Structural liming in agriculture: short- and long-

term effects on soil biota

Authors: Erkki Palmu & Katarina Hedlund*

*Department of Biology, Lund University, Lund, Sweden

Abstract

The European Commission’s committee on organic farming (no. 889/2008)

regulates which compounds are allowed in certified organic farming in EU. As it stands today

structural liming with quicklime and slaked lime is prohibited in certified organic farming.

There is thus a need to review knowledge how these more reactive forms of lime affect the

soil biology.

Liming acidic soils is an effective practice to stabilize soil organic matter

content, improve nutrient mineralization rate and to enhance plant growth. While saprophytic

fungi are the main decomposers in acid soils, mainly bacteria, arbuscular mycorrhizal fungi

and soil fauna perform this function in calcareous soils. Calcium carbonate based liming

benefits soil aggregate structure by stimulating growth of plant roots and fungal hyphae,

earthworm activity and input of above-ground crop residues. Plant growth also benefits from

well-developed soil-aggregate structure and stability. Soil organic matter and biological

activity maintains the soil aggregates, which in turn affect soil aeration, porosity and water

infiltration that are critical for plant growth. Structural liming (quicklime and slaked lime)

“mimics” biological soil processes, by rapidly forming and enhancing soil aggregate structure

through means of chemical reactions rather than biological long-term aggregate formation via

the activity of soil organisms.

Evidence indicate that structural liming may have negative short-term effects on

microbial communities, and earthworm and coleopteran populations. A lack of evidence on

effects of especially structural liming on the arable soil biology is quite apparent for many

taxa, which partially prevents evidence based conclusions. Liming induced changes in

microbial emissions of greenhouse gases (N2O), adds global environmental significance to an

otherwise local to regional sphere of effects. Liming in relation spatial and temporal scale-

dependence of dispersal and recolonization processes have not been sufficiently investigated

in the available literature. As structure liming compounds mainly have short-term effects, the

amount of recently limed arable land in the surrounding landscape may influence the recovery

of the soil community of a focal field. A sufficient heterogeneity of arable production cover

types and management types likely can play an important role, e.g. for animal biodiversity in

agricultural landscapes

.

Contents

Introduction _______________________________________________________________ 1

Objectives of this report __________________________________________________________ 1

Structural liming - A brief technical background _______________________________________ 2

Agricultural liming ______________________________________________________________ 2

Structural liming – Environmental impact ____________________________________________ 3

Soil biota – A brief introduction ____________________________________________________ 4

Review methods ____________________________________________________________ 5

Short- and long-term effects of liming on soil fauna -Summary of results ______________ 7

Short- and long-term effects of liming on soil biota –Full review ____________________ 11

Microbial communities __________________________________________________________ 11 Microbial communities - A brief summary of their contribution to soil functions ___________________ 11 Effects of liming on microbial communities _________________________________________________ 11

Micro- and mesofauna __________________________________________________________ 15 Micro- and mesofauna - A brief summary of their contribution to soil functions ____________________ 15 Effects of liming on micro- and mesofauna __________________________________________________ 15

Macrofauna ___________________________________________________________________ 17 Macrofauna - A brief summary of their contribution to soil functions ____________________________ 17 Effects of liming on macrofauna __________________________________________________________ 18

Knowledge gaps ___________________________________________________________ 21

Conclusions _______________________________________________________________ 23

References ________________________________________________________________ 25

1

Introduction

Objectives of this report

While the physical and chemical influences of structural liming such as

aggregate stability, nutrient leaching and pH are relatively well understood, less is known of

the effects of structural liming with quicklime and slaked lime on soil biology. Therefore, the

objective of this work is to review literature on the effects of structural liming (i.e. treatment

with quicklime or slaked lime) on soil biota. Rapidly increasing soil pH and/or rapid

concomitant changes in other soil parameters, e.g. reduced water availability caused by the

chemical reaction of quicklime and water are likely to impact soil biota in different ways. Due

to the immediate chemical reactions in the soil after structural liming one can expect some

disparity in short- and long term effects, thus the temporal dimension is likely to reveal

important additional insight. Thus, with initial understanding of the fundamental effects of

structural liming on the abiotic soil environment, this review will attempt to find answers, or

identify needs for further research, to the following questions:

How do structural liming compounds (based on quicklime or slaked lime) affect soil-

dwelling biota, as compared to “non-structural” liming compounds (based on

limestone)?

Is the potential impact of structural liming vs. limestone on soil biota dependent on

time, i.e. do short- (days to months) and long term (years) effects vary?

Does the potential impact of structural liming vs. limestone depend on the functional

niche and/or trophic level of the biota, from the microorganism community to the

meso- and macrofauna community?

The European Commission’s committee on organic farming (no. 889/2008)

regulates which compounds are allowed in certified organic farming in EU. As it stands today

structural liming with quicklime and slaked lime is prohibited in certified organic farming.

Generally, studies of the effects of structural liming, and indeed the differentiation of effects

between less reactive (calcium carbonate/limestone) and more reactive (quicklime/slaked

lime) liming compound on biodiversity, have for many years not been prioritised in

agroecology research. There is thus a need to review knowledge how these more reactive

forms of lime affect the soil biology.

2

Structural liming - A brief technical background

The term “structural liming” pertains to the stabilizing effects of either

quicklime or slaked lime on clay soils. Both quicklime (Calcium oxide, CaO) and slaked lime

(Calcium hydroxide, Ca[OH]2) can be used to enhance the structural strength of clayey soil

through a cementitious reaction that takes place between the lime and the clay (Oates 2008).

The structural effect of these compounds has long been used to stabilise “native materials” for

construction purposes. Quicklime, also known as burnt lime, is also used for production of

e.g. fertilizers and concrete. When quicklime is dissolved in water the chemical reaction

releases thermal energy through formation of the less volatile but still reactive hydrate

calcium hydroxide, more commonly known as slaked (or hydrated) lime (Oates 2008). Both

quicklime and slaked lime have relatively strong desiccating properties, but quicklime more

efficiently binds water when compared to slaked lime (Schotsmans et al. 2012). Mixing of

quicklime into soil will, depending on the soil moisture, fraction of quicklime, and the total

amount of the applied liming compound, briefly reduce soil moisture content and increase soil

temperature.

