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76 Jalal et al. Int. J. Biosci. 2014 Introduction Earthworms are an eminent component of soil fauna in the global soils and are useful indicators of soil

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Contribution of earthworms to enhance fertility in ...

76 Jalal et al. Int. J. Biosci. 2014 Introduction Earthworms are an eminent component of soil fauna in the global soils and are useful indicators of soil

Int. J. Biosci. 2014

International Journal of Biosciences | IJB |

ISSN: 2220-6655 (Print) 2222-5234 (Online)
http://www.innspub.net

Vol. 5, No. 9, p. 75-84, 2014

RESEARCH PAPER OPEN ACCESS

Contribution of earthworms to enhance fertility in selected

orchards of faisalabad district

Fatima Jalal1, 2*, Junaid Iqbal Qureshi2, Shazia Anwer Bokhari3, Asma Haque4 Zafar
Mahmood Khalid5, Shahnaz Akhter Rana2

1Deptt. Zoology, Wildlife and Fisheries, Faculty: Science and Technology, GC. University,
Faisalabad Pakistan
2Deptt. Zoology and Fisheries, University of Agriculture (UAF) Faisalabad, Pakistan
3Department of Applied Chemistry and Biochemistry, GCUF, Faisalabad-38000, Pakistan
4Deptt. Bioinformatics, Faculty: Science and Technology, GC. University, Faisalabad Pakistan
5Department of Bioinformatics and Biotechnology, Faculty of Basic and Applied Sciences, IIU,
Islamabad, Pakistan

Key words: Earthworms, nutrients, orchards, Pheretima, climate.

http://dx.doi.org/10.12692/ijb/5.9.75-84 Article published on November 10, 2014

Abstract

The influence of earthworm’s abundance on the soil texture, physiology and available nutrients in natural conditions were
investigated in the four orchards, Orange (Citrus reticulata), Guava (Psidium guajava), Mango (Mangifera indica) and Berri
(Zizyphus mauritiana). Samplings were done every month with five replicates, throughout the years in session (1997-1998).
Up to 18 species belonging to 10 genera were harboured from the selected sites. Overall, about 87.57 % (n=458) of earthworms
were belonging to genus Pheretima while the rest of species are poorly present. Climatic factors affected the diversity and
abundance of the earthworms (p = 0.01, p = 0.05). The number earthworms were abundant near tree trunks where different
species of herbs and shrubs were present which provided shelter against adverse environmental factors. Genus Pheretima had
fairly found throughout session. A fair number of casts were found in the Berri orchards and least in the guava orchards. The
casts and burrows were frequently present near the tree stem within the intermingled roots. The shape and size of the casts and
the burrows depends on the species as well as the age of the earthworms and having a linear correlation between the soil
fertility and abundance of earthworms (p = 0.01, p = 0.05). This correlation indicated that the presence of earthworms in
orchards increase soil fertility and having the ultimate influence to enhance the productivity of the orchards.

* Corresponding Author: Fatima Jalal  [email protected]

75 Jalal et al.

Int. J. Biosci. 2014

Introduction fungal hyphae and the production of bacterial
Earthworms are an eminent component of soil fauna polysaccharides/ the arrangement of primary
in the global soils and are useful indicators of soil particles were investigated (Marinissen and Dexter,
health and quality (Edwards, 2004). Pakistan is an 1990; Schrader and Zhang, 1997; Zhang and
agricultural fertile land, and extensive agricultural Schrader, 1993). A few studies were available on soil
practices decrease the soil fertility by decreasing soil fertility and ecology with respect to earthworms in
porosity (Arshad and Coen, 1992) as a result orchards (Jongmans et al., 2001; Schrader, and
increasing the compactness (Sillon et al., 2003; Lipiec Zhang, 1997).
et al., 2006; Blavet et al., 2009) as compared to the
orchards where tree trunks provide shelter for the The main objective of the present study was to find
earthworms. A large amount of water transported out the relationship between the soil fertility and the
through burrows (Lamande et al., 2003) and the soil earthworm populations that were inhabitated near
animals increase soil porosity through borrowing the tree trunk as well as the climatic influence in the
activities (Lavelle et al., 2001) which is the earthworm’s population, and casts formation, which
consequent source of oxygen supply in the has the ultimate effect on soil geo-physiology of the
underground soil. Endogeic earthworms play an horticulture experimental orchards. The increase in
essential role by accumulation of casts below the soil casts formation and burrows ultimately has an impact
surface modified the soil matrix with the formation of on soil physico-chemical properties in order to
granular aggregates (Jongmans, 2001). The casts’ increase the soil fertility in undisturbed orchards. For
ability is to neutralize soil by buffering acid and basic the reason orchards were selected in order to
conditions and earthworm tunnels create fertile investigate the influence of earthworm on the soil and
channels for the growth of plant roots. climatic effect on earthworms.

