Spatial and temporal variations of soil function in a Mediterranean serpentine ecosystem
Nikolaos Monokrousos A B D , George Charalampidis A , Pantelitsa Kapagianni A , Maria D. Argyropoulou C and Efimia M. Papatheodorou A
+ Author Affiliations
- Author Affiliations
A Department of Ecology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece.
B Department of Biological Applications and Technology, University of Ioannina, 45110 Ioannina, Greece.
C Department of Zoology, School of Biology, Aristotle University, 54124 Thessaloniki, Greece.
D Corresponding author. Email: nmonokro@bio.auth.gr
Soil Research 54(8) 905-913 https://doi.org/10.1071/SR15291
Submitted: 9 October 2015 Accepted: 3 March 2016 Published: 22 August 2016
Abstract
We investigated the variations in space and time of soil functionality in a Mediterranean serpentine soil for heavy metal and nutrient concentrations, microbial biomass and soil enzymatic activities (urease, dehydrogenase and alkaline phosphatase) in the rhizospheres of different plant species and in bare soil, during the humid and dry seasons of the year. Nutrients and heavy metals were also estimated in leaves of shrubs inhabiting the study area.
Four species of serpentine-tolerant shrubs were present: the evergreen-sclerophyllous Juniperus oxycedrus and Buxus sempervirens and the phryganic Cistus creticus and Thymus sibthorpii. The most significant differentiation of the soil environment was between bare and rhizosphere soil, and was mainly driven by the availability of potassium. Spatial variations related to plant identity were clear but less important than temporal variations. There was no relationship between soil and foliar concentrations of nutrients and heavy metals. Higher foliar concentrations were recorded in the phryganic species. Finally, there was no enzyme inhibition due to the heavy metal load of the serpentine soil. Enzymatic activities were lower for bare soil samples, while their temporal variations probably followed the temporal variations of temperature and humidity imposed by the Mediterranean climate.
Additional keywords: enzyme activities, heavy metals, microbial biomass, soil nutrients, ultramafic soil.
References
Aerts R (1995) The advantages of being evergreen. Trends in Ecology & Evolution 10, 402–407.| The advantages of being evergreen.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFejuw%3D%3D&md5=fc60353358a446873ac69f90c566da45CAS |
Allen E (1974) ‘Chemical analysis of ecological materials.’ (Blackwell Scientific Publishing: Oxford)
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’. (Eds B Markert) pp. 179–189. (VCH Publishing: Weinheim, Germany)
Batten KM, Scow KM, Davies KF, Harrison SP (2006) Two invasive plants alter soil microbial community composition in serpentine grasslands. Biological Invasions 8, 217–230.
| Two invasive plants alter soil microbial community composition in serpentine grasslands.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 |
Branco S, Ree RH (2010) Serpentine soils do not limit mycorrhizal fungal diversity. PLoS One 5, e11757.
| Serpentine soils do not limit mycorrhizal fungal diversity.Crossref | GoogleScholarGoogle Scholar | 20668696PubMed |
Breiman L, Friedman JH, Olshen RA, Stone CJ (1984) ‘Classification and regression trees.’ (Chapman and Hall Publishing: New York, NY)
Canadell J, Vilá M (1992) Variation in tissue element concentrations in Quercus ilex over a range of different soils. Vegetatio 99–100, 273–282.
| Variation in tissue element concentrations in Quercus ilex over a range of different soils.Crossref | GoogleScholarGoogle Scholar |
Cavigelli MA, Lengnick LL, Buyer JS, Fravel D, Handoo Z, McCarty G, Millner P, Sikora L, Wright S, Vinyard B, Rabenhorst M (2005) Landscape level variation in soil resources and microbial properties in a no-till corn field. Applied Soil Ecology 29, 99–123.
| Landscape level variation in soil resources and microbial properties in a no-till corn field.Crossref | GoogleScholarGoogle Scholar |
Chaperon S, Sauve S (2007) Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils. Soil Biology & Biochemistry 39, 2329–2338.
| Toxicity interaction of metals (Ag, Cu, Hg, Zn) to urease and dehydrogenase activities in soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFKrs78%3D&md5=b8e47aac638a1b9d3c680c0b4aa37803CAS |
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=c6a2521e3ef56dcddbbf6b04a193bfd2CAS |
Chochliouros SP (2005) Floristic and phytosociological research of Mount Vermion: an ecological approach. PhD Thesis, University of Patra. [In Greek].