Agricultural liming

Many agricultural soils have sub-optimal growth conditions due to low soil-pH,

therefore liming often has a beneficial effect on plant growth and liming acidic soils is an

effective practice to stabilize soil organic matter content and improve the mineralization rate

of the organic matter (Fageria 2012). Plant growth also benefits from well-developed soil-

aggregate structure and stability (Tisdall and Oades 1982). A thorough understanding of soil

properties prior to soil calcium amendment is critical as different calcium sources (e.g.

limestone or gypsum), or combinations of these, will cause different results for soil structural

stability depending on e.g. soil organic matter content (Baldock et al. 1994). In natural and

semi-natural soils these parameters are regulated by plant growth and soil biota activity from

micro- to macro scales. In conventionally tilled Australian arable soils, limestone (CaCO3)

liming increased aggregate stability significantly after 3 years’ (Chan and Heenan 1998).

Increased long-term soil aggregate stability was achieved at lower soil organic-carbon content

which indicated that limestone liming changed the way soil aggregates were stabilized (Chan

and Heenan 1999). Beneficial long-term effects of calcium carbonate (chalk/limestone) on

soil aggregate structure are stimulated by biological activity, e.g. via growth of plant roots

(Briedis et al. 2012b) and fungal hyphae (Tisdall 1991), input of above-ground crop residues

(Briedis et al. 2012a), and by earthworm activity (Lavelle 1997). Structural liming (with

3

quicklime and slaked lime) of arable soils “mimics” biological soil processes, by rapidly

forming and enhancing soil aggregate structure through means of chemical reactions rather

than biological long-term aggregate formation via the activity of soil organisms. Recent

research suggest that structural liming has short-term effects (Keiblinger et al. 2016) while

limestone has long-term effects (Bennett et al. 2014) on soil aggregate stability. Due to

greater alkalinity, liming with quicklime allows for short-term boosts of soil pH and

improvements of soil aggregate stability in clay soils (Keiblinger et al. 2016), simply not

achievable with limestone. It is noteworthy that soil pH is on par with limestone treated or

unlimed soils within 1-3 months (Keiblinger et al. 2016). In a Swedish field experiment on

arable soil, soil aggregate stability was more related to tillage regime than to a structural

liming (CaO) treatment performed 8 years prior to sampling (Stenberg et al. 2000), indicating

a lack of long-term improvements. Meanwhile, limestone (CaCO3) treatments can have

beneficial effects on soil aggregate stability and other soil properties at longer time spans,

more than ten years after application, depending on soil type, soil pH, buffering capacity and

tillage regime (Bennett et al. 2014).

Structural liming – Environmental impact

Local long-term toxicity from structural liming with quicklime or slaked lime

application is unlikely as quicklime when combined with water quickly forms slaked lime,

which further dissolves into hydroxyl and calcium ions and combines with carbon dioxide to

form calcium carbonate. Structural liming is sometimes promoted as an environmentally

beneficial agricultural management practice, mainly because both quicklime (Svanbäck et al.

2014, Ulén and Etana 2014) and slaked lime (Ulén and Etana 2014) can mitigate phosphorous

leaching from ploughed clay soils. However, the effects of structural liming on phosphorous

leaching under different soil phosphorous and clay content conditions are yet to be fully

disentangled (Bergström et al. 2015). Liming in combination with ploughing has also resulted

in significantly higher total nitrogen leaching as compared to shallow-tilled fields (Svanbäck

et al. 2014). This is an important note as nitrogen from agriculture is one of the drivers of

eutrophication processes, e.g. in Swedish coastal areas (Boesch et al. 2008).

Environmental externalities such as the carbon footprint from the energy

intensive quicklime production can decrease the overall environmental benefits of structural

liming in agriculture. Quicklime is produced by heating of limestone (CaCO3) and is one of

three main human activities (the two others being burning of fossil fuels and land-use change)

known to have changed the natural carbon cycle by the release of CO2 into the atmosphere

4

(Martin and Sauerborn 2013). A less intensive product for structure liming is called

“Ekokalk” (or freely translated to English “ecolime”) derived from waste products from the

steel industry and is currently being tested in trials at the Swedish University of Agricultural

Sciences. Liming in forestry in Sweden have however indicated that a lime products from the

steel industry (converter slag) was less beneficial for earthworm abundance as compared to

calcium carbonate/dolomitic lime (Persson et al. 1996).

Soil biota – A brief introduction

Soil hosts a vast number of organisms, from microbial communities and

microfauna with body diameters under 0.2 mm, e.g. archaea, bacteria, fungi, protozoa, and

nematodes; to mesofauna that inhabit a body diameter range from 0.1 to 2 mm, e.g. mites

(Acari), Enchytraeidae and Collembolans; to macrofauna that usually occupy body diameters

from 2 to 20 millimetres, e.g. earthworms (Lumbricidae), woodlice (Isopoda) and millipedes

(Diplopoda) (Swift et al. 1979, Brussaard 1997, Lavelle 1997). With respect to soil pH,

saprophytic fungi are the main agents of litter degradation and nutrient mineralization in acid

soils while mainly bacteria, arbuscular mycorrhizal fungi and soil fauna are the main

decomposers in calcareous soils (Bothe 2015). Soil organic matter and soil organism activity

maintains the soil aggregates (Brussaard 1997), which in turn affect soil properties such as

aeration, porosity and water infiltration that are critical for plant and microbial growth (Nehl

and Knox 2006). Soil aggregates once formed and stabilized as a result of biological activity

can persist for long periods of time (Blanchart et al. 1999), therefore management practices

that directly eliminate soil ecosystem engineers may not cause an immediate corresponding

deterioration of soil quality (Wall 2004). In addition, multiple associations between traits and

ecosystem functions across trophic levels (Brussaard 2012) can obscure direct connections

between concomitant management induced changes in basic soil biodiversity metrics (e.g.

species richness and diversity) and soil parameters such as soil aggregate stability.

