microbial population growth potential as soil fertility treated with charcoal

8/9/2019 Microbial Population Growth Potential as Soil Fertility Treated With Charcoal

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Soil respiration curves as soil fertility

indicators in perennial central Amazonian

plantations treated with charcoal, and mineral

or organic fertilisers

Christoph Steiner

1

*, Murilo Rodrigues de Arruda

2

, Wenceslau G. Teixeira

2

and Wolfgang Zech11Institute of Soil Science and Soil Geography, University of Bayreuth, Bayreuth, Germany. 2Embrapa Amazonia

Ocidental, Manaus, Brazil. *To whom correspondence should be addressed: Biorefining and Carbon CyclingProgram, Driftmier Engineering Center, University of Georgia, Athens, GA 30602, USA

([email protected])

Abstract We assessed substrate-induced respiration and soil chemical properties in order

to study the influence of charcoal, nitrogen and phosphorus fertilisation on two different

perennial crops in a confounded factorial design on a highly weathered Amazonian upland

soil. Each plantation tested three different factors in three different levels making up 27 (33)

treatment combinations. Whereas the banana plantation received mineral fertilisation in

addition to charcoal applications (3rdfactor), the guarana (Paullinia cupana) plantation was fertilised organically using chicken manure and bone meal as the corresponding factors.

Charcoal increased pH, total nitrogen, availability of sodium, zinc, manganese, copper and

soil humidity, and decreased aluminium availability and acidity in the mineral-fertilised

plantation only. This caused a significant increase in basal respiration and microbial effi-

ciency in terms of carbon dioxide release per microbial carbon in the soil. The microbial

biomass, efficiency and population growth after substrate addition was significantly increased

with increasing levels of organic fertiliser amendments. We conclude that charcoal is a valu-

able component especially in inorganic-fertilised agricultural systems. Copyright 2008

John Wiley & Sons, Ltd

Key words: banana, biochar, Ferralsol, guarana, slash and char, soil respiration, TerraPreta

Introduction

Without continuous fertilisation, the extremely nutrient-poor Amazonian upland soils showno potential for agriculture beyond a tree-year lifespan of the forest litter mat, once biologicalnutrient cycles are interrupted by slash-and-burn (Tiessen et al. 1994). Slash-and-burn agri-culture is a common practice in the tropics (Giardina et al. 2000; Goldammer 1993) and is

Tropical ScienceTrop. Sci. (2008)Published online in Wiley InterScience(www.interscience.wiley.com) DOI: 10.1002/ts.216


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Christoph Steineret al.

Copyright 2008 John Wiley & Sons, Ltd Trop. Sci. (2008) DOI: 10.1002/ts

considered to be sustainable if adequate (up to 20 years) fallow periods follow a short periodof cultivation (Kleinman et al. 1995). Fertilisation is necessary for continuous cropping, but

the strongly weathered soils of the tropics have a low nutrient-retention capacity and theintense tropical rains wash easily available and mobile nutrients rapidly into deep soil layersunavailable to most crop plants (Giardina et al. 2000; Hlscher et al. 1997; Renck andLehmann 2004). In those situations, soil organic matter (SOM) plays a key role in soil-fertility maintenance because it contributes significantly to cation exchange capacity, and isthe main source of plant nutrients, including 95% or more nitrogen (N) and sulphur (S) andbetween 20% and 75% phosphorus (P) in surface soils (Duxbury et al. 1989; Zech et al.1997). After slashing and burning, cultivation further reduces the SOM content leading tosoil nutrient depletion (Goldammer 1993; Hlscher et al. 1997; Silva-Forsberg and Fearnside

