Published Dec 13, 2018



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Esteban Tulande-M http://orcid.org/0000-0001-7754-9518

Jose Ignacio Barrera-Cataño

Carlos Eduardo Alonso-Malaver http://orcid.org/0000-0003-4879-835X

Sofia Basto http://orcid.org/0000-0003-3214-8133

Carlos Morantes-Ariza

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Abstract

In Andean high montane areas, the establishment of exotic tree forests changes the soil dynamics and its biodiversity. Soil macrofauna act as indicators of ecosystem successional processes, and may have an important role in ecological restoration processes after clear cutting exotic tree plantations. The aim of the present study was to understand how soil macrofaunal assemblies change in areas with different ages post clear cutting of Pinus patula, and to identify the soil physico-chemical variables that better explain these variations. The macrofauna in a high montane forest was evaluated along with that of three areas with different ages post clearcutting: 0, 2.5, and 5 years after clearcutting (Yac). The effect of soil physico chemical variables on macrofauna abundance was also evaluated. Macrofauna composition changed after clearcutting. Macrofauna abundance, richness, and diversity were lower in the 0 Yac area than in the other areas. Moreover, the macrofuna similarity to the reference forest did not increase with the years after clearcutting. This is due to the changes in soil characteristics, triggered by clearcutting. Slope, temperature, bulk density, real density, loam, pH, P, Na and K were the soil variales with a positive effect on the macrofauna abundance. These physico-chemical variables should be considered when designing restoration plans for Andean forest ecosystems. Moreover, Diplopoda, Coleoptera and Chilopoda might be useful to monitor and evaluate restoration processes after Pinus spp. clearcutting, because of their high abundance, diversity and relationship with environmental conditions.

Keywords

soil macrofauna, Andes, montane forest, restoration ecology

References
[1] Richter M. Tropical mountain forests – distribution and general features, in: Gradstein J. Homeier, D. Gansert, Göttingen, The tropical mountain forest: patterns and procces in a biodiversity hotspot Georg-August Universität, 2008.

[2] Armenteras D, Rodríguez N, Retana J, Morales M. Understanding deforestation in montane and lowland forests of the Colombian Andes, Regional Environmental Change, 11: 693-705, 2011.
doi: 10.1007/s10113-010-0200-y

[3] Allan E, Weisser WW, Fischer M, Schulze ED, Weigelt A, Roscher C, Baade J, Barnard RL, Beßler H, Buchmann N, Ebeling A, Eisenhauer N, Engels C, Fergus AJF, Gleixner G, Gubsch M, Halle S, Klein AM, Kertscher I, Kuu A, Lange M, Le Roux X, Meyer ST, Migunova VD, Milcu A, Niklaus PA, Oelmann Y, Pašalić E, Petermann JS, Poly F, Rottstock T, Sabais ACW, Scherber C, Scherer-Lorenzen M, Scheu S, Steinbeiss S, Schwichtenberg G, Temperton V, Tscharntke T, Voigt W, Wilcke W, Wirth C, Schmid B. A comparison of the strength of biodiversity effects across
multiple functions, Oecologia, 173: 223-237, 2013.
doi: 10.1007/s00442-012-2589-0

[4] Balthazar V, Vanacker V, Molina A, Lambin EF. Impacts of forest cover change on ecosystem services in high Andean mountains, Ecological Indicators, 48: 63-75, 2015.
doi: 10.1016/j.ecolind.2014.07.043

[5] Rodríguez N, Armenteras D, Retana J. National ecosystems services priorities for planning carbon and water resource management in Colombia, Land Use Policy, 42: 609-618, 2015.
doi: 10.1016/j.landusepol.2014.09.013

[6] Echeverría C, Smith-Ramírez C, Aronson J, Barrera-Cataño JI. Good news from Latin America and the Caribbean: national and international restoration networks are moving ahead, Restoration Ecology, 23: 1-3, 2015.
doi: 10.1111/rec.12174

[7] Lal R. Soil Carbon Sequestration Impacts on Global Climate Change and Food Security, Science, 304: 1623-162, 2004.
doi: 10.1126/science.1097396

[8] Armenteras D, Cabrera E, Rodríguez N, Retana J. National and regional determinants of tropical deforestation in Colombia, Regional Environmental Change, 13: 1181-1193, 2013.
doi: 10.1007/s10113-013-0433-7

[9] Cavelier J, Santos C. Efectos de plantaciones abandonadas de especies exóticas y nativas sobre la regeneración natural de un bosque montano en Colombia, Revista de Biología Tropical, 47: 775-784, 1999.