5

Review methods

The literature review was performed using a search string approach on Web of

Science, Google Scholar, and Google, using a number of search terms relating to soil biota

and liming treatments of soils. The literature search focussed mainly on results obtained via

Web of Science, but searches were expanded with Google Scholar and Google. First, an initial

search was performed using the following terms: liming OR lime, as liming regime topics in

the first field; bacteria* OR fung* OR arthropod* OR nematod* OR protozo* OR AMF OR

"arbuscular mycorrhizal fung*" OR "AM fung*" OR acarid* OR invertebrat* OR

collembola* OR isopod* OR chilopod* OR diplopod* OR coleoptera*, as soil-biota topics in

the second field; arable* OR farmland* OR agricultur* OR grassland* OR "semi-natural

grassland*", as strata topics in the third field. The search returned 177 hits on Web of Science.

A more specific search on search terms relating to structural liming was performed together

"structure lim*" OR "structural lim*" OR quicklime OR "burnt lime" OR CaO OR "calcium

oxide" OR "slaked lime" OR "hydrated lime" OR "calcium hydroxide", as topics in the first

field, and the same search topics as the first search in the second and third fields. However, as

this search returned few hits, the search field with strata was expanded to include the term

“soil*”, and thereafter 86 hits were returned on Web of Science. The relevance of each of

these papers was assessed and they were screened for details concerning whether a separate

liming treatment and a (untreated or limestone) control was a part of the experimental design.

Some papers report results of cessation of management, usually both fertilisers, lime, and

grazing, making it difficult or impossible to disentangle effects of the different management

activities. Using a “chain-search” approach, additional literature was identified via reference

lists in the initial round of papers. Soil biota studies encompassing treatments either with

“conventional lime” (e.g. limestone) or with “structural lime” were included in this review.

The review focussed on terrestrial arable soils, but if relevant results were lacking for arable

soils, results based on other soils/substrates were also reviewed. However, for arable soils,

extrapolations and conclusions based on results from e.g. forest soils may not be appropriate,

as initial values of often crucial soil parameters such as pH, clay content, and organic-matter

content can differ drastically. Likewise, the aim was to include only peer-reviewed articles,

but if found appropriate, non-peer-reviewed material (e.g. governmental reports, book

chapters) was also examined. Research results on effects of liming in aquatic ecosystems were

generally excluded as the focus of this review was on terrestrial agroecosystems.

6

The reviewed information was summarized in a table where either (1) liming

with either calcium carbonate/limestone or (2) structural liming with quicklime/slaked lime

were generalized into an either a positive (green up-pointing arrow), negative (red down-

pointing arrow), or variable/unknown (yellow horizontal arrow) category with respect to

effects on groups of soil biota. Here short-term effects are categorized as effects on soil biota

measured on the order of day to a year after an experimental liming treatment, while long-

term effects are categorized as effects on soil biota that have been observed on the order of

three or more years after an experimental liming treatment. In order to facilitate basic

between-study comparisons of liming effects information is provided regarding soil type and

clay content, if these parameters were supplied in the referenced paper. Here, when a

treatment is referred to as limestone based, that implies the use of crushed/granulated

limestone material.

7

Short- and long-term effects of liming on soil fauna -Summary of

results

The evidence of short- and long-term effects of liming on soil biota show

variable results (table 1), and the direction of the effect depends mainly on which focal taxa

that was investigated. The directions of the summarized effects (in table 1) should be viewed

taking in to account that especially arrows followed by question marks represent knowledge

gaps and that more research is needed for that specific taxa. Both calcium carbonate/limestone

based liming and quicklime/slaked lime based structural liming will to some extent modify

soil organism communities through changes in the soil environment, e.g. soil pH increments.

Elevated soil pH may, depending on availability of soil organic matter, enhance the

abundance/biomass of e.g. earthworms, which may in turn have cascading effects on other

smaller sized soil biota (cf. Persson et al. 1996).

Microbial communities. The results highlight a discrepancy between short and

long-term effects on microbial communities in agricultural soils, and that effects also depends

on soil management and properties such as clay and organic matter content. In the long term,

structural liming may have a stronger influence on bacterial communities as compared to

fungal ones, a result of e.g. the functional bacterial community composition shifts from a

dominance of denitrifying to ammonia oxidising bacteria (Baggs et al. 2010).

Micro- and mesofauna. There is a lack of studies that investigate effects of

liming, and especially structural liming, on micro- and mesofauna on arable soils. However,

some tentative conclusions may be formulated. The overall changes in abundance of

nematodes (Hyvönen et al. 1994) and enchytraeids (Persson et al. 1996, Yli-Olli and Huhta

2000) as a result of liming in general may depend on the presence of earthworms. The

diversity of microarthropods (mites and collembolans) are not significantly affected by

limestone liming, but subtler changes in species composition indicates species dependent

increases and decreases in abundances (Cole et al. 2005, Wal et al. 2009).

Macrofauna. The lack of evidence of liming effects in arable soils is perhaps

greatest for the macrofauna. In the short term, some evidence indicates negative effects of

structural liming (CaO) on earthworm abundance (Mijangos et al. 2006). Meanwhile

limestone liming has generally beneficial long-term effects on earthworms. There is however

a lack of evidence from earthworm research in arable soils that disclose results concerning

effects on more informative biodiversity metrics (species richness, diversity, evenness) and

8

species composition. For coleopterans, structure liming compounds have been found to cause

mortality for both juveniles and adults. There is however a lack of evidence from field trials

and effects on entire native species communities rather than just single species experiments.

No results were found concerning effects of liming on other macroarthropods such as

woodlice (Isopoda) and millipedes (Diplopoda).

