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Determinants of Soil Bacterial and Fungal Community Composition Toward Carbon-Use Efficiency Across Primary and Secondary Forests in a Costa Rican Conservation Area

  • Katie M. McGee
  • William D. Eaton
  • Shadi Shokralla
  • Mehrdad Hajibabaei
Soil Microbiology

Abstract

Tropical secondary forests currently represent over half of the world’s remaining tropical forests and are critical candidates for maintaining global biodiversity and enhancing potential carbon-use efficiency (CUE) and, thus, carbon sequestration. However, these ecosystems can exhibit multiple successional pathways, which have hindered our understanding of the soil microbial drivers that facilitate improved CUE. To begin to address this, we examined soil % C; % N; C:N ratio; soil microbial biomass C (Cmic); NO3; NH4+; pH; % moisture; % sand, silt, and clay; and elevation, along with soil bacterial and fungal community composition, and determined which soil abiotic properties structure the soil Cmic and the soil bacterial and fungal communities across a primary forest, 33-year-old secondary forest, and 22-year-old young secondary in the Northern Zone of Costa Rica. We provide evidence that soil microbial communities were mostly distinct across the habitat types and that these habitats appear to have affected the soil ectomycorrhizal fungi and the soil microbial groups associated with the degradation of complex carbon compounds. We found that soil Cmic levels increased along the management gradient from young, to old secondary, to primary forest. In addition, the changes in soil Cmic and soil fungal community structure were significantly related to levels of soil NO3. Our analyses showed that even after 33 years of natural forest regrowth, the clearing of tropical forests can have persistent effects on soil microbial communities and that it may take a longer time than we realized for secondary forests to develop carbon-utilization efficiencies similar to that of a primary forest. Our results also indicated that forms of inorganic N may be an important factor in structuring soil Cmic and the soil microbial communities, leading to improved CUE in regenerating secondary forests. This study is the first in the region to highlight some of the factors which appear to be structuring the soil Cmic and soil microbial communities such that they are more conducive for enhanced CUE in secondary forests.

Keywords

Costa Rica Secondary forests DNA metabarcoding DNA metasystematics 16S rRNA ITS rRNA 

Notes

Acknowledgements

We would like to thank Rafal Dobosz for NGS and bioinformatic analyses, Vinzenz and Kurt Schmack, the staff members at the Laguna del Lagarto Lodge, and undergraduate student Olivia Karas for her assistance in the project and processing.

Author Contributions

KMM, MH, and WDE conceived and coordinated the study planning. SS aided in sequencing soil bacterial and fungal amplicons. KMM conducted fieldwork and molecular and bioinformatics analysis and wrote the manuscript. All authors read, edited, and approved the manuscript.

Funding Information

This study was supported by grants from the Government of Canada through Environment and Climate Change Canada and NSERC to MH. This study was also supported by a grant from the National Science Foundation (DBI-1262907); Costa Rican Government Permit #063-2008-SINAC. Supplementary information is available at Microbial Ecology’s website.

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Supplementary material

248_2018_1206_MOESM1_ESM.docx (124 kb)
ESM 1 (DOCX 124 kb)

