Advertisement

Paddy and Water Environment

, Volume 16, Issue 2, pp 279–286 | Cite as

Effects of detritivorous invertebrates on the decomposition of rice straw: evidence from a microcosm experiment

  • Jörn Panteleit
  • Finbarr G. Horgan
  • Manfred Türke
  • Anja Schmidt
  • Martin Schädler
  • Michael Bacht
  • Roland Brandl
  • Stefan Hotes
Article

Abstract

Decomposition of crop residues is a key process in agricultural systems that influences nutrient cycling and productivity. To clarify the roles of different groups of invertebrates in decomposition in paddy fields, we conducted a microcosm experiment, testing the effects of soil eluate filtered through a 21 μm mesh (control treatment) against the effects of microfauna (< 0.1 mm) and small gastropods (juvenile golden apple snails (Pomacea canaliculata), ca. 2 mm shell diameter), both separately and in combination, on rice straw decomposition. Rice straw in litterbags was incubated at the soil surface and in the soil together with standardized amounts of the respective detritivores for 10 and 21 days. Compared to the control treatment, snails and microfauna enhanced the reduction in straw mass on the soil surface by 19 and 22%, respectively. Both groups combined increased the reduction in straw biomass by 30%. Below the soil surface, the contribution of detritivores to decomposition was smaller, reducing straw biomass by just 1% (snails), 11% (microfauna) and 14% (snails + microfauna) compared to the control. The effects of microfauna and snails on decomposition were not fully additive, a pattern that could be due to competition or trophic interactions. Model selection using Akaike’s information criterion on nested linear mixed effects models led to a model including the main effects (snails, microfauna, position and time), several two-way interactions and the three-way interaction snails * microfauna * litterbag_position as the most parsimonious description of the data. Keeping straw accessible to aquatic invertebrate detritivores should be a suitable management strategy to enhance decomposition in paddy fields, although trade-offs with other management issues such as pest control need to be considered.

Keywords

Microfauna Ecosystem function Golden apple snail Pomacea canaliculata Oryza sativa 

Notes

Acknowledgements

We would like to thank the staff at the Crop and Environmental Science Department of the International Rice Research Institute for their hospitality during the microcosm experiment. We are grateful to Sylvia (Bong) Villareal, Liberty Almazan, Carmencita Bernal, Arriza Arida and Alberto Naredo for their support. This study was funded in part through the project ‘Land-use intensity and Ecological Engineering—Assessment Tools for risks and Opportunities in irrigated rice based production systems’ (LEGATO), German Federal Ministry for Education and Research (BMBF), Grant No. 01LL09 17L.