Clark LA, Pregibon D (1992) Tree-based models. In ‘Statistical models in S’. (Eds JM Chambers, TJ Hastie) pp. 377–420. (Chapman and Hall Publishing: New York, NY)
Daghino S, Murat C, Sizzano E, Girlanda M, Perotto S (2012) Fungal diversity is not determined by mineral and chemical differences in serpentine substrates. PLoS One 7, e44233.
| Fungal diversity is not determined by mineral and chemical differences in serpentine substrates.Crossref | GoogleScholarGoogle Scholar | 23028507PubMed |
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=bb80ef89e0a3e3414469da51709725a9CAS |
Fioretto A, Papa S, Pellegrino A, Ferrigno A (2009) Microbial activities in soils of a Mediterranean ecosystem in different successional stages. Soil Biology & Biochemistry 41, 2061–2068.
| Microbial activities in soils of a Mediterranean ecosystem in different successional stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFKnsrjM&md5=76ee2ad072ed9f1b8369d14c08ad4f84CAS |
Friedl MA, Brodley CE (1997) Decision tree classification of land cover from remotely sensed data. Remote Sensing of Environment 61, 399–409.
| Decision tree classification of land cover from remotely sensed data.Crossref | GoogleScholarGoogle Scholar |
Gerendás J, Sattelmacher B (1999) Influence of Ni supply on growth and nitrogen metabolism of Brassica napus L grown with NH4NO3 or urea as N source. Annals of Botany 83, 65–71.
| Influence of Ni supply on growth and nitrogen metabolism of Brassica napus L grown with NH4NO3 or urea as N source.Crossref | GoogleScholarGoogle Scholar |
Goberna M, Pascual JA, Garcia C, Sanchez J (2007) Do plant clumps constitute microbial hotspots in semiarid Mediterranean patchy landscapes? Soil Biology & Biochemistry 39, 1047–1054.
| Do plant clumps constitute microbial hotspots in semiarid Mediterranean patchy landscapes?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisl2ru7s%3D&md5=6fe3a357e22eef0818e7df2f0311514fCAS |
Harrison S (1999) Local and regional diversity in a patchy landscape: native, alien, and endemic herbs on serpentine. Ecology 80, 70–80.
| Local and regional diversity in a patchy landscape: native, alien, and endemic herbs on serpentine.Crossref | GoogleScholarGoogle Scholar |
Hinojosa MB, Carreira JA, García-Ruíz R, Dick RP (2004a) Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils. Soil Biology & Biochemistry 36, 1559–1568.
| Soil moisture pre-treatment effects on enzyme activities as indicators of heavy metal-contaminated and reclaimed soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslKhtrg%3D&md5=04ffd213a8b473766a4985aa8b8cf7d6CAS |
Hinojosa MB, García-Ruíz R, Viñegla B, Carreira JA (2004b) Microbiological rates and enzyme activities as indicators of functionality in soils affected by the Aznalcóllar toxic spill. Soil Biology & Biochemistry 36, 1637–1644.
| Microbiological rates and enzyme activities as indicators of functionality in soils affected by the Aznalcóllar toxic spill.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslKht7o%3D&md5=ddd5d44fdea72221a0ae4c7e63afd231CAS |
Jenkinson DS, Powlson DS (1976) The effects of biocidal treatments on metabolism in soil. Soil Biology & Biochemistry 8, 209–213.
| The effects of biocidal treatments on metabolism in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28Xkslens7c%3D&md5=64dfb8c97dbea265168a08a1ce268b11CAS |
Kandeler E, Kampichler C, Horak O (1996) Influence of heavy metals on the functional diversity of soil microbial communities. Biology and Fertility of Soils 23, 299–306.
| Influence of heavy metals on the functional diversity of soil microbial communities.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XnsFemurw%3D&md5=32d2d9144217932de9867b1f580bab52CAS |
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.
Kuperman RG, Carreiro MM (1997) Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem. Soil Biology & Biochemistry 29, 179–190.
| Soil heavy metal concentrations, microbial biomass and enzyme activities in a contaminated grassland ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsl2lu7s%3D&md5=142647e07679eb276ffa0d74fd2eb6a5CAS |
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=eb099b87d04a5ac6253b81c30cee857aCAS | 19232424PubMed |
Madejón E, Burgos P, López R, Cabrera F (2001) Soil enzymatic response to addition of heavy metals with organic residues. Biology and Fertility of Soils 34, 144–150.
| Soil enzymatic response to addition of heavy metals with organic residues.Crossref | GoogleScholarGoogle Scholar |
Meyer GA, Keliher PN (1992) An overview of analysis by inductively coupled plasma-atomic emission spectrometry. In ‘Inductively coupled plasmas in analytical atomic spectrometry’. (Eds A Montaser, DW Golightly) pp. 473–505. (VCH Publishing: New York, NY)
Mikanova O (2006) Effects of heavy metals on some soil biological parameters. Journal of Geochemical Exploration 88, 220–223.
| Effects of heavy metals on some soil biological parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVahtL8%3D&md5=17ac37737d7156acd8f442cb48cfe51bCAS |
Moeskops B, Buchan D, Sleutel S, Herawaty L, Husen E, Saraswati R, Setyorini D, De Neve S (2010) Soil microbial communities and activities under intensive organic and conventional vegetable farming in West Java, Indonesia. Applied Soil Ecology 45, 112–120.
