Microbial community composition explains soil respiration responses to changing carbon inputs along an Andes-to-Amazon elevation gradient

Journal of Ecology

Volumn 102, Issue 4, 2014, Pages 1058-1071

  Whitaker, Jeanette ^a   Ostle, Nicholas ^b   Nottingham, Andrew T ^c   Ccahuana, Adan ^d   Salinas, Norma ^e   Bardgett, Richard D ^f   Meir, Patrick ^c,g   Mcnamara, Niall P ^a  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b LANCASTER UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d UNIVERSIDAD NACIONAL DE SAN ANTONIO ABAD DEL CUSCO   (Peru)

^e PONTIFICIA UNIVERSIDAD CATÓLICA DEL PERÚ   (Peru)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

^g AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

Bacterial; Carbon substrates; Decomposition; Ecosystem function; Fungal; Microbial community composition; Montane cloud forest; Plant soil (below ground) interactions

Indexed keywords

BACTERIUM; CARBON CYCLE; CARBON DIOXIDE; CARBON FLUX; CLIMATE CHANGE; CLOUD FOREST; COMMUNITY COMPOSITION; DECOMPOSITION; ECOSYSTEM FUNCTION; ELEVATION; FOREST SOIL; FUNGUS; MICROBIAL ACTIVITY; MICROBIAL COMMUNITY; MONTANE FOREST; RELATIVE ABUNDANCE; SOIL MICROORGANISM; SOIL RESPIRATION; SOIL-VEGETATION INTERACTION; TROPICAL FOREST;

AMAZONIA; ANDES; PERU;

BACTERIA (MICROORGANISMS); FUNGI; NEGIBACTERIA; POSIBACTERIA;

EID: 84903178944     PISSN: 00220477     EISSN: 13652745     Source Type: Journal    
DOI: 10.1111/1365-2745.12247     Document Type: Article

References (97)

