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RESEARCH ARTICLE

Plant-induced differentiation of soil variables and nematode community structure in a Mediterranean serpentine ecosystem

Nikolaos Monokrousos A , George Charalampidis C , George Boutsis B , Varvara Sousanidou B , Efimia M. Papatheodorou C and Maria D. Argyropoulou B D
+ Author Affiliations
- Author Affiliations

A Department of Biological Applications & Technology, University of Ioannina, 45110 Ioannina, Greece.

B Department of Zoology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece.

C Department of Ecology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece.

D Corresponding author. Email: margyrop@bio.auth.gr

Soil Research 52(6) 593-603 https://doi.org/10.1071/SR14011
Submitted: 15 January 2014  Accepted: 4 April 2014   Published: 28 July 2014

Abstract

Abiotic and biotic components of a serpentine Mediterranean soil were studied in terms of heavy metal and nutrient concentrations, microbial biomass, and structural and functional characteristics of the soil nematode community. We explored differentiations of the soil environment imposed by vegetation, sampling the bare soil and soil under Buxus sempervirens, Juniperus oxycedrus, Cistus creticus and Thymus sibthorpii.

Organic matter, microbial biomass, nutrient availability and calcium/magnesium (Ca/Mg) ratio of the serpentine site were similar to those of degraded, non-serpentine Mediterranean ecosystems; the serpentine site showed potassium deficiency and high heavy metal load. Soil nematode abundance, especially of phytoparasites, was very low. Low enrichment and structure indices and high channel index values indicated a degraded, low-resource, stressful environment where fungal decomposition predominates.

There was no differentiation of heavy metal concentrations among microsites. Bare soil exhibited high pH, low water content, low Ca/Mg (0.68), low nutrient concentrations, low abundance of most nematode groups, low values of maturity and plant parasitic indices, low nematode diversity and a distinct generic composition. Rhizosphere soil was differentiated according to the evergreen–sclerophyllous or seasonal–dimorphic habit of shrubs. This was reflected in soil nutrients and in all parameters of the soil nematode community.

Additional keywords: Greece, heavy metals, maquis, nematode functional profile, phrygana, ultramafic soil.


References

Abdel-Azeem AM, Abdel-Moneim TS, Ibrahim ME, Hassan MAA, Saleh MY (2007) Effects of long-term heavy metal contamination on diversity of terricolous fungi and nematodes in Egypt—a case study. Water, Air, and Soil Pollution 186, 233–254.
Effects of long-term heavy metal contamination on diversity of terricolous fungi and nematodes in Egypt—a case study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFarsb3P&md5=260062f8925deac5fb1d8c33a4c63d8aCAS |

Abu-Ashour J, Lee H (2000) Transport of bacteria on sloping soil surfaces by runoff. Environmental Toxicology 15, 149–153.
Transport of bacteria on sloping soil surfaces by runoff.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXivVKgur4%3D&md5=ed40c74d0ea9711500e697d54aaeb1b1CAS |

Alados CL, Navarro T, Cabezudo B (1999) Tolerance assessment of Cistus ladanifer to serpentine soils by developmental stability analysis. Plant Ecology 143, 51–66.
Tolerance assessment of Cistus ladanifer to serpentine soils by developmental stability analysis.Crossref | GoogleScholarGoogle Scholar |

Alexander EB, Coleman RG, Keeler-Wolf T, Harrison SP (2007) ‘Serpentine geoecology of western North America.’ (Oxford University Press: New York)

Allen SE (1974) ‘Chemical analysis of ecological materials.’ (Blackwell: Oxford, UK)

Amir H, Pineau R (2003) Release of Ni and Co by microbial activity in New Caledonian ultramafic soils. Canadian Journal of Microbiology 49, 288–293.
Release of Ni and Co by microbial activity in New Caledonian ultramafic soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlslWqt70%3D&md5=d643cb4e7f9810b010dc1bc360f48fa1CAS | 12897838PubMed |

Arianoutsou M, Rundel PW, Berry WL (1993) Serpentine endemics as biological indicators of soil elemental concentrations. In ‘Plants as biomonitors: indicators for heavy metals in the terrestrial environment’. (Ed. B Markert) p. 179. (Weinheim: New York)

