Free-living nematodes as prey for higher trophic levels of forest soil food webs

Oikos

Volumn 123, Issue 10, 2014, Pages 1199-1211

  Heidemann, Kerstin ^a   Hennies, Annika ^a   Schakowske, Johanna ^a   Blumenberg, Lars ^a   Ruess, Liliane ^b   Scheu, Stefan ^a   Maraun, Mark ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACARI; ACROBELOIDES BUETSCHLII; BACTERIA (MICROORGANISMS); COLLEMBOLA; GAMASINA; INVERTEBRATA; NEMATODA; ORIBATIDA; PANAGRELLUS REDIVIVUS; PLECTUS MINIMUS; PLECTUS PARIETINUS; UROPODINA;

EID: 84927784255     PISSN: 00301299     EISSN: 16000706     Source Type: Journal    
DOI: 10.1111/j.1600-0706.2013.00872.x     Document Type: Article

References (97)

1. Agustí N. et al. 2003. Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers. - Mol. Ecol. 12: 3467-3475.
2. Alphei J. 1995. Die freilebenden Nematoden von Buchenwäldern mit unterschiedlicher Humusform: Struktur der Gemeinschaften und Funktion in der Rhizosphäre der Krautvegetation. - Berichte des Forschungszentrum Waldökosysteme (Göttingen), A 125: 45-48.
3. Anderson J. M. 1975. The enigma of soil animal species diversity. - In: Vanek J.(ed.), Progress in soil ecology. Proc. 5th Int. Colloq. of Soil Zoology, 1973. Academica, Prague, pp. 51-58.
4. Bardgett R. D. and Wardle D. A. 2010. Above-belowground linkages: biotic interactions, ecosystem processes, and global change (Oxford Ser. Ecol. Evol.). - Oxford Univ. Press.
5. Behan-Pelletier V. M. 1999. Oribatid mite biodiversity in agroecosystems: role for bioindication. - Agricult. Ecosyst. Environ. 74: 411-423.
6. Chahartaghi M. et al. 2005. Feeding guilds in Collembola based on nitrogen stable isotope ratios. - Soil Biol. Biochem. 37: 1718-1725.
7. Chamberlain P. M. et al. 2006a. The effect of diet on isotopic turnover in Collembola examined using the stable carbon isotopic compositions of lipids. - Soil Biol. Biochem. 38: 1146-1157.
8. Chamberlain P. M. et al. 2006b. Collembolan trophic preferences determined using fatty acid distributions and compound-specific stable carbon isotope values. - Soil Biol. Biochem. 38: 1257-1281.
9. Chen B. et al. 1995. Food preference and effects of food type on the life history of some soil Collembola. - Pedobiologia 39: 496-505.
10. 15N through soil fauna feeding channels. - Rapid Commun. Mass Spectrom. 25: 1503-1513.
11. Digel C. et al. 2014. Unraveling the complex structure of forest soil food webs: high omnivory and more trophic levels. - Oikos 123: 1157-1172.
12. Domes K. et al. 2007. The phylogenetic relationship between Astigmata and Oribatida (Acari) as indicated by molecular markers. - Exp. Appl. Acarol. 42: 159-171.
13. Eitzinger B. and Traugott M. 2011. Which prey sustains cold-adapted invertebrate generalist predators in arable land? Examining prey choices by molecular gut-content analysis. - J. Appl. Ecol. 48: 591-599.
14. Eitzinger B. et al. 2013. Unveiling soil food web links: new PCR assays for detection of prey DNA in the gut of soil arthropod predators. - Soil Biol. Biochem. 57: 943-945.
15. Erdmann G. et al. 2012. Regional factors rather than forest type drive the community structure of soil living oribatid mites (Acari, Oribatida). - Exp. Appl. Acarol. 57: 157-169.
16. Ferlian O. and Scheu S. 2014. Shifts in trophic interactions with forest type in soil generalist predators as indicated by complementary analyses of fatty acids and stable isotopes. - Oikos 123: 1182-1191.
17. Ferlian O. et al. 2012. Trophic interactions in centipedes (Chilopoda, Myriapoda) as indicated by fatty acid patterns: variations with life stage, forest age and season. - Soil Biol. Biochem. 52: 33-42.
18. Ferris H. 2010. Contribution of nematodes to the structure and function of the soil food web. - J. Nematol. 42: 63-67.
