Adding to 'the enigma of soil animal diversity': Fungal feeders and saprophagous soil invertebrates prefer similar food substrates

European Journal of Soil Biology

Volumn 39, Issue 2, 2003, Pages 85-95

  Maraun, Mark ^a   Martens, Hermann ^b   Migge, Sonja ^b   Theenhaus, Anne ^b   Scheu, Stefan ^a  

^a DARMSTADT UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Collembola; Decomposer animals; Dematiacea; Diplopoda; Gastropoda; Lumbricidae; Nematoda; Oribatida

Indexed keywords

ALTERNARIA; ANIMALIA; ASPERGILLUS; CLADOSPORIUM; COLLEMBOLA; DIPLOPODA; FUNGI; FUSARIUM; GASTROPODA; INVERTEBRATA; LUMBRICIDAE; MORTIERELLA; MUCOR; NEMATODA; ORIBATIDA; PAECILOMYCES; PENICILLIUM; TRICHODERMA; ULOCLADIUM; ZYGOMYCETES;

EID: 0038338528     PISSN: 11645563     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1164-5563(03)00006-2     Document Type: Review

References (109)

1. J.A. Addison, D. Parkinson, Influence of collembolan feeding activities on soil metabolism at a high arctic site, Oikos 30 (1978) 529-538.
2. C.W. Aitchinson, Low temperature and preferred feeding by winter-active Collembola (Insecta, Apterygota), Pedobiologia 25 (1983) 27-36.
3. J.M. erson, The enigma of soil animal species diversity, Proc. 5th Int. Coll. Soil Zool. Prague 1973 (1975) 51-58.
4. J.M. Anderson, Succession, diversity and trophic relationships of some soil animals in decomposing leaf litter, J. Anim. Ecol 44 (1975) 475-495.
5. R.D. Bardgett, J.B. Whittaker, J.C. Frankland, The diet and food preferences of Onychiurus procampatus (Collembola) from upland grassland soil, Biol. Fertil. Soils 16 (1993) 296-298.
6. V.M. Behan, S.B. Hill, Feeding habits and spore dispersal of oribatid mites in the North American arctic, Rev. Ecol. Biol. Sol 15 (1978) 497-516.
7. F. Bernini, Current ideas on the phylogeny and the adaptive radiations of Acarida, Boll. Zool 53 (1986) 279-313.
8. J.G. Blower, Millipedes, Brill/Backhuys, London, 1985.
9. M. Bonkowski, B.S. Griffiths, K. Ritz, Food preferences of earthworms for soil fungi, Pedobiologia 44 (2000) 666-676.
10. T.L. Bultman, P.L. Mathews, Mycophagy by a millipede and its possible impact on an insect-fungus mutualism, Oikos 75 (1996) 67-74.
11. M.J. Butler, A.W. Day, Fungal melanins: a review, Can. J. Microbiol 44 (1998) 1115-1136.
12. B.A. Byzov, A.V. Kurakov, E.B. Tretyakova, V.N. Thanh, N.D. To Luu, Y.M. Rabinovich, Principles of the digestion of microorganisms in the gut of soil millipedes: specificity and possible mechanisms, Appl. Soil Ecol. 9 (1998) 145-151.
13. A. Cooke, M. Luxton, Effect of microbes on food selection by Lumbricus terrestris, Rev. Ecol. Biol. Sol 17 (1980) 365-370.
14. M.C. Dash, J.B. Cragg, Selection of microfungi by Enchytraeidae (Oligochaeta) and other members of the soil fauna, Pedobiologia 12 (1972) 282-286.
15. M.C. Dash, B. Nanda, N. Behera, Fungal feeding by Enchytraeidae (Oligochaeta) in a tropical woodland in Orissa, India, Oikos 34 (1980) 202-205.
16. W.A.M. Didden, Ecology of terrestrial Enchytraeidae, Pedobiologia 37 (1993) 2-29.
17. N.J. Dix, J. Webster, Fungal Ecology, Chapman and Hall, London, 1995.
18. K.H. Domsch, W. Gams, T.H. Anderson, Compendium of Soil Fungi, vols. I and II, IHW-Verlag, Eiching, 1993.
19. C.A. Edwards, P.J. Bohlen, Biology and Ecology of Earthworms, Chapman and Hall, London, 1995.