Bongers T (1990) The maturity index: An ecological measure of environmental disturbance based on nematode species composition. Oecologia 83, 14–19.
The maturity index: An ecological measure of environmental disturbance based on nematode species composition.Crossref | GoogleScholarGoogle Scholar |

Bongers T (1994) ‘De nematoden van Nederland.’ (Pirola: Schoorl, the Netherlands)

Bongers T, Bongers M (1998) Functional diversity of nematodes. Applied Soil Ecology 10, 239–251.
Functional diversity of nematodes.Crossref | GoogleScholarGoogle Scholar |

Boulton AM, Jaffee BA, Scow KM (2003) Effects of a common harvester ant (Messor andrei) on richness and abundance of soil biota. Applied Soil Ecology 23, 257–265.
Effects of a common harvester ant (Messor andrei) on richness and abundance of soil biota.Crossref | GoogleScholarGoogle Scholar |

Boutsis G, Stamou GP, Argyropoulou MD (2011) Short term effects of soil disinfection with metham sodium and organic alternatives on nematode communities. Community Ecology 12, 161–170.
Short term effects of soil disinfection with metham sodium and organic alternatives on nematode communities.Crossref | GoogleScholarGoogle Scholar |

Bouyoucos GJ (1962) Hydrometer method improved for making particle size analyses of soils. Agronomy Journal 54, 464–465.
Hydrometer method improved for making particle size analyses of soils.Crossref | GoogleScholarGoogle Scholar |

Boyd RS (2004) Ecology of metal hyperaccumulation—Commentary. New Phytologist 162, 563–567.
Ecology of metal hyperaccumulation—Commentary.Crossref | GoogleScholarGoogle Scholar |

Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology Evolution and Systematics 36, 243–266.
Evolutionary ecology of plant adaptation to serpentine soils.Crossref | GoogleScholarGoogle Scholar |

Brussaard L, Pulleman MM, Ouedraogo E, Mando A, Six J (2007) Soil fauna and soil function in the fabric of the food web. Pedobiologia 50, 447–462.
Soil fauna and soil function in the fabric of the food web.Crossref | GoogleScholarGoogle Scholar |

Caliskan S, Ozkaya I, Caliskan ME, Arslan M (2008) The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil. Field Crops Research 108, 126–132.
The effects of nitrogen and iron fertilization on growth, yield and fertilizer use efficiency of soybean in a Mediterranean-type soil.Crossref | GoogleScholarGoogle Scholar |

Chen G, Qin J, Shi D, Zhang Y, Ji W (2009) Diversity of soil nematodes in areas polluted with heavy metals and polycyclic aromatic hydrocarbons (PAHs) in Lanzhou, China. Environmental Management 44, 163–172.
Diversity of soil nematodes in areas polluted with heavy metals and polycyclic aromatic hydrocarbons (PAHs) in Lanzhou, China.Crossref | GoogleScholarGoogle Scholar | 19205795PubMed |

Chiarucci A, Maccherini S, Bonini I, De Dominicis V (1999) Effects of nutrient addition on community productivity and structure of serpentine vegetation. Plant Biology 1, 121–126.
Effects of nutrient addition on community productivity and structure of serpentine vegetation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Sjsrk%3D&md5=02dd86645fe69ca4fde4088ec31a88f4CAS |

Chochliouros SP (2005) Floristic and phytosociological research of Mt Vermio—An ecological approach. PhD Thesis, University of Patra, Greece.

de Vries FT, Manning P, Tallowin JRB, Mortimer SR, Pilgrim ES, Harrison KA, Hobbs PJ, Quirk H, Shipley B, Cornelissen JHC, Kattge J, Bardgett RD (2012) Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities. Ecology Letters 15, 1230–1239.
Abiotic drivers and plant traits explain landscape-scale patterns in soil microbial communities.Crossref | GoogleScholarGoogle Scholar | 22882451PubMed |

DeGrood SH, Claassen VP, Scow KM (2005) Microbial community composition on native and drastically disturbed serpentine soils. Soil Biology & Biochemistry 37, 1427–1435.
Microbial community composition on native and drastically disturbed serpentine soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltFSksL4%3D&md5=1579040316e19afc69cce733ee48cad7CAS |

Ekschmitt K, Korthals GW (2006) Nematodes as sentinels of heavy metals and organic toxicants in the soil. Journal of Nematology 38, 13–19.

