Comparison of fine root biomass, earthworm's and nematodes populations in topsoil of natural forest and plantations

Document Type : Complete scientific research article



Background and Objectives: Because of deforestation and reduction of forest areas, plantation is a vital issue for now and the future. The evaluation of planted species is very important to creation of forests with better quality and quantity in the future. Soils, as an important part of the ecosystems, are affected by tree species with differences aboveground and below ground biomass, under same field condition. Biological properties are good indices to assessment of soil quality and health. In this study the effects of different forest covers including natural forest, hardwoods and softwoods plantations, on variability of fine roots biomass, ecological group's earthworm's density/biomass and nematodes abundance were considered.

Materials and Methods: Soil samples were excavated in sixteen points from 0-15 cm (top soil)
depth, for each forest covers including Carpinus betulus (hornbeam) - Parrotia persica (iron wood) as a natural stand, Fraxinus excelsior (ash), Acer velutinum (maple) hardwoods and Pinus brutia (pine), Cupressus sempervirens (cypress) softwoods plantations, located in Wood and Paper Company of Mazandaran. Soil moisture, pH, organic carbon, total nitrogen and biological indices (fine roots biomass, earthworm's density/biomass and nematodes abundance) were measured and recorded at the laboratory.

Results: ANOVA results for soil physico-chemical properties showed significant statistical differences related to forest covers. So that the highest values of soil moisture, organic carbon and C/N ratio were found under pine plantation. Also the higher values of soil pH and total nitrogen were detected in Carpinus betulus - Parrotia persica natural stand. Greater amounts of fine root biomass (89.68 g m-2), earthworm's density (1.81 n m-2)/biomass (24.17 mg m-2) and nematodes abundance (603.37 n m-2) were found in Carpinus betulus - Parrotia persica natural stand. Also maximum epigeic density (1.43 n m-2)/biomass (19.25 mg m-2), were found under Carpinus betulus - Parrotia persica natural stand and ash plantation. Higher anecic earthworm's density (0.37 n m-2)/biomass (4.92 mg m-2) recorded in Carpinus betulus - Parrotia persica natural stand. The endogeic species were not observed under different forest covers. Greater amounts of nematodes abundance (603.37 n m-2) were recorded in Carpinus betulus - Parrotia persica natural stand. The finding of correlation between biological indices and other studied properties indicating that biological characters are influenced by soil water content and chemistry under different forest covers.

Conclusions: The findings of this study are showing the considerable effect of natural forest covers on soil biological properties and quality. In addition, in degraded areas of northern Iran, planting of Fraxinus excelsior species can be considered due to improvement and conservation of soil biological indices, quality and health.


1.Ahmadi Malakut, E., Soltani, A., and Hasanzad Navrodi, I. 2011. A comparison between
understory phytodiversity of a natural forest and forest plantations (Case study: Langerud –
Guilan). Iran. J. For. 20: 2. 157-167. (In Persian)
2.Angst, S., Mueller, C.W., Cajtham, T., Angst, G., Lhotáková, Z., Bartuška, M., Špaldoňová,
A., and Frouz, J. 2017. Stabilization of soil organic matter by earthworms is connected
with physical protection rather than with chemical changes of organic matter. Geoderma.
289: 4. 29-35.
3.Ansari, N., and Seiyed Akhlaghi, S.J. 2009. Comparison of the opinion of rangeland user
and expert about factors influencing natural resources degradation in Iran. Rangeland.
3: 3. 519-532. (In Persian)
4.Asshoff, R., Scheu, S., and Eisenhauer, N. 2010. Different earthworm ecological group
interactively impact seedling establishment. Europ. J. Soil Biol. 46: 5. 330-334.
5.Augusto, L., De Schrijver, A., Vesterdal, L., Smolander, A., Prescott, C., and Ranger, J. 2015.
Influences of evergreen gymnosperm and deciduous angiosperm tree species on the
functioning of temperate and boreal forests. Biological Reviews. 90: 3. 444-466.
6.Beyranvand, M., and Kooch, Y. 2016. Effect of broadleaf tree species on abundance and
diversity of earthworms in forest ecosystems plain. J. Soil Biol. 4: 1. 15-26. (In Persian)
7.Bjørnlund, L., and Christensen, S. 2005. How does litter quality and site heterogeneity interact
on decomposer food webs of a semi-natural forest? Soil Biology and Biochemistry.
