Skip to main content
SpringerLink
Log in

Land-use and soil depth affect resource and microbial stoichiometry in a tropical mountain rainforest region of southern Ecuador

Oecologia Aims and scope Submit manuscript

Cite this article

Abstract

Global change phenomena, such as forest disturbance and land-use change, significantly affect elemental balances as well as the structure and function of terrestrial ecosystems. However, the importance of shifts in soil nutrient stoichiometry for the regulation of belowground biota and soil food webs have not been intensively studied for tropical ecosystems. In the present account, we examine the effects of land-use change and soil depth on soil and microbial stoichiometry along a land-use sequence (natural forest, pastures of different ages, secondary succession) in the tropical mountain rainforest region of southern Ecuador. Furthermore, we analyzed (PLFA-method) whether shifts in the microbial community structure were related to alterations in soil and microbial stoichiometry. Soil and microbial stoichiometry were affected by both land-use change and soil depth. After forest disturbance, significant decreases of soil C:N:P ratios at the pastures were followed by increases during secondary succession. Microbial C:N ratios varied slightly in response to land-use change, whereas no fixed microbial C:P and N:P ratios were observed. Shifts in microbial community composition were associated with soil and microbial stoichiometry. Strong positive relationships between PLFA-markers 18:2n6,9c (saprotrophic fungi) and 20:4 (animals) and negative associations between 20:4 and microbial N:P point to land-use change affecting the structure of soil food webs. Significant deviations from global soil and microbial C:N:P ratios indicated a major force of land-use change to alter stoichiometric relationships and to structure biological systems. Our results support the idea that soil biotic communities are stoichiometrically flexible in order to adapt to alterations in resource stoichiometry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Allison VJ, Yermakov Z, Miller RM, Jastrow JD, Matamala R (2007) Using landscape and depth gradients to decouple the impact of correlated environmental variables on soil microbial community composition. Soil Biol Biochem 39:505–516

    Article  CAS  Google Scholar 

  • Bai ZG, Dent DL, Olsson L, Schaepman ME (2008) Proxy global assessment of land degradation. Soil Use Manag 24:223–234

    Article  Google Scholar 

  • Baldrian P, Voříšková J, Dobiášová P, Merhautová V, Lisá L, Valášková V (2011) Production of extracellular enzymes and degradation of biopolymers by saprotrophic microfungi from the upper layers of forest soil. Plant Soil 338:111–125

    Article  CAS  Google Scholar 

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

  • Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (2008) Gradients in a tropical mountain ecosystem of Ecuador. Springer, Berlin, Heidelberg

    Book  Google Scholar 

  • Bendix J, Homeier J, Cueva Ortiz E, Emck P, Breckle SW, Richter M, Beck E (2006) Seasonality of weather and tree phenology in a tropical evergreen mountain rain forest. Int J Biometeorol 50:370–384

    Article  CAS  PubMed  Google Scholar 

  • Brookes PC, Powlson DS, Jenkinson DS (1982) Measurement of microbial biomass phosphorus in soil. Soil Biol Biochem 14:319–329

    Article  CAS  Google Scholar 

  • Certini G (2005) Effects of fire on properties of forest soils: a review. Oecologia 143:1–10

    Article  PubMed  Google Scholar 

  • Chen G, He Z (2004) Determination of soil microbial biomass phosphorus in acid red soils from southern China. Biol Fertil Soils 39:446–451

    Article  CAS  Google Scholar 

  • Cherif M, Loreau M (2007) Stoichiometric constraints on resource use, competitive interactions, and elemental cycling in microbial decomposers. Am Nat 169:709–724

    Article  PubMed  Google Scholar 

  • Cleveland C, Liptzin D (2007) C:N:P stoichiometry in soil: is there a “Redfield ratio” for the microbial biomass? Biogeochemistry 85:235–252

    Article  Google Scholar 

  • Coleman DC (1994) The microbial loop concept as used in terrestrial soil ecology studies. Microb Ecol 28:245–250