19. Floyd R. et al. 2002. Molecular barcodes for soil nematode identification. - Mol. Ecol. 11: 839-850.
20. Folmer O. et al. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. - Mol. Mar. Biol. Biotechnol. 3: 294-299.
21. Freckman D. W. 1988. Bacterivorous nematodes and organic-matter decomposition. - Agricult. Ecosyst. Environ. 24: 195-217.
22. Gagnon A.-È. et al. 2011. Prey DNA detection success following digestion by intraguild predators: influence of prey and predator species. - Mol. Ecol. Res. 11: 1022-1032.
23. Goodey J. B. 1963. Laboratory methods for work with plant and soil nematodes. - Tech. Bull. Ministry Agric. Fish. Food 2: 1-72.
24. Greenstone M. H. et al. 2007. Feeding mode and prey detectability half-lives in molecular gut-content analysis: an example with two predators of the Colorado potato beetle. - Bull. Entomol. Res. 97: 201-209.
25. Greenstone M. H. et al. 2010. Choosing natural enemies for conservation biological control: use of the prey detectability half-life to rank key predators of Colorado potato beetle. - Entomol. Exp. Appl. 136: 97-107.
26. Griffiths B. S. 1990. A comparison of microbial-feeding nematodes and protozoa in the rhizosphere of different plants. - Biol. Fertil. Soils 9: 83-88.
27. Günther B. et al. 2014. Variations in prey consumption of centipede predators in forest soils as indicated by molecular gut content analysis. - Oikos 123: 1192-1198.
28. Hall T. A. 1999. BioEdit: a user friendly biological sequence alignment editor and analysis program for Win 95/98/NT. - Nucleic Acids Symp. Ser. 41: 95-98.
29. Harwood J. D. et al. 2004. Prey selection by linyphiid spiders: molecular tracking of the effects of alternative prey on rates of aphid consumption in the field. - Mol. Ecol. 13: 3549-3560.
30. Heidemann K. et al. 2011. Molecular detection of nematode predation and scavenging in oribatid mites: laboratory and field experiments. - Soil Biol. Biochem. 43: 2229-2236.
31. Holterman M. et al. 2006. Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. - Mol. Biol. Evol. 23: 1792-1800.
32. Holovachov O. 2006. Morphology and systematics of the order Plectida Malakhov, 1982 (Nematoda). - Ponsen and Looijen BV, Wageningen.
33. Hoogendoorn M. and Heimpel G. E. 2001. PCR-based gut content analysis of insect predators: using ribosomal ITS-1 fragments from prey to estimate predation frequency. - Mol. Ecol. 10: 2059-2067.
34. Hosmer D. W. and Lemeshow S. 1989. Applied logistic regression. - Wiley.
35. Hosseini R. et al. 2008. Factors affecting detectability of prey DNA in the gut contents of invertebrate predators: a polymerase chain reaction-based method. - Entomol. Exp. Appl. 126: 194-202.
36. Jarman S. N. et al. 2004. Group-specific polymerase chain reaction for DNA-based analysis of species diversity and identity in dietary samples. - Mol. Ecol. 13: 1313-1322.
37. Karg W. 1993. Acari (Acarina), Milben. Unterordnung Parasitiformes (Anactinochaeta). Cohors Gamasina Leach. Raubmilben. Die Tierwelt Deutschlands 59. Teil; 2. überarbeitete Auflage. - Gustav Fischer, Jena.
38. Kempson D. et al. 1963. A new extractor for woodland litter. - Pedobiologia 3: 1-21.
39. King R. A. et al. 2008. Molecular analysis of predation: a review of best practice for DNA-based approaches. - Mol. Ecol. 17: 947-963.
40. 14N) of mesostigmatid mites (Acari, Mesostigmata) from central European beech forest. - Soil Biol. Biochem. 57: 323-333.
41. Klarner B. et al. 2014. Trophic shift of soil animal species with forest type as indicated by stable isotope analysis. - Oikos 123: 1173-1181.
42. Koehler H. H. 1999. Predatory mites (Gamasina, Mesostigmata). - Agricult. Ecosyst. Environ. 74: 395-410.
43. Kramer S. et al. 2012. Carbon flow into microbial and fungal biomass as a basis for the belowground food web of agroecosystems. - Pedobiologica 55: 111-119.
44. Kuusk A. K. and Agustí N. 2008. Group-specific primers for DNA-based detection of springtails (Hexapoda: Collembola) within predator gut contents. - Mol. Ecol. Res. 8: 678-681.
45. Lee Q. and Widden P. 1996. Folsomia candida, a fungivorous collembolan, feeds preferentially on nematodes rather than soil fungi. - Soil Biol. Biochem. 28: 689-690.