References

  1. 1.
    Jobbágy EG, Jackson RB (2000) The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol Appl 10:423–436.  https://doi.org/10.2307/2641104 CrossRefGoogle Scholar
  2. 2.
    Nottingham AT, Whitaker J, Turner BL, Salinas N, Zimmermann M, Malhi Y, Meir P (2015) Climate warming and soil carbon in tropical forests: insights from an elevation gradient in the Peruvian Andes. BioScience 65:906–921.  https://doi.org/10.1093/biosci/biv109 PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Beer C, Reichstein M, Tomelleri E, Ciais P (2010) Terrestrial gross carbon dioxide uptake: global distribution and covariation with climate. Science 329:834–838.  https://doi.org/10.1126/science.1192033 PubMedCrossRefGoogle Scholar
  4. 4.
    Gibbs HK, Ruesch AS, Achard F, Clayton MK, Holmgren P, Ramankutty N, Foley JA (2010) Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proc Natl Acad Sci 107:16732–16737.  https://doi.org/10.1073/pnas.0910275107 PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Asner GP, Rudel TK, Aide TM et al (2009) A contemporary assessment of change in humid tropical forests. Conserv Biol 23:1386–1395.  https://doi.org/10.1111/j.1523-1739.2009.01333.x PubMedCrossRefGoogle Scholar
  6. 6.
    Brienen RJW, Phillips OL, Feldpausch TR, Gloor E, Baker TR, Lloyd J, Lopez-Gonzalez G, Monteagudo-Mendoza A, Malhi Y, Lewis SL, Vásquez Martinez R, Alexiades M, Álvarez Dávila E, Alvarez-Loayza P, Andrade A, Aragão LEOC, Araujo-Murakami A, Arets EJMM, Arroyo L, Aymard C. GA, Bánki OS, Baraloto C, Barroso J, Bonal D, Boot RGA, Camargo JLC, Castilho CV, Chama V, Chao KJ, Chave J, Comiskey JA, Cornejo Valverde F, da Costa L, de Oliveira EA, di Fiore A, Erwin TL, Fauset S, Forsthofer M, Galbraith DR, Grahame ES, Groot N, Hérault B, Higuchi N, Honorio Coronado EN, Keeling H, Killeen TJ, Laurance WF, Laurance S, Licona J, Magnussen WE, Marimon BS, Marimon-Junior BH, Mendoza C, Neill DA, Nogueira EM, Núñez P, Pallqui Camacho NC, Parada A, Pardo-Molina G, Peacock J, Peña-Claros M, Pickavance GC, Pitman NCA, Poorter L, Prieto A, Quesada CA, Ramírez F, Ramírez-Angulo H, Restrepo Z, Roopsind A, Rudas A, Salomão RP, Schwarz M, Silva N, Silva-Espejo JE, Silveira M, Stropp J, Talbot J, ter Steege H, Teran-Aguilar J, Terborgh J, Thomas-Caesar R, Toledo M, Torello-Raventos M, Umetsu RK, van der Heijden GMF, van der Hout P, Guimarães Vieira IC, Vieira SA, Vilanova E, Vos VA, Zagt RJ (2015) Long-term decline of the Amazon carbon sink. Nature 519:344–348.  https://doi.org/10.1038/nature14283 PubMedCrossRefGoogle Scholar
  7. 7.
    Rodrigues JLM, Pellizari VH, Mueller R, Baek K, Jesus EC, Paula FS, Mirza B, Hamaoui GS, Tsai SM, Feigl B, Tiedje JM, Bohannan BJM, Nusslein K (2013) Conversion of the Amazon rainforest to agriculture results in biotic homogenization of soil bacterial communities. Proc Natl Acad Sci USA 110:988–993.  https://doi.org/10.1073/pnas.1220608110 PubMedCrossRefGoogle Scholar
  8. 8.
    Loreau M (2010) From populations to ecosystems: theoretical foundations for a new ecological synthesis (MPB-46). Princeton University Press, PrincetonCrossRefGoogle Scholar
  9. 9.
    Fierer N, Grandy AS, Six J, Paul EA (2009) Searching for unifying principles in soil ecology. Soil Biol Biochem 41:2249–2256.  https://doi.org/10.1016/j.soilbio.2009.06.009 CrossRefGoogle Scholar
  10. 10.
    Fierer N, Strickland MS, Liptzin D, Bradford MA, Cleveland CC (2009) Global patterns in belowground communities. Ecol Lett 12:1238–1249.  https://doi.org/10.1111/j.1461-0248.2009.01360.x PubMedCrossRefGoogle Scholar
  11. 11.
    Bradford MA, Crowther TW (2013) Carbon use efficiency and storage in terrestrial ecosystems. New Phytol 199:7–9.  https://doi.org/10.1111/nph.12334 PubMedCrossRefGoogle Scholar
  12. 12.
    Monge GA, Chassot O, Vargas RL (2002) Justificación biológica para el establecimiento del Parque Nacional Maquenque, Costa Rica: Corredor Biológico San Juan-La Selva. Centro Científico Tropical 1–51Google Scholar
  13. 13.
    Chassot O, Monge-Arias G, Powell G, Wright P (2005) Corredor Biológico San Juan-La Selva, Costa Rica: un proyecto del Corredor Biológico Mesoamericano para la protección de la lapa verde y su entorno. Centro Científico Tropical 98 pp.Google Scholar
  14. 14.
    Schelhas J, Sánchez-Azofeifa GA (2006) Post-frontier forest change adjacent to Braulio Carrillo National Park, Costa Rica. Hum Ecol 34:407–431.  https://doi.org/10.1007/s10745-006-9024-2 CrossRefGoogle Scholar