37: 2. 203-213.
8.Blouina, M., Hodsonb, M.E., Delgadoc, E.A., Bakerd, G., Brussaarde, L., Buttf, K.R., Daig, J.,
Dendoovenh, L., Peresi, G., Tondohj, J.E., Cluzeauk, D., and Brunl, J. 2013. A review of
earthworm impact on soil function and ecosystem services. Europ. J. Soil Sci. 64: 1. 161-182.
9.Brassard, B.W., Chen, H.Y., Bergeron, Y., and Paré, D. 2011. Coarse root biomass allometric
equations for Abies balsamea, Picea mariana, Pinus banksiana and Populus tremuloides in
the boreal forest of Ontario, Canada. Biomass and Bioenergy. 35: 10. 4189-4196.
10.Cardinale, B.J., Wright, J.P., Cadotte, M.W., Carroll, I.T., Hector, A., Srivastava, D.S., and
Weis, J.J. 2007. Impacts of plant diversity on biomass production increase through time
because of species complementarity. Proceedings of the National Academy of Sciences.
104: 46. 18123-18128.
11.Cesarz, S., Ruess, L., Jacob, M., Jacob, A., Schaefer, M., and Scheu, S. 2013. Tree species
diversity versus tree species identity: driving forces in structuring forest food webs as
indicated by soil nematodes. Soil Biology and Biochemistry. 62: 2. 36-45.
12.Chen, H., Li, B., Fang, C., Chen, J., and Wu, J. 2007. Exotic plant influences soil nematode
communities through litter input. Soil Biology and Biochemistry. 39: 7. 1782-1793.
13.Cristhy Buch, A., Gardner Brown, G., Fernandes Correia, M.E., Fábio Lourençato, L., and
Vieira Silva-Filho, E. 2017. Ecotoxicology of mercury in tropical forest soils: Impact on
earthworms. Science of the Total Environment, In Press.
14.Eissenstat, D.M., Wells, C.E., Yanai, R.D., and Whitbeck, J.L. 2000. Building roots in a
changing environment: implications for root longevity. New Phytologist. 147: 1. 33-42.
15.Fan, S., Guan, F., Xu, X., Forrester, D.I., Ma, W., and Tang, X. 2016. Ecosystem carbon
stock loss after land use change in subtropical forests in China. Forests. 7: 7. 142;
doi: 10.3390/f7070142.
16.Franco, A., Knox, M.A., Sandriuzzi, W., De Tomasel, C.M., Sala, O.E., and Wall, D.H.
2017. Nematode exclusion and recovery in experimental soil microcosms. Soil Biology and
Biochemistry. 108: 4. 78-83.17.Frouz, J., Livečková, M., Albrechtová, J., Chroňáková, A., Cajthaml, T., Pižl, V., andCepáková, Š. 2013. Is the effect of trees on soil properties mediated by soil fauna? A case
study from post-mining sites. Forest Ecology and Management. 309: 4. 87-95.
18.Fukuzawa, K., Shibata Takagi, K., Satoh, F., Koike, T., and Sasa, K. 2013. Temporal
variation in fine-root biomass، production and mortality in a cool temperate forest covered
with dense understory vegetation in northern Japan. Forest Ecology and Management.
310: 4. 700-710.
19.Gorobtsova, O.N., Gedgafova, F.V., Uligova, T.S., and Tembotov, R.K. 2016. Eco
physiological indicators of microbial biomass status in chernozem soils of the Central
Caucasus (in the territory of Kabardino-Balkaria with the Terek variant of altitudinal
zonation). Russ. J. Ecol. 47: 4. 19-25.
20.Groffman, P.M., Fahey, T.J., Fisk, M.C., Yavitt, J.B., Sherman, R.E., Bohlen, P.J., and Maerz,
J.C. 2015. Earthworms increase soil microbial biomass carrying capacity and nitrogen
retention in northern hardwood forests, Soil Biology and Biochemistry, 87: 2. 51-58.
