, Kuehn K A, Chauvet E, Suberkropp K (2007). Fungal decomposers of plant litter in aquatic ecosystems. In: Kubicek C P, Druzhinina I S, eds. Environmental and Microbial Relationships. The Mycota IV, 2nd ed. Berlin Heidelberg: Springer-Verlag, 302–324

30 Graça M A S, Bärlocher F, Gessner M O (2005). Methods to Study Litter Decomposition: A Practical Guide. Netherlands: Springer, 153–167

31 Graça M A S, Cressa C (2010). Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int Rev Hydrobiol, 95(1): 27–41

32 Guevara R, Rayner A M, Reynolds S E (2000). Effects of fungivory by two specialist ciid beetles (Octotemnus glabriculus and Cis boleti) on the reproductive fitness of their host fungus, Coriolus versicolor. New Phytol, 145(1): 137–144

33 Gulis V, Marvanová L, Descals E (2005). An illustrated key to the common temperate species of aquatic hyphomycetes. In: Graça M A S, Bärlocher F, Gessner M O, eds. Methods to Study Litter Decomposition: A Practical Guide. Netherlands: Springer, 153–167

34 Gulis V, Suberkropp K (2006). Fungi: Biomass, production and sporulation of aquatic hyphomycetes. In: Hauer F R, Lamberti G A, eds. Methods in Stream Ecology. 2nd ed. Elsevier Inc, 311–325

35 Guruge W A H P (2002). In: Omar R, Ali R Z, Latif M T, Lihan T, Adam J H, eds. Proceedings of the Regional Symposium on Environment and Natural Resources, Volume 1. Malaysia: Kuala Lumpur, 154–160

36 Hynes H B N (1970). The Ecology of Running Waters. Toronto: University of Toronto Press

37 Ingold C T (1975). An Illustrated Guide to Aquatic and Waterborne Hyphomycetes (Fungi Imperfecti) with Notes on their Biology. UK: Freshwater Biological Association Scientific Publication # 30

38 Iqbal S H, Webster J (1973). Aquatic hyphomycete spora of the River Exe and its tributaries. Trans Br Mycol Soc, 61(2): 331–346

39 Knöppel H A (1970). Food of Central Amazonian fishes. Contribution to the nutrient-ecology of Amazonian rainforest-streams. Amazoniana, 2: 257–352

40 Konishi M, Nakano S, Iwata T (2001). Trophic cascading effects of predatory fish on leaf litter processing in a Japanese stream. Ecol Res, 16(3): 415–422

41 Larned S T, Chong C T, Punewai N (2001). Detrital fruit processing in a Hawaiian stream ecosystem. Biotropica, 33: 241–248

42 Li A O Y, Dudgeon D (2008). Food resources of shredders and other benthic macroinvertebrates in relation to shading conditions in tropical Hong Kong streams. Freshwat Biol, 53(10): 2011–2025

43 Magurran A E (1988). Ecological Diversity and its Measurement. New Jersey: Princeton University Press

44 Maharning A R, Bärlocher F (1996). Growth and reproduction in aquatic hyphomycetes. Mycologia, 88(1): 80–88

45 Mancinelli G, Costantini M L, Rossi L (2002). Cascading effects of predatory fish exclusion on the detritus-based food web of a lake littoral zone (Lake Vico, central Italy). Oecologia, 133(3): 402–411

46 Mancinelli G, Costantini M L, Rossi L (2007). Top-down control of reed detritus processing in a lake littoral zone: experimental evidence of a seasonal compensation between fish and invertebrate predation. Int Rev Hydrobiol, 92(2): 117–134

47 March J G, Benstead J P, Pringle C M, Ruebel M W (2001). Linking shrimp assemblages with rates of detrital processing along an elevational gradient in a tropical stream. Can J Fish Aquat Sci, 58(3): 470–478

48 Medeiros A O, Pascoal C, Graça M A S (2009). Diversity and activity of aquatic fungi under low oxygen conditions. Freshwat Biol, 54(1): 142–149

49 Moss B (2007). Rapid shredding of leaves by crabs in a tropical African stream. Ver Int Verein Limnol, 29: 147–150

50 Nakamori T, Suzuki A (2010). Spore resistance and gut-passage time of macrofungi consumed by Ceratophysella denisana (Collembola: Hypogastruridae). Fungal Ecol, 3(1): 38–42