46. Maraun M. and Scheu S. 2000. The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. - Ecography 23: 374-382.
47. Maraun M. et al. 1998. Selection of microfungal food by six oribatid mite species (Oribatida, Acari) from two different beech forests. - Pedobiologia 42: 232-240.
48. Maraun M. et al. 2003a. Adding to "the enigma of soil animal diversity": fungal feeders and saprophagous soil invertebrates prefer similar food substrates. - Eur. J. Soil Biol. 39: 85-95.
49. Maraun M. et al. 2003b. Radiation in sexual and parthenogenetic oribatid mites (Oribatida, Acari) as indicated by genetic divergence of closely related species. - Exp. Appl. Acarol. 29: 265-277.
50. Moore J. C. and Hunt H. W. 1988. Resource compartmen tation and the stability of real ecosystems. - Nature 333: 261-263.
51. Moore J. C. et al. 2003. Top-down is bottom-up: does predation in the rhizosphere regulate aboveground dynamics?- Ecology 84: 846-857.
52. Mulder C. and Vonk J. A. 2011. Nematode traits and environmental constraints in 200 soil systems: scaling within the 60-6000 μm body size range. - Ecology 92: 2004.
53. Muraoka M. and Ishibashi N. 1976. Nematode-feeding mites and their feeding behaviour. - Appl. Entomol. Zool. 11: 1-7.
54. Oliveira A. R. et al. 2007. Consumption rate of phytonematodes by Pergalumna sp. (Acari: Oribatida: Galumnidae) under laboratory conditions determined by a new method. - Exp. Appl. Acarol. 41: 183-189.
55. Peschel K. et al. 2006. Do oribatid mites live in enemy-free space? Evidence from feeding experiments with the predatory mite Pergamasus septentrionalis. - Soil Biol. Biochem. 38: 2985-2989.
56. Petersen H. and Luxton M. 1982. A comparative analysis of soil fauna populations and their role in decomposition processes. - Oikos 39: 288-309.
57. Pimm S. L. et al. 1991. Food web patterns and their consequences. - Nature 350: 669-674.
58. Pompanon F. et al. 2011. Who is eating what: diet assessment using next generation sequencing. - Mol. Ecol. 21: 1931-1950.
59. 13C fatty acid analysis. - Funct. Ecol. 26: 978-990.
60. Read D. S. et al. 2006. Molecular detection of predation by soil micro-arthropods on nematodes. - Mol. Ecol. 15: 1963-1972.
61. Rockett C. L. 1980. Nematode predation by oribatid mites (Acari: Oribatida). - Int. J. Acarol. 6: 219-224.
62. Rockett C. L. and Woodring J. P. 1966. Oribatid mites as predators of soil nematodes. - Ann. Entomol. Soc. Am. 59: 669-671.
63. Ruess L. 1995. Studies on the nematode fauna of an acid forest soil: spatial distribution and extraction. - Nematologica 41: 229-239.
64. Ruess L. et al. 2004. Nitrogen isotope ratios and fatty acid composition as indicators of animal diets in belowground systems. - Oecologia 139: 336-346.
65. Ruess L. et al. 2005. Application of lipid analysis to understand trophic interactions in soil. - Ecology 86: 2075-2082.
66. Rusek J. 1998. Biodiversity of Collembola and their functional role in the ecosystem. - Biodivers. Conserv. 7: 1207-1219.
67. Schaefer M. 1990. The soil fauna of a beech forest on limestone: trophic structure and energy budget. - Oecologia 82: 128-136.
68. Schatz H. 2002. Die Oribatidenliteratur und die beschriebenen Oribatidenarten (1758-2001) - Eine Analyse. - Abhandlungen und Berichte des Naturkunde Museums Görlitz 74: 37-45.
69. Scheu S. and Falca M. 2000. 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: 285-286.
70. Scheu S. and Setälä H. 2002. Multitrophic interactions in decomposer food webs. - In: Tscharntke T and Hawkins B. A.(eds), Multitrophic level interactions. Cambridge Univ. Press, pp. 223-264.
71. Scheu S. et al. 2005. Interactions between microorganisms and soil micro-and mesofauna. - In: Buscot F. and Varma A.(eds), Soil biology, vol. 3 - Microorganisms in soils: roles in genesis and functions. Springer, pp. 253-275.
72. 14N). - Soil Biol. Biochem. 36: 1769-1774.