1. Aragao, L., Malhi, Y., Metcalfe, D.B., Silva-Espejo, J.E., Jimenez, E., Navarrete, D. et al. (2009) Above- and below-ground net primary productivity across ten Amazonian forests on contrasting soils. Biogeosciences, 6, 2759-2778.
2. Asner, G.P., Anderson, C., Martin, R.E., Knapp, D.E., Tupayachi, R., Kennedy-Bowdoin, T., Sinca, F. & Malhi, Y. (2014) Landscape-scale changes in forest structure and functional traits along an Andes-to-Amazon elevation gradient. Biogeosciences Discussions, 10, 15415-15454.
3. Bailey, V.L., Smith, J.L. & Bolton, H. (2002) Fungal-to-bacterial ratios in soils investigated for enhanced C sequestration. Soil Biology & Biochemistry, 34, 997-1007.
4. Baker, T.R., Coronado, E.N.H., Phillips, O.L., Martin, J., van der Heijden, G.M., Garcia, M. & Espejo, J.S. (2007) Low stocks of coarse woody debris in a southwest Amazonian forest. Oecologia, 152, 495-504.
5. Bardgett, R.D., Freeman, C. & Ostle, N.J. (2008) Microbial contributions to climate change through carbon cycle feedbacks. Isme Journal, 2, 805-814.
6. Bardgett, R.D., Hobbs, P.J. & Frostegard, A. (1996) Changes in soil fungal:bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biology and Fertility of Soils, 22, 261-264.
7. Bardgett, R.D. & McAlister, E. (1999) The measurement of soil fungal: bacterial biomass ratios as an indicator of ecosystem self-regulation in temperate meadow grasslands. Biology and Fertility of Soils, 29, 282-290.
8. Berg, B. & Laskowski, R. (2006) Litter Decomposition: A Guide to Carbon and Nutrient Turnover. Elsevier Academic Press, London.
9. Berlemont, R. & Martiny, A.C. (2013) Phylogenetic distribution of potential cellulases in bacteria. Applied and Environmental Microbiology, 79, 1545-1554.
10. Bezemer, T.M., Fountain, M.T., Barea, J.M., Christensen, S., Dekker, S.C., Duyts, H. et al. (2010) Divergent composition but similar function of soil food webs of individual plants: plant species and community effects. Ecology, 91, 3027-3036.
11. de Boer, W., Folman, L.B., Summerbell, R.C. & Boddy, L. (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiology Reviews, 29, 795-811.
12. Bond-Lamberty, B., Wang, C.K. & Gower, S.T. (2004) A global relationship between the heterotrophic and autotrophic components of soil respiration? Global Change Biology, 10, 1756-1766.
13. Bouillon, S., Moens, T., Koedam, N., Dahdouh-Guebas, F., Baeyens, W. & Dehairs, F. (2004) Variability in the origin of carbon substrates for bacterial communities in mangrove sediments. FEMS Microbiology Ecology, 49, 171-179.
14. Bragazza, L., Freeman, C., Jones, T., Rydin, H., Limpens, J., Fenner, N. et al. (2006) Atmospheric nitrogen deposition promotes carbon loss from peat bogs. Proceedings of the National Academy of Sciences, 103, 19386-19389.
15. Bragazza, L., Parisod, J., Buttler, A. & Bardgett, R.D. (2013) Biogeochemical plant-soil microbe feedback in response to climate warming in peatlands. Nature Climate Change, 3, 273-277.
16. Brant, J.B., Sulzman, E.W. & Myrold, D.D. (2006) Microbial community utilization of added carbon substrates in response to long-term carbon input manipulation. Soil Biology & Biochemistry, 38, 2219-2232.
17. Brookes, P.C., Landman, A., Pruden, G. & Jenkinson, D.S. (1985) Chloroform fumigation and the release of soil-nitrogen - a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biology and Biochemistry, 17, 837-842.
18. Carlotto, V., Gil, W., Cardenas, J. & Chavez, R. (1996) Mapa Geologico del Cuadrangula de Calca (27-s). Ministerio de engergia y minas Instituto geologico minero y metalurgico (INGEMMET), Republica del Peru.
19. Carney, K.M. & Matson, P.A. (2005) Plant communities, soil microorganisms, and soil carbon cycling: does altering the world belowground matter to ecosystem functioning? Ecosystems, 8, 928-940.
20. 2 emissions from a sandy loam soil - the role of soil aeration. Soil Biology & Biochemistry, 51, 125-134.