[10] Endo M. CAMCORE: Twelve years of contribution to reforestation in the Andean region of Colombia, Forest Ecology and Management, 63: 219-233, 1994.
doi: 10.1016/0378-1127(94)90112-0

[11] Ponge JF. Plant-soil feedbacks mediated by humus forms: A review, Soil Biology and Biochemistry, 57: 1048-1060, 2013.
doi: 10.1016/j.soilbio.2012.07.019

[12] Zanella A, Jabiol B, Ponge JF, Sartori G, De Waal R, Van Delft B, Graefe U, Cools N, Katzensteiner K, Hager H, Englisch M. A European morpho-functional classification of humus forms, Geoderma, 164: 138-145, 2011.
doi: 10.1016/j.geoderma.2011.05.016

[13] Ponge J, Zanella A, Sartori G, Jabiol B. Terrestrial humus forms: ecological relevance and classification, European Atlas of Soil Biodiversity, European Union, 14-15, 2010.
doi: 10.13140/RG.2.1.3713.5521

[14] Ponge JF. Humus forms in terrestrial ecosystems: A framework to biodiversity, Soil Biology and Biochemistry, 35: 935-945, 2003.
doi: 10.1016/S0038-0717(03)00149-4

[15] Cavelier J, Tobler A. The effect of abandoned plantations of Pinus patula and Cupressus lusitanica on soils and regeneration of a tropical montane rain forest in Colombia, Biodiversity and Conservation, 7: 335-347, 1998.
doi: 10.1023/A:1008829728564

[16] Loaiza-Usuga JC, León-Peláez JD, González-Hernández MI, Gallardo-Lancho JF, Osorio-Vega W, Correa-Londoño G. Alterations in litter decomposition patterns in tropical montane forests of Colombia: a comparison of oak forests and coniferous plantations, Canadian Journal of Forest Research, 43: 528-533, 2013.
doi: 10.1139/cjfr-2012-0438

[17] Ramírez JA, León-Peláez JD, Craven D, Herrera DA, Zapata CM, González-Hernández MI, Gallardo-Lancho J, Osorio W. Effects on nutrient cycling of conifer restoration in a degraded tropical montane forest, Plant and Soil, 378: 215-226, 2014.
doi: 10.1007/s11104-014-2024-x

[18] León JD, González MI, Gallardo JF. Ciclos biogeoquímicos en bosques naturales y plantaciones de coníferas en ecosistemas de alta montaña de Colombia, Revista de Biologia Tropical, 59: 1883- 1894, 2011.

[19] Vera M, Sierra M, Díez M, Sierra C, Martínez A, Martínez FJ, Aguilar J. Deforestation and land use effects on micromorphological and fertility changes in acidic rainforest soils in Venezuelan Andes, Soil and Tillage Research, 97: 184-194, 2007.
doi: 10.1016/j.still.2007.09.015

[20] Eclesia RP, Jobbagy EG, Jackson RB, Biganzoli F, Piñeiro G. Shifts in soil organic carbon for plantation and pasture establishment in native forests and grasslands of South America, Global Change Biology, 18: 3237-3251, 2012.
doi: 10.1111/j.1365-2486.2012.02761.x

[21] Drewnik M. The effect of environmental conditions on the decomposition rate of cellulose in mountain soils, Geoderma, 132: 116-130, 2006.
doi: 10.1016/j.geoderma.2005.04.023

[22] Goebel MO, Bachmann J, Woche SK, Fischer WR. Soil wettability, aggregate stability, and the decomposition of soil organic matter, Geoderma, 128: 80-93, 2005.
doi: 10.1016/j.geoderma.2004.12.016

[23] Couteaux M, Sarmiento L, Bottner P, Acevedo D, Thiery J. Decomposition of standar plant material along an altitudinal transect (65 - 3964 m) in the tropical andes, Soil Biology and Biochemistry, 34: 69-78, 2002.

[24] Haynes RJ. Nature of the Belowground Ecosystem and Its Development during Pedogenesis, in: Advances in Agronomy, Elsevier, 2014: pp. 43-109.
doi: 10.1016/B978-0-12-800131-8.00002-9

[25] Bardgett RD. The biology of soil: a community and ecosystem approach, Oxford university press, New York USA 2005.
doi: 10.1093/acprof:oso/9780198525035.001.0001

[26] Handa IT, Aerts R, Berendse F, Berg MP, Bruder A, Butenschoen O, Chauvet E, Gessner MO, Jabiol J, Makkonen M, McKie BG, Malmqvist B, Peeters ETHM, Scheu S, Schmid B, Van Ruijven J, Vos VCA, Hättenschwiler S. Consequences of biodiversity loss for litter decomposition across biomes, Nature, 509: 218-21, 2014.
doi: 10.1038/nature13247