73. Sheppard S. K. and Harwood J. D. 2005. Advances in molecular ecology: tracking trophic links through predator-prey food-webs. - Funct. Ecol. 19: 751-762.
74. Sheppard S. K. et al. 2004. Infiltration by alien predators into invertebrate food webs in Hawaii: a molecular approach. - Mol. Ecol. 13: 2077-2088.
75. Sheppard S. K. et al. 2005. Detection of secondary predation by PCR analyses of the gut contents of invertebrate generalist predators. - Mol. Ecol. 14: 4461-4468.
76. Siepel H. 1990. Niche relationships between two panphyto phagous soil mites, Nothrus silvestris Nicolet (Acari, Oribatida, Nothridae) and Platynothrus peltifer (Koch) (Acari, Oribatida, Camisiidae). - Biol. Fertil. Soils 9: 139-144.
77. Sint D. et al. 2011. Optimizing methods for PCR-based analysis of predation. - Mol. Ecol. Res. 11: 795-801.
78. Sokal R. R. and Rohlf F. J. 1995. Biometry. - W. H. Freeman.
79. Strickland M. S. et al. 2012. The fate of glucose, a low molecular weight compound of root exudates, in the belowground foodweb of forests and pastures. - Soil Biol. Biochem. 49: 23-29.
80. Steinaker D. F. and Wilson S. D. 2008. Scale and density dependent relationships among roots, mycorrhizal fungi and collembola in grassland and forest. - Oikos 117: 703-710.
81. Sturhan D. and Hampel G. 1977. Pflanzenparasitische Nematoden als Beute der Wurzelmilbe Rhizoglyphus echinopus (Acarina, Tyroglyphidae). - Anz. Schädlingskde., Pflanzenschutz, Umweltschutz 50: 115-118.
82. Sunderland K. D. 1988. Quantitative methods for detecting invertebrate predation occurring in the field. - Ann. Appl. Biol. 112: 201-224.
83. Symondson W. O. C. 2002. Molecular identification of prey in predator diets. - Mol. Ecol. 11: 627-641.
84. Terborgh J. and Estes J. A. 2010. Trophic cascades and the changing dynamics of nature. - Island Press.
85. Traugott M. and Symondson W. O. C. 2008. Molecular analysis of predation on parasitized hosts. - Bull. Entomol. Res. 98: 223-231.
86. van Hees P. A. W. et al. 2005. The carbon we do not see - the impact of low molecular weight compounds on carbon dynamics and respiration in forest soils: a review. - Soil Biol. Biochem. 37: 1-13.
87. Visser S. et al. 1987. Fungi associated with Onychiurus subtenuis (Collembola) in an aspen woodland. - Can. J. Bot. 65: 635-642.
88. von Berg K. et al. 2008a. The effects of temperature on detection of prey DNA in two species of carabid beetle. - Bull. Entomol. Res. 98: 263-269.
89. von Berg K. et al. 2008b. Impact of abiotic factors on predator- prey interactions: DNA-based gut content analysis in a microcosm experiment. - Bull. Entomol. Res. 98: 257-261.
90. Walter D. E. 1988a. Predation and mycophagy by endostigmatid mites (Acariformes: Prostigmata). - Exp. Appl. Acarol. 4: 159-166.
91. Walter D. E. 1988b. Nematophagy by soil arthropods from the Shortgrass Steppe, Chihuahuan Desert and Rocky Mountains of the Central United States. - Agricult. Ecosyst. Environ. 24: 307-316.
92. Wardle D. A. and Yeates G. W. 1993. The dual system of competition and predation as regulatory forces in terrestrial ecosystems: evidence from decomposer food-webs. - Oecologia 93: 303-306.
93. Yeates G. W. 2010. Nematodes in ecological webs. - In: Encyclopedia of life sciences. Wiley, pp. 1-11.
94. Yeates G. W. et al. 1993. Feeding-habits in soil nematode families and genera - an outline for soil ecologists. - J. Nematol. 25: 315-331.
95. Yeates G. W. et al. 2000. Changes in soil fauna and soil conditions under Pinus radiata agroforestry regimes during a 25-year tree rotation. - Biol. Fertil. Soils 31: 391-406.
96. Zaidi R. H. et al. 1999. Can multiple-copy sequences of prey DNA be detected amongst the gut contents of invertebrate predators?- Mol. Ecol. 8: 2081-2087.
97. Zunke U. and Perry R. N. 1997. Nematodes: harmful and beneficial organisms. - In: Benckiser G.(ed.), Fauna in soil ecosystems. Marcel Dekker, pp. 85-133.