20. C.A. Edwards, K.E. Fletcher, Interactions between earthworms and microorganisms in organic-matter breakdown, Agric. Ecosyst. Environ 24 (1988) 235-247.
21. F. Ekelund, R. Ronn, Notes on protozoa in agricultural soils, with emphasis on heterotrophic flagellates and naked amoebae and their ecology, FEMS Microbiol. Rev 15 (1994) 321-363.
22. M.B. Ellis, Dematiaceous Hyphomycetes, CAB International, Wallingford, 1971.
23. M.B. Ellis, More Dematiaceous Hyphomycetes, CAB International, Wallingford, 1976.
24. W. Foissner, Soil protozoa: fundamental problems, ecological significance, adaptations in ciliates and testaceans, bioindicators and guide to the literature, Progress Protistol 2 (1978) 69-212.
25. K.H. Forsslund, Über die Ernährungsverhältnisse der Hornmilben (Oribatiden) und ihre Bedeutung für die Prozesse im Waldboden, Verh. VII Kongr. Entomol. 3 (1938) 1950-1957.
26. H. Fukushige, Propagation of Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) on fungi growing in pineshoot segments, Appl. Entomol. Zool 26 (1991) 371-376.
27. H. Fukushige, Effects of fungi coexisting with Ceratocystis sp. on propagation of Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), Appl. Entomol. Zool 26 (1991) 377-380.
28. A. Gange, Arbuscular mycorrhizal fungi, Collembola and plant growth, Trends Ecol. Evol 15 (2000) 369-372.
29. P.S. Giller, The diversity of soil communities, the 'poor man's tropical rain forest', Biodivers. Conserv 5 (1996) 135-168.
30. R.D.G. Hanlon, J.M. Anderson, The effects of collembolan grazing on microbial activity in decomposing leaf litter, Oecologia 38 (1978) 93-99.
31. D.J.L. Harding, R.A. Stuttard, Microarthropods, in: C.H. Dickinson, G.I.F. Pugh (Eds.), Biology of Plant Litter Decomposition, vols. I and II, Academic Press, London, 1974, pp. 489-532.
32. R. Hartenstein, I. Soil oribatei, Feeding specificity among forest soil oribatei (Acarina), Ann. Ent. Soc. Am. 55 (1962) 202-206.
33. A.J. Hayes, Studies on the feeding preferences of some phthiracarid mites (Acari, Oribatidae), Ent. Exp. App. 6 (1963) 241-256.
34. K. Hedlund, A. Augustsson, Effects of enchytraeid grazing on fungal growth and respiration, Soil Biol. Biochem 27 (1995) 905-909.
35. K. Hedlund, G. Bengtsson, S. Rundgren, Fungal odour discrimination in two sympatric species of fungivorous collembolans, Funct. Ecol 9 (1995) 869-875.
36. W.E. Hekman, P.J.H.F. Van den Boogert, K.B. Zwart, The physiology and ecology of a novel, obligate mycophagous flagellate, FEMS Microbiol. Ecol 86 (1992) 255-265.
37. C.M. Herrera, O. Pellmyr, Plant-Animal Interactions, an Evolutionary Approach, Blackwell Science, 2002.
38. S.D. Hopkin, H.J. Read, The Biology of Millipedes, Oxford University Press, Oxford, 1992.
39. A.P. Jacot, Oribatid mites of the subfamily Phthiracarinae of the north-eastern United States, Proc. Boston Soc. Nat. Hist 39 (1930) 209-261.
40. A.P. Jacot, Spruce litter reduction, Can. Ent 68 (31) (1936).
41. A.P. Jacot, Reduction of spruce and fir litter by minute animals, J. For. 37 (1939) 858-860.
42. T.J. Jennings, J.P. Barkham, Litter decomposition byslugs in mixed deciduous woodland, Holarct. Ecol 2 (1979) 21-29.
43. P. Jolivet, Ant and Plants, an Example of Coevolution, Blackhuis, Netherlands, 1996.