Esch EH, Hernández DL, Pasari JR, Kantor RSG, Selmants PC (2013) Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland. Plant and Soil 366, 671–682.
Response of soil microbial activity to grazing, nitrogen deposition, and exotic cover in a serpentine grassland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlGgtb4%3D&md5=b8eb8385873c936b659efb9b1a641c07CAS |

Estrela T, Marcuello C, Iglesias A (1996) Water resources problems in southern Europe—an overview report. European Topic Centre on Inland Waters, European Environment Agency, Copenhagen, Denmark.

Ferris H, Bongers T, de Goede RGM (2001) A framework for soil food web diagnostics: extension of the nematode faunal analysis concept. Applied Soil Ecology 18, 13–29.
A framework for soil food web diagnostics: extension of the nematode faunal analysis concept.Crossref | GoogleScholarGoogle Scholar |

Fiscus DA, Neher DA (2002) Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances. Ecological Applications 12, 565–575.
Distinguishing sensitivity of free-living soil nematode genera to physical and chemical disturbances.Crossref | GoogleScholarGoogle Scholar |

Freitas H, Prasad MNV, Pratas J (2004) Analysis of serpentinophytes from north–east of Portugal for trace metal accumulation––relevance to the management of mine environment. Chemosphere 54, 1625–1642.
Analysis of serpentinophytes from north–east of Portugal for trace metal accumulation––relevance to the management of mine environment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVWgsbg%3D&md5=e74cb2997f70f78fa96cd2c00a64651fCAS | 14675842PubMed |

Georgieva SS, McGrath SP, Hooper DJ, Chambers BS (2002) Nematode communities under stress: the long-term effects of heavy metals in soil treated with sewage sludge. Applied Soil Ecology 20, 27–42.
Nematode communities under stress: the long-term effects of heavy metals in soil treated with sewage sludge.Crossref | GoogleScholarGoogle Scholar |

Hungate BA, Jaeger CH, Gamara G, Chapin FS, Field CB (2000) Soil microbiota in two annual grasslands: responses to elevated atmospheric CO2. Oecologia 124, 589–598.
Soil microbiota in two annual grasslands: responses to elevated atmospheric CO2.Crossref | GoogleScholarGoogle Scholar |

Ivezic M, Raspudic E (1998) Nematodes community structure of natural wet grassland vegetation of Kopaechi rit in Croatia. In ‘Nematode communities of northern temperate grassland ecosystems’. (Eds RGM de Goede, T Bongers) p. 145. (Focus: Giessen, Germany)

Jenkinson DS, Powlson DS (1976) Effects of biocidal treatments on metabolism in soil: method for measuring soil biomass. Soil Biology & Biochemistry 8, 209–213.
Effects of biocidal treatments on metabolism in soil: method for measuring soil biomass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xkslens7c%3D&md5=cd591a7c27f6c902b18967d7486d926dCAS |

Kachenko AG (2008) Ecophysiology and phytoremediation potential of heavy metal(loid) accumulating plants. PhD Thesis, Faculty of Agriculture Food and Natural Resources, The University of Sydney, NSW, Australia.

Kandeler E, Kampichler C, Horak O (1996) Inflluence of heavy metals on the functional diversity of soil microbial communities. Biology and Fertility of Soils 23, 299–306.
Inflluence of heavy metals on the functional diversity of soil microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFemurw%3D&md5=e3d162eaadbd3c65c781148abcc3b447CAS |

Kapagianni PD, Boutsis G, Argyropoulou MD, Papatheodorou EM, Stamou GP (2010) The network of interactions among soil quality variables and nematodes: short-term responses to disturbances induced by chemical and organic disinfection. Applied Soil Ecology 44, 67–74.
The network of interactions among soil quality variables and nematodes: short-term responses to disturbances induced by chemical and organic disinfection.Crossref | GoogleScholarGoogle Scholar |

Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biological Reviews of the Cambridge Philosophical Society 83, 495–508.

