Scherotheca gigas

## Source: ResearchGate

1. Introduction

It is well known that the abundance of earthworms in

the soil depends on soil properties and on climate. Most

of the studies related to the earthworms behaviour are

from the tropical and subhumid temperate soils. Their

behaviour in more limiting conditions, such as agricultural

soils in semiarid or arid regions, has been less studied [1].

Some particularities of earthworms such as large body size,

slow growth rate, ability to feed on soils poor in organic

matter, occupying deeper soil proﬁle, have been described

in Mediterranean soils [2]. However, our knowledge is still

limited. For instance, in the Iberian Peninsula, much less

information on earthworm occurrence and activity exists for

the Mediterranean domain than for the more humid NW

area [3]. The reality is that in the majority of agricultural

soils with Mediterranean type of climate, like in the Ebro

Valley of Spain, located in the Mediterranean-Iberian-

Levantine biogeographical superprovince [2], earthworms

are scarce and often absent when tillage is intense

[4].

It is also well known that, in general, when tillage

is reduced earthworm activity increases. No-till and other

methods of conservation tillage such as chisel plowing can

thus increase earthworm populations [5]. Decreased tillage

disturbances particularly beneﬁt anecic species, which can

move in the same burrow between deeper soil layers and

the soil surface in search of food. This is so because when

tillage destroys these burrows, some earthworms may not

have the energy reserve needed to form a new burrow to

their food source [6]. Previous studies in rainfed agricultural

soils, cropped to cereals in the Ebro Valley (Navarra,

Spain), provided evidence of increased earthworm density

and biomass with reduced tillage [7,8]. The three species

commonly found in no-till soils in the area are Allolobophora

rosea, Scherotheca gigas, and Prosellodrilus praticola.S. gigas

(Dug´

es 1828) is the only anecic species to deposit cast on the

soil surface. Though this species is widespread in the area, it

2Applied and Environmental Soil Science

has a narrow geographical distribution worldwide [9]. In a

study in the role of earthworms in soil aggregate formation,

S. gigas was cited by Bouch´

e and Al-Addan [10] as one of the

most abundant species in a dry grassland on calcareous soil.

As for most earthworm species, soil moisture and

temperature aﬀect the activity of S. gigas. Field observations

led us to distinguish two periods of surface casting activity

over the year [8], each interrupted by a period of inactivity

in January/February and June/September. As observed in

other semiarid areas [11], during the dry summer months

the species undergo diapause and cannot be found at the soil

surface.

The contribution of earthworms to organic matter incor-

poration into the soil can be studied by comparing surface

casts and the surrounding soil. Properties of surface casts

usually diﬀer from those of the bulk soil, but contradictory

ﬁndings have been reported. Diﬀerences are related to the

type of soil [12] and/or to earthworm species [13]. Brown

et al. [14] have described in detail the role of earthworms

in organic matter stabilization. These authors consider that

the inclusion of the active fractions of the soil organic

matter (SOM) into earthworm casts can contribute to its

protection and stabilization when casts dry up, a process that

can happen within hours or days after its deposition. It has

also been demonstrated that soil management can greatly

inﬂuence this process [15–17].

The protection of SOM from biological degradation in

surface casts [18,19] has a special signiﬁcance for soils with

high mineralization rates and low contents in SOM, as is the

case for the soils of the Ebro Valley. In addition, soils rich

in calcium carbonate also contribute to the persistence of

casts over longer time periods and thus to long-time SOM

protection.

The purpose of this study was to gain knowledge on the

behavior of S. gigas in no-till carbonated Mediterranean soils

by studying its role in the incorporation and preservation of

organic matter into the soil and the inﬂuence of aridity in

this process.

2. Methodology

2.1. Study Sites. The study was conducted at three long-

term experimental sites that include diﬀerent soil man-

agement treatments in the Ebro Valley in Navarre (NE,

Spain). These sites were located in Pamplona (42◦4732N;

1◦3754W), Olite (42◦2733 N; 1◦4107 W), and San-

tacara (42◦2344N; 1◦3232 W). Only the plots under

no-till (NT) of each experimental site were chosen for

earthworms and soil sampling. This was done because greater

earthworm activity has been observed in the area in NT

plots [8]. The three sites contain carbonated soils which are

cropped to rainfed barley (Hordeum vulgare L.), but diﬀer

in some soil properties and, especially, in their agroclimatic

characteristics (Table 1). They represent an aridity gradient

because average rainfall is greater in Pamplona (Mediter-

ranean sub-humid type of climate) and decreases southward

to Olite (semiarid Mediterranean) and then Santacara (arid

Mediterranean), while average annual temperatures and

reference evapotranspiration (ET0) increase in the same

order.