44. N. Kaneko, M.A. McLean, D. Parkinson, Grazing preferences of Onychiurus subtenuis (Collembola) and Oppiella nova (Oribatei) for fungal species inoculated on pine needles, Pedobiologia 39 (1995) 538-546.
45. E. Kiefer, J.P. Cancela da Fonseca, Sur les rapports entre microarthropodes et micromycètes d'un sol forestier, Zentralbl. Bakt. Parasitkd. Abt. II 126 (1971) 510-520.
46. J.N. Klironomos, B. Kendrick, Palatability of microfungi to soil arthropods in relation to the functioning of arbuscular mycorrhizae, Biol. Fertil. Soils 21 (1996) 43-52.
47. J.N. Klironomos, M.M. Hart, Animal nitrogen swap for plant carbon, Nature 410 (2001) 651-652.
48. J.N. Klironomos, P. Widden, I. Deslandes, Feeding preferences of the collembolan Folsomia candida in relation to microfungal succession on decaying litter, Soil Biol. Biochem 24 (1992) 685-692.
49. J.N. Klironomos, E.M. Bednarczuk, J. Neville, Reproductive significance of feeding on saprobic and arbuscular mycorrhizal fungi by the collembolan, Folsomia candida, Funct. Ecol 13 (1999) 756-761.
50. C.B. Knight, R.A. Angel, A preliminary study of the dietary requirements of Tomocerus (Collembola), Am. Midl. Nat 77 (1967) 510-517.
51. W.H. Krull, Observations on the distribution and ecology of oribatid mites, J. Wash. Acad. Sci 29 (1939) 519-528.
52. C.C. Labandeira, T.L. Phillips, R.A. Norton, Oribatid mites and the decomposition of plant tissues in palaeozoic coalswamp forests, Palaios 12 (1997) 319-353.
53. P.M. Latter, Decomposition of a moorland litter, in relation to Marasmius androsaceus and soil fauna, Pedobiologia 17 (1977) 418-427.
54. P.M. Latter, G. Howson, Studies on the microfauna of a blanket bog with particular reference to Enchytraeidae. II. Growth and survival of Cognettia sphagnetorum on various substrates, J. Anim. Ecol 47 (1978) 434-463.
55. K.E. Lee, Earthworms: Their Ecology and Relationships with Soil and Land Use, Academic Press, London, 1985.
56. M. Luxton, Laboratory studies on the feeding habits of saltmarsh acarina, with notes on their behaviour, Acarologia 8 (1966) 163-175.
57. M. Luxton, Studies on the oribatid mites of a Danish beech wood soil, I. Nutritional biology, Pedobiologia 12 (1972) 434-463.
58. M. Luxton, Substrate utilization by the soil fauna, Oikos 39 (1982) 340-341.
59. N. Maehara, K. Futai, Population changes of the pinewood nematode, Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae), on fungi growing in pine-branch segments, Appl. Entomol. Zool 35 (2000) 413-417.
60. M. Maraun, S. Visser, S. Scheu, Oribatid mites enhance the recovery of the microbial community after a strong disturbance, Appl. Soil Ecol 9 (1998) 179-186.
61. M. Maraun, S. Migge, M. Schaefer, S. Scheu, Selection of microfungal food by six oribatid mite species (Oribatida, Acari) from two different beech forests, Pedobiologia 42 (1998) 232-240.
62. O.E. Marfenina, I.A. Ishchenko, Preference of earthworms for soil microscopic fungi, Izv. Akad. Nauk. SSSR Ser. Biol. 4 (1997) 504-506 (in Russian; English translation in: Biol. Bull. 24, 414-416).
63. M.M. Martin, Biochemical implications of insect mycophagy, Biol. Rev 54 (1979) 1-21.
64. M.A. McLean, N. Kaneko, D. Parkinson, Does selective grazing by mites and collembola affect litter fungal community structure? Pedobiologia 40 (1996) 97-105.