Krnjaic D (1998) Nematode communities of Deliblato sand in Yugoslavia. In ‘Nematode communities of northern temperate grassland ecosystems’. (Eds RGM de Goede, T Bongers) p. 163. (Focus: Giessen, Germany)

Leita L, DeNobili M, Mondini C, Muhlbachoura G, Marchinol L, Bragato G, Contin M (1999) Influence of inorganic and organic fertilization on soil microbial biomass, metabolic quocient and heavy metal bioavailability. Biology and Fertility of Soils 28, 371–376.
Influence of inorganic and organic fertilization on soil microbial biomass, metabolic quocient and heavy metal bioavailability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntFOnsg%3D%3D&md5=1b99ccdf18511965d64b72bd9d61f570CAS |

Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese and copper. Soil Science Society of America Journal 42, 421–428.
Development of a DTPA soil test for zinc, iron, manganese and copper.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXltVKntLs%3D&md5=a414baee85bf121a33f563f42506ebdeCAS |

Llugany M, Lombini A, Dinelli E, Poschenrieder C, Barceló J (2009) Transfer of selected mineral nutrients and trace elements in the host–hemiparasite association, Cistus-Odontites lutea, growing on and off metal-polluted sites. Plant Biology 11, 170–178.
Transfer of selected mineral nutrients and trace elements in the host–hemiparasite association, Cistus-Odontites lutea, growing on and off metal-polluted sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXntFWqsr0%3D&md5=47cf13a31196551b55da86bba0aeaa21CAS | 19228324PubMed |

Ludewig A, Sturham D (1998) Nematode diversity in grassland soil near Munster, Germany. In ‘Nematode communities of northern temperate grassland ecosystems’. (Eds RGM de Goede, T Bongers) p. 175. (Focus: Giessen, Germany)

Ma Y, Rajkumar M, Freitas H (2009) Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp. Chemosphere 75, 719–725.
Isolation and characterization of Ni mobilizing PGPB from serpentine soils and their potential in promoting plant growth and Ni accumulation by Brassica spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXksVChur4%3D&md5=6b5c4795d78cb6cf3f100aced3a8d10aCAS | 19232424PubMed |

McLean EO (1982) Soil pH and lime requirement. In ‘Methods of soil analysis, Part 2’. (Eds AL Page, RH Miller, DR Kenney) pp. 199–224. (American Society of Agronomy: Madison, WI, USA)

Monokrousos N, Papatheodorou EM, Diamantopoulos JD, Stamou GP (2004) Temporal and spatial variability of soil chemical and biological variables in a Mediterranean shrubland. Forest Ecology and Management 202, 83–91.
Temporal and spatial variability of soil chemical and biological variables in a Mediterranean shrubland.Crossref | GoogleScholarGoogle Scholar |

Monokrousos N, Papatheodorou EM, Diamantopoulos JD, Stamou GP (2006) Soil quality variables in organically and conventionally cultivated field sites. Soil Biology & Biochemistry 38, 1282–1289.
Soil quality variables in organically and conventionally cultivated field sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksVOns70%3D&md5=96a1a7e0944b2b5ef4bca211741b04f1CAS |

Nagy P (1999) Effect of an artificial metal pollution on nematode assemblage of a calcareous loamy chernozem soil. Plant and Soil 212, 35–43.
Effect of an artificial metal pollution on nematode assemblage of a calcareous loamy chernozem soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntlKnsb8%3D&md5=43ca92f73553fc6a6736100a1bda947aCAS |

Nagy P, Bakonyi G, Bongers T, Kadar I, Fabian M, Kiss I (2004) Effects of microelements on soil nematode assemblages seven years after contaminating an agricultural field. The Science of the Total Environment 320, 131–143.
Effects of microelements on soil nematode assemblages seven years after contaminating an agricultural field.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhvV2nu7o%3D&md5=61d1fde773b4a531b408246fea94f9a1CAS | 15016503PubMed |

Najmadeen HH, Mohammad AO, Mohamed-Amin HH (2010) Effects of soil texture on chemical compositions, microbial populations and carbon mineralization in soil. Egyptian Journal of Experimental Biology (Bot.) 6, 59–64.