[27] Brose U, Scheu S. Into darkness: unravelling the structure of soil food webs, Oikos, 123: 1153-1156, 2014.
doi: 10.1111/oik.01768

[28] Wardle DA, Yeates GW, Barker GM, Bonner KI. The influence of plant litter diversity on decomposer abundance and diversity, Soil Biology and Biochemistry, 38: 1052-1062, 2006.
doi: 10.1016/j.soilbio.2005.09.003

[29] Lavelle P. Faunal activities and soil processes: adaptative strategy that determine ecosystem function, 27: 93-132,1997.
doi: 10.1016/S0065-2504(08)60007-0

[30] Wickings K, Grandy AS, Reed SC, Cleveland CC. The origin of litter chemical complexity during decomposition, Ecology Letters, 15: 1180-1188, 2012.
doi: 10.1111/j.1461-0248.2012.01837.x

[31] Wickings K, Grandy AS. Management intensity interacts with litter chemistry and climate to drive temporal patterns in arthropod communities during decomposition, Pedobiologia, 56: 105-112, 2013.
doi: 10.1016/j.pedobi.2013.01.001

[32] Wickings K, Grandy AS, Reed S, Cleveland C. Management intensity alters decomposition via biological pathways, Biogeochemistry, 104: 365-379, 2011.
doi: 10.1007/s10533-010-9510-x

[33] Kibblewhite MG, Ritz K, Swift MJ. Soil health in agricultural systems. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 363: 685-701, 2008.
doi: 10.1098/rstb.2007.2178

[34] Moreira FM. Manual de biología de suelos tropicales, Earthscan, Coyoacan Mexico 2012.

[35] Wall DH, Bardgett RD, Behan-Pelletier V, Herrick JE, Jones TH, Six J, Strong DR. Soil ecology and ecosystem services, Oxford, New York USA 2012.

[36] Wardle DA. Communities and ecosystems-linking the aboveground and belowground components. Princeton University, New Jersey, USA 2002.

[37] De Deyn GB, Van Ruijven J, Raaijmakers CE, De Ruiter PC, Van Der Putten WH. Above and belowground insect herbivores differentially affect soil nematode communities in species-rich plant communities, Oikos, 116: 923-930, 2007.
doi: 10.1111/j.2007.0030-1299.15761x

[38] Carbajo V, den Braber B, van der Putten WH, De Deyn GB. Enhancement of late successional plants on ex arable land by soil inoculations, PLoS ONE, 6: 2011.
doi: 10.1371/journal.pone.0021943

[39] De Deyn GB, Raaijmakers CE, Zoomer HR, Berg MP, De Ruiter PC, Verhoef HA, Bezemer TM, Van der Putten WH. Soil invertebrate fauna enhances grassland succession and diversity, Nature, 422: 711-713, 2003.
doi: 10.1038/nature01548

[40] Rousseau L, Fonte SJ, Téllez O, van der Hoek R, Lavelle P. Soil macrofauna as indicators of soil quality and land use impacts in smallholder agroecosystems of western Nicaragua, Ecological Indicators, 27: 71-82, 2013.
doi: 10.1016/j.ecolind.2012.11.020

[41] Cluzeau D, Guernion M, Chaussod R, Martin-Laurent F, Villenave C, Cortet J, Ruiz-Camacho N, Pernin C, Mateille T, Philippot L, Bellido A, Rougé L, Arrouays D, Bispo A, Pérès G. Integration of biodiversity in soil quality monitoring: Baselines for microbial and soil fauna parameters for different land-use types, European Journal of Soil Biology, 49: 63-72, 2012.
doi: 10.1016/j.ejsobi.2011.11.003

[42] Paquin P, Coderre D. Deforestation and fire impact on edaphic insect larvae and other macroarthropods, Environmental Entomology, 26: 21-30, 1997.

[43] Hedlund K, Griffiths B, Christensen S, Scheu S, Setälä H, Tscharntke T, Verhoef H. Trophic interactions in changing landscapes: Responses of soil food webs, Basic and Applied Ecology, 5: 495-503, 2004.
doi: 10.1016/j.baae.2004.09.002

[44] Frouz J, Prach K, Pižl V, Háněl L, Starý J, Tajovský K, Materna J, Balík V, Kalčík J, Řehounková K. Interactions between soil development, vegetation and soil fauna during spontaneous succession in post mining sites, European Journal of Soil Biology, 44: 109-121, 2008.
doi: 10.1016/j.ejsobi.2007.09.002

