Trophic position of microbivorous and predatory soil nematodes in a boreal forest as indicated by stable isotope analysis

Soil Biology and Biochemistry

Volumn 86, Issue , 2015, Pages 193-200

  Kudrin, Alexey A ^a   Tsurikov, Sergey M ^b   Tiunov, Alexei V ^b  

^a INSTITUTE OF BIOLOGY   (Russian Federation)

^b SEVERTSOV INSTITUTE OF ECOLOGY AND EVOLUTION   (Russian Federation)

Author keywords

Canopy effect; Ectomycorrhiza; Predators; Soil food web; Stable isotope analysis

Indexed keywords

ANIMALS; BUDGET CONTROL; FEEDING; FORESTRY; FUNGI; ISOTOPES; PLANTS (BOTANY);

CANOPY EFFECT; ECTOMYCORRHIZAS; PREDATORS; SOIL FOOD WEB; STABLE-ISOTOPE ANALYSIS;

SOILS;

FOREST CANOPY; ISOTOPES; SOIL; WORMS;

ACARI; ANIMALIA; ARTHROPODA; DORYLAIMIDA; ENCHYTRAEIDAE; ENTOMOBRYA; FILENCHUS; INVERTEBRATA; MONONCHIDA; MYCELIUM (GENUS); NEMATODA; ORIBATIDA; PICEA ABIES; PLECTIDAE; TYLENCHIDAE;

EID: 84928523477     PISSN: 00380717     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.soilbio.2015.03.017     Document Type: Article

References (93)