Neher DA, Noffsinger M, Campbell CL (1998) Nematode diversity in grassland soil near Munster, Germany. In ‘Nematode communities of northern temperate grassland ecosystems’. (Eds RGM de Goede, T Bongers) p. 321. (Focus: Giessen, Germany)

Neher DA, Wu J, Barbercheck ME, Anas O (2005) Ecosystem type affects interpretation of soil nematode community measures. Applied Soil Ecology 30, 47–64.
Ecosystem type affects interpretation of soil nematode community measures.Crossref | GoogleScholarGoogle Scholar |

Neher DA, Weicht TR, Barbercheck ME (2012) Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils. Applied Soil Ecology 54, 14–23.
Linking invertebrate communities to decomposition rate and nitrogen availability in pine forest soils.Crossref | GoogleScholarGoogle Scholar |

O’Dell RE, James JJ, Richards JH (2006) Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca:Mg than in tolerance of low N, low P, or heavy metals. Plant and Soil 280, 49–64.
Congeneric serpentine and nonserpentine shrubs differ more in leaf Ca:Mg than in tolerance of low N, low P, or heavy metals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhslOrsbw%3D&md5=bc03b10b88ae837eb478a61795670e8dCAS |

Okada H, Harada H, Kadota I (2005) Fungal-feeding habits of six nematode isolates in the genus Filenchus. Soil Biology & Biochemistry 37, 1113–1120.
Fungal-feeding habits of six nematode isolates in the genus Filenchus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFGrtbc%3D&md5=e45b35f82e04e7095402d723f7d77b01CAS |

Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United States Department of Agriculture, Washington DC, Circular No. 939, p. 19.

Papatheodorou EM, Stamou GP (2004) Nutrient attributes of tissues in relation to grazing in an evergreen sclerophyllous shrub (Quercus coccifera L.) dominating vegetation in Mediterranean-type ecosystems. Journal of Arid Environments 59, 217–227.
Nutrient attributes of tissues in relation to grazing in an evergreen sclerophyllous shrub (Quercus coccifera L.) dominating vegetation in Mediterranean-type ecosystems.Crossref | GoogleScholarGoogle Scholar |

Papatheodorou EM, Stamou GP, Giannotaki A (2004) Response of soil chemical and biological variables to small and large scale changes in climatic factors. Pedobiologia 48, 329–338.
Response of soil chemical and biological variables to small and large scale changes in climatic factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVekt7bM&md5=a70cee87825126ba98a758cdd05d4d14CAS |

Papatheodorou EM, Kordatos H, Kouseras T, Monokrousos N, Menkissoglu-Spiroudi U, Diamantopoulos J, Stamou GP, Argyropoulou MD (2012) Differential responses of structural and functional aspects of soil microbes and nematodes to abiotic and biotic modifications of the soil environment. Applied Soil Ecology 61, 26–33.
Differential responses of structural and functional aspects of soil microbes and nematodes to abiotic and biotic modifications of the soil environment.Crossref | GoogleScholarGoogle Scholar |

Parry ML, Canziani OF, Palutikof JP, van der Linden PJ, Hanson CE (2007) ‘Ecosystems, their properties, goods and services; Mediterranean ecosystems.’ Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. (Cambridge University Press: Cambridge, UK)

Pen-Mouratov S, Hu C, Hindin E, Steinberger Y (2011) Soil microbial activity and a free-living nematode community in the playa and in the sandy biological crust of the Negev Desert. Biology and Fertility of Soils 47, 363–375.
Soil microbial activity and a free-living nematode community in the playa and in the sandy biological crust of the Negev Desert.Crossref | GoogleScholarGoogle Scholar |

Pennanen T (2001) Microbial communities in boreal coniferous forest humus exposed to heavy metals and changes in soil pH—a summary of the use of phospholipid fatty acids, Biolog® and 3H-thymidine incorporation methods in field studies. Geoderma 100, 91–126.
Microbial communities in boreal coniferous forest humus exposed to heavy metals and changes in soil pH—a summary of the use of phospholipid fatty acids, Biolog® and 3H-thymidine incorporation methods in field studies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXpsVGhsA%3D%3D&md5=0f1e1286746c9f935f7689dfee255be6CAS |

Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial structure and function in a heavy metal contaminated soil: effects of plant growth and different amendments. Soil Biology & Biochemistry 38, 327–341.
Microbial structure and function in a heavy metal contaminated soil: effects of plant growth and different amendments.Crossref | GoogleScholarGoogle Scholar |