1995; Zech et al. 1990). In addition, carbon dioxide (CO2) emissions from burning and SOMdecay contribute significantly to global warming (Fearnside and Barbosa 1998). There arethree principal ways to optimise nutrient uptake and nutrient release, and to minimise nutrientlosses: (i) multistrata agroforestry systems, which tend to mimic the dense mat of deep- andflat-rooting trees to minimise nutrient losses; (ii) organic fertilisation, such as the use ofcompost, mulch or manure, which releases nutrients in a gradual manner depending on themineralisation rate (Burger and Jackson 2003); and (iii) labour-intensive frequent applicationsof mineral fertiliser in small dosages. In a study by Lehmann et al. (1999), 63% of the Napplied as ammonium sulphate [(NH4)2SO4] was lost into subsoil, but just 1% of the organi-

cally applied mulched N was lost.The widespread existence of an anthropogenic fertile dark soil in the Amazon proves that

human soil-manipulation can create permanently fertile soil (Woods and McCann 1999). TheAmazonian dark earths (or Terra Preta de ndio) are found at pre-Columbian settlementsthroughout Amazonia in patches ranging in size from less than a hectare to many squarekilometres (McCann et al. 2001). Today, and as assumed in the past, those soils are and wereintensively cultivated by the native population. Their fertility is most likely to be linked toan anthropogenic accumulation of P and calcium (Ca) from bones (Lima et al. 2002), deposi-tions of these and many other nutrients from a variety of human habitation activities (Woods

2003), and black carbon (C) as charcoal (Glaser et al. 2001b; Lima et al. 2002). Amazoniandark earths contain significantly more C, N, Ca and potassium (K) and up to 13.9 g kg1phosphorus (P2O Pentoxide 5) (almost 4 g kg1 available P) (Lima et al. 2002), and cationexchange capacity, pH value and base saturation are significantly higher than in the surround-ing Oxisols (Glaser et al. 2000; Zech et al. 1990). Charcoal persists in the environment overcenturies and is responsible for the stability of the Amazonian dark earths SOM (Glaseret al. 2001a).

The recreation of Terra Preta provided the incentive to study charcoal as a soil amend-ment. Organic fertilisers such as chicken manure, bone meal and charcoal are easily available

in the vicinity of Manaus and frequently used as soil amendments. Carbonised materials areformally authorised for use as soil amendment material in Japan (Okimori et al. 2003) andare easily available for soil amelioration purposes in rural areas of Brazil (Steiner et al.2004b). As an alternative to slash-and-burn, charcoal could be produced out of the above-


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Charcoal as a soil amendment in central Amazonian plantations


ground biomass instead of converting it to CO2 through burning (Lehmann et al. 2002; Ogawa1994; Steiner et al. 2004b). Steiner et al. (2004a) found a strong correlation between microbial

population growth potential and plant biomass production in short cropping cycles, thusgiving reliable information about soil fertility. Many perennial crops need more than one yearto generate the first harvest. Continuous soil fertility assessment can be done using foliarnutrient contents and soil samples, but it is too late to avoid deficiencies if detected in planttissue, and yield data could be influenced by other adversities during this time period. Dataon soil respiration are fundamental for evaluating soil quality and analysing organic mattertransformation in ecosystems (Dilly 2003). Therefore, we addressed the following objectives:(i) to assess soil fertility using soil respiration curves in two different perennial crops; (ii) tocompare the microbial response to organic fertilisation in comparison to inorganic fertilisa-

tion; and (iii) to assess charcoals influence on soil fertility and microbial activity.

Materials and methods

This study was conducted at the Embrapa (Empresa Brasileira de Pesquisa Agropecuria)Amaznia Ocidental station, near Manaus, Brazil. The average annual precipitation is2503 mm (197193) with a maximum between December and May. The natural vegetationis tropical rainforest. The soils are classified as xanthic Ferralsols (FAO 1990) and are clayey(with over 80% clay) and strongly aggregated. Two experiments were established with two

different perennial crops banana (Musa sp.) and guarana (Paullinia cupana Kunth) in aconfounded factorial design. Each plantation tested three different factors (charcoal, N andP) at three different levels making up 27 (33) treatment combinations. Such a design is com-monly used to test levels of fertilisation (Montgomery 1976; Pimentel-Gomes 1990).