References

  1. Astor T, Lenoir L, Berg MP (2015) Measuring feeding traits of a range of litter-consuming terrestrial snails: leaf litter consumption, faeces production and scaling with body size. Oecologia 178:833–845CrossRefPubMedGoogle Scholar
  2. Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511CrossRefPubMedGoogle Scholar
  3. Bartoń K (2015) Multi-model inference. R package version 1.15.6. https://CRAN.R-project.org/package=MuMIn. Accessed 9 April 2017
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Beare MH, Reddy MV, Tian G, Srivastava SC (1997) Agricultural intensification, soil biodiversity and agroecosystem function in the tropics: the role of decomposer biota. Appl Soil Ecol 6:87–108CrossRefGoogle Scholar
  6. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer, New YorkGoogle Scholar
  7. Cazzaniga NJ (1990) Predation of Pomacea canaliculata (Ampullaridae) on adult Biomphalaria peregrina (Planorbidae). Ann Trop Med Parasitol 84:97–100CrossRefPubMedGoogle Scholar
  8. de Vries FT, Thebault E, Liiri M, Birkhofer K, Tsiafouli MA, Bjornlund L, Jorgensen HB, Brady MV, Christensen S, de Ruiter PC, d’Hertefeldt T, Frouz J, Hedlund K, Hemerik L, Hol WHG, Hotes S, Mortimer SR, Setala H, Sgardelis SP, Uteseny K, van der Putten WH, Wolters V, Bardgett RD (2013) Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci USA 110:14296–14301CrossRefPubMedGoogle Scholar
  9. Dobermann A, Fairhurst TH (2002) Rice straw management. Better Crops Int 16:7–11Google Scholar
  10. Freckman DW (1988) Bacterivorous nematodes and organic-matter decomposition. Agr Ecosyst Environ 24:195–217CrossRefGoogle Scholar
  11. Fujino C, Wada S, Konoike T, Toyota K, Suga Y, Ikeda J (2008) Effect of different organic amendments on the resistance and resilience of the organic matter decomposing ability of soil and the role of aggregated soil structure. Soil Sci Plant Nutr 54:534–542CrossRefGoogle Scholar
  12. García-Palacios P, Maestre FT, Kattge J, Wall DH (2013) Climate and litter quality differently modulate the effects of soil fauna on litter decomposition across biomes. Ecol Lett 16:1045–1053CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gelman A, Su Y-S (2016) Arm: data analysis using regression and multilevel/hierarchical models. R package version 1.9-3. https://CRAN.R-project.org/package=arm. Accessed 9 April 2017
  14. Gessner MO, Chauvet E, Dobson M (1999) A perspective on leaf litter breakdown in streams. Oikos 85:377–384CrossRefGoogle Scholar
  15. Gessner MO, Swan CM, Dang CK, McKie BG, Bardgett RD, Wall DH, Haettenschwiler S (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380CrossRefPubMedGoogle Scholar
  16. Gregorich EG, Janzen H, Ellert BH, Helgason BL, Qian BD, Zebarth BJ, Angers DA, Beyaert RP, Drury CF, Duguid SD, May WE, McConkey BG, Dyck MF (2017) Litter decay controlled by temperature, not soil properties, affecting future soil carbon. Glob Change Biol 23:1725–1734CrossRefGoogle Scholar
  17. Hattenschwiler S, Tiunov AV, Scheu S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218CrossRefGoogle Scholar
  18. Horgan FG (2017) Ecology and management of apple snails in rice. In: Chauhan B, Jabran K, Mahajan G (eds) Rice production worldwide. Springer, New York, pp 393–417CrossRefGoogle Scholar
  19. Horgan FG, Stuart AM, Kudavidanage EP (2014) Impact of invasive apple snails on the functioning and services of natural and managed wetlands. Acta Oecol Int J Ecol 54:90–100CrossRefGoogle Scholar
  20. Huang L-M, Thompson A, Zhang G-L, Chen L-M, Han G-Z, Gong Z-T (2015) The use of chronosequences in studies of paddy soil evolution: a review. Geoderma 237:199–210CrossRefGoogle Scholar
  21. Hunting ER, Vonk JA, Musters CJM, Kraak MHS, Vijver MG (2016) Effects of agricultural practices on organic matter degradation in ditches. Sci Rep 6:21474CrossRefPubMedPubMedCentralGoogle Scholar