Proctor J, Woodell SRJ (1975) The ecology of serpentine soils. Advances in Ecological Research 9, 255–366.
The ecology of serpentine soils.Crossref | GoogleScholarGoogle Scholar |

Rajakaruna N, Bohm BA (1999) The edaphic factor and patterns of variation in Lasthenia californica (Asteraceae). American Journal of Botany 86, 1576–1596.
The edaphic factor and patterns of variation in Lasthenia californica (Asteraceae).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngs1GltA%3D%3D&md5=74c2b70dc3b53c5b23d4b18729435ba4CAS | 10562249PubMed |

Ricci C, Pagani M (1997) Desiccation of Panagrolaimus rigidus (Nematoda): survival, reproduction and the influence on the internal clock. Hydrobiologia 347, 1–13.
Desiccation of Panagrolaimus rigidus (Nematoda): survival, reproduction and the influence on the internal clock.Crossref | GoogleScholarGoogle Scholar |

Ritz K, Trudgill DL (1999) Utility of nematode community analysis as an integrated measure of the functional state of soils: perspectives and challenges. Plant and Soil 212, 1–11.
Utility of nematode community analysis as an integrated measure of the functional state of soils: perspectives and challenges.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntlKnsLo%3D&md5=f968e52e9ea7ec382b160b7b7dd2d829CAS |

Ritz K, McNicol W, Nunan N, Grayston S, Millard P, Atkinson D, Gollotte A, Habeshaw D, Boag B, Clegg CD, Griffiths BS, Wheatley RE, Glover LA, McCaig AE, Prosser JI (2004) Spatial structure in soil chemical and microbiological properties in an upland grassland. FEMS Microbiology Ecology 49, 191–205.
Spatial structure in soil chemical and microbiological properties in an upland grassland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsl2iur0%3D&md5=941f8c410403fe1cb33f9cb213692e6aCAS | 19712414PubMed |

Roane TM, Kellogg ST (1996) Characterization of bacterial communities in heavy metal contaminated soils. Canadian Journal of Microbiology 42, 593–603.
Characterization of bacterial communities in heavy metal contaminated soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xjtlykt7w%3D&md5=8b4d0358e9bfa4375bdd087e176a4fd1CAS | 8801006PubMed |

Ross DJ (1990) Measurements of microbial biomass C and N in grassland soils by fumigation incubation procedures—influence of inoculum size and the control. Soil Biology & Biochemistry 22, 289–294.
Measurements of microbial biomass C and N in grassland soils by fumigation incubation procedures—influence of inoculum size and the control.Crossref | GoogleScholarGoogle Scholar |

S’Jacob JJ, van Bezooijen J (1984) ‘A manual for practical work in nematology.’ (Department of Nematology, Wageningen Agricultural University: Wageningen, the Netherlands)

Samecka-Cymerman A, Garbiec K, Kolon K, Kempers AJ (2009) Factor analysis of the elemental composition of Pteridium aquilinum from serpentine and granite soils as a tool in the classification of relations between this composition and the type of parent rock in the Ślęża Massif in Lower Silesia, Poland. Environmental Geology 58, 509–514.
Factor analysis of the elemental composition of Pteridium aquilinum from serpentine and granite soils as a tool in the classification of relations between this composition and the type of parent rock in the Ślęża Massif in Lower Silesia, Poland.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosVGhu7k%3D&md5=28aaa7c0de1237a69d1f3344b17c258fCAS |

Sánchez-Moreno S, Camargo J, Navas A (2006) Ecotoxicological assessment of the impact of residual heavy metals on soil nematodes in the Guadiamar river basin (Southern Spain). Environmental Monitoring and Assessment 116, 245–262.
Ecotoxicological assessment of the impact of residual heavy metals on soil nematodes in the Guadiamar river basin (Southern Spain).Crossref | GoogleScholarGoogle Scholar | 16779593PubMed |

Schipper LA, Lee WG (2004) Microbial biomass, respiration and diversity in ultramafic soils of West Dome, New Zealand. Plant and Soil 262, 151–158.
Microbial biomass, respiration and diversity in ultramafic soils of West Dome, New Zealand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtlGns7w%3D&md5=2f0fb5100b1719bdef0e16b0a31b10feCAS |