[45] Frouz J, Thébault E, Pižl V, Adl S, Cajthaml T, Baldrián P, Háněl L, Starý J, Tajovský K, Materna J, Nováková A, De Ruiter PC. Soil Food Web Changes during Spontaneous Succession at Post Mining Sites: A Possible Ecosystem Engineering Effect on Food Web Organization?, PLoS ONE, 8: e79694, 2013.
doi: 10.1371/journal.pone.0079694

[46] Meloni F, Varanda EM. Litter and soil arthropod colonization in reforested semi-deciduous seasonal Atlantic forests, Restoration Ecology, 23: 690-697, 2015.
doi: 10.1111/rec.12236

[47] Van der Putten WH, Bardgett RD, de Ruiter PC, Hol WHG, Meyer KM, Bezemer TM, Bradford MA, Christensen S, Eppinga MB, Fukami T, Hemerik L, Molofsky J, Schädler M, Scherber C, Strauss SY, Vos M, Wardle DA. Empirical and theoretical challenges in aboveground–belowground ecology, Oecologia, 161: 1-14, 2009.
doi: 10.1007/s00442-009-1351-8

[48] Kostenko O, van de Voorde TFJ, Mulder PPJ, Van der Putten WH, Martijn Bezemer T. Legacy effects of abovegroundbelowground interactions, Ecology Letters, 15: 813-821, 2012.
doi: 10.1111/j.1461-0248.2012.01801.x

[49] Kardol P, Wardle DA. How understanding abovegroundbelowground linkages can assist restoration ecology, Trends in Ecology and Evolution, 25: 670-679, 2010.
doi: 10.1016/j.tree.2010.09.001

[50] Stanturf JA, Palik BJ, Dumroese RK. Contemporary forest restoration: A review emphasizing function, Forest Ecology and Management, 331: 292-323, 2014.
doi: 10.1016/j.foreco.2014.07.029

[51] Camero É, Diaz JE, Salinas A. Estudio de la artropofauna asociada a suelos de dos tipos de ecosistemas en la cuenca del río Cauca - Colombia, Acta Biologica Colombiana, 10: 35-44, 2005.

[52] Ruiz-Cobo HD, Feijoo A, Rodriguez C, Comunidades de macroinvertebrados edáficos en diferentes sistemas de uso del terreno en la cuenca del río Otún - Colombia, Acta Zoologica Mexicana, Numero esp: 165-178, 2010.

[53] Kattan GH, Correa D, Escobar F, Medina C. Leaf-litter arthropods in restored forests in the Colombian Andes: A comparison between secondary forest and tree plantations, Restoration Ecology, 14: 95-102, 2006.
doi: 10.1111/j.1526-100X.2006.00109.x

[54] Cerón P, Montenegro S, Noguera E. Macrofauna en suelos de Bosque y Pajonal de la reserva natural Pueblo Viejo, Nariño, Colombia, Revista de la Academia Colombiana de Ciencias Exactas, Físicas y Naturales, 32: 447-453, 2008.

[55] Feijoo A, Quintero H, Fragoso CE. Earthworm communities in forest and pastures of the Colombian Andes, Caribbean Journal of Science, 42: 301-310, 2006.

[56] Feijoo A, Lavelle P. Relationships between land use and the earthworm communities in the basin of La Vieja river , Colombia, Pastos y Forrajes, 30: 235-249, 2015.

[57] Feijoo A, Carvajal AF, Zúñiga MC, Quintero H, Fragoso C. Diversity and abundance of earthworms in land use systems in central-western Colombia, Pedobiologia, 54: S69-S75, 2011.
doi: 10.1016/j.pedobi.2011.09.016

[58] Feijoo AM, Knapp EB, Lavelle P, Moreno AG. Quantifying soil macrofauna in a Colombian watershed, Pedobiologia, 43: 513-517, 1999.

[59] León-gamboa AL, Ramos C, García MR. Efecto de plantaciones de pino en la artropofauna del suelo de un bosque Altoandino, Revista de Biologia Tropical, 58: 1031-1048, 2010.

[60] USDA. Soil Taxonomy, Geological Magazine, 114: 492, 1999.
doi: 10.1017/S0016756800045489

[61] Bockheim JG, Gennadiyev AN, Hartemink AE, Brevik EC. Soil-forming factors and Soil Taxonomy, Geoderma, 226-227: 231- 237, 2014.

[62] Kotschwar A. Plan de manejo de la Cuenca del embalse de Neusa. Corporación auntónoma de la Sabana de Bogotá y de los Valles de Ubaté y Chiquinquirá. Bogotá, Colombia, 1980.

[63] Anderson J, Ingram J. Tropical Soil Biology and Fertility: A Handbook of Methods, Oxfordshire: CAB international, United Kingdom, 1993.

[64] Adis J, ed. Amazonian Arachnida and Myriapoda, Pensoft Publishers, Sofia-Moscow, 2002.