Clones from tissue culture of the banana variety Caipira were used for the experiment.The bananas were planted in holes (0.4 0.4 0.6 m) with a spacing of 3.0 2.0 m in May2001. The planting holes were prepared 30 days before planting and filled with a mixture ofsoil, charcoal (0, 2.7 or 5.4 kg), chicken manure (2.5 kg), simple superphosphate (200, 300or 400 g) and lime (200 g). Urea (0, 200 or 400 g) was applied on the soil surface. The

application of urea, simple superphosphate and charcoal was repeated on the soil surface(Table 1). Furthermore, the plants were fertilised with potassium chloride (KCl, 200 g) inJanuary 2003 and March 2004, zinc sulphate (ZnSO4, 50 g) in October 2002 and FTR BR12 (micronutrient mix, 50 g) in February 2004. The combinations of three doses of charcoal,P and N form 27 treatments consisting of 162 plants (6 plants per treatment).

The guarana plantation covered 4 ha with 1604 plants. From October to December 2002the area was cleared and the plants were planted in March 2003. As the intention of theexperiment was to produce organic guarana, weed and pest control were done without pesti-cides. The invading natural ground cover was mowed periodically. Fertilisation was restricted

to organic amendments only. In July 2003 ground charcoal was applied to the soil surface.Bone meal was applied in August 2003 and chicken manure in October 2003. Charcoal, bonemeal and chicken manure were applied in three different doses allowing the formation of 27different treatment combinations (see Table 1), each treatment consisting of six guarana


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Table1.Factorsandapplicationlevelsoforganicandinorganicamendments.Eachp

lantationwastestingthreedifferent

factorsinthreedifferentlevelsmakingup27

(33)different

treatmentcombinations

Crop/Fertilisa

tion

Factor

Level

Surfaceapplication

month/year

Nutrientcontents(gkg1)

0

1

2

N

P

K

Ca

Mg

Banana/Inorg

anic

Charcoal(kg)

0

2.7

5.4

07/0301/04

5.4

0.03

0.23

0.82

0.17

P(SSP)(g)

200

300

400

07/0303/04

77.4

130200

N(urea)(g)

0

200

400

10/0201/0307/0303/04

420

Guarana/Organic

Charcoal(kg)

0

2.7

5.4

07/03

5.4

0.03

0.23

0.82

0.17

Bonemeal(g)

0

200

400

08/03

57.6

100

2.4

200

3.5

Chickenmanure(kg)

0

4

8

09/03

22.5

4.8

17.2

1.7

0.56

SSP=S

implesuperphosphate.Otherabbreviationsaredefinedinthetext.


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plants. The entire experiment was established in five repetitions with five different varietiesof guarana. For soil respiration curves only one variety (Maus) was chosen.

Topsoil (0.00.1 m) samples were taken on 8 April 2004 in the banana plantation and 23April 2004 in the guarana plantation. Most microbial activity was expected in the topsoil.One composite sample was formed out of four sub-samples taken in the fertilised area, andwas placed in plastic bags (500 g soil per sample). The first and sixth plants were notsampled, to minimise the influence of adjacent treatments. Immediately after sampling, thesoil was treated and analysed using the following procedure.

The soil was sieved (


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For soil characterisation, we analysed the soil samples for N, P, K, sodium (Na), Ca,magnesium (Mg), aluminium (Al), acidity (Al + H), iron (Fe), zinc (Zn), manganese (Mn)and copper (Cu). Plant-available P, K, Na, Zn, Mn and Cu was analysed in Mehlich 1 extractsand Mg, Ca and Al in KCl extracts. The micro-nutrients (Fe, Zn, Mn and Cu), Ca and Mgwere determined by atomic spectrometry (GBC Avanta Analitica, Dandenong, Australia).Al was determined by titration and P was measured using a photometer (Heios , ThermoSpectronic, Cambridge, UK) with the molybdenum blue method (Olsen and Sommers 1982).K was analysed with a flame photometer (Micronal B 262, Sao Paulo, Brazil). Total C and

N were analysed by dry combustion with an automatic C/N analyser (Elementar, Hanau,Germany). The soil pH was determined in water using an electronic pH meter with a glasselectrode (WTW pH 330).