  15. 15.
    Chassot O, Chaves H, Finengan B, Monge G (2010) Dinámica de paisaje en la Zona Norte de Costa Rica: implicaciones para la conservación del bosque tropical muy húmedo. Trop J Environ Sci 39:37–53.  https://doi.org/10.15359/rca.39-1.5 CrossRefGoogle Scholar
  16. 16.
    Chassot O, Monge G (2012) Connectivity conservation of the great green macaw’s landscape in Costa Rica and Nicaragua (1994–2012). Parks 18:1–10Google Scholar
  17. 17.
    Leopold AC, Andrus R, Finkeldey A, Knowles D (2001) Attempting restoration of wet tropical forests in Costa Rica. For Ecol Manag 142:243–249.  https://doi.org/10.1016/S0378-1127(00)00354-6 CrossRefGoogle Scholar
  18. 18.
    Oelbermann M, Paul Voroney R, Gordon AM (2004) Carbon sequestration in tropical and temperate agroforestry systems: a review with examples from Costa Rica and southern Canada. Agric Ecosyst Environ 104:359–377.  https://doi.org/10.1016/j.agee.2004.04.001 CrossRefGoogle Scholar
  19. 19.
    Arroyo-Rodríguez V, Melo FPL, Martínez-Ramos M, Bongers F, Chazdon RL, Meave JA, Norden N, Santos BA, Leal IR, Tabarelli M (2015) Multiple successional pathways in human-modified tropical landscapes: new insights from forest succession, forest fragmentation and landscape ecology research. Biol Rev 92:326–340.  https://doi.org/10.1111/brv.12231 PubMedCrossRefGoogle Scholar
  20. 20.
    Chazdon RL (2003) Tropical forest recovery: legacies of human impact and natural disturbances. Perspect Plant Ecol 6:51–71.  https://doi.org/10.1078/1433-8319-00042 CrossRefGoogle Scholar
  21. 21.
    Chazdon RL, Letcher SG, van Breugel M, Martinez-Ramos M, Bongers F, Finegan B (2007) Rates of change in tree communities of secondary Neotropical forests following major disturbances. Philos Trans R Soc B 362:273–289.  https://doi.org/10.1098/rstb.2006.1990 CrossRefGoogle Scholar
  22. 22.
    Chazdon RL, Broadbent EN, Rozendaal DMA, Bongers F, Zambrano AMA, Aide TM, Balvanera P, Becknell JM, Boukili V, Brancalion PHS, Craven D, Almeida-Cortez JS, Cabral GAL, de Jong B, Denslow JS, Dent DH, DeWalt SJ, Dupuy JM, Duran SM, Espirito-Santo MM, Fandino MC, Cesar RG, Hall JS, Hernandez-Stefanoni JL, Jakovac CC, Junqueira AB, Kennard D, Letcher SG, Lohbeck M, Martinez-Ramos M, Massoca P, Meave JA, Mesquita R, Mora F, Munoz R, Muscarella R, Nunes YRF, Ochoa-Gaona S, Orihuela-Belmonte E, Pena-Claros M, Perez-Garcia EA, Piotto D, Powers JS, Rodriguez-Velazquez J, Romero-Perez IE, Ruiz J, Saldarriaga JG, Sanchez-Azofeifa A, Schwartz NB, Steininger MK, Swenson NG, Uriarte M, van Breugel M, van der Wal H, Veloso MDM, Vester H, Vieira ICG, Bentos TV, Williamson GB, Poorter L (2016) Carbon sequestration potential of second-growth forest regeneration in the Latin American tropics. Sci Adv 2:e1501639–e1501639.  https://doi.org/10.1126/sciadv.1501639 PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Uriarte M, Canham CD, Thompson J, Zimmerman JK, Murphy L, Sabat AM, Fetcher N, Haines BL (2009) Natural disturbance and human land use as determinants of tropical forest dynamics: results from a forest simulator. Ecol Monogr 79:423–443.  https://doi.org/10.1890/08-0707.1 CrossRefGoogle Scholar
  24. 24.
    Guariguata MR, Ostertag R (2001) Neotropical secondary forest succession: changes in structural and functional characteristics. For Ecol Manag 148:185–206.  https://doi.org/10.1016/s0378-1127(00)00535-1 CrossRefGoogle Scholar
  25. 25.
    Powers JS, Haggar JP, Fisher RF (1997) The effect of overstory composition on understory woody regeneration and species richness in 7-year-old plantations in Costa Rica. For Ecol Manag 99:43–54.  https://doi.org/10.1016/S0378-1127(97)00193-X CrossRefGoogle Scholar
  26. 26.
    Holl KD (1999) Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31:229–242.  https://doi.org/10.1111/j.1744-7429.1999.tb00135.x CrossRefGoogle Scholar
  27. 27.
    Reiss J, Bridle JR, Montoya JM, Woodward G (2009) Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol Evol 24:505–514.  https://doi.org/10.1016/j.tree.2009.03.018 PubMedCrossRefGoogle Scholar
  28. 28.
    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.  https://doi.org/10.1016/j.soilbio.2006.08.021 CrossRefGoogle Scholar
  29. 29.
    Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511.  https://doi.org/10.1038/nature13855 PubMedCrossRefGoogle Scholar
  30. 30.
