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A multitrophic interaction: consequences of grazing on decomposition of needles of Pinus pinea L. by Ommatoiulus sabulosus L.

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Abstract

The aim of this study was to assess how the physical (needle fragmentation by trampling) and chemical (nutritional enrichment from faeces) changes brought about by grazing influence the consumption of needles of Pinus pinea L. by Ommatoiulus sabulosus L. Adult individuals of O. sabulosus were introduced into trays with pine needles subjected to four treatments: (i) intact needles, (ii) trampled needles, (iii) intact needles fertilized with liquid manure, and (iv) trampled needles fertilized with liquid manure. After 30 days, litter decomposition was determined as a function of mass loss over time. Biometric and chemical characteristics of the needles were also measured. The pine needle decomposition rate was significantly higher in the presence of O. sabulosus (20–40%) than in its absence, presenting in addition a significantly higher rate in the treatments enriched with nitrogen. Average needle length was significantly shorter in the trampled treatments (6.89 ± 0.50 cm) than in those with intact needles (11.95 ± 0.69 cm). With regard to leaf mass per area and resistance to breakage, no significant differences were found. The fertilized treatments presented significantly higher N content (50% higher) than those in the non-fertilized ones with a significantly lower C:N ratio. The results of the present study indicate that goat grazing (which produces both trampling and fertilization) favoured the consumption of pine needles by O. sabulosus, which thus influences, along with the microbial community, the decomposition rate of these needles and thereby promotes incorporation of N into the system.

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References

  • Aerts R (1997) Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–449

    Article  Google Scholar 

  • Akkari N, Enghoff H (2012) Review of the genus Ommatoiulus in Andalusia, Spain (Diplopoda: Julida) with description of ten new species and notes on a remarkable gonopod structure, the fovea. Zootaxa 3538:1–53

    Google Scholar 

  • Arnebrant K, Bååth E, Söderström B (1990) Changes in microfungal community structure after fertilization of Scots pine forest soil with ammonium nitrate or urea. Soil Biol Biochem 22:309–312

    Article  Google Scholar 

  • Baas M, Cherett JM (1995) Leaf-cutting ants (Formicidae, Attini) prune their fungus to increase and direct its productivity. Funct Ecol 10:55–61

    Article  Google Scholar 

  • Bååth E, Arnebrant K (1993) Microfungi in coniferous forest soils treated with lime or wood ash. Biol Fertil Soils 26:995–1001

    Article  Google Scholar 

  • Bardgett RD, Wardle DA (2003) Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–2268

    Article  Google Scholar 

  • Bardgett RD, Wardle DA (2010) Aboveground-belowground linkages: biotic interactions, ecosystem processes, and global change. Oxford University Press, Oxford

    Google Scholar 

  • Bardgett RD, Wardle DA, Yeates GW (1998) Linking aboveground and below-ground interactions: how plant responses to foliar herbivory influence soil organisms. Soil Biol Biochem 30:1867–1878

    Article  CAS  Google Scholar 

  • Bazely DR, JeVeries RL (1985) Goose faeces: a source of nitrogen for plant growth in a grazed salt marsh. J App Ecol 22:693–703

    Article  Google Scholar 

  • Berg B, McClaugherty C, Santo AVD, Johnson D (2001) Humus buildup in boreal forests: effects of litter fall and its N concentration. Canad J For Res 31:988–998

    Article  CAS  Google Scholar 

  • Bonkowski M, Scheu S, Schaefer M (1998) Interactions of earth-worms (Octolasion lacteum), millipedes (Glomeris marginata) and plants (Hordelymus europaeus) in a beechwood on a basalt hill: implications for litter decomposition and soil formation. Appl Soil Ecol 9:161–166

    Article  Google Scholar 

  • Bryant JP, Provenza FD, Pastor J, Reichardt PB, Clausen TP, Du Toit JT (1991) Interactions between woody plants and browsing mammals mediated by secondary metabolites. Ann Rev Ecol Systs 22:431–446

    Article  Google Scholar 

  • Chapin FS III, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology. Springer Science & Business Media, New York