21.Guei, A.M., Baidai, Y., Tondoh, J.E., and Huising, J. 2012. Functional attributes:compacting
vs. decomposing earthworms and influence on soil structure. Current Zoology. 58: 2. 556-565.
22.Haghparast, T., and Khakzyan, M.R. 1994. Arable soils. Islamic Azad University of Rasht
Publication, 341p. (In Persian)
23.Hashemi, S.F., Hojjati, S.M., Hosseini Nasr, S.M., and Jalilvand, H. 2012. Comparison of
nutrient elements and elements retranslocation of Acer velutinum, Zelkova carpinifolia and
Pinus brutia in Darabkla-Mazindaran. Iran. J. For. 4: 2. 175-185. (In Persian)
24.Helmisaari, H.S., Saarsalmi, A., and Kukkola, M. 2009. Effects of wood ash and nitrogen
fertilization on fine root biomass and soil and foliage nutrients in a Norway spruce stand in
Finland. Plant and Soil. 314: 1-2. 121-132.
25.Holdsworth, A.R., Frelich, L.E., and Reich, P.B. 2012. Leaf litter disappearance in
earthworm-invaded northern hardwood forests: role of tree species and the chemistry and
diversity of litter. Ecosystems. 15: 6. 913-926.
26.Jafari Haghighi, M. 2003. Soil analysis methods. Nedaye Zohi Publication, 236p.
(In Persian)
27.Khodashenas, A., Koocheki, A., Rezvani Moghaddam, P., and Lakzian, A. 2012. Evaluation
of structural biodiversity in natural systems of arid and semiarid regions. J. Natur. Environ.
Iran. J. Natur. Resour. 65: 2. 163-179. (In Persian)
28.Kooch, Y., and Zoghi, Z. 2014. Comparison of soil fertility of Acer insigne, Quercus
castaneifolia and Pinus brutia stands in the hyrcanian forests of Iran. Chine. J. Appl.
Environ. Biol. 20: 5. 899-905.
29.Kooch, Y., Hosseini, S.M., Scharenbroch, B.C., Hojjati, S.M., and Mohammadi, J. 2015.
Pedodiversity analysis in the Caspian Forests of Iran. Geoderma Regional. 5: 1. 4-14.
30.Kooch, Y., Samadzadeh, B., and Hosseini, S.M. 2017a. The effects of broad-leaved tree
species on litter quality and soil properties in a plain forest stand. Catena. 150: 1-3. 223-229.
31.Kooch, Y., Tarighat, F.S., and Hosseini, S.M. 2017b. Tree species effects on soil chemical,
biochemical and biological features in mixed Caspian lowland forests. Trees. In Press,
Doi: 10.1007/s00468-016-1511-5.
32.Kooch, Y., Zaccone, C., Lamersdorf, N.P., and Tonon, G. 2014. Pit and mound influence
on soil features in an Oriental Beech (Fagus orientalis Lipsky) forest. Europ. J. For. Res.
133: 2. 347-354.
33.Lamande´, M., Hallaire, V., Curmi, P., Peres, G., and Cluzeau, D. 2003. Changes of pore
morphology, infiltration and earthworm community in a loamy soil under different
agricultural managements. Forest Ecology and Management. 54: 3. 637-649.
34.Lee, K.H., and Jose, S. 2003. Soil respiration, fine root production and microbial biomass in
cottonwood and loblolly pine plantations along a nitrogen fertilization gradient. Forest
Ecology and Management. 185: 3. 263-273.
35.Leuschner, C., and Hertel, D. 2003. Fine root biomass of temperate forests in relation to soil
acidity and fertility, climate, age and species. In Progress in botany. 64: 3. 405-438.
36.Mohammad Nezhad Kiasari, Sh., Saqib Talibi, KH., Rahmani, R., and Amozad, M. 2011.
Comparison diversity of soil invertebrates in natural forests and plantations in Sari Region.
J. Natur. Resour. Sci. Technol. 6: 3. 118-125. (In Persian)
37.Mojarabi, M., Moftakhar Joibary, M., Kooch, Y., and Jalilvand, H. 2011. Comparison of
regeneration density and biodiversity of afforestations of Populus deltoides Marsh. and Acer
velutinum Boiss. in Dallak Khil of Mazandaran. Iran. J. Biol. 24: 4. 614-622. (In Persian)
38.Moslehi, M., and Nazari, J. 2012. Relations between earthworms and trees and its effects on
forest soils. Human and Environmental. 20: 1. 108-113. (In Persian)
39.Munoz, F., and Beer, J. 2001. Fine root dynamics of shaded cacao plantations in Costa Rica.