[65] Golovatch S, Wytwer J. The South American Millipede Genus Phaneromerium Verhoeff, 1941. With the Description of a New Cavernicolousspecies From Brazil (Diplopoda: Polydesmida: Fuhrmannodesmidae), Annales Zoologici (Warzawa), 54: 511-514, 2004.

[66] Schileyko A. A new species of Newportia Gervais, 1847 from Puerto Rico, with a revised key to the species of the genus (Chilopoda, Scolopendromorpha, Scolopocryptopidae), Zookeys, 276: 39-54, 2013.
doi: 10.3897/zookeys.276.4876

[67] Pereira LA. A new schendylid centipede (Myriapoda: Chilopoda: Geophilomorpha) from the Bolivian Amazon Forest, Zootaxa, 3905: 1-26, 2015.
doi: 10.11646/zootaxa.3905.1.1

[68] Guzmán De Tomé ME. Clave de las especies de Conoderus Grupo II (Coleoptera: Elateridae), Revista de la Sociedad Entomológica de Argentina, 64: 119-129, 2005.

[69] Carl J. Diplopoden von columbien, Mémoires de la Société des Sciences Naturelles de Neuchâtel, 821-993, 1914.

[70] Arnett Jr. R, Thomas M, Skelley P, Frank J. American Beetles, Vol. 2: Polyphaga: Scarabaeoidea through Curculionoidea, CRC Press, Boca Raton, USA, 2002.

[71] Carvazos T. Manual de prácticas de física de suelos, Trillas, Mexico D.F, 1992.

[72] IGAC, Suelos de Colombia, IGAC, Bogota D.C., Colombia, n.d.

[73] Flint A, Flint L. Particle density, in: D. Dane, G. Topp (Eds.), Methods Soil Anal. Part 4. Physical. Minearological
Methods, 2nd edition, American society of agronomy and soil science society of America, Madison, Wisconsin, USA, pp. 235-240, 2002.

[74] Blake G, Hartge K. Particle-size analysis, in: L. Page, R. Miller, D. Keeney (Eds.), Methods Soil Anal. Part 1 Phys. Minearological Methods, second, American society of agronomy and soil science society of America, Madison, Wisconsin, USA, 1997.

[75] Sheldric B, Wang C. Particle size distribution, in: M. Carter (Ed.), Soil Sampling. Methods Analisys. Lewis publisher, Boca Raton, USA, 499-511, 1993.

[76] Codazzi IGA. Métodos analíticos del laboratorio de suelos, sexta edic, Imprenta Nacional de Colombia, Bogota D.C., Colombia, 2006.

[77] Walkley A, Black IA. An examination f the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method, Soil Science, 37: 29-38, 1934.
doi: 10.1097/00010694-193401000-00003

[78] Hendershot W, Lalande H, Duquette M. Ion exchange and exchangeable cations, in: M. Carter (Ed.), Soil Sampl. Methods Anal, Lewis publisher, Boca Raton, USA, 162-177, 1993.

[79] Dufrene M, Legendre P. Species Assemblages and Indicator Species: the need for a flexible asymetrical approach, Ecological Monographs, 67: 345-366, 1997.

[80] Roberts DW. Ordination and Multivariate Analysis for Ecology, 21-51, 2016.

[81] R Development Core Team, R: A language and environment for statistical computing, R Foundation for Statistical Computing, Vienna, Austria, 2016.

[82] McArdle BH, Anderson MJ. Fitting multivariate models to community data: A comment on distance-based redundancy analysis, Ecology, 2001.
doi: 10.1890/0012-9658(2001)082[0290:FMMTCD]2.0.CO;2

[83] Kindt R, Coe R. Tree diversity analysis, 2005.
doi: 10.1198/tas.2008.s264

[84] Warton DI. Many zeros does not mean zero inflation: Comparing the goodness-of-fit of parametric models to multivariate abundance data, Environmetrics, 2005.
doi: 10.1002/env.702

[85] Wang Y, Naumann U, Wright ST, Warton DI. Package “mvabund”: Statistical methods for analysing multivariate abundance data, 2013.

[86] Imdadullah M, Aslam M, Altaf S. mctest: An {R} Package for Detection of Collinearity Among Regressors, R J. 2016.

[87] Villani MG, Allee LL, Díaz A, Robbins PS. Adaptive strategies of edaphic arthropods, Annual Review of Entomology, 44: 233-256, 1999.
doi: 10.1146/annurev.ento.44.1.233

[88] Schowalter TD. Insect Responses to Major Landscape-Level Disturbance, Annual Review of Entomology, 57: 1-20, 2012.
doi: 10.1146/annurev-ento-120710-100610

[89] Neita-Moreno JC, Morón MA. Estados inmaduros de Ancognatha ustulata (Coleoptera: Melolonthidae: Dynastinae: Cyclocephalini), Revista Mexicana de Biodiversidad, 79: 355-361, 2008.