    Article  CAS  PubMed  Google Scholar 

  • Davidson EA, de Carvalho CJ, Figueira AM, Ishida FY, Ometto JP, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira IC, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–998

    Article  CAS  PubMed  Google Scholar 

  • de Deyn GB, Quirk H, Bardgett RD (2011) Plant species richness, identity and productivity differentially influence key groups of microbes in grassland soils of contrasting fertility. Biol Lett 7:75–78

    Article  PubMed Central  PubMed  Google Scholar 

  • Diaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JH, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez-Rontomé MC, Shirvany FA, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, de Torres-Espuny L, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro-Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: Evidence from three continents. J Veg Sci 15:295–304

    Article  Google Scholar 

  • Ehrenfeld JG, Ravit B, Elgersma K (2005) Feedback in plant-soil system. Annu Rev Environ Resour 30:75–115

    Article  Google Scholar 

  • Elser JJ, Dobberfuhl DR et al (1996) Organism size, life history, and N: P stoichiometry. BioSci 46:674

    Article  Google Scholar 

  • Falster DS, Warton DI, Wright IJ (2006) SMATR: standardised major axis test and routines, ver2.0

  • Fanin N, Fromin N, Buatois B, Hättenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecol Lett 16:764–772

    Article  PubMed  Google Scholar 

  • FAO (2006) World reference base for soil resources 2006: a framework for international classification, correlation and communication. Food and Agriculture Organization of the United Nations, Rome

    Google Scholar 

  • Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    Article  CAS  Google Scholar 

  • Fierer N, Grandy AS, Six J, Paul EA (2009) Searching for unifying principles in soil ecology. Soil Biol Biochem 41:2249–2256

    Article  CAS  Google Scholar 

  • Franklin O, Hall EK, Kaiser C, Battin TJ, Richter A (2011) Optimization of biomass composition explains microbial growth–stoichiometry relationships. Am Nat 177:E29

    Article  PubMed  Google Scholar 

  • Gerique A (2010) Biodiversity as a resource: Biodiversity as a resource: plant use and land use among the Shuar, Saraguros, and Mestizos in tropical rainforest areas of southern Ecuador. Dissertation, Friedrich-Alexander Universität Erlangen-Nürnberg

  • Göttlicher D, Obregón A, Homeier J, Rollenbeck R, Nauss T, Bendix J (2009) Land-cover classification in the Andes of southern Ecuador using Landsat ETM+ data as a basis for SVAT modelling. Int J Remote Sens 30:1867–1886

    Article  Google Scholar 

  • Grime JP (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281

    Article  Google Scholar 

  • Güsewell S, Gessner MO (2009) N:P ratios influence litter decomposition and colonization by fungi and bacteria in microcosms. Funct Ecol 23:211–219

    Article  Google Scholar 

  • Hamer U, Rumpel C, Dignac M (2012) Cutin and suberin biomarkers as tracers for the turnover of shoot and root derived organic matter along a chronosequence of Ecuadorian pasture soils. Eur J Soil Sci 63:808–819

    Article  CAS  Google Scholar 

  • Hamer U, Potthast K, Burneo J, Makeschin F (2013a) Nutrient stocks and phosphorus fractions in mountain soils of Southern Ecuador after conversion of forest to pasture. Biogeochemistry 112:495–510

    Article  CAS  Google Scholar 

  • Hamer U, Potthast K, Wilcke W, Wullaert H, Valarezo C, Sandmann D, Maraun M, Scheu S, Homeier J (2013b) Nutrient additions affecting matter turnover in forest and pasture ecosystems. In: Bendix J, Beck E, Bräuning A, Makeschin F, Mosandl R, Scheu S, Wilcke W (eds) Ecosystem services, biodiversity and environmental change in a tropical mountain ecosystem of South Ecuador. Springer, Heidelberg, pp 297–314

    Chapter  Google Scholar 

  • Hartig K, Beck E (2003) The bracken fern (Pteridium arachnoideum (Kaulf.) Maxon) dilemma in the Andes of southern Ecuador. Ecotropica (Bonn) 9:3–13