A direct seeder that opens a seed-furrow 30 to 50mm

deep is used for barley seeding in fall in the studied NT plots

at the three sites, using similar seeding doses (∼160 kg/ha)

and fertilization treatments. Average barley yield decreases

with increasing aridity (Ta b l e 1 ).

2.2. Sampling Methods. As already mentioned, earthworm

activity in the region is clearly seasonal, and coincides

with the two rainfall peaks and mild temperatures observed

in spring and fall. Three ﬁeld NT replicates (plots) were

sampled in November 2007 at each study site, in order to

identify the earthworm species present in the soil. Two soil

blocks (0.20 by 0.20 by 0.20 m) were taken in each plot.

Earthworms were sampled by hand-sorting and counted

in the ﬁeld. Individuals were ﬁxed with ethanol-formalin,

and preserved in 10% formalin [20]. They were classiﬁed

at the Department of Ecology and Animal Biology of the

University of Vigo (Spain). Thirty to 50 individuals of S.

gigas were found per square meter at the three study sites.

Considering the size and the ability of this species to dig deep

into the soil, these numbers are likely an underestimation

of the actual abundance of S. gigas in the studied soils.

It was observed that S. gigas was the only anecic species

found, which indicates that surface casts present in the three

soils were created by individuals of this species. This also

illustrates the ubiquity of this species in NT soils in the

region, regardless of soil characteristics and agroclimatic

conditions.

Simultaneously, four replicates of surface earthworm

casts were collected at three random points in the NT plots at

each study site. Casts were air-dried, ground to pass through

a 2-mm sieve and stored for further analyses.

Soil (0–30 cm) was sampled using an Edelman-type

auger. Disturbed subsamples were collected at four random

points per plot, and combined to obtain a composite sample

per plot, so that three ﬁeld replicates were analyzed at each

site. Samples were air-dried and ground to pass through a

2-mm sieve.

2.3. Laboratory Analyses. Clay, total organic C content, and C

in the form of particulate organic matter (C-POM [21]) were

determined both in the casts and the bulk soil. Clay content

was determined by the pipette method [22], using a modiﬁed

Robinson pipette. Samples were chemically dispersed with a

solution of 5% (NaPO3)6before analysis. Due to the elevated

carbonate content of the three soils (Table 1), wet oxidation

was used to analyze total organic C [23].

Particulate organic matter is acknowledged to represent

the most labile fraction of organic matter in the soil, and

it is related to the formation of stable aggregates [24]. For

this study, POM was isolated by dispersion and sieving of

10 g of air-dried soil, as described by Marriott and Wander

[25]. Brieﬂy, samples were dispersed with 150 mL of 5%

(NaPO3)6and the fraction >53 µm (which includes the POM

and sand-size mineral components of the soil) was collected

on a 53-µm-opening polycarbonate mesh (Gilson Co. Inc.,

Applied and Environmental Soil Science 3

Tab le 1: Agroclimatic and soil characteristics of the three studied sites.

Study site Pamplona Olite Santacara

Rainfall (P, mm) 830 525 423

Evapotranspiration∗(ET0, mm) 972 1163 1145

P/ET00.85 0.45 0.37

Te m p e r a t u re ( ◦C) 12.4 13.5 14.2

Average barley yield (t grain ha−1) 3.93 3.70 2.75

Soil type (FAO, 2003) Calcic Cambisol Calcic Cambisol Haplic Calcisol

pH (0–30 cm) (1 : 2.5) 8.63 8.25 8.48

CaCO3(0–30 cm)(g kg soil−1) 252 359 363

∗Reference evapotranspiration, (FAO).

Columbus, OH) after 3 rinses with distilled water, and

then oven-drying at 50◦C. Samples were then ground to a

powdery consistency before measuring their C content to

determine POM-C by wet oxidation [23].