[90] Kalinkat G, Jochum M, Brose U, Dell AI. Body size and the behavioral ecology of insects: linking individuals to ecological communities, Current Opinion in Insect Science, 9: 24-30, 2015.
doi: 10.1016/j.cois.2015.04.017

[91] Heikkala O, Seibold S, Koivula M, Martikainen P, Müller J, Thorn S, Kouki J. Retention forestry and prescribed burning result in functionally different saproxylic beetle assemblages than clear-cutting, Forest, Ecology and. Management, 359: 51-58, 2016.
doi: 10.1016/j.foreco.2015.09.043

[92] Ponge JF. Succession of fungi and fauna during decomposition of needles in a small area of Scots pine litter, Plant and Soil. 138: 99-113, 1991.
doi: 10.1007/BF00011812

[93] Hättenschwiler S, Tiunov AV, Scheu S. Biodiversity and Litter Decomposition in Terrestrial Ecosystems, Annual Review of Ecology, Evolution and Systematics, 36: 191-218, 2005.
doi: 10.1146/annurev.ecolsys.36.112904.151932

[94] Bormann BT, Darbyshire RL, Homann PS, Morrissette BA, Little SN. Managing early succession for biodiversity and longterm productivity of conifer forests in southwestern Oregon, Forest Ecology Management, 340: 114-125, 2015.
doi: 10.1016/j.foreco.2014.12.016

[95] Vasconcellos RLF, Segat JC, Bonfim JA, Baretta D, Cardoso EJBN. Soil macrofauna as an indicator of soil quality in an undisturbed riparian forest and recovering sites of different ages, European Journal of Soil Biology and Biochemistry. 58: 105-112, 2013.
doi: 10.1016/j.ejsobi.2013.07.001

[96] Amazonas NT, Viani RAG, Rego MGA, Camargo FF, Fujihara RT, Valsechi OA. Soil macrofauna density and diversity across a chronosequence of tropical forest restoration in Southeastern Brazil, Brazilian journal of biology, 1-8, 2018.

[97] Tapia-Armijos MF, Homeier J, Ivan Espinosa C, Leuschner C, de la Cruz M. Deforestation and Forest Fragmentation in South Ecuador since the 1970s-Losing a Hotspot of Biodiversity, PLoS ONE. 10: 1-19, 2015.
doi: 10.1371/journal.pone.0133701

[98] Tilman D, Isbell F, Cowles JM. Biodiversity and Ecosystem Functioning, Annual Review of Ecology, Evolution and Systematics, 45: 471-493, 2014.
doi: 10.1146/annurev-ecolsys-120213-091917

[99] Trap J, Bureau F, Brethes A, Jabiol B, Ponge JF, Chauvat M, Decaëns T, Aubert M. Does moder development along a pure beech (Fagus sylvatica L.) chronosequence result from changes in litter production or in decomposition rates?, Soil Biology and Biochemistry, 43: 1490-1497, 2011.
doi: 10.1016/j.soilbio.2011.03.025

[100] Zanella A, Jabiol B, Ponge JF, Sartori G, De Waal R, Van Delf B, Graefe U, Cools N, Katzensteiner K, Hager H, English M, Brethes A. Toward an European Humus forms Reference Base, Studi trentini di scienze naturali. 85: 145-151, 2009.

[101] Paillet Y, Bergès L, HjÄltén J, Ódor P, Avon C, Bernhardt- Römermann M, Bijlsma RJ, De Bruyn L, Fuhr M, Grandin U, Kanka R, Lundin L, Luque S, Magura T, Matesanz S, Mészáros I, SebastiÀ MT, Schmidt W, Standovár T, Tothmérész B, Uotila A, Valladares F, Vellak K, Virtanen R. Biodiversity differences between managed and unmanaged forests: Meta-analysis of species richness in Europe, Conservation Biology, 24: 101-112, 2010.
doi: 10.1111/j.1523-1739.2009.01399.x

[102] Sylvain ZA, Wall DH. Linking soil biodiversity and vegetation: Implications for a changing planet, American Journal of Botany, 98: 517-527, 2011.
doi: 10.3732/ajb.1000305

[103] Paul EA. The nature and dynamics of soil organic matter: Plant inputs, microbial transformations, and organic matter stabilization, Soil Biology and Biochemistry, 98: 109-126, 2016.