21. Chapin, S.F., McFarland, J., David McGuire, A., Euskirchen, E.S., Ruess, R.W. & Kielland, K. (2009) The changing global carbon cycle: linking plant-soil carbon dynamics to global consequences. Journal of Ecology, 97, 840-850.
22. Clark, K.E., Hilton, R.G., West, A.J., Malhi, Y., Gröcke, D.R., Bryant, C.L., Ascough, P.L., Robles Caceres, A. & New, M. (2013) New views on "old" carbon in the Amazon River: insight from the source of organic carbon eroded from the Peruvian Andes. Geochemistry, Geophysics, Geosystems, 14, 1644-1659.
23. Cleveland, C.C. & Liptzin, D. (2007) C: N: P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry, 85, 235-252.
24. Cleveland, C.C., Nemergut, D.R., Schmidt, S.K. & Townsend, A.R. (2007) Increases in soil respiration following labile carbon additions linked to rapid shifts in soil microbial community composition. Biogeochemistry, 82, 229-240.
25. Coleman, D.C., Cole, C.V., Hunt, H.W. & Klein, D.A. (1978) Trophic interactions in soils as they affect energy and nutrient dynamics. 1. Introduction. Microbial Ecology, 4, 345-349.
26. Craine, J.M., Fierer, N. & McLauchlan, K.K. (2010) Widespread coupling between the rate and temperature sensitivity of organic matter decay. Nature Geoscience, 3, 854-857.
27. De Deyn, G.B., Quirk, H., Oakley, S., Ostle, N. & Bardgett, R.D. (2011) Rapid transfer of photosynthetic carbon through the plant-soil system in differently managed species-rich grasslands. Biogeosciences, 8, 1131-1139.
28. Dieleman, W.I.J., Venter, M., Ramachandra, A., Krockenberger, A.K. & Bird, M.I. (2013) Soil carbon stocks vary predictably with altitude in tropical forests: implications for soil carbon storage. Geoderma, 204, 59-67.
29. Eilers, K.G., Lauber, C.L., Knight, R. & Fierer, N. (2010) Shifts in bacterial community structure associated with inputs of low molecular weight carbon compounds to soil. Soil Biology & Biochemistry, 42, 896-903.
30. Emmett, B.A., Frogbrook, Z.L., Chamberlain, P.M., Griffiths, R., Pickup, R., Poskitt, J., Reynolds, B., Rowe, E., Rowland, P., Wilson, J. & Wood, C.M. (2008) Countryside Survey Technical Report No. 3/07. Centre for Ecology & Hydrology (Natural Environment Research Council), Wallingford, UK.
31. Engelbrecht, B.M.J., Comita, L.S., Condit, R., Kursar, T.A., Tyree, M.T., Turner, B.L. & Hubbell, S.P. (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature, 447, 80-82.
32. Feeley, K.J., Silman, M.R., Bush, M.B., Farfan, W., Cabrera, K.G., Malhi, Y., Meir, P., Revilla, N.S., Quisiyupanqui, M.N.R. & Saatchi, S. (2011) Upslope migration of Andean trees. Journal of Biogeography, 38, 783-791.
33. Fierer, N., McCain, C.M., Meir, P., Zimmermann, M., Rapp, J.M., Silman, M.R. & Knight, R. (2011) Microbes do not follow the elevational diversity patterns of plants and animals. Ecology, 92, 797-804.
34. Fisher, J., Malhi, Y., Torres, I., Metcalfe, D., Weg, M., Meir, P., Silva-Espejo, J. & Huasco, W. (2013) Nutrient limitation in rainforests and cloud forests along a 3, 000-m elevation gradient in the Peruvian Andes. Oecologia, 172, 889-902.
35. Frey, S.D., Lee, J., Melillo, J.M. & Six, J. (2013) The temperature response of soil microbial efficiency and its feedback to climate. Nature Climate Change, 3, 395-398.
36. Garcia-Palacios, P., Maestre, F.T., Bardgett, R.D. & de Kroon, H. (2012) Plant responses to soil heterogeneity and global environmental change. Journal of Ecology, 100, 1303-1314.
37. Girardin, C.A.J., Malhi, Y., Aragão, L.E.O.C., Mamani, M., Huaraca Huasco, W., Durand, L., Feeley, K.J., Rapp, J., Silva-Espejo, J.E., Silman, M., Salinas, N. & Whittaker, R.J. (2010) Net primary productivity allocation and cycling of carbon along a tropical forest elevational transect in the Peruvian Andes. Global Change Biology, 16, 3176-3192.
38. Girardin, C.A.J., Espejob, J.E.S., Doughty, C.E., Huasco, W.H., Metcalfe, D.B., Durand-Baca, L. et al. (2014) Productivity and carbon allocation in a tropical montane cloud forest in the Peruvian Andes. Plant Ecology & Diversity, 7, 107-123.