    Kardol P, Wardle DA (2010) How understanding aboveground-belowground linkages can assist restoration ecology. Trends Ecol Evol 25:670–679.  https://doi.org/10.1016/j.tree.2010.09.001 PubMedCrossRefGoogle Scholar
  31. 31.
    Wardle DA, Bardgett RD, Klironomos JN, Setälä H, van der Putten W, Wall DH (2004) Ecological linkages between aboveground and belowground biota. Science 304:1629–1633.  https://doi.org/10.1126/science.1094875 PubMedCrossRefGoogle Scholar
  32. 32.
    Tedersoo L, Bahram M, Cajthaml TAS, Põlme S, Hiiesalu I, Anslan S, Harend H, Buegger F, Pritsch K, Koricheva J, Abarenkov K (2015) Tree diversity and species identity effects on soil fungi, protists and animals are context dependent. ISME J 10:346–362.  https://doi.org/10.1038/ismej.2015.116 PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Guggenberger G, Christensen BT, Zech W (1994) Land-use effects on the composition of organic matter in particle-size separates of soil: I. Lignin and carbohydrate signature. Eur J Soil Sci 45:449–458.  https://doi.org/10.1111/j.1365-2389.1994.tb00530.x CrossRefGoogle Scholar
  34. 34.
    Guggenberger G, Zech W, Thomas RJ (1995) Lignin and carbohydrate alteration in particle-size separates of an oxisol under tropical pastures following native savanna. Soil Biol Biochem 27:1629–1638.  https://doi.org/10.1016/0038-0717(95)00080-X CrossRefGoogle Scholar
  35. 35.
    Guggenberger G, Zech W (1999) Soil organic matter composition under primary forest, pasture, and secondary forest succession, Región Huetar Norte, Costa Rica. For Ecol Manag 124:93–104.  https://doi.org/10.1016/S0378-1127(99)00055-9 CrossRefGoogle Scholar
  36. 36.
    Bradford MA, Keiser AD, Davies CA, Mersmann CA, Strickland MS (2013) Empirical evidence that soil carbon formation from plant inputs is positively related to microbial growth. Biogeochemistry 113:271–281.  https://doi.org/10.1007/s10533-012-9822-0 CrossRefGoogle Scholar
  37. 37.
    Bradford MA, Fierer N, Reynolds JF (2008) Soil carbon stocks in experimental mesocosms are dependent on the rate of labile carbon, nitrogen and phosphorus inputs to soils. Funct Ecol 22:964–974.  https://doi.org/10.1111/j.1365-2435.2008.01404.x CrossRefGoogle Scholar
  38. 38.
    Moscatelli MC, Lagomarsino A, Marinari S, de Angelis P, Grego S (2005) Soil microbial indices as bioindicators of environmental changes in a poplar plantation. Ecol Indic 5:171–179.  https://doi.org/10.1016/j.ecolind.2005.03.002 CrossRefGoogle Scholar
  39. 39.
    Anderson T-H (2003) Microbial eco-physiological indicators to assess soil quality. Agric Ecosyst Environ 98:285–293.  https://doi.org/10.1016/S0167-8809(03)00088-4 CrossRefGoogle Scholar
  40. 40.
    de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811.  https://doi.org/10.1016/j.femsre.2004.11.005 PubMedCrossRefGoogle Scholar
  41. 41.
    van der Wal A, van Veen JA, Smant W, Boschker HTS, Bloem J, Kardol P, van der Putten WH, de Boer W (2006) Fungal biomass development in a chronosequence of land abandonment. Soil Biol Biochem 38:51–60.  https://doi.org/10.1016/j.soilbio.2005.04.017 CrossRefGoogle Scholar
  42. 42.
    Koch AL (2001) Oligotrophs versus copiotrophs. Bioessays 23:657–661.  https://doi.org/10.1002/bies.1091 PubMedCrossRefGoogle Scholar
  43. 43.
    Talbot JM, Allison SD, Treseder KK (2008) Decomposers in disguise: mycorrhizal fungi as regulators of soil C dynamics in ecosystems under global change. Funct Ecol 22:955–963.  https://doi.org/10.1111/j.1365-2435.2008.01402.x CrossRefGoogle Scholar
  44. 44.
    Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404.  https://doi.org/10.1016/j.soilbio.2009.10.014 CrossRefGoogle Scholar
  45. 45.
    Luis P, Walther G, Kellner H, Martin F, Buscot F (2004) Diversity of laccase genes from basidiomycetes in a forest soil. Soil Biol. Biochem. 36:1025–1036.  https://doi.org/10.1016/j.soilbio.2004.02.017 CrossRefGoogle Scholar
  46. 46.
    Smith SE, Read D (2008) Mycorrhizas in ecological interactions. Mycorrhizal symbiosis. Academic, New York, pp 573–611CrossRefGoogle Scholar
  47. 47.
    Jin H, Sun OJ, Liu J (2010) Changes in soil microbial biomass and community structure with addition of contrasting types of plant litter in a semiarid grassland ecosystem. J Plant Ecol 3:209–217.  https://doi.org/10.1093/jpe/rtq001 CrossRefGoogle Scholar
  48. 48.