    Book  Google Scholar 

  • Coleman DC, Crossley DA Jr, Hendrix PF (2004) Fundamentals of soil ecology. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Coulis M, Hättenschwiler S, Fromin N, David JF (2013) Macroarthropod-microorganism interactions during the decomposition of Mediterranean shrub litter at different moisture levels. Soil Biol Biochem 64:114–121

    Article  CAS  Google Scholar 

  • Couteaux MM, Bottner P, Berg B (1995) Litter decomposition, climate and litter quality. Trends Ecol Evol 2:63–66

    Article  Google Scholar 

  • David JF (1999) Abundance, biomass and functional structure of the saprophagous macrofauna in the litter and soil of Mediterranean oak forests. Pedobiologia 43:319–327

    Google Scholar 

  • David JF, Devernay S, Loucougaray G, Le Floc’h E (1999) Belowground biodiversity in a Mediterranean landscape: relationships between saprophagous macroarthropod communities and vegetation structure. Biodivers Conserv 8:753–767

    Article  Google Scholar 

  • Dubeux JCB, Sollenberger LE, Interrante SM, Vendramini JMB, Stewart RL (2006) Litter decomposition and mineralization in bahia grass pastures managed at different intensities. Crop Sci 46:1305–1310

    Article  CAS  Google Scholar 

  • Dyer MI, Turner CL, Seastedt TR (1991) Mowing and fertilizing effects on productivity and spectral reflectance in Bromus inermis plots. Ecol Appl 1:559–564

    Article  Google Scholar 

  • Frank DA, Groffman PM, Evans RD, Tracy BF (2000) Ungulate stimulation of nitrogen cycling and retention in Yellowstone Park grasslands. Oecologia 123:116–121

    Article  Google Scholar 

  • Gallardo A, Merino J (1993) Leaf decomposition in two Mediterranean ecosystems of southwest Spain: influence of substrate quality. Ecology 74:152–161

    Article  Google Scholar 

  • Garibaldi LA, Semmartin M, Chaneton EJ (2007) Grazing induced changes in plant composition affect litter quality and nutrient cycling in flooding Pampa grasslands. Oecologia 151:650–662

    Article  PubMed  Google Scholar 

  • Gillon D, Jofre R, Ibrahamina A (1994) Initial litter properties and decay rates: a microcosm experiments on Mediterranean species. Can J Bot 72:946–954

    Article  Google Scholar 

  • Hargrave BT (1972) Prediction of egestion by the deposit-feeding amphipod Hyalella azteca. Oikos 23:116–124

    Article  Google Scholar 

  • Harmon ME, Silver WL, Fasth B, Chen H, Burke IC, Parton WJ, Hart SC, Currie WS, LIDET (2009) Long-term patterns of mass loss during decomposition of leaf and fine root litter: an intersite comparison. Glob Change Biol 15:1320–1338

    Article  Google Scholar 

  • Haynes RJ, Williams PH (1999) Influence of stock camping behaviour on the soil microbiological and biochemical properties of grazed pastoral soils. Biol fertil soils 28:253–258

    Article  CAS  Google Scholar 

  • Hobbie SE (1996) Temperature and plant species control over litter decomposition in Alaskan tundra. Ecolog Monogr 66:503–522

    Article  Google Scholar 

  • Holland EA, Parton WJ, Detling JK, Coppock DL (1992) Physiological responses of plant populations to herbivory and their consequences for ecosystem nutrient flow. Am Nat 4:685–706

    Article  Google Scholar 

  • Holland JN, Chenge W, Crossley DA (1996) Herbivore-induced changes in plant carbon allocation: assessment of below-ground C fluxes using carbon-14. Oecologia 107:87–94

    Article  Google Scholar 

  • Joffre R, Ågren GI, Gillon D, Bosatta E (2001) Organic matter quality in ecological studies: theory meets experiment. Oikos 93:451–458

    Article  CAS  Google Scholar 

  • Kadamannaya BS, Sridhar KR (2009) Leaf litter ingestion and assimilation by two endemic pill millipedes (Arthrosphaera). Biol Fertil Soils 45:761–768

    Article  Google Scholar 

  • Kooijman AM, Smit A (2001) Grazing as a measure to reduce nutrient availability and plant productivity in acid dune grasslands and pine forests in The Netherlands. Grass Sci 17:63–77