    Google Scholar 

  • Hessen DO, Ågren GI, Anderson TR, Elser JJ, de Ruiter PC (2004) Carbon sequestration in ecosystems: the role of stoichiometry. Ecology 85:1179–1192

    Article  Google Scholar 

  • Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339

    Article  CAS  PubMed  Google Scholar 

  • Homeier J, Breckle S, Günter S, Rollenbeck RT, Leuschner C (2010) Tree diversity, forest structure and productivity along altitudinal and topographical gradients in a species-rich Ecuadorian montane rainforest. Biotropica 42:140–148

    Article  Google Scholar 

  • Homeier J, Hertel D, Camenzind T, Cumbicus NL, Maraun M, Martinson GO, Poma LN, Rillig MC, Sandmann D, Scheu S, Veldkamp E, Wilcke W, Wullaert H, Leuschner C (2012) Tropical andean forests are highly susceptible to nutrient inputs—rapid effects of experimental N and P addition to an Ecuadorian montane forest. PLoS One 7(10):e47128 EP

    Google Scholar 

  • Joergensen RG (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the k EC value. Soil Biol Biochem 28:25–31

    Article  CAS  Google Scholar 

  • Joergensen RG, Mueller T (1996) The fumigation-extraction method to estimate soil microbial biomass: calibration of the k EN value. Soil Biol Biochem 28:33–37

    Article  CAS  Google Scholar 

  • Kardol P, Bezemer TM, van der Wal A, van der Putten WH (2005) Successional trajectories of soil nematode and plant communities in a chronosequence of ex-arable lands. Biol Conserv 126:317–327

    Article  Google Scholar 

  • Kingston HM, Jassie LB (1986) Microwave energy for acid decomposition at elevated temperatures and pressures using biological and botanical samples. Anal Chem 58:2534–2541

    Article  CAS  PubMed  Google Scholar 

  • Knops JM, Bradley KL, Wedin DA (2002) Mechanisms of plant species impacts on ecosystem nitrogen cycling. Ecol Lett 5:454–466

    Article  Google Scholar 

  • Kögel-Knabner I (2002) The macromolecular organic composition of plant and microbial residues as inputs to soil organic matter. Soil Biol Biochem 34:139–162

    Article  Google Scholar 

  • Larsen T, Ventura M, O’Brien DM, Magid J, Lomstein BA, Larsen J (2011) Contrasting effects of nitrogen limitation and amino acid imbalance on carbon and nitrogen turnover in three species of Collembola. Knowl Gaps Soil C N Interact 43:749–759

    CAS  Google Scholar 

  • Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415

    Article  CAS  Google Scholar 

  • Lopez-Sangil L, Rousk J, Wallander H, Casals P (2011) Microbial growth rate measurements reveal that land-use abandonment promotes a fungal dominance of SOM decomposition in grazed Mediterranean ecosystems. Biol Fertil Soils 47:129–138

    Article  Google Scholar 

  • Maharning AR, Mills AA, Adl SM (2009) Soil community changes during secondary succession to naturalized grasslands. Appl Soil Ecol 41:137–147

    Article  Google Scholar 

  • Makeschin F, Haubrich F, Abiy M, Burneo JI, Klinger T (2008) Pasture management and natural soil regeneration. In: Beck E, Bendix J, Kottke I, Makeschin F, Mosandl R (eds) Gradients in a tropical mountain ecosystem of Ecuador. Springer, Berlin, pp 397–408

    Chapter  Google Scholar 

  • Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106

    Article  Google Scholar 

  • McGrath DA, Smith CK, Gholz HL, de Assis Oliveira F (2001) Effects of land-use change on soil nutrient dynamics in Amazonia. Ecosystems 4:625–645

    Article  CAS  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C:N:P stoichiometry in forests worldwide:implications of terrestrial Redfield -type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Miltner A, Bombach P, Schmidt-Brücken B, Kästner M (2012) SOM genesis: microbial biomass as a significant source. Biogeochemistry 111:41–55

    Article  CAS  Google Scholar 

  • Moe SJ, Stelzer RS, Forman MR, Harpole WS, Daufresne T, Yoshida T (2005) Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29–39