    Banning NC, Gleeson DB, Grigg AH, Grant CD, Andersen GL, Brodie EL, Murphy DV (2011) Soil microbial community successional patterns during forest ecosystem restoration. Appl Environ Microbiol 77:6158–6164.  https://doi.org/10.1128/aem.00764-11 PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Allison SD, Gartner TB, Mack MC, McGuire K, Treseder K (2010) Nitrogen alters carbon dynamics during early succession in boreal forest. Soil Biol Biochem 42:1157–1164.  https://doi.org/10.1016/j.soilbio.2010.03.026 CrossRefGoogle Scholar
  50. 50.
    Gougoulias C, Clark JM, Shaw LJ (2014) The role of soil microbes in the global carbon cycle: tracking the below-ground microbial processing of plant-derived carbon for manipulating carbon dynamics in agricultural systems. J Sci Food Agric 94:2362–2371.  https://doi.org/10.1002/jsfa.6577 PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Food and Agricultural Organization (FAO) (2010) Global forest resources assessment. Forestry Paper 163:1–378Google Scholar
  52. 52.
    Cove MV, Spínola RM, Jackson VL, Saénz JC (2014) The role of fragmentation and landscape changes in the ecological release of common nest predators in the Neotropics. PeerJ 2:e464.  https://doi.org/10.7717/peerj.464 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Hartshorn GS, Hammel B (1994) Vegetation types and floristic patterns. La Selva: ecology and natural history of a neotropical rain forest. The University of Chicago Press, ChicagoGoogle Scholar
  54. 54.
    van der Gast CJ, Gosling P, Tiwari B, Bending GD (2010) Spatial scaling of arbuscular mycorrhizal fungal diversity is affected by farming practice. Environ Microbiol 13:241–249.  https://doi.org/10.1111/j.1462-2920.2010.02326.x PubMedCrossRefGoogle Scholar
  55. 55.
    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, Fierer N, Knight R (2011) Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci 108:4516–4522.  https://doi.org/10.1073/pnas.1000080107 PubMedCrossRefGoogle Scholar
  56. 56.
    Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118.  https://doi.org/10.1111/j.1365-294X.1993.tb00005.x PubMedCrossRefGoogle Scholar
  57. 57.
    Sundquist A, Bigdeli S, Jalili R, Druzin ML, Waller S, Pullen KM, el-Sayed YY, Taslimi MM, Batzoglou S, Ronaghi M (2007) Bacterial flora-typing with targeted, chip-based pyrosequencing. BMC Microbiol 7:108–111.  https://doi.org/10.1186/1471-2180-7-108 PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis N, Gelfand D, Sninsky J, White T (eds) PCR protocols. Academic, New York, pp 315–322Google Scholar
  59. 59.
    Schmieder R, Edwards R (2011) Quality control and preprocessing of metagenomic datasets. Bioinformatics 27:863–864.  https://doi.org/10.1093/bioinformatics/btr026 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 PubMedCrossRefGoogle Scholar
  61. 61.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267.  https://doi.org/10.1128/AEM.00062-07 PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Zhang Z, Schwartz S, Wagner L, Miller W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214.  https://doi.org/10.1089/10665270050081478 PubMedCrossRefGoogle Scholar
  63. 63.
    Anderson JM, Ingram J (1989) Tropical soil biology and fertility: a handbook of methods2nd edn. CAB International, CambridgeGoogle Scholar
  64. 64.
    Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Elsevier, LondonGoogle Scholar
  65. 65.
    Höper H (2006) Substrate-induced respiration. In: Bloem J, Hopkins DW, Benedetti A (eds) Microbiological methods for assessing soil quality. CAB International, Cambridge, pp 84–92Google Scholar
  66. 66.
    Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial. PRIMER-E Ltd., PlymouthGoogle Scholar
  67. 67.
    Anderson MJ, Gorley RN, Clarke RK (2008) PERMANOVA+ for Primer: guide to software and statistical methods. PRIMER-E Ltd., PlymouthGoogle Scholar
  68. 68.
    Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143.  https://doi.org/10.1111/j.1442-9993.1993.tb00438.x CrossRefGoogle Scholar
  69. 69.
    Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2/fullGoogle Scholar
  70. 70.
    DiStefano J, Fidler F, Cumming G (2005) Effect size estimates and confidence intervals: an alternative focus for the presentation and interpretation of ecological data. New trends in ecology and evolution. Nova Science, New YorkGoogle Scholar
  71. 71.
    Legendre P (2000) Comparison of permutation methods for the partial correlation and partial mantel tests. J Stat Comput Simul 67:37–73.  https://doi.org/10.1080/00949650008812035 CrossRefGoogle Scholar