SYSTAT 8.0 was used to undertake a General Linear Model analysis to evaluate signifi-cant influences of each factor (charcoal, N and P) and interactions. Regressions and figureswere drawn using SigmaPlot. Pearson correlation with two-tailed test of significance wasperformed with SPSS 12.0.

Results and discussion

Charcoal was the only factor that the organic guarana plantation and the inorganically fer-tilised banana plantation had in common. Charcoal increased basal respiration and respirationper microorganism (metabolic quotient) significantly (p= 0.003 and 0.002, respectively) in

Figure 1. Example of a respiration curve. BR = basal respiration; SIR = substrate-induced respiration; k = the slope(indicating rate of population increase).


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the banana plantation. However, the organically fertilised soil showed only increased respira-tion per microorganism (p= 0.018) due to charcoal application. Reasons responsible for this

might be the significantly increased pH (p< 0.001), total N (p= 0.025), availability of Na(p= 0.004), Zn (p= 0.036), Mn (p= 0.012), Cu (p= 0.016) and humidity (p= 0.033), andthe decreased Al (p< 0.001) and acidity (p= 0.005), in the banana plantation due to charcoalapplication (Figure 2). Previous studies have shown that soil charcoal amendments increasedplant growth of annual crops significantly (Steiner et al. 2007), increased the uptake of P, K,Ca, Zn and Cu by the plants, reduced N leaching (Lehmann et al. 2003) and stimulated soilmicrobial community (Steiner et al. 2008a). The organic fertilisers (chicken manure and bonemeal) had more influence than charcoal in the guarana plantation. However, the significantlyinfluenced parameters (available Na, Zn, Mn, total N, pH and decreased acidity) due to

charcoal applications in the banana plantation could be correlated with increasing basalrespiration in the guarana plantation (Figure 3). Although four sub-samples were taken, it ispossible that not every sample was representative due to the texture and floating nature ofcharcoal. The banana plantation received more charcoal over time, which explains the stron-ger influence on soil chemistry and soil respiration. In the mineral-fertilised treatment a sig-nificant negative correlation was found between the soils C content and microbial biomassper soil C content (Cmic/Corg). Such a correlation was not possible in the case of organic fer-tilisation. The chicken manure factor increased the Cmic/Corg ratio significantly (p= 0.017).We suppose that this difference is due to recalcitrance (Seiler and Crutzen 1980; Skjemstad

2001) and low available nutrient contents of charcoal in contrast to easily degradable andnutrient-rich chicken manure (Figure 4).

Although both organic amendments contained P and N (Table 1), we will concentrate ourdiscussion on the influence of chicken manure together with inorganic N fertilisation. Chickenmanure significantly increased basal respiration (p= 0.011), microbial biomass (p= 0.010),microbial population growth after substrate addition (p= 0.015), Cmic/Corg ratio (p= 0.017)and specific respiration per microorganism (p = 0.004). Inorganic N fertilisation did notinfluence respiration parameters significantly. Chicken manure increased total N (p= 0.031),pH (p= 0.001), available P (p= 0.001), K (p= 0.012), Na (p= 0.018), Ca (p= 0.001), Mg

(p< 0.001), Zn (p= 0.007), Mn (p= 0.005) and Cu (p= 0.011), and decreased acidity (p=0.013) and the availability of Al (p< 0.001). Dilly (2003) found much higher basal respira-tion and microbial growth if glucose was added together with N. We found increased basalrespiration and total N content of the soil due to charcoal application. Increased retention offertilised N has been observed by Lehmann et al. (2003) and Steiner et al. (2008b). At thetime of assessment (April 2004) inorganic N fertilisation (March 2004) did not influence thesoils N content significantly. Due to low nutrient-retention capacity and high permeabilityof these soils, strong tropical rainfalls cause rapid leaching of mobile nutrients, particularlyof N (Giardina et al. 2000; Hlscher et al. 1997; Renck and Lehmann 2004).