    Article  Google Scholar 

  • Moore JC, Berlow EL, Coleman DC, de Ruiter PC, Dong Q, Hastings A, Johnson NC, McCann KS, Melville K, Morin PJ, Nadelhoffer K, Rosemond AD, Post DM, Sabo JL, Scow KM, Vanni MJ, Wall DH (2004) Detritus, trophic dynamics and biodiversity. Ecol Lett 7:584–600

    Article  Google Scholar 

  • 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. Glob Change Biol 17:2211–2226

    Article  Google Scholar 

  • Murty D, Kirschbaum MU, McMurtrie RE, Mcgilvray H (2002) Does conversion of forest to agricultural land change soil carbon and nitrogen? A review of the literature. Glob Change Biol 8:105–123

    Article  Google Scholar 

  • Paterson E, Osler G, Dawson LA, Gebbing T, Sim A, Ord B (2008) Labile and recalcitrant plant fractions are utilised by distinct microbial communities in soil: independent of the presence of roots and mycorrhizal fungi. Soil Biol Biochem 40:1103–1113

    Article  CAS  Google Scholar 

  • Potthast K, Hamer U, Makeschin F (2012a) In an Ecuadorian pasture soil the growth of Setaria sphacelata, but not of soil microorganisms, is co-limited by N and P. Appl Soil Ecol 62:103–114

    Article  Google Scholar 

  • Potthast K, Hamer U, Makeschin F (2012b) Land-use change in a tropical mountain rainforest region of southern Ecuador affects soil microorganisms and nutrient cycling. Biogeochemistry 111:151–167

    Article  CAS  Google Scholar 

  • Ratledge C, Wilkinson SG (eds) (1988) Microbial lipids 1. Academic Press Inc., San Diego

    Google Scholar 

  • Rinkes ZL, Weintraub MN, DeForest JL, Moorhead DL (2011) Microbial substrate preference and community dynamics during decomposition of Acer saccharum. Decomposition in forest ecosystems. Fungal Ecol 4:396–407

    Article  Google Scholar 

  • Roos K, Rollenbeck R, Peters T, Bendix J, Beck E (2010) Growth of tropical bracken (Pteridium arachnoideum). Response to weather variations and burning. Invasive Plant Sci Manag 3:402–411

    Article  Google Scholar 

  • Rousk J, Bååth E (2011) Growth of saprotrophic fungi and bacteria in soil. FEMS Microbiol Ecol 78:17–30

    Article  CAS  PubMed  Google Scholar 

  • Ruess L, Schütz K, Migge-Kleian S, Häggblom MM, Kandeler E, Scheu S (2007) Lipid composition of Collembola and their food resources in deciduous forest stands—implications for feeding strategies. Soil Biol Biochem 39:1990–2000

    Article  CAS  Google Scholar 

  • Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78

    Article  CAS  PubMed  Google Scholar 

  • Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569

    Article  CAS  Google Scholar 

  • StatSoft (2010) Statistica for Windows, v 9.1, StatSoft Inc., Tulsa, USA

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry. The biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Stres B, Tiedje JM (2006) New frontiers in soil microbiology: how to link structure and function of microbial communities? In: Nannipieri P, Smalla K (eds) Soil biology. Nucleic acids and proteins in soil. Springer, Berlin, Heidelberg, pp 1–22

    Chapter  Google Scholar 

  • Strickland MS, Rousk J (2010) Considering fungal:bacterial dominance in soils—methods, controls, and ecosystem implications. Soil Biol Biochem 42:1385–1395

    Article  CAS  Google Scholar 

  • Swift MJ, Heal OW, Anderson JM (1979) Decomposition in terrestrial ecosystems. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • ter Braak CJ, Smilauer P (2002) CANOCO reference manual and CanoDraw for Windows user’s guide: software for canonical community ordination, 4th edn. Wageningen, Biometris

    Google Scholar 

  • Throckmorton HM, Bird JA, Dane L, Firestone MK, Horwath WR (2012) The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems. Ecol Lett 15:1257–1265