  72. 72.
    Legendre P, Fortin M-J (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844.  https://doi.org/10.1111/j.1755-0998.2010.02866.x PubMedCrossRefGoogle Scholar
  73. 73.
    Akaike H (1978) A new look at the Bayes procedure. Biometrika 65:53.  https://doi.org/10.2307/2335276 CrossRefGoogle Scholar
  74. 74.
    Burnham KP, Anderson DR (1998) Model selection and multi-model inference: a practical information-theoretical approach, 2nd ed. Model selection and inference 75–117. doi:  https://doi.org/10.1007/978-1-4757-2917-7_3
  75. 75.
    Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307.  https://doi.org/10.1093/biomet/76.2.297 CrossRefGoogle Scholar
  76. 76.
    Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. KTK Scientific Publishers, TokyoGoogle Scholar
  77. 77.
    Sugiura N (1978) Further analysts of the data by Akaike’s information criterion and the finite corrections. Commun Stat Theory Methods A7:13–26.  https://doi.org/10.1080/03610927808827599 CrossRefGoogle Scholar
  78. 78.
    Booth MS, Stark JM, Rastetter E (2005) Controls on nitrogen cycling in terrestrial ecosystems: a synthetic analysis of literature data. Ecol Monogr 75:139–157CrossRefGoogle Scholar
  79. 79.
    Feldpausch TR, Rondon MA, Fernandes ECM, Riha SJ, Wandelli E (2004) Carbon and nutrient accumulation in secondary forests regenerating on pastures in central Amazonia. Ecol Appl 14:164–176.  https://doi.org/10.1890/01-6015 CrossRefGoogle Scholar
  80. 80.
    Gehring C, Vlek PLG, de Souza LAG, Denich M (2005) Biological nitrogen fixation in secondary regrowth and mature rainforest of central Amazonia. Agric Ecosyst Environ 111:237–252.  https://doi.org/10.1016/j.agee.2005.06.009 CrossRefGoogle Scholar
  81. 81.
    Jia G-M, Cao J, Wang C, Wang G (2005) Microbial biomass and nutrients in soil at the different stages of secondary forest succession in Ziwulin, northwest China. For Ecol Manag 217:117–125.  https://doi.org/10.1016/j.foreco.2005.05.055 CrossRefGoogle Scholar
  82. 82.
    Carney KM, Matson PA, Bohannan BJM (2004) Diversity and composition of tropical soil nitrifiers across a plant diversity gradient and among land-use types. Ecol Lett 7:684–694.  https://doi.org/10.1111/j.1461-0248.2004.00628.x CrossRefGoogle Scholar
  83. 83.
    Bossio DA, Girvan MS, Verchot L, Bullimore J, Borelli T, Albrecht A, Scow KM, Ball AS, Pretty JN, Osborn AM (2005) Soil microbial community response to land use change in an agricultural landscape of western Kenya. Microb Ecol 49:50–62.  https://doi.org/10.1007/s00248-003-0209-6 PubMedCrossRefGoogle Scholar
  84. 84.
    Eaton WD, Giles E, Barry D (2010) Microbial community indicators of soil development in tropical secondary forests (Costa Rica). Ecol Restor 28:236–238.  https://doi.org/10.3368/er.28.3.236 CrossRefGoogle Scholar
  85. 85.
    Eaton WD (2011) A comparison of nutrient dynamics and microbial community characteristics across seasons and soil types in two different old growth forests in Costa Rica. Trop Ecol 52:35–48Google Scholar
  86. 86.
    Schwendenmann L, Veldkamp E (2006) Long-term CO2 production from deeply weathered soils of a tropical rain forest: evidence for a potential positive feedback to climate warming. Glob Chang Biol 12:1878–1893.  https://doi.org/10.1111/j.1365-2486.2006.01235.x CrossRefGoogle Scholar
  87. 87.
    da C Jesus E, Marsh TL, Tiedje JM, de S Moreira FM (2009) Changes in land use alter the structure of bacterial communities in western Amazon soils. ISME J 3:1004–1011.  https://doi.org/10.1038/ismej.2009.47 CrossRefGoogle Scholar
  88. 88.
    Lee-Cruz L, Edwards DP, Tripathi BM, Adams JM (2013) Impact of logging and forest conversion to oil palm plantations on soil bacterial communities in Borneo. Appl Environ Microbiol 79:7290–7297.  https://doi.org/10.1128/AEM.02541-13 PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    McGuire KL, D’Angelo H, Brearley FQ et al (2014) Responses of soil fungi to logging and oil palm agriculture in southeast Asian tropical forests. Microb Ecol 69:733–747.  https://doi.org/10.1007/s00248-014-0468-4 PubMedCrossRefGoogle Scholar
  90. 90.
    Rampelotto PH, de Siqueira Ferreira A, Barboza ADM, Roesch LFW (2013) Changes in diversity, abundance, and structure of soil bacterial communities in Brazilian savanna under different land use systems. Microb Ecol 66:593–607.  https://doi.org/10.1007/s00248-013-0235-y PubMedCrossRefGoogle Scholar