  22. Jenkins BM, Bakker RR, Wei JB (1996) On the properties of washed straw. Biomass Bioenergy 10:177–200CrossRefGoogle Scholar
  23. Kampichler C, Bruckner A (2009) The role of microarthropods in terrestrial decomposition: a meta-analysis of 40 years of litterbag studies. Biol Rev Camb Philos Soc 84:375–389CrossRefPubMedGoogle Scholar
  24. Kataki S, Hazarika S, Baruah DC (2017) Assessment of by-products of bioenergy systems (anaerobic digestion and gasification) as potential crop nutrient. Waste Manag 59:102–117CrossRefPubMedGoogle Scholar
  25. Katayama N, Baba YG, Kusumoto Y, Tanaka K (2015) A review of post-war changes in rice farming and biodiversity in Japan. Agric Syst 132:73–84CrossRefGoogle Scholar
  26. Kaur D, Bhardwaj NK, Lohchab RK (2017) Prospects of rice straw as a raw material for paper making. Waste Manag 60:127–139CrossRefPubMedGoogle Scholar
  27. Koegel-Knabner I, Amelung W, Cao Z, Fiedler S, Frenzel P, Jahn R, Kalbitz K, Koelbl A, Schloter M (2010) Biogeochemistry of paddy soils. Geoderma 157:1–14CrossRefGoogle Scholar
  28. Kuznetsova A, Brockhoff PB, Christensen RHB (2016) lmerTest: tests in linear mixed effects models. R package version 2.0-33. https://CRAN.R-project.org/package=lmerTest. Accessed 9 April 2017
  29. Kwong KL, Chan RKY, Qiu JW (2009) The potential of the invasive snail Pomacea canaliculata as a predator of various life stages of five species of freshwater snails. Malacologia 51:343–356CrossRefGoogle Scholar
  30. Langan AM, Shaw EM (2006) Responses of the earthworm Lumbricus terrestris (L.) to iron phosphate and metaldehyde slug pellet formulations. Appl Soil Ecol 34:184–189CrossRefGoogle Scholar
  31. Marxen A, Klotzbucher T, Jahn R, Kaiser K, Nguyen VS, Schmidt A, Schadler M, Vetterlein D (2016) Interaction between silicon cycling and straw decomposition in a silicon deficient rice production system. Plant Soil 398:153–163CrossRefGoogle Scholar
  32. Monkiedje A, Anderson AC, Englande AJ (1991) Acute toxicity of Phytolacca dodecandra (endod-S) and niclosamide to snails, Schistosoma mansoni cercaria, tilapia fish, and soil microorganisms. Environ Toxicol Water Qual 6:405–413CrossRefGoogle Scholar
  33. Moore JC, Walter DE, Hunt HW (1988) Arthropod regulation of micro- and mesobiota in below-ground detrital food webs. Annu Rev Entomol 33:419–435CrossRefGoogle Scholar
  34. Natuhara Y (2013) Ecosystem services by paddy fields as substitutes of natural wetlands in Japan. Ecol Eng 56:97–106CrossRefGoogle Scholar
  35. Okada H, Niwa S, Takemoto S, Komatsuzaki M, Hiroki M (2011) How different or similar are nematode communities between a paddy and an upland rice fields across a flooding-drainage cycle? Soil Biol Biochem 43:2142–2151Google Scholar
  36. Oliveira EC, Paumgartten FJR (2000) Toxicity of Euphorbia milli latex and niclosamide to snails and nontarget aquatic species. Ecotoxicol Environ Saf 46:342–350CrossRefGoogle Scholar
  37. Peltzer DA, Allen RB, Lovett GM, Whitehead D, Wardle DA (2010) Effects of biological invasions on forest carbon sequestration. Glob Change Biol 16:732–746CrossRefGoogle Scholar
  38. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 9 April 2017
  39. Schaller J (2013) Invertebrate grazers are a crucial factor for grass litter mass loss and nutrient mobilization during aquatic decomposition. Fundam Appl Limnol 183:287–295CrossRefGoogle Scholar
  40. Schaller J, Struyf E (2013) Silicon controls microbial decay and nutrient release of grass litter during aquatic decomposition. Hydrobiologia 709:201–212CrossRefGoogle Scholar
  41. Schmidt A, Auge H, Brandl R, Heong KL, Hotes S, Settele J, Villareal S, Schaedler M (2015a) Small-scale variability in the contribution of invertebrates to litter decomposition in tropical rice fields. Basic Appl Ecol 16:674–680CrossRefGoogle Scholar