Bone meal application increased microbial biomass (p= 0.031), population growth aftersubstrate addition (p= 0.031) and specific respiration per microorganism (p= 0.013). MineralP fertilisation did not influence soil respiration significantly, but did increase the availabilityof P (p< 0.001) and Ca (p= 0.033), whereas bone meal increased the total N content (p=


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Figure 2. Regressions of the factor charcoal with the most-influenced soil chemistry parameters in the inorganicallyfertilised banana plantation. Abbreviations are defined in the text.


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Figure 3. Regression of soil chemical parameters with basal respiration in the organically fertilised guarana planta-tion. Abbreviations are defined in the text.


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0.047) and decreased Al availability (p= 0.004). P is usually considered the primary limitingnutrient to plant production on the highly weathered soils of the humid tropics because it isstrongly bound to Al and Fe oxides and is thus not available for plants (Garcia-Montiel et al.2000). P could become available through fine-root endomycorrhizal associations (Garcia-

Montiel et al. 2000) and through heterotrophic phosphate-solubilising microorganisms, whichare supposed to be stimulated by soil charcoal additions (Kimura and Nishio 1989). As themicrobial population growth after substrate addition was not affected by mineral fertilisationit is unlikely that P was a limiting factor.

The influence of charcoal on soil respiration as well as on soil chemistry was stronger inthe mineral-fertilised banana plantation in contrast to the organically fertilised guarana wherechicken manure had the most influence on soil fertility and thus microbial population andactivity. The highest microbial biomass (614.55 g Cmic g1 soil) and high microbial popula-tion growth after substrate addition (k = 0.1043) were found in the treatment with the highest

level of chicken manure, bone meal and charcoal. Steiner et al. (2004a) found higher micro-bial population growth on the same soil after charcoal and mineral fertiliser application incomparison to mineral fertilisation alone after four cropping cycles. The increased availabilityof micronutrients due to charcoal application might be caused by direct fertilisation because

Figure 4. Regression of the soils carbon (C) content and microbial biomass per soil C content (Cmic/Corg) in theinorganically fertilised banana plantation in comparison to the organically fertilised guarana plantation.


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solubility of inorganic forms of micronutrients decreases with increasing pH (Duxbury et al.1989). Reactive Al and Fe surfaces can form complexes with SOM (Duxbury et al. 1989),

which might explain the reduced Al and Fe concentrations due to charcoal application. Alcan reduce crop production severely (Sierra et al. 2003).

Charcoal contains only small quantities of nutrients (Table 1): therefore, the increase intotal N content caused by charcoal application is probably due to N retention. This retentionwas significant in the case of mineral fertilisation because mineral N is very mobile and sus-ceptible to leaching losses. The microbial biomass itself represents a significant sink or sourceof nutrients (Duxbury et al. 1989). Microbial immobilisation is described as an importantmechanism to retain N in those soils highly affected by leaching (Bengtsson et al. 2003;Burger and Jackson 2003). It is questionable how far charcoal C can be utilised by microbes

and thus favour N immobilisation. Charcoal decreased the ratio of microbial C to soil C(Cmic/Corg,p= 0.012) due to its refractory nature, whereas the chicken manure factor increasedthis ratio (p= 0.017). The soil C content was increased by all organic amendments (charcoal,bone meal and chicken manure, p< 0.05).

This study represents just a snapshot of actual soil fertility. Time series data are necessaryto compare mineral fertilisation with organic fertilisation in terms of nutrient conservation.We conclude that charcoal is an important soil constituent, especially if the agro-system isfertilised inorganically.

Acknowledgements

The research was conducted within the Terra Preta Nova project at Embrapa AmazniaOcidental and SHIFT ENV 45, a GermanBrazilian cooperation (BMBF No. 0339641 5A,CNPq 690003/98-6). A financial contribution was given by the doctoral scholarshipprogramme of the Austrian Academy of Sciences.

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microbial population growth potential as soil fertility treated with charcoal

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