    Article  PubMed  Google Scholar 

  • Tian H, Chen G, Zhang C, Melillo J, Hall CS (2010) Pattern and variation of C:N: P ratios in China’s soils: a synthesis of observational data. Biogeochemistry 98:139–151

    Article  CAS  Google Scholar 

  • Tischer A, Blagodatskaya E, Hamer U (2014) Extracellular enzyme activities in a tropical mountain rainforest region of southern Ecuador affected by low soil P status and land-use change. Appl Soil Ecol 74:1–11

    Article  Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante MM (2007) Controls over foliar N: P ratios in tropical rain forests. Ecology 88:107–118

    Article  PubMed  Google Scholar 

  • Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19:703–707

    Article  CAS  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Vitousek PM, Fahey T, Johnson DW, Swift MJ (1988) Element interactions in forest ecosystems: succession, allometry and input-output budgets. Biogeochemistry 5:7–34

    Article  CAS  Google Scholar 

  • von Lützow M, Kögel-Knabner I, Ekschmitt K, Flessa H, Guggenberger G, Matzner E, Marschner B (2007) SOM fractionation methods. Relevance to functional pools and to stabilization mechanisms. Soil Biol Biochem 39:2183–2207

    Article  Google Scholar 

  • Walker TW, Adams AF (1958) Studies on soil organic matter: I. Influence of phosphorus content of parent materials on accumulations of carbon, nitrogen, sulfur, and organic phosphorus in grassland soils. Soil Sci 85(6):307–318

    Google Scholar 

  • Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291

    Article  PubMed  Google Scholar 

  • Webster R (2007) Analysis of variance, inference, multiple comparisons and sampling effects in soil research. Eur J Soil Sci 58:74–82

    Article  Google Scholar 

  • Xu X, Thornton PE, Post WM (2013) A global analysis of soil microbial biomass carbon, nitrogen and phosphorus in terrestrial ecosystems. Glob Ecol Biogeogr 22:737–749

    Article  Google Scholar 

  • Zar JH (2010) Biostatistical analysis, 5th edn. Prentice-Hall/Pearson, Upper Saddle River

    Google Scholar 

  • Zelles L (1999) Fatty acid patterns of phospholipids and lipopolysaccharides in the characterisation of microbial communities in soil: a review. Biol Fertil Soils 29:111–129

    Article  CAS  Google Scholar 

  • Zelles L, Bai QY, Rackwitz R, Chadwick D, Beese F (1995) Determination of phospholipid- and lipopolysaccharide-derived fatty acids as an estimate of microbial biomass and community structures in soils. Biol Fertil Soils 19:115–123

    Article  CAS  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Google Scholar 

Download references

Acknowledgments

We thank the two anonymous reviewers for their highly valuable comments which substantially improved the manuscript. The authors gratefully acknowledge the support by the DFG (German Research Foundation), subproject B3.1 within the research Unit 816 “Biodiversity and Sustainable Management of a Megadiverse Mountain Ecosystem in South Ecuador” (HA 4597/1-2). We thank Manuela Unger, Martin Werisch and Guido Ehrlich (TU Dresden) for their assistance in collecting and preparing soil samples for laboratory measurements.

Author information

Authors and Affiliations

  1. Institute of Soil Science and Site Ecology, Dresden University of Technology, Pienner Straße 19, 01737, Tharandt, Germany

    Alexander Tischer, Karin Potthast & Ute Hamer

  2. Institute of Landscape Ecology, WWU, University of Münster, Heisenbergstraße 2, 48149, Münster, Germany

    Ute Hamer

Authors
  1. Alexander Tischer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karin Potthast
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ute Hamer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander Tischer.

Additional information

Communicated by Amy Austin.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tischer, A., Potthast, K. & Hamer, U. Land-use and soil depth affect resource and microbial stoichiometry in a tropical mountain rainforest region of southern Ecuador. Oecologia 175, 375–393 (2014). https://doi.org/10.1007/s00442-014-2894-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-014-2894-x

Keywords

search

Navigation