1. Allen M.F., Kitajima K. Net primary production of ectomycorrhizas in a California forest. Fungal Ecology 2014, 10:81-90.
2. Berg M., de Ruiter P., Didden W., Janssen M., Schouten T., Verhoef H. Community food web, decomposition and nitrogen mineralisation in a stratified Scots pine forest soil. Oikos 2001, 94:130-142.
3. Bilgrami A.L. Resistance and susceptibility of prey nematodes to predation and strike rate of the predators, Mononchus aquaticus, Dorylaimus stagnalis, and Aquatides thornei. Fundamental and Applied Nematology 1992, 15:265-270.
4. Bilgrami A.L., Ahmad I., Jairajpuri M.S. Astudy on the intestinal contents of some mononchs. Revue Nématology 1986, 17:339-340.
5. Bongers T. De nematoden van Nederland. Nederlandse Natuurhistorische Vereniging 1994, Utrect, The Netherlands, 408pp.
6. Briar S.S., Culman S.W., Young-Mathews A., Jackson L.E., Ferris H. Nematode community responses to a moisture gradient and grazing along a restored riparian corridor. European Journal of Soil Biology 2012, 50:32-38.
7. Briones M.J.I., Ineson P. Use of 14C carbon dating to determine feeding behaviour of enchytraeids. Soil Biology and Biochemistry 2002, 34:881-884.
8. Brooks J.R., Flanagan L.B., Buchmann N., Ehleringer J.R. Carbon isotope composition of boreal plants: functional grouping of life forms. Oecologia 1997, 110:301-311.
9. Brzeski M.W. Nematodes of Tylenchina in Poland and Temperate Europe 1998, Muz. Inst. Zool. PAN. Warszawa, 397 pp.
10. Buchmann N., Kao W., Ehleringer J.R. Influence of stand structure on carbon-13 of vegetation, soils, and canopy air within deciduous and evergreen forests of Utah (USA). Oecologia 1997, 110:109-119.
11. Cesarz S., Ruess L., Jacob M., Jacob A., Schaefer M., Scheu S. Tree species diversity versus tree species identity: driving forces in structuring forest food webs as indicated by soil nematodes. Soil Biology and Biochemistry 2013, 62:36-45.
12. Chastain R.A., Currie W.S., Townsend P.A. Carbon sequestration and nutrient cycling implications of the evergreen understory layer in Appalachian forests. Forest Ecology and Management 2006, 231:63-77.
13. Chahartaghi M., Langel R., Scheu S., Ruess L. Feeding guilds in Collembola based on nitrogen N stable isotope ratios. Soil Biology and Biochemistry 2005, 37:1718-1725.
14. Clemmensen K.E., Bahr A., Ovaskainen O., Dahlberg A., Ekblad A., Wallander H., Stenlid J., Finlay R.D., Wardle D.A., Lindahl B.D. Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 2013, 339:1615-1618.
15. Crotty F.V., Blackshaw R.P., Murray P.J. Tracking the flow of bacterially derived 13s{cyrillic} and 15N through soil faunal feeding channels. Rapid Communications in Mass Spectrometry 2011, 25:1503-1513.
16. Crotty F.V., Blackshaw R.P., Adl S.M., Inger R., Murray P.J. Divergence of feeding channels within the soil food web determined by ecosystem type. Ecology and Evolution 2014, 4:1-13.
17. Curry J.P., Schmidt O. The feeding ecology of earthworms - a review. Pedobiologia 2007, 50:463-477.
18. Darby B.J., Neher D.A. Stable isotope composition of microfauna supports the occurrence of biologically fixed nitrogen from cyanobacteria in desert soil food webs. Journal of Arid Environments 2012, 85:76-78.
19. Dijkstra P., Ishizu A., Doucett R., Hart S.C., Schwartz E., Menyailo O.V., Hungate B.A. 13C and 15N natural abundance of the soil microbial biomass. Soil Biology and Biochemistry 2006, 38:3257-3266.
20. Ekblad A., Wallander H., Godbold D.L., Cruz C., Johnson D., Baldrian P., Bjork R.G., Epron D., Kieliszewska-Rokicka B., Kjoller R., Kraigher H., Matzner E., Neumann J., Plassard C. The production and turnover of extramatrical mycelium of ectomycorrhizal fungi in forest soils: role in carbon cycling. Plant and Soil 2013, 366:1-27.
21. Elliott E.T., Anderson R.V., Coleman D.C., Cole C.V. Habitable pore space and microbial trophic interactions. Oikos 1980, 35:327-335.
22. Fabian M. The effects of different methods of preservation on the 15N concentration in Folsomia candida (Collembola). Applied Soil Ecology 1998, 9:101-104.
23. Ferris H., Bongers T., De Goede R.G.M. Aframework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 2001, 18:13-29.