  42. Schmidt A, John K, Arida G, Auge H, Brandl R, Horgan FG, Hotes S, Marquez L, Radermacher N, Settele J, Wolters V, Schadler M (2015b) Effects of residue management on decomposition in irrigated rice fields are not related to changes in the decomposer community. PLoS ONE 10(7):e0134402. https://doi.org/10.1371/journal.pone.0134402 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Schmidt A, John K, Auge H, Brandl R, Horgan FG, Settele J, Zaitsev AS, Wolters V, Schadler M (2016) Compensatory mechanisms of litter decomposition under alternating moisture regimes in tropical rice fields. Appl Soil Ecol 107:79–90CrossRefGoogle Scholar
  44. Schoenly KG, Justo HD, Barrion AT, Harris MK, Bottrell DG (1998) Analysis of invertebrate biodiversity in a Philippine farmer’s irrigated rice field. Environ Entomol 27:1125–1136CrossRefGoogle Scholar
  45. Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS, Pajarningsih, Sartanto (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:1975–1988CrossRefGoogle Scholar
  46. Shibu ME, Leffelaar PA, Van Keulen H, Aggarwal PK (2006) Quantitative description of soil organic matter dynamics—a review of approaches with reference to rice-based cropping systems. Geoderma 137:1–18CrossRefGoogle Scholar
  47. Standing D, Knox OGG, Mullins CE, Killham KK, Wilson MJ (2006) Influence of nematodes on resource utilization by bacteria—an in vitro study. Microb Ecol 52:444–450CrossRefPubMedGoogle Scholar
  48. Turbé A, De Toni A, Benito P, Lavelle P, Lavelle P, Ruiz N, Van der Putten WH, Labouze E, Mudgal S (2010) Soil biodiversity: functions, threats and tools for policy makers. Report for European Commission (DG Environment). Bio Intelligence Service, Institut de Recherche pour le Dévelloppement (IRD) and Netherlands Institute of Ecology (NIOO), ParisGoogle Scholar
  49. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363CrossRefPubMedGoogle Scholar
  50. van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schadler M, Scherber C, Strauss SY, Vos M, Wardle DA (2009) Empirical and theoretical challenges in aboveground-belowground ecology. Oecologia 161:1–14CrossRefPubMedPubMedCentralGoogle Scholar
  51. Wada T, Yoshida K (2000) Burrowing by the apple snail, Pomacea canaliculata (Lamarck); daily periodicity and factors affecting burrowing. Proc Assoc Plant Prot Kyushu 46:88–93CrossRefGoogle Scholar
  52. Wall DH, Bradford MA, St MG, John JA, Trofymow V, Behan-Pelletier DDE, Bignell JM, Dangerfield WJ, Parton J, Rusek W, Voigt V, Wolters HZ, Gardel FO, Ayuke R, Bashford OI, Beljakova PJ, Bohlen A, Brauman S, Flemming JR, Henschel DL, Johnson TH, Jones M, Kovarova JM, Kranabetter L, Kutny K-C, Lin M, Maryati D, Masse A, Pokarzhevskii H, Rahman MG, Sabara J-A, Salamon MJ, Swift A, Varela HL, Vasconcelos D White, Zou X (2008) Global decomposition experiment shows soil animal impacts on decomposition are climate-dependent. Glob Change Biol 14:2661–2677Google Scholar

Copyright information

© The International Society of Paddy and Water Environment Engineering and Springer Japan KK, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of EcologyPhilipps-University MarburgMarburgGermany
  2. 2.Centre for Compassionate Conservation, School of Life SciencesUniversity of Technology SydneySydneyAustralia
  3. 3.German Centre for Integrative Biodiversity Research (iDiv), Halle-Jena-LeipzigLeipzigGermany
  4. 4.Department BiozönoseforschungHelmholtz Centre for Environmental Research GmbH - UFZHalleGermany
  5. 5.Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, Center for Food and Life Sciences WeihenstephanTechnical University of MunichFreising-WeihenstephanGermany
  6. 6.Institute of BiologyLeipzig UniversityLeipzigGermany

Personalised recommendations