2.4. Statistics. Data are presented as ±standard error of the

mean for casts and soil characteristics. Data were analysed

using ANOVA (univariate linear model), and means were

compared among the three soils and between soil and casts

at each study site using signiﬁcant diﬀerences. Post hoc

analysis was performed by Duncan’s multiple range test.

Signiﬁcant results are based on a probability level of P<.05.

All statistical analyses were performed using the SPSS 16.0

software [26].

3. Results and Discussion

3.1. Role of S. gigas in the Incorporation of Organic Matter

into the Soil. Lower clay contents were observed in the

S. gigas casts than the bulk soil in the three studied ﬁelds

(Table 2). Our ﬁndings support thus the suggestion of

Schrader and Zhang [27] that selective particle ingestion

by earthworms leading to increased clay contents in casts

than in the surrounding soil [28] appears to be conﬁned to

sandy soils, and/or might be more common in other smaller

species of earthworms than the anecic S. gigas.Analternative

explanation could be the existence of ultra-stable silt-size or

sand-size aggregates in the casts, which would resist chemical

dispersion.

Results from the analysis of the organic components of

casts and bulk soils revealed that S. gigas casts contained

more total organic C and POM than the soil (Table 2), as

has also been reported through other studies [14]. More

interestingly, the percentage of C in the form of POM was

also greater within the casts than in the soil at the three

studied sites, suggesting a selective ingestion of the more

edible fresh plant residues and labile organic materials by

S. gigas [14]. This ﬁnding is of special importance in the

studied soils, which are naturally poor in organic matter,

because POM entrapped within casts is likely to be more

protected against microbial activity than elsewhere in the

soil [12]. Guggenberger et al. [29] reported that the incor-

poration of organic matter in the casts of anecic earthworms

on an Oxisol occurred preferentially in the form of POM.

They related this to the higher aggregate stability observed

in the casts in comparison to the surrounding soil. They

further suggested that the mechanisms that protect organic

matter from decomposition during aggregate formation and

stabilization, as also described by Tisdall and Oades [30]and

Six et al. [24], can be enhanced or facilitated by earthworm

casting activity. Direct incorporation of POM into stable

microaggregates through earthworm transit in the soil has

also been described by Pulleman et al. [15] as an “alternative

pathway” to the microbial-mediated one for the stabilization

of POM by occlusion within microaggregates in undisturbed

soils.

Long-term stabilization of organic matter occluded

within aggregates inside earthworm casts is in fact possible

[31] and depends on the type of soil [32], earthworm species

[33], the age of casts, the way they dry [34–36], and the level

of disturbance to which casts are subjected [12]. A number

of studies have shown that the quantity of organic matter

incorporated into the soil by earthworms also signiﬁcantly

aﬀects the stability of casts. In the present study elevated clay

and carbonates contents of the soils allow for overall high

aggregate stability [8]. In Olite and Santacara, scarce rainfall

and high average temperatures cause a rapid dehydration of

casts and, as a result, intact earthworm casts are observed

several months after their formation at these two study sites.

In addition, NT techniques ensure low disruption of the

soil surface and protection against raindrops by the mulch.

Considering the observed contribution of S. gigas to POM

preservation within the casts, the contribution of this species

to the stabilization of organic materials and the overall

increase of organic C observed in NT soils in the region

[37,38]islikelytobeofimportance.

3.2. Inﬂuence of Aridity in the Behavior of S. gigas. Diﬀerences

related to the agroclimatic context of the three studied soils

were found in the enrichment factor and composition of

casts in relation to bulk soil (Table 3).

While in all the three sites casts contained less clays than

the bulk soil, the relative amount of clay found in the casts

of the more humid soil in Pamplona was signiﬁcantly greater

than in Olite and Santacara (Table 3). If we consider that the

soil clay content was similar in Pamplona and Santacara and

4Applied and Environmental Soil Science

Tab le 2: Content in clay, total organic C, and C in the form of POM (C-POM) in bulk soil samples and in Scherotheca gigas casts at the three

study sites. Values marked with ∗are signiﬁcantly diﬀerent (P<.05) between soil and casts for each parameter and site. Values followed

by the same letter in the same row belong to the same Duncan’s homogeneous groups (P<.05) for each parameter among sites. Means ±

standard error (n=3).