Fresh casts are easily dissolved in water but with the Materials and methods
passage of time they become dry and more water- Site selection and physical factors
stable (Shipitalo, 1988). The climatic factors such as For the analysis of earthworm’s effect on soil
rainfall, raindrop impacts and wet-dry cycles, cattle morphology in the form of burrows and casts, the
trampling (Decaens, 2000) and the activities of small research area comprised of four orchards viz Orange
dwellers invertebrates, primarily disrupt the above (Citrus reticulata), Guava (Psidium guajava), Mango
ground casts in natural ecosystem. Therefore, the life (Mangifera indica) and Berri (Zizyphus
span of the below ground casts, are suggested to be mauritiana).situated at horticulture experimental
longer (Mariani et al., 2007; Lukkari et al., 2006) orchards (Square No. 9) of the University of
than those of above grounds. Subsurface casts create Agriculture, Faisalabad, Pakistan (31° 26' N, 73° 06' E
a “mammilated vughs” porosity which changes the and at an altitude of 184.4 m above the sea level.).
meso and macroporosity of the soil (VandenBygaart The hottest months are May, June and July, while
et al., 2000). In addition, their casts and porosity December, January and February are the coldest
enhance the biogenic soil structure (Pulleman et al., months. Two rivers, the Ravi flows on the Eastern,
2003). hSome studies on the subsurface casts and while the Chenab on the Western boundary of the
their dynamics have been reported (Mcinerney and district. The field observation and collection of
Bolger, 2000; Feng et al., 2001 and Mariani et al., earthworms was carried out at interval of one month
2007). No doubt the abundance of earthworms and in fully randomized field experiment. The orchards
their positive activities (cast, burrows and had plain surface topography with clay loam soil
biodegradation) in the soil increase the productivity texture (Clay = 60.5 %, Silt = 22.5 % and Sand = 17
of the orchards. In the previous studies, the cast %). The average rainfall ranged from 280.7 to 800.80
stabilization mechanisms with the development of mm and the relative humidity was ranging from 6.7 to