Agro forestry System. 51: 2. 119-130.
40.Neatrour, M.A., Jones, R.H., and Golladay, S.W. 2005. Correlations between soil nutrient
availability and fine- root biomass at two spatial scales in forested wetlands with contrasting
hydrological regimes. NRC Research Press. 35: 12. 2934-2941.
41.Neher, D.A., Wu, J., Barbercheck, M.E., and Anas, O. 2005. Ecosystem type affects
interpretation of soil nematode community measures. Applied Soil Ecology. 30: 1. 47-64.
42.Neirynck, J., Mirtcheva, S., Sioen, G., and Lust, N. 2000. Impact of Tilia platyphyllos Scop.
Fraxinus exceslsior L., Acer pseudoplatanus L., Quercus robur L. and Fagus sylvatica L. on
earthworm biomass and physico – chemical properties of loamy topsoil. Forest Ecology and
Management. 133: 3. 275-286.
43.Noguchi, K., Konôpka, B., Satomura, T., Kaneko, S., and Takahashi, M. 2007. Biomass and
production of fine roots in Japanese forests. J. For. Res. 12: 2. 83-95.
44.Noguchi, K., Sakata, T., Mizoguchi, T., and Takahashi, M. 2005. Estimating the production
and mortality of fine roots in a Japanese cedar (Cryptomeria japonica D. Don) plantation
using a minirhizotron technique. J. For. Res. 10: 6. 435-441.
45.Paolo, A.G., Raffaella, B., Danio, A., Attilio, D.R., and Ettore, C. 2010. Assessment of
soil-quality index based on micro arthropods in corn cultivation in Northern Italy. Ecological
Indicators. 10: 2. 129-135.
46.Qiu, Q., Li, J.Y., Wang, J.H., He, Q., Su, Y., and Ma, J.W. 2015. Interactions between soil
water and fertilizer application on fine root biomass yield and morphology of Catalpa bungei
seedlings. In Applied Mechanics and Materials, Trans Tech Publications. 700: 323-333.
47.Reneo, M., and Eerevkova, A. 2017. Windstorms as mediator of soil nematode community
changes: evidence from European spruce forest. Helminthologia. 54: 2. 36-47.
48.Römbke, J., Jänsch, S., and Didden, W. 2005. The use of earthworms in ecological
soil classification and assessment concepts. Ecotoxicology and Environmental Safety.
62: 2. 249-265.
49.Salamon, J.A., Schaefer, M., Alphei, J., Schmid, B., and Scheu, S. 2004. Effects of plant
diversity on Collembola in an experimental grassland ecosystem. Oikos. 106: 4. 51-60.
50.Sayer, E.J., Tanner, E.V.J., and Cheesman, A.W. 2006. Increased litter fall changes fine root
distribution in a moist tropical forest. Plant and Soil. 281: 1. 5-13.
51.Sayyad, E., Hosseini, S.M., Hosseini, V., and Salehe-Shooshtari, M.H. 2012. Soil
macrofauna in relation to soil and leaf litter properties in tree plantations. J. For. Sci.
58: 3. 170-180.
52.Scharenbroch, B.C., and Johnston, D.P. 2011. A microcosm study of the common night
crawler earthworm (Lumbricus terrestris) and physical, chemical and biological properties of
a designed urban soil. Urban ecosystems. 14: 1. 119-134.
53.Schelfhout, S., Mertens, J., Verheyen, K., Vesterdal, L., Baeten, L., Muys, B., and
De Schrijver, A. 2017.Tree species identity shapes earthworm communities. Forests.
8: 85. doi:10.3390/f8030085.
54.Schwarz, B. 2015. Non-significant tree diversity but significant identity effects on
earthworm communities in three tree diversity experiments. Europ. J. Soil Biol. 67: 4. 17-26.