Study site Pamplona Olite Santacara

Clay (g/kg) Soil 306.2 ±6.7∗a426.2 ±2.04∗b284.8 ±2.6∗a

Casts 233.4 ±2.5∗b234.8 ±22.2∗b165.2 ±6.8∗a

To t a l O C (g / k g ) Soil 14.03 ±0.42∗b14.32 ±0.66∗b12.55 ±0.22∗a

Casts 21.93 ±0.78∗a26.23 ±1.81∗b19.13 ±0.36∗a

C-POM (g/kg) Soil 2.77 ±0.12∗ab 3.66 ±0.52∗b2.16 ±0.07∗a

Casts 6.47 ±0.37∗a9.52 ±0.27∗b8.47 ±0.89∗ab

C-POM/Total OC Soil 0.20 ±0.01∗a0.25 ±0.03∗b0.17 ±0.00∗a

Casts 0.29 ±0.01∗a0.36 ±0.02∗ab 0.44 ±0.04∗b

Tab le 3: Cast-to-soil ratios of clay, total organic C, and C in the form of POM (C-OPM) at the three study sites. Values followed by the same

letter in the same row belong to the same Duncan’s homogeneous groups (P<.05) for each parameter among sites. Means ±standard error

(n=3).

Study site Pamplona Olite Santacara

Cast-to-soil ratios

Clay 0.76 ±0.02b0.53 ±0.07a0.59 ±0.02a

To t a l O C 1 . 5 7 ±0.11 1.82 ±0.12 1.50 ±0.04

C-POM 2.44 ±0.19a3.00 ±0.37ab 4.01 ±0.45b

greater in Olite (Table 2), this ﬁnding suggests that climate

is a more important factor for this relative diminution in

the clay content of the casts than the soil texture itself. Not

much information is available on the inﬂuence of climate

on the burrowing and casting activity of any particular

earthworm species. In temperate areas, annual variations in

the casting activity of anecic species (Lumbricus terrestris)

have been described as related to rainfall and soil moisture

[39].

In tropical semiarid areas, no earthworms are found

during the dry seasons in soils that show earthworm activity

during the rainy season [17].

Higher moisture in the soil in Pamplona than in the

more aridic Olite and Santacara could be one reason for the

enhanced casting activity and thus for more intense remixing

of the casts with bulk soil. Lower concentration of carbonates

inthissoil(Ta b l e 1 ) probably also favored the formation of

less cemented casts with less nondispersible sand- and silt-

size aggregates within casts. Further research is needed in this

sense.

Regarding the incorporation of organic materials into

the casts, it was observed that the enrichment factor in

total organic C in the casts compared to bulk soil was

similar among the three studied soils, but a clear and

signiﬁcant trend towards higher enrichment ratios in POM

was observed with increasing aridity (Ta b l e 3 ).Theroleof

S. gigas in incorporation of POM was most signiﬁcant in

the arid soils of Santacara, which had the lowest total SOC

and POM values as well as the lowest crop yield (Tab l e 1 ),

as compared to the other two sites. This more evident

preferential ingestion of POM in this soil probably is due to

fresh stubble being the most signiﬁcant available source of C

in this ﬁeld.

4. Conclusions

By studying the composition of surface casts of S. gigas and

the surrounding soil under diﬀerent agroclimatic conditions

in NT ﬁelds in the Ebro Valley, we found that this species

has an important role in the incorporation of organic matter,

and in particular of the most labile fractions, to the soil. The

casting activity of S. gigas seems thus related to the observed

progressive increments of organic C stocks in NT soils in the

region. We also found a proportionally greater enrichment in

labile organic particles in casts with increasing aridity, which

suggests that the importance of S. gigas in organic matter

stabilization under NT increases with aridity in the region.

The relationship between climate, S. gigas casts texture, and

organic C content remains however incompletely understood

and merits further research.

Acknowledgments

C. Gonz´

alez and M. Moriones are thanked for their technical

laboratory assistance, and the Instituto Nacional de Investi-

gaci´

on Agraria y Agroalimentaria (INIA, Spanish Agency) is

acknowledged for funding this study in the framework of the

Research Call “Acci ´

on: Sumideros Agroforestales de Efecto

Invernadero” of the National Program I+D+i (Project no.

SUM 2006-00012-00-00). The authors are grateful also to

Professor M. J. Briones (University of Vigo, Spain) for her
kind advice and for the classiﬁcation of earthworms