Sylvain ZA, Wall DH (2011) Linking soil biodiversity and vegetation: implications for a changing planet. American Journal of Botany 98, 517–527.
Linking soil biodiversity and vegetation: implications for a changing planet.Crossref | GoogleScholarGoogle Scholar | 21613143PubMed |

Thomas GW (1982) Exchangable cations. In ‘Methods of soil analysis, Part 2’. (Eds AL Page, RH Miller, DR Kenney) pp. 154–224. (American Society of Agronomy: Madison, WI, USA)

Tsiafouli MA, Argyropoulou MD, Stamou GP, Sgardelis SP (2006) Soil nematode biodiversity in organic and conventional agroecosystems of Northern Greece. Russian Journal of Nematology 14, 159–169.

Tsiafouli MA, Argyropoulou MD, Stamou GP, Sgardelis SP (2007) Is duration of organic management reflected on nematode communities of cultivated soils? Belgian Journal of Zoology 137, 165–175.

Tsiripidis I, Papaioannou A, Sapounidis V, Bergmeier E (2010) Approaching the serpentine factor at a local scale—a study in an ultramafic area in northern Greece. Plant and Soil 329, 35–50.
Approaching the serpentine factor at a local scale—a study in an ultramafic area in northern Greece.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtFGlurk%3D&md5=4c4c3d2fc108eae8a932d4c788b9c787CAS |

Turgay OC, Görmez A, Bilen S (2012) Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey. Environmental Monitoring and Assessment 184, 515–526.
Isolation and characterization of metal resistant-tolerant rhizosphere bacteria from the serpentine soils in Turkey.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKju77M&md5=6f971a3ac9de07e58de8d89ecf738673CAS | 21404012PubMed |

van Bezooijen J (2006) ‘Methods and techniques for nematology.’ Revised version. (Department of Nematology, Wageningen Agricultural University: Wageningen, the Netherlands)

Van-Camp L, Bujarrabal B, Gentile AR, Jones RJA, Montanarella L, Olazabal C, Selvaradjou SK (2004) ‘Reports of the Technical Working Groups Established under the Thematic Strategy for Soil Protection.’ EUR 21319 EN/3. (Office for Official Publications of the European Communities: Luxembourg)

Vinciguerra MT (1998) Nematodes from Italian coastal dunes. In ‘Nematode communities of northern temperate grassland ecosystems’. (Eds RGM de Goede, T Bongers) p. 303. (Focus: Giessen, Germany)

Walker RB (1954) Factors affecting plant growth on serpentine soils. Ecology 35, 259–266.

Wharton DA (2003) The environmental physiology of Antarctic terrestrial nematodes: a review. Journal of Comparative Physiology 173, 621–628.
The environmental physiology of Antarctic terrestrial nematodes: a review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3srkt1Sjtw%3D%3D&md5=6c555dd2df6be1669ea1df348644dc23CAS |

Woodell SRJ, Mooney HA, Lewis H (1975) The Adaptation to Serpentine Soils in California of the Annual Species Linanthus androsaceus (Polemoniaceae). Bulletin of the Torrey Botanical Club 102, 232–238.
The Adaptation to Serpentine Soils in California of the Annual Species Linanthus androsaceus (Polemoniaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XktVChtLw%3D&md5=381262ce5272abc296dd90898e555193CAS |

Woolhouse HW (1983) Toxicity and tolerance in the responses of plant to metals. In ‘Encyclopedia of plant physiology (Vol. 12C)’. (Ed. OL Lange) (Springer: New York)

Yeates GW, Bongers T, de Goede RGM, Freckman DW, Georgieva SS (1993) Feeding habits in nematode families and genera—an outline for soil ecologists. Journal of Nematology 25, 315–331.

Zhi DJ, Li HY, Nan WB (2008) Nematode communities in the artificially vegetated belt with or without irrigation in the Tengger Desert, China. European Journal of Soil Biology 44, 238–246.
Nematode communities in the artificially vegetated belt with or without irrigation in the Tengger Desert, China.Crossref | GoogleScholarGoogle Scholar |