9

Table 1. Summary of effects of calcium carbonate/limestone based liming and calcium oxide/calcium

hydroxide based “structural” liming on different functional and taxonomical groups of soil biota in

arable soil. Green arrows indicate a generally positive effect, red arrows indicate generally negative

effects, yellow arrows indicate that a general effect could not be determined, “?” indicates need for

more research, “d” indicates dependence on presence of other soil fauna and “m” indicates mixed

effect on abundance, diversity and evenness.

Soil functional

group Soil taxa Liming substance

Short-term

effects

Long-term

effect

Microbial

communities

Bacteria

CaCO3

CaO/ Ca[OH]2 ?

Fungi

CaCO3

CaO/ Ca[OH]2 ? ?

Micro-/mesofauna

Nematoda

CaCO3 ? dm

CaO/ Ca[OH]2 ? ?

Acari

CaCO3 ?

CaO/ Ca[OH]2 ? ?

Collembola

CaCO3

CaO/ Ca[OH]2 ? ?

Enchytraeidae

CaCO3 ? d

CaO/ Ca[OH]2 ? ?

Macrofauna

Earthworms

CaCO3

CaO/ Ca[OH]2 ? ?

Coleoptera

CaCO3 ? ?

CaO/ Ca[OH]2 ? ?

10

11

Short- and long-term effects of liming on soil biota –Full review

Microbial communities

Microbial communities - A brief summary of their contribution to soil functions

Microbial communities including bacteria and fungi deliver several ecosystem

services depending on microbial interactions and interactions with other soil organisms. Plant-

growth promoting bacteria that occur in the narrow area around the plant roots (rhizosphere)

can inhibit plant disease (Lugtenberg and Kamilova 2009), and the presence of arbuscular

mychorrizal fungi (AMF) may further stimulate rhizosphere colonization by beneficial

rhizobacteria (Lioussanne 2013). In natural ecosystems and in low intensity agroecosystems

fungal communities drive nutrient cycling processes as they are the dominant micro-

decomposers of organic residue near the soil surface (Six et al. 2006, Schreiner et al. 2014).

AMF can increase the resilience of host plants to endoparasitic nematodes (Vos et al. 2012,

Vos et al. 2013), and reduces nitrogen leaching (de Vries et al. 2013). Fungal hyphae, both of

AMF and saprotrophic fungi contribute to stabilisation and formation of soil aggregates

(Tisdall 1991), which depends on supply of decomposable organic material and carbon from

plant roots (Tisdall and Oades 1982). Agricultural management practises contribute to

observed changes of soil quality and microbial biomass and activity (Fließbach et al. 2007,

Davis et al. 2012). Increases in tillage intensity has been found to be the main factor in

decreasing soil decomposition rates (Marwitz et al. 2014) and nutrient and water retention

potential (Williams and Hedlund 2014). AMF are more sensitive to soil disturbance than

saprotrophic fungi and other microorganisms and management options such as reduced tillage

increase biomass of both saprotrophic fungi and AM fungi (van Groenigen et al. 2010).

Effects of liming on microbial communities

Microbial communities are the most well studied group, with respect to effects

of liming. Soil pH has strong effects on diversity and composition of bacterial communities

(Lauber et al. 2009), while effects on fungal communities are weaker and less pronounced

(Rousk et al. 2010). Different liming materials have different effects for abiotic soil properties

and microbial activity, and effects on soil pH and microbial activity (as indicated by

enzymatic activity) has been found to be dependent on the interaction between soil type and

soil depth (Lalande et al. 2009). On English grassland clay loam, a very large one time

application of chalk (150-250 Mg ha-1) in the mid-19th century still results in a clear soil pH

gradient which significantly shifts the functional composition of microbial communities

12

(Rousk et al. 2009, Rousk et al. 2010). Further, soil type and organic carbon content regulate

the effects of soil pH on soil microorganisms (Locke et al. 2008, Huang et al. 2013). Although

increments in soil pH can be achieved with both chalk, limestone and with structural lime (i.e.

quicklime and slaked lime) alike, the strong pH effect of structure liming may cause caustic

effects on the soil biology that does not occur with calcium carbonate compounds.

The temporal effect of liming has to some extent been tested both in the lab and

in field experiments. Microcosm experiments using both arable and grassland soils, indicated

adverse short-term effects (1-28 days) of quicklime treatments on soil microbial biomass and

respiratory activity (Muhlbachova and Tlustos 2006). While calcium carbonate yielded the

highest microbial biomass and respiratory activity as compared to quicklime and control,

quicklime yielded the lowest microbial biomass. In arable soils, the immediate pH effect and

the reactive behaviour of quicklime causes a decline in microbial biomass and respiratory

activity and a concomitant increase in easily available carbon (Muhlbachova and Tlustos

2006). After a year however, when soil pH levels were similar (pH = 7.25-7.76), quicklime

(CaO) yielded the highest values for respiratory activity and easily available carbon in arable

soils, while calcium carbonate (CaCO3) yielded the highest values for the same parameters in

grassland soils (Muhlbachova and Tlustos 2006). On improved Scottish upland grassland

brown soils, limestone (CaCO3) liming caused a short-term (repeated measures, 1-9 months

between treatment and sampling) increase in microbial activity and above-ground plant

biomass and a concomitant decrease in microbial biomass and plant root quality (field trial,

Cole et al. 2005). On Australian clay loam (27% clay in top 20 cm layer), surface application

of limestone (Aglime) on non-tillage arable soil resulted in significantly higher microbial

biomass in the 0-5 cm layer after 1.5 years (Chan and Heenan 1998). After 3 years in the

same study system, non-tillage soils exhibited the same pattern as 1.5 years previously, but

now significantly higher microbial biomass in limed as compared to unlimed was also

detected in the 0-5 cm layer of one (of three) cultivated (conventional tillage) arable soils

(Chan and Heenan 1999). The Australian results indicate that growth stimulating effects of

limestone liming on microbial communities on conventional tillage soil will only appear some

years after a liming. However, perhaps not so unexpected as the lime in the cultivated

treatments was mixed into the top 10 cm layer by scarifying, effectively decreasing the

concentration of lime in any specific part of the top soil layer. In a field study on clay loam in

central Sweden (Stenberg et al. 2000), soil-tillage regime overall had larger influence on a set

of abiotic and biotic soil parameters as compared to long-term (8 years) effects of structural

liming (CaO). Especially the surface layers (0-12 cm) of stubble-cultivated plots had e.g.