65. R. Mignolet, Étude des relation entre la flore fongique et quelques espèces d'Oribates (Acari), IV. International Colloquium Pedobiologique (Dijon, 1970), INRA, Paris, 1971, pp. 155-164.
66. P.M. Miller, S. Anagnostakis, Suppression of Pratylenchus penetrans and Tylenchorhynchus dubius by Trichoderma viride, J. Nemat 9 (1977) 182-183.
67. J.T. Mills, R.N. Sinha, Interactions between a springtail, Hypogastrura tullbergi, and soil-borne fungi, J. Econ. Entomol 64 (1971) 398-401.
68. M.J. Mitchell, D. Parkinson, Fungal feeding of oribatid mites (Acari: Cryptostigmata) in an aspen woodland, Ecology 57 (1976) 302-312.
69. S.A. Moody, M.J.I. Briones, T.G. Piearce, J. Dighton, Selective consumption of decomposing wheat straw by earthworms, Soil Biol. Biochem 27 (1995) 1209-1213.
70. J.C. Moore, E.R. Ingham, D.C. Coleman, Inter-and intraspecific feeding selectivity of Folsomia candida (Willem) (Collembola, Isotomidae) on fungi, Biol. Fertil. Soils 5 (1987) 6-12.
71. K.M. Old, J.F. Darbyshire, Soil fungi as food for giant amoebae, Soil Biol. Biochem 10 (1978) 93-100.
72. Y.D. Pande, P. Berthet, Studies on the food and feeding habits of soil oribatei in a black pine plantation, Oecologia 12 (1973) 413-426.
73. D. Parkinson, S. Visser, J.B. Whittaker, Effect of Collembola grazing on fungal colonisation of leaf litter, Soil Biol. Biochem 11 (1979) 529-535.
74. M. Peter, Untersuchungen zur Ökologie der Springschwänze (Insecta: Collembola) eines Kalkbuchenwaldes: Die Bedeutung des Nahrungsangebotes, Unpublished Diploma Thesis, Göttingen, 1997.
75. T.G. Piearce, Gut contents of some lumbricid earthworms, Pedobiologia 18 (1978) 153-157.
76. J.F. Ponge, Food resources and diets of soil animals in a small area of Scots pine litter, Geoderma 49 (1991) 33-62.
77. J.F. Ponge, Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests, Biol. Fertil. Soils 32 (2000) 508-522.
78. J.F. Ponge, M.J. Charpentié, Étude des relations microflore-microfaune: expériences sur Pseudosinella alba (Packard), collembole mycophage, Rev. Ecol. Biol. Sol. 18 (1981) 291-303.
79. T.B. Poole, Studies on the food of Collembola in a Douglas fir plantation, Proc. Zool. Soc. Lond 132 (1959) 71-82.
80. A. Reichert, U. Mothes-Wagner, K.A. Seitz, Ecohistological investigations on the feeding behaviour of the enchytraeid Enchytraeus coronatus (Annelida, Oligochaeta), Pedobiologia 40 (1996) 118-133.
81. K.O. Richter, Aspects of nutrient cycling by Ariolimax columbianus (Mollusca: Arionidae) in Pacific Northwest coniferous forests, Pedobiologia 19 (1979) 60-74.
82. G. Riha, Zur Ökologie der Oribatiden eines Kalkbuchenwaldes, Zool. Jb. Syst. 80 (1951) 407-450.
83. L. Ruess, E.J. Garcia Zapata, J. Dighton, Food preferences of a fungal feeding Aphelenchoides species, Nematology 2 (2000) 223-230.
84. N. Sadaka-Laulan, J.F. Ponge, M.F. Roquebert, E. Bury, A. Boumezzough, Feeding preferences of the collembolan Onychiurus sinensis for fungi colonizing holm oak litter (Quercus rotundifolia Lam.), Eur. J. Soil Biol 34 (1998) 179-188.
85. M. Schaefer, The animal community: diversity and resources, in: E. Röhrig, B. Ulrich (Eds.), Ecosystems of the World. 7. Temperate Deciduous Forests, Elsevier, Amsterdam, 1991, pp. 51-120.
86. S. Scheu, The soil food web: structures and perspectives, Eur. J. Soil Biol 38 (2002) 11-20.