    Google Scholar 

  • Latrou GD, Stamou GP (1991) The life cycle and spatial distribution of Glomeris balcanica (Diplopoda, Glomeridae) in an evergreen-sclerophyllous formation in northern Greece. Pedobiologia 35:1–10

    Google Scholar 

  • Lavelle P, Spain AV (2001) Soil ecology. Kluwer Academic, Dordrecht

    Book  Google Scholar 

  • Li X, Han S, Zhang Y (2007) Foliar decomposition in a broadleaf-mixed Korean pine (Pinus koraiensis Sieb. Et Zucc) plantation forest: the impact of initial litter quality and the decomposition of three kinds of organic matter fraction on mass loss and nutrient release rates. Plant Soil 295:151–167

    Article  CAS  Google Scholar 

  • Liu K, Sollenberger LE, Silveira ML, Vendramini JMB, Newman YC (2011) Grazing intensity and nitrogen fertilization affect litter responses in ‘Tifton 85’ bermudagrass pastures: II. Decomposition and nitrogen mineralization. Agron J 103:163–168

    Article  Google Scholar 

  • Mancilla-Leytón JM, Sánchez-Lineros V, Martín Vicente A (2013a) Influence of grazing on the decomposition of Pinus pinea L. needles in a silvopastoral system in Doñana, Spain. Plant Soil 373:173–181

    Article  Google Scholar 

  • Mancilla-Leytón JM, Pino Mejías R, Martín Vicente A (2013b) Do goats preserve the forest? Evaluating the effects of grazing goats on combustible Mediterranean scrub. App Veg Sci 16:63–73

    Article  Google Scholar 

  • Maraun M, Scheu S (1996) Changes in microbial biomass, respiration and nutrient status of beech (Fagus sylvatica) leaf litter processed by millipedes (Glomeris marginata). Oecologia 107:131–140

    Article  Google Scholar 

  • Matus FJ, Rodríguez J (1994) A simple model for estimating the contribution of nitrogen mineralization to the nitrogen supply of crops from a stabilized pool of soil organic matter and recent organic input. Plant Soil 162:259–271

    Article  CAS  Google Scholar 

  • McIntire EJB, Hik DS (2002) Grazing history versus current a grazing: leaf demography and compensatory growth of three alpine plants in response to a native herbivore (Ochotona collaris). J Ecol 90:348–359

    Article  Google Scholar 

  • McNaughton SJ (1985) Ecology of a grazing ecosystem: the Serengeti. Ecol Monogr 55:259–294

    Article  Google Scholar 

  • Moro MJ, Domingo F (2000) Litter decomposition in four woody species in a Mediterranean climate: weight loss, N and P dynamics. Ann Bot 86:1065–1071

    Article  CAS  Google Scholar 

  • Odum EP, de la Cruz AA (1967) Particulate organic detritus in a Georgia salt marsh-estuarine system. In: Lauff GH (ed) Estuaries, vol 83. American Association for the Advancement of Science Publication, Washington, DC, pp 383–388

    Google Scholar 

  • Olofsson J, Oksanen L (2002) Role of litter decomposition for the increased primary production in areas heavily grazed by reindeer: a litterbag experiment. Oikos 96:507–515

    Article  Google Scholar 

  • Pastor J, Naiman RJ (1992) Selective foraging and ecosystem processes in boreal forests. Am Nat 4:690–705

    Article  Google Scholar 

  • Pausas JG (1997) Litter fall and litter decomposition in Pinus sylvestris forests of the eastern Pyrenees. J Veg Sci 8:643–650

    Article  Google Scholar 

  • Pennanen T, Liski J, Bååth E, Kitunen V, Uotila J, Westman CJ, Fritze H (1999) Structure of the microbial communities in coniferous forest soils in relation to site fertility and stand development stage. Microb Ecol 38:168–179

    Article  CAS  PubMed  Google Scholar 

  • Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor versus nutrient-rich ecosystems. Ecology 79:2581–2592

    Article  Google Scholar 

  • Ritchie ME, Tilman D, Knops JM (1998) Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–177