[104] Hostacka A, Ciznar I, Stefkovicova M. Temperature and pH affect the production of bacterial biofilm, Folia Microbiologica, 55(1): 75-78, 2010.
doi: 10.1007/s12223-010-0012-y

[105] Podgaiski LR, Rodrigues GG. Leaf-litter decomposition of pioneer plants and detritivore macrofaunal assemblages on coal ash disposals in southern Brazil, European Journal of Soil Biology, 46: 394-400, 2010.
doi: 10.1016/j.ejsobi.2010.09.001

[106] Ponge JF. Humus and time: a love story, Hal. 2010.
doi: 10.13140/RG.2.1.1354.2561

[107] Tonneijck FH, Jongmans AG. The influence of bioturbation on the vertical distribution of soil organic matter in volcanic ash soils: A case study in northern Ecuador, European Journal of Soil Science, 59: 1063-1075, 2008.
doi: 10.1111/j.1365-2389.2008.01061.x

[108] Jiménez JJ, Lal R. Mechanisms of C Sequestration in Soils of Latin America, CRC, Critical Reviews in Plant Science, 25: 337-365,2006.
doi: 10.1080/0735268060094240

[109] Corrales A, Duque A, Uribe J, Londoño V. Abundance and diversity patterns of terrestrial bryophyte species in secondary and planted montane forests in the northern portion of the Central Cordillera of Colombia, Bryologist, 113: 8-21, 2010.
doi: 10.1639/0007-2745-113.1.8

[110] De Lima SS, de Aquino AM, Leite LFC, Velásquez E, Lavelle P. Relação entre macrofauna edáfica e atributos químicos do solo em diferentes agroecossistemas, Pesquisa Agropecuaria Brasileira, 45: 322-331, 2010.
doi: 10.1590/S0100-204X2010000300013

[111] Ott D, Digel C, Klarner B, Maraun M, Pollierer M, Rall BC, Scheu S, Seelig G, Brose U. Litter elemental stoichiometry and biomass densities of forest soil invertebrates, Oikos, 1212-1223, 2014.
doi: 10.1111/oik.01670

[112] Feijoo A, Quintero H, Fragoso C, Moreno A. Patrón de distribución y listado de especies de las lombrices de tierra (Annelida, Oligochaeta) en Colombia, Acta Zoologica Mexicana, 20: 197-220, 2004.

[113] Feijoo A, Zuñiga MC, Quintero H, Carvajal-Vanegas AF, Ortiz DP. Patrones de asociación entre variables del suelo y usos del terreno en la cuenca del río La Vieja, Colombia, Acta Zoologica Mexicana, Numero especial: 151-164, 2010.

[114] Grove SJ. Saproxylic Insect Ecology and the Sustainable Management of Forests, Annual Review of Ecology and Systematics, 33: 1-23, 2002.
doi: 10.1146/annurev.ecolsys.33.010802.150507

[115] Frouz J, Roubíčková A, Heděnec P, Tajovský K. Do soil fauna really hasten litter decomposition? A meta analysis of enclosure studies, European Journal of Soil Biology, 68: 18-24, 2015.
doi: 10.1016/j.ejsobi.2015.03.002

[116] Zhang DQ, Hui DF, Luo YQ, Zhou GY. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors, Journal of Plant Ecology-Uk, 1: 85-93, 2008.
doi: 10.1093/Jpe/Rtn002

[117] Eisenhauer N, Milcu A, Sabais ACW, Bessler H, Brenner J, Engels C, Klarner B, Maraun M, Partsch S, Roscher C, Schonert F, Temperton V,M, Thomisch K, Weigelt A, Weisser WW, Scheu S. Plant diversity surpasses plant functional groups and plant productivity as driver of soil biota in the long term, PLoS ONE, 6: 15-18, 2011.
doi: 10.1371/journal.pone.0016055

[118] Bezemer TM, Fountain MT, Barea JM, Christensen S, Dekker SC, Duyts H, Van Hal R, Harvey J, Maraun M, Mikola J, Mladenov G, Robin C, De Ruiter PC, Scheu S, Setälä H, Smilauer P, Van Der Putten WH. Divergent composition but similar function of soil food webs beneath individual plants: plant species and community effects, Ecology, 91: 3027-3036, 2010.
doi: 10.1890/09-2198.1

[119] Ruiz-Cobo DH, Bueno-Villegas J, Feijoo-Martinez A. Land use and alpha, beta, and gamma diversity of Diplopoda in the Otún basin, Colombia, Universitas scientiarum, 15(1): 59-67, 2010.
doi: 10.11144/javeriana.SC15-1.luaa