13

higher microbial biomass (as indicated by substrate induced respiration), N-mineralisation

rate, and organic carbon content than both their corresponding sub-surface layers (12-24 cm)

and surface/sub-surface layers of mouldboard ploughed plots (Stenberg et al. 2000). Greater

soil-aggregate stability was related to shallow-tillage (stubble-cultivated) management rather

than to the structural liming treatment (Stenberg et al. 2000), indicating that biological factors

had more influence on soil structure than the quicklime treatment after eight years. However,

ammonium oxidation and higher soil pH was more related to limed plots, while denitrification

and lower soil pH was more related unlimed plots (Stenberg et al. 2000), which indicated a

liming-induced functional shift from denitrifiers to ammonium oxidisers. These results

indicate that limestone based liming generally benefits microbial communities but that it may

even take some years before beneficial effects are detected. Meanwhile some evidence

indicates that quicklime (CaO) has adverse short-term effects for microbial communities.

There is a lack of evidence especially concerning long-term effects of structural liming.

Long term effects from liming in field trials apply annual liming rather than a

one-time liming treatment. In the Netherlands on heavy clay meadow soils, a rather small

amount (1 Mg “CaO” ha-1y-1) of chalk was applied annually for 53 years prior to sampling,

and caused an increase in bacterial, but not fungal, diversity and evenness as compared to an

untreated control (Cassman et al. 2016). Similar responses in bacterial, but not fungal

communities, to soil pH manipulations have been found previously (Rousk et al. 2010). As

compared to control plots and nutrient amendments, liming significantly alter soil structural

factors (increasing soil pH and moisture content) as well as micro- and macronutrient

(reducing heavy-metal) availability (Cassman et al. 2016). In fact, prior papers (Wal et al.

2009, Korevaar and Geerts 2015) from the same study system stated that “lime marl” was

used, applied with the amounts 0.71 Mg ha-1 y-1 during years 1959-1980 and 0.36 Mg ha-1 y-1

during years 1981-2008 (Wal et al. 2009). Quite clearly annual long-term liming with lime

marl (most likely the case for all papers discussed in this paragraph) also changes the

microbial community composition, with the clearest effects on bacteria. But if can hardly be

stated that CaCO3-based liming is harmful to soil microbial communities.

Antibacterial properties of calcium carbonate (He et al. 2014), quicklime (Tang

et al. 2013) and slaked lime (Nyberg et al. 2011) have been experimentally validated. For

calcium carbonate (CaCO3), the particle size of the applied liming compound plays an

important part for short-term anti-bacterial properties. Smaller particle sizes increase soil pH

above the pathogens optimal growth conditions and increased amounts of soluble Ca2+ further

inhibits growth of Ralstonia solanacearum colony-forming units (He et al. 2014). The high

14

pH created by more reactive forms of lime (quicklime and slaked lime) destroys cell

membranes and thus exhibits stronger anti-bacterial properties than e.g. calcium carbonate.

Quicklime and can effectively be used to control pathogenic E. coli in e.g. meat products (Ro

et al. 2015) or pathogenic bacteria in poultry litter (Lopes et al. 2013). The antibacterial

properties of quicklime in litter has also been proposed to be a result of a combined effect of

elevated temperature, a side effects of the reaction with water, the pH change and a reduced

water availability in the litter (Lopes et al. 2013). While this may decrease short-term

problems with soil-borne pathogens, it likely also decreases the ability of the indigenous

microbial community to, via competition, control the growth of microbial pathogens such as

Salmonella typhimurium and Escherichia coli O157:H7 (Jiang et al. 2002, Vidovic et al.

2007). In soils with a lower diversity and abundance of the microbial communities, biotic

resistance will be lower and pathogens potentially more abundant (Hol et al. 2014). An

adequately abundant and diverse microbial community is a therefore a cornerstone of healthy

soils (Hol et al. 2014). Although both limestone powder and quicklime/slaked lime have been

used as anti-bacterial compounds, the results of experiments assembled in this paragraph

indicates that the reactive nature of structure liming compounds have high influence on

microbial organisms as compared to CaCO3-based ones.

The aspects of nutrient cycling and potential production of greenhouse gases as

(N2O) by microbial communities can be influenced by liming applications. Effects of

application of limestone (CaCO3) on N2O-emissions from soils of English arable fields have

been studies in both the short- (24 days) and long-term (almost 50 years) (Baggs et al. 2010).

In the short-term experiment, liming increased or decreased soil N2O emissions depending on

soil moisture, but N2O emissions were several times higher both when fertilized and

unfertilized in long-term adjusted (addition of either aluminium sulphate or calcium

carbonate) pH 4.5 soils as compared to long-term adjusted pH 7 soils (field/microcosm

experiment, Baggs et al. 2010). In similarity to Stenberg et al. (2000), increased pH was

associated with a shift in microbial N2O production from denitrifiers to ammonia oxidisers

(Baggs et al. 2010). N2O emissions were in the short term (3 months), significantly higher in

acidified (HCl) plots as compared limed (CaO) treatments (field trial, Robinson et al. 2014).

In addition, lower N2O emissions and concomitant increases in microbial biomass and

dissolved organic carbon resulted from additions of dolomitic lime (2.5 Mg ha-1) as compared

to unlimed soils (Shaaban et al. 2016). The results suggest that in the long term, liming can be

used to mitigate climate impact from microbial N2O emissions, but in the short term liming

can increase or decrease N2O-emissions depending on soil (moisture) conditions.