87. S. Scheu, M. Falca, The soil food web of two beech forests (Fagus sylvatica) of contrasting humus type: stable isotope analysis of a macro- and a mesofauna-dominated community, Oecologia 123 (2000) 285-296.
88. S. Scheu, H. Setälä, Multitrophic interactions in decomposer food-webs, in: T. Tscharnke, B.A. Hawkins (Eds.), Multitrophic interactions in terrestrial systems, Cambridge University Press, Cambridge, 2001, pp. 223-264.
89. 14C-labelled holocellulose, Pedobiologia 38 (1994) 344-352.
90. R. Schuster, Der Anteil der Oribatiden an den Zersetzungsvorgängen im Boden, Z. Morph. Ökol. Tiere 45 (1956) 1-33.
91. P.J.A. Shaw, A consistent hierarchy of fungal feeding preferences of the Collembola Onychiurus armatus, Pedobiologia 31 (1988) 179-187.
92. A. South, Terrestrial Slugs. Biology, Ecology and Control, Chapman and Hall, London, 1992.
93. J.A. Springett, P.M. Latter, Studies on the microfauna of blanketbog with particular reference to Enchytraeidae, J. Anim. Ecol 46 (1977) 959-974.
94. V. Standen, P.M. Latter, Distribution of a population of Cognettia sphagnetorum (Enchytraeidae) in relation to microhabitats in a blanket bog, J. Anim. Ecol 46 (1977) 213-229.
95. O. Stefaniak, S. Seniczak, The effect of fungal diet on the development of Oppia nitens (Acari, Oribatei) and on the microflora of its alimentary tract, Pedobiologia 21 (1981) 202-210.
96. G.R. Stirling, Biological Control of Plant Parasitic Nematodes, CAB International, Wallingford, 1991.
97. M.J. Swift, O.W. Heal, J.M. Anderson, Decomposition in Terrestrial Ecosystems, Studies in Ecology vol. 5 (1979) Blackwell, Oxford.
98. E.C. Taylor, Fungal feeding preferences by a desert millipede Orthoporus ornatus (Spirostreptidae), Pedobiologia 23 (1982) 331-336.
99. J.N. Thompson, The Coevolutionary Process, Chicago University Press, USA, 1994.
100. S.C. Tiwari, R.R. Mishra, Fungal abundance and diversity in earthworm casts and in uningested soil, Biol. Fertil. Soils 16 (1993) 131-134.
101. S. Visser, Role of the soil invertebrates in determining the composition of soil microbial communities, in: A.H. Fitter, D. Atkinson, D.J. Read, M.B. Usher (Eds.), Ecological Interactions in Soil, British Ecological Society, Blackwell, Oxford, 1985, pp. 297-317 (Special Publication No. 4).
102. S. Visser, D. Parkinson, Fungal succession on aspen poplar leaf litter, Can. J. Bot 53 (1975) 1640-1651.
103. S. Visser, J.B. Whittaker, Feeding preferences for certain litter fungi by Onychiurus subtenuis (Collembola), Oikos 29 (1977) 320-325.
104. S. Visser, D. Parkinson, M. Hassall, Fungi associated with Onychiurus subtenuis (Collembola) in an aspen woodland, Can. J. Bot 65 (1987) 635-642.
105. J.A. Wallwork, Notes on the feeding behaviour of some forest soil Acarina, Oikos 9 (1958) 260-271.
106. J.A. Wallwork, Oribatids in forest ecosystems, Ann. Rev. Entomol 28 (1983) 109-130.
107. M.I. Walsh, T. Bolger, Effects of diet on the growth and reproduction of some collembola in laboratory cultures, Pedobiologia 34 (1990) 161-171.
108. H. Wilding, M. Collins, P.M. Hammond, J.F. Webber, Insect-Fungus Interactions, Academic Press, London, 1989.
109. T.D. Wyllie, L.G. Morehouse, Mycotoxic Fungi, Mycotoxins and Mycotoxicoses, vol. 1, Marcel Dekker, New York, 1977.