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Int. J. Biosci. 2014

8.0 and 32.2 to 30.9 at 00 UTC and 12 UTC throwing at 05 different positions within an area of
respectively, per year. Wind speed (knots) average 0.3 selected tree trunk in the selected orchard. Simple
and 1.2 at 00 UTC and 12 UTC, respectively annually. hand sorting technique was employed to procure
The annual average maximum and minimum earthworms (Pelosi et al., 2009). Each specimen of
temperatures were 24.0 and 12.5 °C. The earthworm earthworm was given a number and was labeled with
abundance was high close to the tree trunks as site, locality and date of collection. Each specimen
compared to the open; regularly tillage areas of the was washed with tap water and then anaesthetized in
orchards sampled as control/ disturbed areas. 5.0 % ethyl-alcohol for one to two hours. Each
specimen was straightened in a Petri-dish containing
Methods 10.0 % formalin and kept as such in 24 hours in order
Four study orchards [orange (n = 500), guava (n = to hardened it. Permanent storage was done in 5.0 %
422), mango (n = 336) and berri (n = 82)] were formalin.
selected and five samples from each were collected
randomly by throwing a quadrate of 12''X 12''. Morphological characteristics (Bhatti, 1962; Sims and
Standard field procedures used in soil research and Gerard, 1985) were recorded for the identification of
total number and diameter of burrows were various species. These are as before and after the
measured. Sample was taken from the randomly preservation, the colour of the specimen as well as the
selected tree trunk A total area of 432 sq. inches was colour of its clitellum was noted. Setal arrangement,
dug divided in to three consecutive of one foot each position of clitellum, position of dorsal pores, male
(12'' X 12'') upto three ft2 depth as a third layer. The and female pores, genital papillae, genital pores,
number of burrows was changed from the above spermathical pores, no. of spermathical pores,
ground level to sub- and below ground level. The annulation on the segments, shape of prostomium,
change in burrows diameter and length consequently peristomium, total no. of segments, and total length
change in texture of the selected soil. Within orchards of each specimen etc. were recorded.
variations were also observed. Data on temperature,
rainfall, wetness and humidity was collected from Results
Meteorological Department, University of Table 3 shows the soil physiochemical properties of
Agriculture, Faisalabad, Pakistan. Soil temperature of the 0 – 12 inches top layer in experimental orchards.
each sample was also taken round the orchards. The soil had an average pH (8.02), overall average
OM (1.62 %), average phosphorous and potassium
Casts collection (9.23 ppm, 165.64 ppm) respectively. The soil pH of
All the casts present on the surface inside the all orchards was alkaline in nature. It was observed
quadrate were collected and air dried for further that OM showed high 2.47 % in Guava and steadily
analysis to know the compactness of the casts. Fresh decreased in the other orchards, least in orange and
casts were collected and used as such at spot of mango (1.03, 1.07). The concentration of
analysis for research. A simple method explored as phosphorous was high in Berri orchards and least in
the 10 ml tap water added in 10 g casts in 100 ml Gauva. The concentration of potassium was high in
conical flasks with gentle shaking and the dissolving Berri orchards (189.37 ppm) and least in Mango
time was noted. For this purpose, the earthworms (142.59 ppm), respectively. The number of
were rear in the laboratory. A hew was used to collect earthworms was high in the Berri followed by orange
the soil sample (without casts) from randomly and least in guava orchards.
selected position within the quadrate for control.
Five hundred twenty three earthworms were collected
Earthworm collection from the four orchards. About eighteen species
A steel quadrate of 12' X 12' was randomly located by belonging to ten genera were found (Tables 1 and 2)

77 Jalal et al.

Int. J. Biosci. 2014

Pheretima (n = 458,), Aporrectodea (19, 3.36 %), number of harboured were P. morrisi (n = 18, 3.44
Eutypheous (1, 0.19 %), Allolobophora (1, 01 %) %), R. bishambari (n = 14, 2.68 %), E. eugeniae (n =
Dendrbaena (5, 0.96 %), Eudrilus (09, 1.72 %), 09, 1.72 %), A. caliginosa (n = 08,1.53 %), A. rosea (n
Ramiella (14, 2.68 %), Microscolex (6, 1.15 %), = 07, 1.33 %), M. phosphoreus (n = 06, 1.15 %), D.
Octochaetus (05, 0.96 %) and Diccogaster (5, 0.96 %) pygmaea, O. beatrix and D. modilianii, A. limicola
were identified on morphological characteristics (03), P. elongate (n = 02, 0.38 %) and P. suctoria, A.
bases . A fair number of Pheretima posthuma (n = longa, E. waltoni, A. chlorotica (n = 01, 0.20 %),
366, 69.98 %), P. hawayana (n = 43, 8.22 %) and P. respectively.
houleti (n = 27, 5.16 %) were recorded. The least

Table 1. Distribution of the earthworm species in the selected orchards.

Earthworm species Orange Gauva Mango Berri

Pheretima posthuma ++ ++ ++ ++
++
Pheretima hawayana ++ ++ + ++
+
Pheretima houlleti +- ++ +
+
Pheretima morrisi +- - -
-
Pheretima suctoria -- - -
+
Pheretima elongate -- - -
-
Aporrectodea limicola -- + +
+
Aporrectodea collignosa - ++ + +
+
Aporrectodea longa +- - -
-
Aporrectodea rosea +- +

Eutypheous woltoni -+ -

Allolobophora chlorotica -- +

Denddrobaena pygmaea -- -

Eudrilus eugniea -+ -

Ramiella bishambari +- -

Microscolex phophorrous ++ -

Octochaetus beatrix -- +

Dichgaster modigliani -- +

- = Absent, ++ = High density population (≥ 6), + = Low density population (6≥).