15

Micro- and mesofauna

Micro- and mesofauna - A brief summary of their contribution to soil functions

Nematodes represents one the generally most abundant animal groups in soil

communities (Løkke and van Gestel 1998). Most nematode species are not pests to plants and

animals as they stimulate nutrient cycling and entomopathogenic nematodes are even cultured

and used commercially as insect pest control agents (Jeffery et al. 2010). Generally, the

nematodes as a group encompasses a wide range of feeding strategies from grazers of bacteria

& fungi, plant pathogens, predators of other nematodes (Lavelle 1997, Brussaard 2012).

Bacterivorous nematodes are crucial intermediary decomposers of organic matter as they

promote nitrogen mineralization and by doing so increase the fraction of plant available

nitrogen. Nematode communities are influenced by management techniques like mouldboard

ploughing, which has been found to increase abundance of bacterivorous nematodes while

decreasing abundance of fungivorous ones (Brmež et al. 2006), likely as a result of decreasing

fungal biomass. Mesofauna like enchytraeids and collembolans catalyse decomposition and

nutrient cycling processes by e.g. grazing the microbial communities and by breaking up and

partially digesting dead organic matter thus making it more readily available for further

decomposition by microfauna (Lavelle 1997, Barrios 2007). While enchytraeid worms are

much smaller than earthworms (Løkke and van Gestel 1998), they nonetheless improve soil

structure through creating burrows in the upper soil layers where they generally dwell. Both

enchytraeids (Hedlund and Augustsson 1995, Brussaard 1997) and collembolans (Hedlund et

al. 1991, Gormsen et al. 2004) are undoubtedly important regulators of fungal presence in

soil. Mites (Acari) cover a wide range of trophic niches, from bacteriophages to top-predators

among micro- and mesofauna, within soil food webs (Brussaard 1997, Lavelle 1997).

Effects of liming on micro- and mesofauna

Short term ( 1-9 months) limestone (CaCO3) liming on improved Scottish

upland grassland brown soils, caused an increase in collembolan abundance (field trial, Cole

et al. 2005). However, liming did not effect diversity nor evenness of microarthropods (mites

and collembolans). Only a weak shift in species composition was detected, indicating that the

abundance of some species was increased by liming while abundance of others was decreased

(Cole et al. 2005). Addition of slaked lime (Ca[OH]2) on conifer forest soils, in the short- to

mid-term (3-24 months) caused collembolan species to react either positively or negatively

(field and lab experiments, Vilkamaa and Huhta 1986). With the exception of a negative

effect on biomass of collembolans, microarthropod biomass, as well as diversity and evenness

16

were rather unaffected by a liming treatment in a Dutch long-term grassland field experiment

(Wal et al. 2009). The results indicate that limited or no conclusions regarding the direction of

effect of liming on microarthropods can be drawn at this time.

Although neither dolomitic (CaCO3) limestone (field trial, McSorley and

Gallaher 1994) nor slaked lime (Ca[OH]2) (lab and greenhouse experiments, Meyer et al.

2005) have been found to efficiently control abundance of a phytopathogenic nematode

species, significant effects of limestone treatments on nematode soil communities both in lab

and field environments have been detected. In conifer forest soils on a sandy moraine,

nematode abundance was 2-3 times higher in limed (CaCO3) as compared to a unlimed soil

after a short-term (6 months) experimental duration (microcosm experiment, Hyvönen et al.

1994). Long-term annual application of lime marl (CaCO3) resulted in higher nematodes

biomass, as compared to control and nutrient amendment treatments, in Dutch grassland

experimental fields (Wal et al. 2009). The lime marl treatment had a relatively adverse

influence on nematode and enchytraeid diversity and evenness (Wal et al. 2009). No results

regarding effects of structure liming compounds on nematode nor enchytraeid communities

were found. The results presented here indicate that limestone liming has mixed effects for

nematodes, while enchytraeids may be negatively affected in the long term.

The pH changes induced by liming may cause complex trophic cascades within

the soil fauna community. In a short-term experiment (29 weeks), presence of the common

epigeic earthworm Dendrobaena octaedra, liming (CaCO3) did not affect nematode

abundance (microcosm experiment, Hyvönen et al. 1994). Meanwhile, liming resulted in 2-3

times greater nematode abundance in the absence of the earthworm (Hyvönen et al. 1994).

The authors attributed the effect to increased (accidental) predation on nematodes by D.

octaedra, as the very small relative body size of nematodes as compared to D. octaedra

increases the risk of decreasing nematode biomass and not to the effect of liming. Increased

nematode abundance due to a reduction of earthworm presence in the fields has also been

proposed by other authors (Lenz and Eisenbeis 1998). In a short-term (28 weeks) microcosm

experiment with pine-stand humus soils (lower pH) and spruce-stand soils (higher pH),

specimens of the earthworm species Dendrobaena octaedra Savigny (Lumbricidae) and the

enchytraeid species Cognettia sphagnetorum Veydovsky (Enchytraeidae) were introduced

into defaunated soils (Yli-Olli and Huhta 2000). Addition of slaked lime (Ca[OH]2) into pine-

stand soils resulted in significantly higher biomass of D. octaedra as compared to unlimed

controls (Yli-Olli and Huhta 2000). Meanwhile, the same limed soils initially (after 7 weeks)

17

exhibited significantly lower biomass of C. sphagnetorum as compared to unlimed (Yli-Olli

and Huhta 2000). Previous Swedish trials in conifer forest soils also indicate that the impact

of liming on mesofauna such as enchytraeids is highly dependent on the presence of

earthworms (Persson et al. 1996). These results indicate that adverse effects of liming on

nematodes and enchytraeids may, in the presence of earthworms, partially result from

increasing resource competition (and incidental ingestion) from earthworms.

Macrofauna

Macrofauna - A brief summary of their contribution to soil functions

Below-ground macrofauna provide ecosystem functions and services by

incorporating litter into soil, forming & maintaining soil porosity, and aggregating &

regulating microbial communities (Brussaard 1997, Lavelle 1997, Lavelle et al. 2006).