24. Ferris H. Contribution of nematodes to the structure and function of the soil food web. Journal of Nematology 2010, 42:63-67.
25. Fischer B.M., Schatz H., Maraun M. Community structure, trophic position and reproductive mode of soil and bark-living oribatid mites in an alpine grassland ecosystem. Experimental and Applied Acarology 2010, 52:221-237.
26. Freckman D.W. Bacterivorous nematodes and organic-matter decomposition. Agriculture, Ecosystems and Environment 1988, 24:195-217.
27. Freckman D.W., Ettema C.H. Assessing nematode communities in agroecosystems of varying human intervention. Agriculture, Ecosystems and Environment 1993, 45:239-261.
28. Godbold D.L., Hoosbeek M.R., Lukac M., Cotrufo M.F., Janssens I.A., Ceulemans R., Polle A., Velthorst E.J., Scarascia-Mugnozza G., De Angelis P., Miglietta F., Peressotti A. Mycorrhizal hyphal turnover as a dominant process for carbon input into soil organic matter. Plant Soil 2006, 281:15-24.
29. Griffiths B.S. Acomparison of microbial-feeding nematodes and protozoa in the rhizosphere of different plants. Biology and Fertility of Soils 1990, 9:83-88.
30. Gupta M.C., Singh R.S., Sitaramaiah K. Anew endoparasitic fungus on Xiphinema and cultivation of Rhabditis spp. and Aphelenchus avenae on same fungus. Nematologica 1979, 25:142-145.
31. Hagar J.C. Wildlife species associated with non-coniferous vegetation in Pacific Northwest conifer forests: a review. Forest Ecology and Management 2007, 246:108-122.
32. Hammer O., Harper D.A.T., Ryan P.D. PAST: Paleontological Statistics software package for education and data analysis. Palaeontologia Electronica 2001, 4:1-9.
33. Hanel L. Soil nematodes in five spruce forests of the Beskydy mountains, Czech Republic. Fundamental and Applied Nematology 1996, 19:15-24.
34. Hanel L. Distribution of nematodes in soil, mycorrhizal soil, mycorrhizae and roots of spruce forests at the Boubin Mount, Czech Republic. Biologia 1998, 53:593-603.
35. Hanel L. An outline of soil nematode succession on abandoned fields in South Bohemia. Applied Soil Ecology 2010, 46:355-371.
36. Heidemann K., Hennies A., Schakowske J., Blumenberg L., Ruess L., Scheu S., Maraun M. Free-living nematodes as prey for higher trophic levels of forest soil food web. Oikos 2014, 123:1199-1211.
37. Heidemann K., Ruess L., Scheu S., Maraun M. Nematode consumption by mite communities varies in different forest microhabitats as indicated by molecular gut content analysis. Experimental and Applied Acarology 2014, 64:49-60.
38. Heidemann K., Scheu S., Ruess L., Maraun M. Molecular detection of nematode predation and scavenging in oribatid mites: laboratory and field experiments. Soil Biology and Biochemistry 2011, 43:2229-2236.
39. Henn M.R., Chapela I.H. Ecophysiology of 13C and 15N isotopic fractionation in forest fungi and the roots of the saprotrophic-mycorrhizal divide. Oecologia 2001, 128:480-487.
40. Hobbie E.A., Macko S.A., Shugart H.H. Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 1999, 118:353-360.
41. Hobbie E.A., Ouimette A.P. Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 2009, 95:355-371.
42. Hobbie E.A., Sanchez F.S., Rygiewicz P.T. Controls of isotopic patterns in saprotrophic and ectomycorrhizal fungi. Soil Biology and Biochemistry 2012, 48:60-68.
43. Högberg P., Plamboeck A.H., Taylor A.F.S., Fransson P.M.A. Natural 13C abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests. Proceedings of the National Academy of Sciences of the USA 1999, 96:8534-8539.
44. Hunt H.W., Coleman D.C., Ingham E.R., Ingham R.E., Elliott E.T., Moore J.C., Rose S.L., Reid C.P.P., Morley C.R. The detrital food web in a shortgrass prairie. Biology and Fertility of Soils 1987, 3:57-68.
45. Huygens D., Denef K., Vandeweyer R., Godoy R., Van Cleemput O., Boeckx P. Do nitrogen isotope patterns reflect microbial colonization of soil organic matter fractions?. Biology and Fertility of Soils 2008, 44:955-964.
46. Jairajpuri M.S., Ahmad W. Dorylaimida. Free-living, Predaceous and Plant Parasitic Nematodes 1992, E.J. Brill, Leiden, 458 pp.
47. Klarner B., Ehnes R.B., Erdmann G., Eitzinger B., Pollierer M.M., Maraun M., Scheu S. Trophic shift of soil animal species with forest type as indicated by stable isotope analysis. Oikos 2014, 123:1173-1181.