    Article  Google Scholar 

  • Ruess WR, McNaughton SJ (1987) Grazing and the dynamics of nutrient and energy regulated microbial processes in the Serengeti grasslands. Oikos 49:101–110

    Article  Google Scholar 

  • Scheu S, Parkinson D (1994) Effects of earthworms on nutrient dynamics, carbon turnover and microorganisms in soils from cool temperate forests of the Canadian Rocky Mountains laboratory studies. App Soil Ecol 1:113–125

    Article  Google Scholar 

  • Scheu S, Schlitt N, Tiunov AV, Newington JE, Jones TH (2002) Effects of the presence and community composition of earthworms on microbial community functioning. Oecologia 133:254–260

    Article  Google Scholar 

  • Silver W, Miya R (2001) Global patterns in root decomposition: comparisons of climate and litter quality effects. Oecologia 129:407–419

    Article  Google Scholar 

  • Sirotnak JM, Huntly NJ (2000) Direct and indirect effects of herbivores on nitrogen dynamics: voles in riparian areas. Ecology 81:78–87

    Article  Google Scholar 

  • Swift MC (1976) Energetics of vertical migration in Chaoborus trivittatus larvae. Ecology 57:900–914

    Article  Google Scholar 

  • Tajovský K, Šantrůčková H, Hánĕl L, Balík LA (1992) Decomposition of faecal pellets of the millipede Glomeris hexasticha (Diplopoda) in forest soil. Pedobiologia 36:146–158

    Google Scholar 

  • Vanlauwe B, Sanginga N, Merckx R (1997) Decomposition of four Leucaena and Senna prunings in alley cropping systems under subhumid tropical conditions: the process and its modifiers. Soil Biol Biochem 29:131–137

    Article  CAS  Google Scholar 

  • Visser S (1985) Role of the soil invertebrates in determining the composition of soil microbial communities. In: Fitter AH, Atkinson D, Read DJ, Usher MB (eds) Ecological interactions in soil. Special publication No. 4. British Ecological Society. Blackwell, Oxford, pp 297–317

  • Wang QS, Huang Y (2008) Comparisons of litter fall, litter decomposition and nutrient return in a monoculture Cunninghamia lanceolata and a mixed stand in southern China. For Ecol Manag 255:1210–1218

    Article  Google Scholar 

  • Wilson JB, Agnew ADQ (1992) Positive-feedback switches in plant communities. Adv Ecol Res 23:263–336

    Article  Google Scholar 

  • Wolters V (2000) Invertebrate control of soil organic matter stability. Biol Fertil Soils 3:1–19

    Article  Google Scholar 

  • Zimov SA, Chuprynin VI, Oreshko AP, Chapin FS III, Reynolds JF, Chapin MC (1995) Steppe-tundra transition: a herbivore-driven biome shift at the end of the Pleistocene. Am Nat 146:765–794

    Article  Google Scholar 

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Acknowledgements

This study was funded by the Consejería de Medio Ambiente (Junta de Andalucía) (OG-052/07). The authors wish to thank Doñana Natural Park and Dehesa de Gatos S.L. for the logistic support and field facilities. The authors also thank Dr. Pérez-Ramos and Dra. Muñoz-Vallés for their useful comments on the earlier version of this manuscript. The useful field and laboratory assistance by Cristina Palomares is also acknowledged. A. Serrano checked the language grammar of this paper. J.M. Mancilla-Leytón gratefully acknowledges the receipt of a Postdoctoral Research Contract (V Plan Propio de Investigación de la Universidad de Sevilla, Ref. II.5.B/2015).

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  1. Departamento de Biología Vegetal y Ecología, Universidad de Sevilla, Apdo.1095, 41080, Seville, Spain

    J. M. Mancilla-Leytón, J. Cambrollé & A. Martín Vicente

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  1. J. M. Mancilla-Leytón
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Mancilla-Leytón, J.M., Cambrollé, J. & Martín Vicente, A. A multitrophic interaction: consequences of grazing on decomposition of needles of Pinus pinea L. by Ommatoiulus sabulosus L.. Plant Ecol 218, 241–249 (2017). https://doi.org/10.1007/s11258-016-0679-5

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