55.Sileshi, G., and Mafongoya, P.L. 2006. Long-term effect of improved legume fallows on soil
invertebrate macrofauna and maize yield in eastern Zambia. Agriculture, Ecosystems and
Environment, 115: 1-4. 69-78.
56.Smith, R.G., McSwiney, C.P., Grandy, A.S., Suwanwaree, P., Snider, R.M., and Robertson,
G.P. 2008. Diversity and abundance of earthworms across an agricultural land-use intensity
gradient. Soil and Tillage Research. 100: 1. 83-88.
57.Sun, X., Zhang, X., Zhang, S., Dai, G., Han, S., and Liang, W. 2013. Soil nematode
responses to increases in nitrogen deposition and precipitation in a temperate forest.
Plos One. 8: 12. e82468.
58.Tolfa, I., Velki, M., Vukovic, R., Ecimovic, S., Katanic, Z., and Loncaric, Z. 2017. Effect ofdifferent forms of selenium on the plant–soil–earthworm system. J. Plant Nutr. Soil Sci.1-10. DOI: 10.1002/jpln.201600492.
59.Tufekcioglu, A., Raich, J.W., Isenhart, T.M., and Schultz, R.C. 1998. Fine root dynamics,coarse root biomass, root distribution and soil respiration in a multispecies riparian buffer inCentral Iowa, USA. Agroforestry Systems. 44: 2-3. 163-174.
60.Wang, X., Ma, L., Jia, Z., and Jia, L. 2014. Root inclusion net method: novel approach todetermine fine root production and turnover in Larix principis-rupprechtii Mayr plantation inNorth China. Turk. J. Agric. Forest. 38: 3. 388-398.
61.Wu, L., Ouyang, Z., Li, B., and Xu, Y. 2016. Effects of different forms of plant-derivedorganic matter on nitrous oxide emissions. Environmental Science: Processes and Impacts.
62.Xu, W., Liu, J., Liu, X., Li, K., Zhang, D., and Yan, J. 2013. Fine root production, turnoverand decomposition in a fast-growth Eucalyptus urophylla plantation in southern China.J. Soil Sed. 13: 7. 1150-1160.
63.Yan, S., Singh, A., Shenglei, N., Chonghui, F., Silong, L., Yuanliang, W., Cui, Y., andHu, L. 2012. A soil fauna index for assessing soil quality. Soil Biology and Biochemistry.47: 3. 158-165.
64.Yeates, G.W. 2003. Nematodes as soil indicators: functional and biodiversity aspects.Biology and Fertility of Soils. 37: 4. 199-210.
65.Yeates, G.W. 2007. Abundance, diversity and resilience of nematode assemblages in forestsoils. Can. J. For. Res. 37: 2. 216-225.
66.Yuan, Z.Y., and Chen, H.Y. 2010. Fine root biomass, production, turnover rates and nutrientcontents in boreal forest ecosystems in relation to species, climate, fertility and stand age:literature review and meta-analyses. Critical Reviews in Plant Sciences. 29: 4. 204-221.
67.Yusheng, Y., Jianfen, G., Guangshui, C., Zongming, H., and Jinsheng, X. 2003. Effect ofslash burning on nutrient removal and soil fertility in Chinese Fir and evergreen broadleavedforests of Mid-Subtropical China. Pedosphere. 13: 1. 87-96.
68.Zhang, K., Zheng, H., Chen, F.L., Ouyang, Z.Y., Wang, Y., Wu, Y.F., Lan, J., Fu, M., andXiang, X.W. 2015. Changes in soil quality after converting Pinus to Eucalyptus plantationsin southern China. Solid Earth. 6: 2: 115-123.
69.Zhang, M., Liang, W.J., and Zhang, X.K. 2012. Soil nematode abundance and diversity indifferent forest types at Changbai Mountain, China. Zoological Studies. 51: 5. 619-626.
70.Zushi, K. 2006. Spatial distribution of soil carbon and nitrogen storage and forestproductivity in a watershed planted to Japanese cedar (Cryptomeria Japonica D. Don).J. For. Res. 11: 5. 351-358.
71.Zuzloli, A. 2015. The effect of natural forest and plantations on plant biodiversity, litterquality and soil physical characters in Sari region. M.Sc. Thesis of Forestry, Sari AgricultureSciences and Natural Resources University, 86p.