48. Klarner B., Maraun M., Scheu S. Trophic diversity and niche partitioning in a species rich predator guild - natural variations in stable isotope ratios (13C/12C, 15N/14N) of mesostigmatid mites (Acari, Mesostigmata) from Central European beech forests. Soil Biology and Biochemistry 2013, 57:327-333.
49. Kohzu A., Yoshioka T., Ando T., Takahashi M., Koba K., Wada E. Natural 13C and 15N abundance of field-collected fungi and their ecological implications. New Phytologist 1999, 144:323-330.
50. Korobushkin D.I., Gongalsky K.B., Tiunov A.V. Isotopic niche (δ13s{cyrillic} and δ15N values) of soil macrofauna in temperate forests. Rapid Communication Mass Spectrometry 2014, 28:1303-1311.
51. Krab E.J., van Logtestijn R.S.P., Cornelissen J.H.C., Berg M.P. Reservations about preservations: storage methods affect δ13s{cyrillic} signatures differently even in closely related soil fauna. Methods in Ecology and Evolution 2012, 3:138-144.
52. Lee Q., Widden P. Folsomia candida, a fungivorous collembolan, feeds preferentially on nematodes rather than soil fungi. Soil Biology & Biochemistry 1996, 28:689-690.
53. Maraun M., Erdmann G., Fischer B.M., Pollierer M.M., Norton R.A., Schneider K., Scheu S. Stable isotopes revisited: their use and limits for oribatid mite trophic ecology. Soil Biology & Biochemistry 2011, 43:877-882.
54. Mayor J.R., Schuur E.A.G., Henkel T.W. Elucidating the nutritional dynamics of fungi using stable isotopes. Ecology Letters 2009, 12:171-183.
55. McCutchan J.H., Lewis W.M., Kendall C., McGrath C.C. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 2003, 102:378-390.
56. Moore J.C., McCann K., De Ruiter P.C. Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 2005, 49:499-510.
57. Mulder C., Vonk J.A. Nematode traits and environmental constraints in 200 soil systems: scaling within the 60-6000 mm body size range. Ecology 2011, 92:2004. 2004.
58. Newsham K.K., Rolf J., Pearce D.A., Strachan R.J. Differing preferences of Antarctic soil nematodes for microbial prey. European Journal of Soil Biology 2004, 40:1-8.
59. Newsome S.D., Martinez del Rio C., Bearhop S., Phillips D.L. Aniche for isotopic ecology. Frontiers in Ecology and the Environment 2007, 5:429-436.
60. Nilsson M., Wardle D.A. Understory vegetation as a forest ecosystem driver: evidence from the northern Swedish boreal forest. Frontiers in Ecology and the Environment 2005, 8:421-428.
61. Oelbermann K., Scheu S. Trophic guilds of generalist feeders in soil animal communities as indicated by stable isotope analysis (15N/14N). Bulletin of Entomological Research 2010, 100:511-520.
62. Okada H., Harada H. Effects of tillage and fertilizer on nematode communities in a Japanese soybean field. Applied Soil Ecology 2007, 35:582-598.
63. Okada H., Harada H., Kadota I. Fungal-feeding habits of six nematode isolates in the genus Filenchus. Soil Biology and Biochemistry 2005, 37:1113-1120.
64. Okada H., Kadota I. Host status of 10 fungal isolates for two nematode species, Filenchus misellus and Aphelenchus avenae. Soil Biology and Biochemistry 2003, 35:1601-1607.
65. Okada H., Tsukiboshi T., Kadota I. Mycetophagy in Filenchus misellus (Andrassy, 1958) Lownsbery & Lownsbery, 1985 (Nematoda: Tylenchidae), with notes on its morphology. Nematology 2002, 4:795-801.
66. Pollierer M.M., Langel R., Korner C., Maraun M., Scheu S. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecology Letters 2007, 10:729-736.
67. Pollierer M.M., Langel R., Scheu S., Maraun M. Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotope ratios (15N/14N and 13C/12C). Soil Biology & Biochemistry 2009, 41:1221-1226.
68. Pollierer M.M., Dyckmans J., Scheu S., Haubert D. Carbon flux through fungi and bacteria into the forest soil animal food web as indicated by compound-specific 13C fatty acid analysis. Functional Ecology 2012, 26:978-990.
69. Post D.M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 2002, 83:703-718.
70. Potapov A.M., Semenina E.E., Kurakov A.V., Tiunov A.V. Large 13C/12C and small 15N/14N isotope fractionation in an experimental detrital foodweb (litter-fungi-collembolans). Ecological Research 2013, 28:1069-1079.