51 Orłowska M, Lengiewicz I, Suszycka M (2004). Hyphomycetes developing on water plants and bulrushes in fish ponds. Pol J Environ Stud, 13: 703–707

52 Pabst S, Scheifhacken N, Hesselschwerdt J, Wantzen K (2008). Leaf litter degradation in the wave impact zone of a pre-alpine lake. Hydrobiologia, 613(1): 117–131

53 Pearson R G, Boyero L (2009). Gradients in regional diversity of freshwater taxa. J N Am Benthol Soc, 28(2): 504–514

54 Pielou F D (1975). Ecological Diversity. New York: Wiley InterScience

55 Rosemond A D, Pringle C M, Ramírez A (1998). Macroconsumer effects on insect detritivores and detritus processing in a tropical stream. Freshwat Biol, 39(3): 515–523

56 Rosemond A D, Pringle C M, Ramírez A, Paul M J (2001). A test of top-down and bottom-up control in a detritus-based food web. Ecology, 82(8): 2279–2293

57 Sridhar K R, Bärlocher F (1994). Viability of aquatic hyphomycete conidia in foam. Can J Bot, 72(1): 106–110

58 Sridhar K R, Bärlocher F (2000). Initial colonization, nutrient supply, and fungal activity on leaves decaying in streams. Appl Environ Microbiol, 66(3): 1114–1119

PMID

59 Sridhar K R, Bärlocher F, Wennrich R, Krauss G-J, Krauss G (2008). Fungal biomass and diversity in sediments and on leaf litter in heavy metal contaminated waters of Central Germany. Fund Appl Limnol, 171(1): 63–74

60 Sridhar K R, Beaton M, Bärlocher F(2010).Fungal propagules and DNA in feces of two detritus feeding amphipods.Microb Ecol,

PMID

61 StatSoft (2008). Statistica, Version 8. Tulsa, Oklahoma, USA: StatSoft

62 Stout R J (1989). Effects of condensed tannins on leaf processing in mid-latitude and tropical streams: a theoretical approach. Can J Fish Aquat Sci, 46(7): 1097–1106

63 Suberkropp K (1991). Relationships between growth and sporulation of aquatic hyphomycetes on decomposing leaf litter. Mycol Res, 95(7): 843–850

64 Suberkropp K (1992). Interactions with invertebrates. In: Bärlocher F, ed. The Ecology of Aquatic Hyphomycetes. Berlin: Springer-Verlag, 118–134

65 Wantzen K M, Junk W J (2000). The importance of stream-wetland-systems for biodiversity: a tropical perspective. In: Gopal B, Junk W J, Davies J A, eds. Biodiversity in Wetlands: Assessment, Function and Conservation. Netherlands: Backhuys, Leiden, 11–34

66 Wantzen K M, Wagner R (2006). Detritus processing by shredders: a tropical-temperate comparison. J N Am Benthol Soc, 25: 214–230

67 Wantzen K M, Wagner R, Suetfel R, Junk W J (2002). How do plant-herbivore interactions of trees influence coarse detritus processing by shredders in aquatic ecosystems of different latitudes? Ver Int Verein Limnol28: 815–821

68 Wantzen K M, Yule C M, Mathooko J M, Pringle C M (2008). Organic litter processing in tropical streams. In: Dudgeon D, ed. Tropical Stream Ecology. London: Elsevier, 43–64

69 Webster J (1987). Convergent evolution and the functional significance of spore shape in aquatic and semi-aquatic fungi. In: Rayner A D M, Brasier C M, Moore D, eds. Evolutionary Biology of the Fungi. Cambridge: Cambridge University Press, 191–201

70 Wootton J T, Oemke M P (1992). Latitudinal differences in fish community trophic structure and the role of fish herbivory in a Costa Rican stream. Environ Biol Fishes, 35(3): 311–319

71 Wurzbacher C M, Bärlocher F, Grossart H-P (2010). Fungi in lake ecosystems. Aquat Microb Ecol, 59: 125–149

72 Yule C M, Leong M Y, Liew K C, Ratnarajah L, Schmidt K, Wong H M, Pearson R G, Boyero L (2009). Shredders in Malaysia: abundance and richness are higher in cool upland tropical streams. J N Am Benthol Soc, 28(2): 404–415