39. Grubb, P.J. (1977) Control of forest growth and distribution on wet tropical mountains: with special reference to mineral nutrition. Annual Review of Ecology and Systematics, 8, 83-107.
40. Gurdak, D.J., Aragão, L.E.O.C., Rozas-Dávila, A., Huasco, W.H., Cabrera, K.G., Doughty, C.E., Farfan-Rios, W., Silva-Espejo, J.E., Metcalfe, D.B., Silman, M.R. & Malhi, Y. (2014) Assessing above-ground woody debris dynamics along a gradient of elevation in Amazonian cloud forests in Peru: balancing above-ground inputs and respiration outputs. Plant Ecology & Diversity, 7, 143-160.
41. Hanson, C.A., Allison, S.D., Bradford, M.A., Wallenstein, M.D. & Treseder, K.K. (2008) Fungal taxa target different carbon sources in forest soil. Ecosystems, 11, 1157-1167.
42. Hartman, W.H. & Richardson, C.J. (2013) Differential nutrient limitation of soil microbial biomass and metabolic quotients (qCO(2)): is there a biological stoichiometry of soil microbes? PLoS One, 8, 1-14.
43. Hattenschwiler, S. & Jorgensen, H.B. (2010) Carbon quality rather than stoichiometry controls litter decomposition in a tropical rain forest. Journal of Ecology, 98, 754-763.
44. Hättenschwiler, S., Aeschlimann, B., Coûteaux, M.-M., Roy, J. & Bonal, D. (2008) High variation in foliage and leaf litter chemistry among 45 tree species of a neotropical rainforest community. New Phytologist, 179, 165-175.
45. 4 exchange. Standard Soil Methods for Long-Term Ecological Research (ed. G.P. Robertson, D.C. Coleman, C.S. Bledsoe & P. Sollins ), pp. 185-201. Oxford University Press, New York.
46. Huasco, W.H., Girardin, C.A.J., Doughty, C.E., Metcalfe, D.B., Baca, L.D., Silva-Espejo, J.E. et al. (2014) Seasonal production, allocation and cycling of carbon in two mid-elevation tropical montane forest plots in the Peruvian Andes. Plant Ecology & Diversity, 7, 125-142.
47. IPCC (2013) Working Group I Contribution to the IPCC Fifth Assessment Report. Climate Change 2013: The Physical Science Basis. Inter-governmental Panel on Climate Change, Geneva.
48. Jobbagy, E.G. & Jackson, R.B. (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications, 10, 423-436.
49. Joergensen, R.G. & Wichern, F. (2008) Quantitative assessment of the fungal contribution to microbial tissue in soil. Soil Biology and Biochemistry, 40, 2977-2991.
50. Kaiser, C., Frank, A., Wild, B., Koranda, M. & Richter, A. (2010) Negligible contribution from roots to soil-borne phospholipid fatty acid fungal biomarkers 18:2 omega 6, 9 and 18:1 omega 9. Soil Biology & Biochemistry, 42, 1650-1652.
51. Kaspari, M. & Yanoviak, S.P. (2008) Biogeography of litter depth in tropical forests: evaluating the phosphorus growth rate hypothesis. Functional Ecology, 22, 919-923.
52. Keinanen, M.M., Korhonen, L.K., Lehtola, M.J., Miettinen, I.T., Martikainen, P.J., Vartiainen, T. & Suutari, M.H. (2002) The microbial community structure of drinking water biofilms can be affected by phosphorus availability. Applied and Environmental Microbiology, 68, 434-439.
53. Keiser, A., Knoepp, J. & Bradford, M. (2013) Microbial communities may modify how litter quality affects potential decomposition rates as tree species migrate. Plant and Soil, 372, 167-176.
54. Klamer, M. & Bååth, E. (2004) Estimation of conversion factors for fungal biomass determination in compost using ergosterol and PLFA 18: 2 omega 6, 9. Soil Biology & Biochemistry, 36, 57-65.
55. Kramer, C. & Gleixner, G. (2008) Soil organic matter in soil depth profiles: distinct carbon preferences of microbial groups during carbon transformation. Soil Biology & Biochemistry, 40, 425-433.
56. Leff, J.W., Nemergut, D.R., Grandy, A.S., O'Neill, S.P., Wickings, K., Townsend, A.R. & Cleveland, C.C. (2012) The effects of soil bacterial community structure on decomposition in a tropical rain forest. Ecosystems, 15, 284-298.
57. Malhi, Y., Silman, M., Salinas, N., Bush, M., Meir, P. & Saatchi, S. (2010) Introduction: elevation gradients in the tropics: laboratories for ecosystem ecology and global change research. Global Change Biology, 16, 3171-3175.