71. Potapov A.M., Semenyuk I.I., Tiunov A.V. Seasonal and age-related changes in the stable isotope composition (15N/14N and 13C/12C) of millipedes and collembolans in a temperate forest soil. Pedobiologia 2014, 57:215-222.
72. Remen C., Fransson P., Persson T. Population responses of oribatids and enchytraeids to ectomycorrhizal and saprotrophic fungi in plant-soil microcosms. Soil Biology and Biochemistry 2010, 42:978-985.
73. Rohlfs M., Churchill A.C.L. Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genetics and Biology 2011, 48:23-34.
74. Rønn R., Vestergård M., Ekelund F. Interactions between bacteria, Protozoa and nematodes in soil. Acta Protozoologica 2012, 51:223-235.
75. Ruess L., Dighton J. Cultural studies on soil nematodes and their fungal hosts. Nematologica 1996, 42:330-346.
76. Ruess L., Tiunov A.V., Haubert D., Richnow H.H., Haggblom M.M., Scheu S. Carbon stable isotope fractionation and trophic transfer of fatty acids in fungal based soil food chains. Soil Biology & Biochemistry 2005, 37:945-953.
77. Sampedro L., Dominguez J. Stable isotope natural abundances (δ13C and δ15N) of the earthworm Eisenia fetida and other soil fauna living in two different vermicomposting environments. Applied Soil Ecology 2008, 38:91-99.
78. Saur E., Arpin P. Ultrastructural analysis of the intestinal contents of Clarkus pupillatus (Nemata: Mononchina): ecological interest of the survey. Revue Nématology 1989, 12:413-422.
79. Scheu S., Falca M. 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 2000, 123:285-296.
80. Scheu S., Ruess L., Bonkowski M. Interactions between Microorganisms and Soil Micro- and Mesofauna. Microorganisms in Soils: Roles in Genesis and Functions 2005, 253-275. Springer, Berlin. F. Buscot, A. Varma (Eds.).
81. Schneider K., Migge S., Norton R.A., Scheu S., Langel R., Reineking A., Maraun M. Trophic niche differentiation in soil microarthropods (Oribatida, Acari): evidence from stable isotope ratios (15N/14N. Soil Biology and Biochemistry 2004, 36:1769-1774.
82. Sohlenius B. Influence of clear-cutting and forest age on the nematode fauna in a Swedish pine forest soil. Applied Soil Ecology 2002, 19:261-277.
83. Sticht C., Schrader S., Giesemann A. Influence of chemical agents commonly used for soil fauna investigations on the stable C-isotopic signature of soil animals. European Journal of Soil Biology 2006, 42:S326-S330.
84. Sticht C., Schradera S., Giesemannb A., Weigela H. Sensitivity of nematode feeding types in arable soil to free air CO2 enrichment (FACE) is crop specific. Pedobiologia 2009, 52:337-349.
85. Tiunov A.V., Bonkowski M., Alphei J., Scheu S. Microflora, Protozoa and Nematoda in Lumbricus terrestris burrow walls: a laboratory experiment. Pedobiologia 2001, 45:46-60.
86. Tiunov A.V. Stable isotopes of carbon and nitrogen in soil ecological studies. Biology Bulletin 2007, 34:395-407.
87. Wallander H., Goransson H., Rosengren U. Production, standing biomass and natural abundance of 15N and 13C in ectomycorrhizal mycelia collected at different soil depths in two forest types. Oecologia 2004, 139:89-97.
88. Wardle D.A., Yeates G.W. The dual importance of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food-webs. Oecologia 1993, 93:303-306.
89. Wardle D.A., Nilsson M.C., Zackisson O. An ecosystem-level perspective of allelopathy. Biological Review 1998, 73:305-319.
90. Wynn J.G. Carbon isotope fractionation during decomposition of organic matter in soils and paleosols: implications for paleoecological interpretations of paleosols. Palaeogeography Palaeoclimatology Palaeoecology 2007, 251:437-448.
91. Yeates G.W., Bongers T., de Goede R.G., Freckman D.W., Georgieva S.S. Feeding habits in soil nematode families and genera - an outline for soil ecologists. Journal of Nematology 1993, 25:315-331.
92. Yeates G.W., Ferris H., Moens T., Van der Putten W.H. The role of nematodes in ecosystems. Nematodes as Environmental Indicators. CABI 2009, 1-45. Wallingford, UK. M.J. Wilson, T. Kakouli-Duarte (Eds.).
93. Zhao J., Neher D.A. Soil energy pathways of different ecosystems using nematode trophic group analysis: a meta analysis. Nematology 2013, 16:379-385.