| Soil microbial communities and activities under intensive organic and conventional vegetable farming in West Java, Indonesia.Crossref | GoogleScholarGoogle Scholar |
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, Charalampidis G, Boutsis G, Sousanidou V, Papatheodorou EM, Argyropoulou MD (2014) Plant-induced differentiation of soil variables and nematode community structure in a Mediterranean serpentine ecosystem. Soil Research 52, 593–603.
| Plant-induced differentiation of soil variables and nematode community structure in a Mediterranean serpentine ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVOntbrP&md5=94dca01575b6bc03e852510860e16991CAS |
Nannipieri P, Kandeler E, Ruggiero P (2002) Enzyme activities and microbiological and biochemical processes in soil. In ‘Enzymes in the environment’. (Eds RG Burns, R Dick) pp. 1–33. (Marcel Dekker Publishing: New York, NY)
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=1b1f4c4ca79c2d44ad13119830fe4371CAS |
Obreza TA, Zekri M, Hanlon EA, Morgan K, Schumann A, Rouse R (2015) Soil and leaf tissue testing for commercial citrus production. University of Florida, Soil and Water Science Department, Publication no. SL253.04. Available at http://edis.ifas.ufl.edu/pdffiles/SS/SS53100.pdf [verified 2 August 2016].
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 Publishing: Washington DC)
Parkin TB (1993) Spatial variability of microbial processes in soil-a review. Journal of Environmental Quality 22, 409–417.
| Spatial variability of microbial processes in soil-a review.Crossref | GoogleScholarGoogle Scholar |
Paz-Ferreiro J, Gascó G, Gutierrez B, Méndez A (2012) Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil. Biology and Fertility of Soils 48, 511–517.
| Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil.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=4f054aa4c269b15eb991f35e9eac1c52CAS |
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 |
Pessoa-Filho M, Barreto CC, dos Reis FB Pessoa-Filho M, Barreto CC, dos Reis FB (2015) Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna. Antonie van Leeuwenhoek 107, 935–949.
| Microbiological functioning, diversity, and structure of bacterial communities in ultramafic soils from a tropical savanna.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhslemtbY%3D&md5=b664d735909d1dac763c019c8a37927bCAS | 25616909PubMed |
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 |
Qasemian L, Guiral D, Farnet A-M (2014) How do microlocal environmental variations affect microbial activities of a Pinus halepensis litter in a Mediterranean coastal area? The Science of the Total Environment 496, 198–205.
| How do microlocal environmental variations affect microbial activities of a Pinus halepensis litter in a Mediterranean coastal area?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Ois77F&md5=c1903f984b71e0962ff5cebc830eae3bCAS |
Quilchano C, Marañón T (2002) Dehydrogenase activity in Mediterranean forest soils. Biology and Fertility of Soils 35, 102–107.
| Dehydrogenase activity in Mediterranean forest soils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisF2qt7c%3D&md5=bd0cf9ebf0e674f6493ba98b1d3d7ea0CAS |
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=2acbb3b990522e54f92a9d315066fae6CAS | 8801006PubMed |
Roberts C, Jones JA (2000) Soil patchiness in juniper–sagebrush–grass communities of central Oregon. Plant and Soil 223, 47–61.
| Soil patchiness in juniper–sagebrush–grass communities of central Oregon.Crossref | GoogleScholarGoogle Scholar |
Ross DJ (1990) Estimation of soil microbial C by a fumigation extraction method: influence of seasons, soils and calibration with the fumigation-incubation procedure. Soil Biology & Biochemistry 22, 295–300.
| Estimation of soil microbial C by a fumigation extraction method: influence of seasons, soils and calibration with the fumigation-incubation procedure.Crossref | GoogleScholarGoogle Scholar |
Saul-Tcherkas V, Steinberger Y (2009) Temporal and shrub adaptation effect on soil microbial functional diversity in a desert system. European Journal of Soil Science 60, 871–882.
| Temporal and shrub adaptation effect on soil microbial functional diversity in a desert system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Sju77L&md5=d353c250aee0d1a363302f47f2c832b8CAS |
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=88c00608825a5a774da2af40d9941f95CAS |
Speir TW, Kettles HA, Percival HJ, Parshotam A (1999) Is soil acidification the cause of biochemical response when soils are amended with heavy metal salts? Soil Biology & Biochemistry 31, 1953–1961.
| Is soil acidification the cause of biochemical response when soils are amended with heavy metal salts?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntVOitbs%3D&md5=3da3b90540dfacb7ad13fd095d617839CAS |
Tabatabai MA (1994) Soil enzymes. In ‘Methods of soil analysis. Part 2: Microbiological and biochemical properties’. (Eds PS Bottomley, JS Angle, RW Weaver) pp. 775–833. (Soil Science Society of America Publishing: Madison, WI)
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=ae6941464ed917944cc6ec91f19cc954CAS | 21404012PubMed |