58. Malhi, Y., Farfán Amézquita, F., Doughty, C.E., Silva-Espejo, J.E., Girardin, C.A.J., Metcalfe, D.B. et al. (2014) The productivity, metabolism and carbon cycle of two lowland tropical forest plots in south-western Amazonia, Peru. Plant Ecology & Diversity, 7, 85-105.
59. Manzoni, S., Taylor, P., Richter, A., Porporato, A. & Agren, G.I. (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytologist, 196, 79-91.
60. Margesin, R., Jud, M., Tscherko, D. & Schinner, F. (2009) Microbial communities and activities in alpine and subalpine soils. FEMS Microbiology Ecology, 67, 208-218.
61. McGuire, K.L., Bent, E., Borneman, J., Majumder, A., Allison, S.D. & Treseder, K.K. (2010) Functional diversity in resource use by fungi. Ecology, 91, 2324-2332.
62. Meier, C.L., Rapp, J., Bowers, R.M., Silman, M. & Fierer, N. (2010) Fungal growth on a common wood substrate across a tropical elevation gradient: temperature sensitivity, community composition, and potential for above-ground decomposition. Soil Biology & Biochemistry, 42, 1083-1090.
63. Moser, G., Leuschner, C., Hertel, D., Graefe, S., Soethe, N. & Iost, S. (2011) Elevation effects on the carbon budget of tropical mountain forests (S Ecuador): the role of the belowground compartment. Global Change Biology, 17, 2211-2226.
64. Myers, N., Mittermeier, R.A., Mittermeier, C.G., da Fonseca, G.A.B. & Kent, J. (2000) Biodiversity hotspots for conservation priorities. Nature, 403, 853-858.
65. Nannipieri, P., Ascher, J., Ceccherini, M.T., Landi, L., Pietramellara, G. & Renella, G. (2003) Microbial diversity and soil functions. European Journal of Soil Science, 54, 655-670.
66. Ohlinger, R. (1995) Methods in soil physics: maximum water holding capacity. Methods in Soil Biology (eds F. Schinner, R. Ohlinger, E. Kandeler & R. Margesin ), pp. 385-386. Springer, Berlin, Germany.
67. Ostle, N.J., Smith, P., Fisher, R., Woodward, F.I., Fisher, J.B., Smith, J.U., Galbraith, D., Levy, P., Meir, P., McNamara, N.P. & Bardgett, R.D. (2009) Integrating plant-soil interactions into global carbon cycle models. Journal of Ecology, 97, 851-863.
68. Pinto, E., Shin, Y., Cowling, S.A. & Jones, C.D. (2009) Past, present and future vegetation-cloud feedbacks in the Amazon Basin. Climate Dynamics, 32, 741-751.
69. Quesada, C.A., Lloyd, J., Schwarz, M., Patino, S., Baker, T.R., Czimczik, C. et al. (2010) Variations in chemical and physical properties of Amazon forest soils in relation to their genesis. Biogeosciences, 7, 1515-1541.
70. R Development Core Team (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
71. Rinnan, R. & Bååth, E. (2009) Differential utilization of carbon substrates by bacteria and fungi in tundra soil. Applied and Environmental Microbiology, 75, 3611-3620.
72. Ross, D.J. (1992) Influence of sieve mesh size on estimates of microbial carbon and nitrogen by fumigation-extraction procedures in soils under pasture. Soil Biology & Biochemistry, 24, 343-350.
73. Rousk, J. & Bååth, E. (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiology Ecology, 78, 17-30.
74. Salinas, N., Malhi, Y., Meir, P., Silman, M., Cuesta, R.R., Huaman, J., Salinas, D., Huaman, V., Gibaja, A., Mamani, M. & Farfan, F. (2011) The sensitivity of tropical leaf litter decomposition to temperature: results from a large-scale leaf translocation experiment along an elevation gradient in Peruvian forests. New Phytologist, 189, 967-977.
75. Schawe, M., Glatzel, S. & Gerold, G. (2007) Soil development along an altitudinal transect in a Bolivian tropical montane rainforest: podzolization vs. hydromorphy. Catena, 69, 83-90.
76. Schimel, J.P. & Schaeffer, S.M. (2012) Microbial control over carbon cycling in soil. Frontiers in Microbiology, 3, 348.
77. Schindlbacher, A., Rodler, A., Kuffner, M., Kitzler, B., Sessitsch, A. & Zechmeister-Boltenstern, S. (2011) Experimental warming effects on the microbial community of a temperate mountain forest soil. Soil Biology and Biochemistry, 43, 1417-1425.