[120] Johansson T, Hjältén J, Olsson J, Dynesius M, Roberge JM. Long-term effects of clear-cutting on epigaeic beetle assemblages in boreal forests, Forest Ecology and Management. 359: 65-73, 2016.
doi: 10.1016/j.foreco.2015.09.041

[121] Del Río MG, Malvardi AE, Lanteri A. Systematics and cladistics of a new naupactini genus (Coleoptera: Curculionidae: Entiminae) from the Andes of Colombia and Ecuador, Zoological Journal of the Linnean Society, 166: 54-71, 2012.
doi: 10.1111/j.1096-3642.2012.00833.x

[122] Lanteri A, Guedes J, Parra J. Weevils injurious for roots of citrus in São Paulo State, Brazil, Neotropical Entomology, 31(4): 561-569, 2002.
doi: 10.1590/S1519-566X2002000400008

[123] Aguirre-Tapiero MDP. Clave de identificación de géneros conocidos y esperados de Elateridae Leach (Coleoptera: Elateroidea) en Colombia, Boletín del Museo de Entomología de la Universidad del Valle, 10: 25-35, 2009.

[124] Decaëns T, Mariani L, Lavelle P. Soil surface macrofaunal communities associated with earthworm casts in grasslands of the Eastern Plains of Colombia, Applied Soil Ecology, 13: 87-100, 1999.
doi: 10.1016/S0929-1393(99)00024-4

[125] Florez E. Las arañas del departamento del Valle del Cauca: Un manual introductorio a su diversidad y clasificación. 1996.
doi: 10.4067/S0071-17132000003500023

[126] Minelli A. The Myriapoda Treatise on Zoology - Anatomy, Taxonomy, Biology, Volumen 1, Brill, Leiden - Boston, 2011.
doi: 10.1163/9789004188266

[127] Adis J. Amazonian Arachnida and Myriapoda, Pensoft Publishers, Sofia-Moscow, 2002.

[128] Hembree DI. Neoichnology of burrowing millipedes: Linking modern burrow morphology, organism behavior, and sediment properties to interpret continental ichnofossils, Palaios, 24: 425-439, 2009.
doi: 10.2110/palo.2008.p08-098r

[129] Chacón G, Gagnon D, Paré D. Comparison of soil properties of native forests, Pinus patula plantations and adjacent pastures in the Andean highlands of southern Ecuador: Land use history or recent vegetation effects?, Soil Use and Management, 25: 427-433, 2009.
doi: 10.1111/j.1475-2743.2009.00233.x

[130] Barnes AD, Jochum M, Mumme S, Haneda NF, Farajallah A, Widarto TH, Brose U. Consequences of tropical land use for multitrophic biodiversity and ecosystem functioning, Nature Communications, 5: 1-7, 2014.
doi: 10.1038/ncomms6351

[131] Mumme S, Jochum M, Brose U, Haneda NF, Barnes AD. Functional diversity and stability of litter invertebrate communities following land-use change in Sumatra, Indonesia, Biological Conservation, 191: 750-758, 2015.
doi: 10.1016/j.biocon.2015.08.033

[132] Jobbágy EG, Jackson RB. The vertical distribution of soil organic carbon and its relation to climate and vegetation, Ecological Applications, 10: 423-436, 2000.
doi: 10.1890/1051-0761(2000)010[0423:TVDOSO]2.0.CO;2

[133] Homeier J, Leuschner C, Bräuning A, Cumbicus NL, Hertel D, Martinson GO, Spannl S, Veldkamp E. Ecosystem Services, Biodiversity and Environmental Change in a Tropical Mountain Ecosystem of South Ecuador, Springer-Verlag, Berlin Heidelberg, 2013.
doi: 10.1007/978-3-642-38137-9

[134] Gunaratne AMT, Gunatilleke CVS, Gunatilleke IA, Madawala HMSP, Burslem DFRP. Overcoming ecological barriers to tropical lower montane forest succession on anthropogenic grasslands: Synthesis and future prospects, Forest Ecology and Management, 329: 340-350, 2014.
doi: 10.1016/j.foreco.2014.03.035

[135] Weslien J, Djupström LB, Schroeder M, Widenfalk O. Long-term priority effects among insects and fungi colonizing decaying wood, Journal of Animal Ecology, 80: 1155-1162, 2011.
doi: 10.1111/j.1365-2656.2011.01860.x
How to Cite
Tulande-M, E., Barrera-Cataño, J. I., Alonso-Malaver, C. E., Basto, S., & Morantes-Ariza, C. (2018). Soil macrofauna in areas with different ages after Pinus patula clearcutting. Universitas Scientiarum, 23(3), 383–417. https://doi.org/10.11144/Javeriana.SC23-3.smia
Section
Ecology & Conservation