Keystone taxa within the detritivore communities are earthworms that have a strong

regulating effect on soil nutrient cycling, soil aggregate formation and water retention

(Lavelle 1997). Earthworms can regulate soil microbial activity and carbon inputs by

enhancing litter decomposition rate through burial and partial digestion, and by protecting soil

carbon in stable aggregates such as their castings (Brown et al. 2000). As a result of

differences in feeding behaviour and localization in the soil, earthworms are commonly

categorised into epigeic, endogeic, and anecic earthworms. (e.g. Lavelle 1997). The epigeic

group comprises relatively small litter-dwelling species that feed directly on surface litter and

do not form burrows. The endogeic group also comprises relatively small species but these

mainly feed on rich soil and form horizontal burrows in the topsoil. The anecic group

comprises relatively large species that feed both on litter and rich soil and form extensive

vertical burrows. The extensive vertical cast systems of anecic earthworms are destroyed by

mouldboard ploughing and thus earthworm communities in arable soils under intensive crop

rotation are dominated by smaller sized endogeic species (Curry et al. 2002, Crittenden et al.

2014). Thus the potential of earthworms to contribute to e.g. soil aggregate formation is

highly dependent on agricultural management intensity, and interactions with organic matter

management (Crittenden et al. 2014).

Members of the above-ground macrofauna, coleopterans such as ground beetles

(Carabidae) are common on arable soils (Thiele 1977). Species of these beetles occupy many

different trophic niches (Lindroth and Bangsholt 1985, Lindroth et al. 1992), foremostly many

ground beetle species are important predators of crop pests. Although they are traditionally

18

considered above-ground fauna and not considered a part of the soil biota, many carabid

species hibernate as larvae or adults within arable soils and are thus also exposed to

agricultural management practices during significant periods of their life-cycles.

Effects of liming on macrofauna

Effects of liming on earthworms (Lumbricidae) is mostly studied in forest soils,

while studies on the same topic in agroecosystems are scarce. In former grassland on silty

clay loam soil in the Basque country (Spain), the earthworm abundance was significantly

negatively affected in the short term (about 2 months) by quicklime treatment (Mijangos et al.

2006). The authors suggested the reactive nature of the quicklime as a cause for the observed

pattern (Mijangos et al. 2006), a reasonable argumentation as quicklime when mixed into the

soil would, depending on soil moisture conditions, cause a rapid concomitant increase in pH

and temperature, and decrease available water within the affected soil layer (Oates 2008).

However, according to the authors themselves a general low earthworm abundance in their

study means that the results have to be interpreted with caution (Mijangos et al. 2006).

Although no statistical tests were performed, earthworm abundance and biomass was greater

8 years after structural liming (CaO), as compared to control, and the positive effect was

enhanced by shallow-tillage management as compared to mouldboard ploughing (student

degree project, Ivarsson 1996), indicating beneficial, or lack of harmful, long-term effects for

earthworms. Long-term annual application of lime marl (CaCO3-rich mudstone) on Dutch

meadow heavy clay soils had high earthworm biomass as compared to nutrient amendments

and controls (Wal et al. 2009). Other intensive agricultural management practises such as

mouldboard ploughing have been found, in similarity to structural liming, to decrease overall

earthworm abundances in the short term, but not in mid to long term (Crittenden et al. 2014).

In forestry, significant positive long-term effects of limestone treatments for earthworms have

been frequently reported, e.g. for abundance in beech forests in Brittany (France, Deleporte

and Tillier 1999), and on abundance and biomass for a range of species in conifer plantations

(Ireland and France, Robinson et al. 1992).

For coleopterans, as well as for other soil-dwelling macroarthropods, there is a

severe lack of evidence on effects of liming on naturally occurring species communities in

agricultural landscapes. The results that are reported here are experiments that have been

designed to investigate the pest-control potential different liming compounds, which means

that only one species at a time is investigated. These types of experiments may provide partial

insights into the effects of liming, but cannot be extrapolated to species communities, where

19

liming may or may not have the same effect for different species that are more or less by e.g.

soil fertility. Slaked lime can cause significant short-term mortality (days) among poultry-

litter dwelling darkling beetles (Alphitobius diaperinus Panzer), especially for larvae but also

for adults (Watson et al. 2003, Wolf et al. 2014). Watson et al. (2003) attributed the increased

mortality of slaked lime with increasing litter moisture directly to elevated soil pH as the

highest added amount of slaked lime produced a soil pH>11, for a duration of at least 4 days.

However, 4 months after similar treatments in field conditions (in turkey houses), larval and

adult abundances were significantly greater in the treatments that received the highest

amounts of slaked lime, indicating a lack of negative long-term effects for this species in

turkey litter. Slaked-lime treatments in organic-rich and clay-poor sand caused significant

mortality in small hive beetle (Aethina tumida Murray) while limestone treated, and untreated

controls had no effect at all (Buchholz et al. 2009). Buchholz et al. proposed that the mortality

was related to liming induced reduction of soil moisture and that an interacting effect between

soil sterilisation and slaked-lime dosage could be explained by enhanced pathogen activity in

non-sterilised soil at the lowest dosage. On American sandy grassland loam, no negative

short-term (about 6 weeks) effects on larvae of a scarab beetle (Popillia japonica Newman)

were found from dolomitic limestone nor from slaked lime surface application (Vittum 1984).

On turf established on silt loam soil, surface application of either calcium carbonate or

calcium magnesium silicate reduced white grub (Scarabidae beetle larvae) numbers by more

than 50% as compared to non-limed plots after 9 months (Provance-Bowley et al. 2014).

However, a repetition of the treatment in the second year of the same study, no significant

effects were detected. Provance-Bowley et al. (2014) attribute effects to the liming induced

increase of soil pH but also to soil interactions involving Ca and P within a specific pH range.