78. Six, J., Frey, S.D., Thiet, R.K. & Batten, K.M. (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal, 70, 555-569.
79. Smith, P., Fang, C.M., Dawson, J.J.C. & Moncrieff, J.B. (2008) Impact of global warming on soil organic carbon. Advances in Agronomy, 97, 1-43.
80. ec-factor. Soil Biology & Biochemistry, 22, 301-307.
81. Steinweg, J.M., Plante, A.F., Conant, R.T., Paul, E.A. & Tanaka, D.L. (2008) Patterns of substrate utilization during long-term incubations at different temperatures. Soil Biology & Biochemistry, 40, 2722-2728.
82. Strickland, M.S., Lauber, C., Fierer, N. & Bradford, M.A. (2009) Testing the functional significance of microbial community composition. Ecology, 90, 441-451.
83. Tanner, E.V.J., Vitousek, P.M. & Cuevas, E. (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology, 79, 10-22.
84. Treseder, K.K., Kivlin, S.N. & Hawkes, C.V. (2011) Evolutionary trade-offs among decomposers determine responses to nitrogen enrichment. Ecology Letters, 14, 933-938.
85. Turner, B.L. & Wright, J.S. (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry, 117, 115-130.
86. Vance, E.D., Brookes, P.C. & Jenkinson, D.S. (1987) Microbial biomass measurements in forest soils - the use of the chloroform fumigation incubation method in strongly acid soils. Soil Biology & Biochemistry, 19, 697-702.
87. de Vries, F.T., Manning, P., Tallowin, J.R.B., Mortimer, S.R., Pilgrim, E.S., Harrison, K.A., Hobbs, P.J., Quirk, H., Shipley, B., Cornelissen, J.H.C., Kattge, J. & Bardgett, R.D. (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecology Letters, 15, 1230-1239.
88. Ward, S.E., Bardgett, R.D., McNamara, N.P., Adamson, J.K. & Ostle, N.J. (2007) Long-term consequences of grazing and burning on northern peatland carbon dynamics. Ecosystems, 10, 1069-1083.
89. Ward, S.E., Ostle, N.J., Oakley, S., Quirk, H., Henrys, P.A. & Bardgett, R.D. (2013) Warming effects on greenhouse gas fluxes in peatlands are modulated by vegetation composition. Ecology Letters, 16, 1285-1293.
90. Waring, B.G., Averill, C. & Hawkes, C.V. (2013) Differences in fungal and bacterial physiology alter soil carbon and nitrogen cycling: insights from meta-analysis and theoretical models. Ecology Letters, 16, 887-894.
91. Waring, B., Weintraub, S. & Sinsabaugh, R. (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry, 117, 101-113.
92. van de Weg, M.J., Meir, P., Grace, J. & Atkin, O.K. (2009) Altitudinal variation in leaf mass per unit area, leaf tissue density and foliar nitrogen and phosphorus content along an Amazon-Andes gradient in Peru. Plant Ecology & Diversity, 2, 243-254.
93. Wilcke, W., Oelmann, Y., Schmitt, A., Valarezo, C., Zech, W. & Horneier, J. (2008) Soil properties and tree growth along an altitudinal transect in Ecuadorian tropical montane forest. Journal of Plant Nutrition and Soil Science-Zeitschrift Fur Pflanzenernahrung Und Bodenkunde, 171, 220-230.
94. Zimmermann, M., Meir, P., Bird, M.I., Malhi, Y. & Ccahuana, A.J.Q. (2009) Climate dependence of heterotrophic soil respiration from a soil-translocation experiment along a 3000 m tropical forest altitudinal gradient. European Journal of Soil Science, 60, 895-906.
95. Zimmermann, M., Meir, P., Bird, M.I., Malhi, Y. & Ccahuana, A.J.Q. (2010) Temporal variation and climate dependence of soil respiration and its components along a 3000 m altitudinal tropical forest gradient. Global Biogeochemical Cycles, 24, 1-13.
96. Zimmermann, M., Leifeld, J., Conen, F., Bird, M.I. & Meir, P. (2012) Can composition and physical protection of soil organic matter explain soil respiration temperature sensitivity? Biogeochemistry, 107, 423-436.
97. Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A. & Smith, G.M. (2010) 5. Mixed effects modelling for nested data. Mixed Effects Models and Extensions in Ecology with R (ed. A.F. Zuur, E.N. Ieno, N.J. Walker, A.A. Saveliev & G.M. Smith ), pp. 101-142. Springer, New York, USA.