  91. 91.
    Tripathi BM, Kim M, Singh D, Lee-Cruz L, Lai-Hoe A, Ainuddin AN, Go R, Rahim RA, Husni MHA, Chun J, Adams JM (2012) Tropical soil bacterial communities in Malaysia: pH dominates in the equatorial tropics too. Microb Ecol 64:474–484.  https://doi.org/10.1007/s00248-012-0028-8 PubMedCrossRefGoogle Scholar
  92. 92.
    Cong J, Yang Y, Liu X, Lu H, Liu X, Zhou J, Li D, Yin H, Ding J, Zhang Y (2015) Analyses of soil microbial community compositions and functional genes reveal potential consequences of natural forest succession. Sci Rep 5:1–11.  https://doi.org/10.1038/srep10007 CrossRefGoogle Scholar
  93. 93.
    Wu YT, Wubet T, Trogisch S, Both S, Scholten T, Bruelheide H, Buscot F (2013) Forest age and plant species composition determine the soil fungal community composition in a Chinese subtropical forest. PLoS One 8:e66829–e66812.  https://doi.org/10.1371/journal.pone.0066829 PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Malik AA, Thomson BC, Whiteley AS et al (2017) Bacterial physiological adaptations to contrasting edaphic conditions identified using landscape scale metagenomics. mBio 8:e00799–e17–13.  https://doi.org/10.1128/mBio.00799-17 PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Asina F, Brzonova I, Voeller K, Kozliak E, Kubátová A, Yao B, Ji Y (2016) Biodegradation of lignin by fungi, bacteria and laccases. Bioresour Technol 220:414–424.  https://doi.org/10.1016/j.biortech.2016.08.016 PubMedCrossRefGoogle Scholar
  96. 96.
    de Gonzalo G, Colpa DI, Habib MHM, Fraaije MW (2016) Bacterial enzymes involved in lignin degradation. J Biotechnol 236:110–119.  https://doi.org/10.1016/j.jbiotec.2016.08.011 PubMedCrossRefGoogle Scholar
  97. 97.
    Wang L, Nie Y, Tang Y-Q, Song XM, Cao K, Sun LZ, Wang ZJ, Wu XL (2016) Diverse bacteria with lignin degrading potentials isolated from two ranks of coal. Front Microbiol 7:1609–1614.  https://doi.org/10.3389/fmicb.2016.01428 CrossRefGoogle Scholar
  98. 98.
    Zimmermann W (1990) Degradation of lignin by bacteria. J Biotechnol 13:119–130.  https://doi.org/10.1016/0168-1656(90)90098-V CrossRefGoogle Scholar
  99. 99.
    Wohl DL, McArthur JV (1998) Actinomycete-flora associated with submersed freshwater macrophytes. FEMS Microbiol Ecol 26:135–140.  https://doi.org/10.1111/j.1574-6941.1998.tb00499.x CrossRefGoogle Scholar
  100. 100.
    Smith AP, Marín-Spiotta E, de Graaff MA, Balser TC (2014) Microbial community structure varies across soil organic matter aggregate pools during tropical land cover change. Soil Biol Biochem 77:292–303.  https://doi.org/10.1016/j.soilbio.2014.05.030 CrossRefGoogle Scholar
  101. 101.
    Quirós-Brenes KG (2002) Composicíon florística y estructural para el bosque primario del hotel La Laguna del Lagarto Lodge, Boca Tapada de Pital, San Carlos, Alajuela, Costa Rica. 1–91Google Scholar
  102. 102.
    McNulty C, Barry D (2009) Tropical rainforest stand dynamics, species composition, growth, and mortality at Laguna del Lagarto, Costa Rica. Mesoamericana 13:23–33Google Scholar
  103. 103.
    Seitzman BH, Ouimette A, Mixon RL, Hobbie EA, Hibbett DS (2017) Conservation of biotrophy in Hygrophoraceae inferred from combined stable isotope and phylogenetic analyses. Mycologia 103:280–290.  https://doi.org/10.3852/10-195 CrossRefGoogle Scholar
  104. 104.
    Smith ME, Henkel TW, Catherine Aime M, Fremier AK, Vilgalys R (2011) Ectomycorrhizal fungal diversity and community structure on three co-occurring leguminous canopy tree species in a Neotropical rainforest. New Phytol 192:699–712.  https://doi.org/10.1111/j.1469-8137.2011.03844.x PubMedCrossRefGoogle Scholar
  105. 105.
    Dokmai P, Phorsi C, Khangrang R, Suwannasai N (2015) Above- and below-ground ectomycorrhizal diversity in a pine- oak forest in northeastern Thailand. Chiang Mai J Sci 42:80–88Google Scholar
  106. 106.
    Tang AMC, Jeewon R, Hyde KD (2009) A re-evaluation of the evolutionary relationships within the Xylariaceae based on ribosomal and protein-coding gene sequences. Fungal Divers 34:127–155Google Scholar
  107. 107.
    Liers C, Arnstadt T, Ullrich R, Hofrichter M (2011) Patterns of lignin degradation and oxidative enzyme secretion by different wood- and litter-colonizing basidiomycetes and ascomycetes grown on beech-wood. FEMS Microbiol Ecol 78:91–102.  https://doi.org/10.1111/j.1574-6941.2011.01144.x PubMedCrossRefGoogle Scholar