The results show that structure-liming compounds (quicklime and slaked lime) can cause

mortality both for juvenile and adult coleopterans. Effects of limestone based materials on

coleopteran larvae are likely a result of a shift away from the preferred soil conditions (e.g.

pH) for the specific species, and not due to rapid chemical reactivity that dissolve cell

membranes. However, as a result of the volatile nature of structure liming compounds,

negative long-term effects are unlikely. Thus it is rather the spatial scale of structure liming

that can be more influential for the prevalence of coleopteran and other soil-dwelling

invertebrates.

20

21

Knowledge gaps

The lack of evidence on effects of liming and especially structural liming on the

biology of arable soils is quite apparent for many taxa and especially the larger soil

organisms, which often prevents an evidence based conclusions. Additionally, the spatial and

temporal scale-dependence of dispersal and recolonization processes have not been

sufficiently investigated in the available literature. The amount of recently limed arable land

in the surrounding landscape could influence the recovery of the soil community of a focal

field. The fact that structure liming compounds (quicklime and slaked lime) are relatively

potent pathogen- and pest-control agents warrants more research on potential adverse effects

on non-target organisms under field conditions. While some results indicate that abundance

and/or biomass of some taxa can recover some time after structural liming, there is a lack of

information on how the species composition and diversity is affected. The functions of

naturally occurring species communities depend the abundance distribution across species and

more diverse and evenly distributed species communities are commonly performing better

than those that are dominated by one or a few species, e.g. for pest control functioning

(Crowder et al. 2010). Functional groups, such as different trophic levels of detritivore

community, that are dominated by one or few taxa are more likely to be vulnerable to

pathogens and environmental changes, vice versa diverse functional groups are more likely to

withstand pathogen attacks and environmental changes. Analyses of species communities are

required in order to make sufficiently informed decisions concerning management

implications for soil functions. In addition, techniques that evaluate the activity and feeding

rate of soil biota, such as the “bait-lamina test” (von Törne 1990) and the “mini-container

test” (Eisenbeis et al. 1999), could provide valuable information concerning impact of e.g.

structural liming on functional aspects of the soil communities.

While most research to this date has focused on effects on below-ground

detritivore communities, knowledge gaps concerning effects of structural liming in arable soil

still exist for soil macroarthropods (Chilopoda, Diplopoda, Isopoda) in general, but also for

groups of ground-dwelling natural enemies such as ground beetles (Carabidae) and rove

beetles (Staphylinidae). While parts of their life-cycles take place within the soil, many

species of these above-ground coleopterans spend significant periods of time, as larvae and/or

adults, in the surface layers of arable soil. It is important to in understand how these natural

enemy communities react to structural liming, as they play an important role in sustainable

pest control. For agro-environmental schemes such as integrated pest management and

22

organic farming, where a fundamental concept is to rely more on pest regulation from natural

enemies, this is a key consideration. Very few studies on effects on natural enemies have been

made, and to the knowledge of the author of this report, none on arable land. One field study

that attempted to investigate effects of liming on invertebrates in mires across a large

geographical study area (Buckton and Ormerod 1997), found negative effects on ground-

dwelling taxa such as ground beetles (Coleoptera: Carabidae) and wolf spiders (Araneae:

Lycosidae). Unfortunately, Buckton and Ormerod did not specify what type of lime that was

used, and limed sites were also geographically clustered and separated from unlimed sites,

making it difficult to separate a liming effect from the natural variation. Generally, there is an

urgent need for more research that attempt to evaluate short- and long-term effects of

structural liming on soil biota e.g. these beneficial ground- and soil-dwelling arthropods in

agricultural landscapes.

As argued by e.g. Keiblinger et al. (2016), another confounding problem is that

much of the existing research on effects of liming have failed to specify what type of liming

compound that was used in the treatments. In agroecology research, the differentiation

between limestone/calcium carbonate based and quicklime/slaked lime based liming has

simply not been described detailed enough in the materials and methods sections. This may

partially be due to a general lack of awareness of the differences in chemical properties and

reactivity between types of lime within the research community. In fact, even in a recent

paper (Cassman et al. 2016), fuzzy information is given in the main text regarding which type

of liming compound has been used in the experimental liming treatment. The term “chalk”,

mostly used to describe a sedimentary rock (like limestone) mostly composed of calcium

carbonate (CaCO3), is used interchangeably with quicklime (CaO). Quicklime can form as a

result of natural processes, from coal seam fires and from volcanic activity, but quickly

decomposes if exposed to water and (as mentioned in the introduction) and is for industrial

purposes mainly produced through thermal decomposition of chalk or limestone. As chalk

(the sedimentary rock) and quicklime (CaO) have very different chemical reactivity,

especially for biological studies, great care should be taken not use these terms

interchangeably.

23

Conclusions

Generally, the reviewed results contain evidence that indicates adverse short-

term effects on some soil organisms, such as microbial communities, earthworms and

coleopterans. However, there are no indications of negative long-term effects, rather the

opposite. It is unclear what allows soil organisms to recover, mid- to long term, from

disturbance caused by structural liming. Effects on microbial communities has an added

global environmental significance, as emissions of greenhouse gases (e.g. N2O) are

significantly impacted by liming regime, which causes shifts in functional microbial

composition (denitrifiers vs. ammonia oxidizers). Coleopteran soil-dwelling larvae may be

especially sensitive to (structural) liming, but a lack of evidence prevents more informed

inference. Meanwhile results indicate that earthworm populations may be negatively affected

in the short term but enhanced in the long term, perhaps benefitting from improved

soil/microhabitat conditions such as increased pH and more beneficial soil structure. More

research is however needed also concerning earthworms. The spatial scale of structure liming

management needs to be considered when treatments are performed. Potential negative effects

of structural liming will likely be amplified if large continuous areas are treated at the same

time and recovery times especially in the core areas of the treated field likely will be longer

than around the edges. A sufficient heterogeneity of arable production cover types and

management types likely can play an important role, e.g. for animal biodiversity in

agricultural landscapes (Fahrig et al. 2011).

24

25

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