  108. 108.
    Cannon PF, Kirk PM (2007) Fungal families of the world. CAB International, Cambridge 456 pCrossRefGoogle Scholar
  109. 109.
    O’Donnell KL (1979) Zygomycetes in culture. Dept. of Botany, University of Georgia. 257 pGoogle Scholar
  110. 110.
    Lavelle P, Spain A (2005) Soil ecology, 2nd ed. Kluwer Academic, Dordrecht 654 p Google Scholar
  111. 111.
    Twieg BD, Durall DM, Simard SW (2007) Ectomycorrhizal fungal succession in mixed temperate forests. New Phytol 176:437–447.  https://doi.org/10.1111/j.1469-8137.2007.02173.x PubMedCrossRefGoogle Scholar
  112. 112.
    Berg B (2000) Litter decomposition and organic matter turnover in northern forest soils. For Ecol Manag 133:13–22.  https://doi.org/10.1016/s0378-1127(99)00294-7 CrossRefGoogle Scholar
  113. 113.
    DeForest JL, Zak DR, Pregitzer KS, Burton AJ (2004) Atmospheric nitrate deposition, microbial community composition, and enzyme activity in northern hardwood forests. Soil Sci Soc Am J 68:132–138.  https://doi.org/10.2136/sssaj2004.1320 CrossRefGoogle Scholar
  114. 114.
    de Vries FT, Bloem J, van Eekeren N, Brusaard L, Hoffland E (2007) Fungal biomass in pastures increases with age and reduced N input. Soil Biol Biochem 39:1620–1630.  https://doi.org/10.1016/j.soilbio.2007.01.013 CrossRefGoogle Scholar
  115. 115.
    Knorr M, Frey SD, Curtis PS (2005) Nitrogen additions and litter decomposition: a meta-analysis. Ecology 86:3252–3257.  https://doi.org/10.1890/05-0150 CrossRefGoogle Scholar
  116. 116.
    Hobbie SE (2008) Nitrogen effects on decomposition: a five-year experiment in eight temperate sites. Ecology 89:2633–2644PubMedCrossRefGoogle Scholar
  117. 117.
    Sinsabaugh RL, Carreiro MM, Repert DA (2002) Allocation of extracellular enzymatic activity in relation to litter composition, N deposition, and mass loss. Biogeochemistry 60:1–24.  https://doi.org/10.1023/A:1016541114786 CrossRefGoogle Scholar
  118. 118.
    Sinsabaugh RL, Zak DR, Gallo M, Lauber C, Amonette R (2004) Nitrogen deposition and dissolved organic carbon production in northern temperate forests. Soil Biol Biochem 36:1509–1515.  https://doi.org/10.1016/j.soilbio.2004.04.026 CrossRefGoogle Scholar
  119. 119.
    Sait M, Davis KE, Janssen PH (2006) Effect of pH on isolation and distribution of members of subdivision 1 of the phylum Acidobacteria occurring in soil. Appl Environ Microbiol 72:1852–1857.  https://doi.org/10.1128/AEM.72.3.1852-1857.2006 PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    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.  https://doi.org/10.1016/j.soilbio.2008.05.021 CrossRefGoogle Scholar
  121. 121.
    Högberg MN, Högberg P, Myrold DD (2006) Is microbial community composition in boreal forest soils determined by pH, C-to-N ratio, the trees, or all three? Oecologia 150:590–601.  https://doi.org/10.1007/s00442-006-0562-5 PubMedCrossRefGoogle Scholar
  122. 122.
    Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental climate change drivers. Appl Environ Microbiol 76:999–1007.  https://doi.org/10.1128/AEM.02874-09 PubMedCrossRefGoogle Scholar
  123. 123.
    Freedman Z, Zak DR (2015) Soil bacterial communities are shaped by temporal and environmental filtering: evidence from a long-term chronosequence. Environ Microbiol 17:3208–3218.  https://doi.org/10.1111/1462-2920.12762 PubMedCrossRefGoogle Scholar
  124. 124.
    Cline LC, Zak DR (2013) Dispersal limitation structures fungal community assembly in a long-term glacial chronosequence. Environ Microbiol 16:1538–1548.  https://doi.org/10.1111/1462-2920.12281 PubMedCrossRefGoogle Scholar
  125. 125.
    Cline LC, Zak DR (2015) Soil microbial communities are shaped by plant-driven changes in resource availability during secondary succession. Ecology 96:3374–3385.  https://doi.org/10.1890/15-0184.1 PubMedCrossRefGoogle Scholar
  126. 126.
    Shebitz DJ, Eaton W (2013) Forest structure, nutrients, and Pentaclethra macroloba growth after deforestation of Costa Rican lowland forests. ISRN Ecol 2013:1–10.  https://doi.org/10.1155/2013/414357 CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Centre for Biodiversity Genomics at Biodiversity Institute of Ontario and Department of Integrative BiologyUniversity of GuelphGuelphCanada
  2. 2.Department of BiologyPace UniversityNew YorkUSA

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