Beri and mango were diversified with 10 species A total area of 144 sq. inches of soil surface contained
belonging to 05 genera, respectively, followed by 127 samples (3.97±0.99g/5) of wet/dry casts and
orange (08 species and 04 genera) and guava (07 calculated total number of burrows 984 (30.75±7.14).
belonging to 06 genera). In Beri orchards, a total of The wet casts did not make aggregate when dissolved
301 earthworms were captured, of which 46.27 % (n = in water observed after one hour, while dry casts
242) were P. posthuma and it did not occur in the aggregate depended upon the length of dryness and
samples of February, March, April, only one specimen the climatic conditions. The length of burrows, at the
was harboured in the sample of January. Mango edge of the fields along the water channels were very
orchards were 7.84 % (n = 41) of P. posthuma out of difficult to measure because of saturation of burrows
79 earthworms, were absent in January to February. and casts during the experimental period. In the
Again P. posthuma was abundant 13.38 % (n = 70) in sugarcane field, between the edge and center, the
orange orchards but P. hawayana were high in length of burrows were ranges from 3-53 inches,
number 2.48 % (n= 13) and followed by P. posthuma within the selected quadrate (25.33"±2.37") and in
2.42 % (n = 12). Moreover the diversity abundance, the center the orchards away from tree trunk were
richness, evenness and dominance of the earthworm present but in low quantity (10.78"±4.11"). In the Beri
species through Shannon and Weaver index were orchards, their calculated range was 4"-50"
confirmed (Tables. 1 and 2). (10.97"±7.22"). In the orange orchards, their range

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Int. J. Biosci. 2014

was 3"-53" (12.97"±7.72") and in mango orchards, differences and stage of the life of earthworms. In
their range was 2"-49" (14.49"±7.92"). The results case of casts compactness analysis, the fresh casts
indicated that the orchards to orchards variations in were easily dissolved in tap water while the dry casts
the burrowing length were present which were took time to dissolve and the control (sample without
ultimately indicated the earthworm’s diversity and casts) also required a time to dissolve, but the length
abundance of the species in the selected orchards. of required time depended on the dryness as well the
Tables 3 & 4 revealed that the burrows and the casts compactness of the casts and soil.
were varied which might be due the species

Table 2. Diversity, abundance and the dominance of the earthworm species in the selected orchards.

Orchards Species Richness Species Abundance Diversity Max. Diversity Evenness Dominance

Berri 10 301 0.8058 2.3026 0.3499 0.6501

Orange 08 97 1.1867 2.079 0.5708 0.4292

Mango 10 79 1.5525 2.3026 0.6742 0.3258

Gauva 07 46 1.7516 1.9449 0.9006 0.0999

Tables 4 indicated diameter of the earthworms and even the elevated edges showed abundant of burrows
the diameter of casts of the abundant genus with excavated casts. Earthworm burrows increase
Pheretima. There is a significant difference between the rain water holding capacity by filling air spaces of
orchards to orchards. The results pointed that there is the burrows with rain water. The water holding
a significant increase water holding capacity near the capacity of a field was also depend on the soil
tree trunks. Although along the water channels one structure, type and the underground fauna.
meter zone were saturated with earthworm burrows

Table 3. Soil characteristics and diameter of earthworm burrows underground casts of the selected orchards.

Orchards variety pH OM (%) P (ppm) K (ppm) Underground casts
(Diameter: mm)

Berri 8.05 ± 0.01 1.92 ± 0.25 11.4 0±0.26 189.37±15.48 5.22 (range 2.5 to 6.0)
Orange 7.99 ± .035 1.03 ± 0.17 10.48 ± 0.38 160.8 ± 15.9 4.98 (range 2.5 to 7.5)
Mango 8.03 ± 0.02 1.07 ± 0.14 10.68 ± 0.15 142.59 ± 18.10 4.2 (range 3.4 to 8.0)
Gauva 8.01 ± 0.02 2.47 ± 0.68 4.39 ± 0.69 169.8 ± 13.53 5.11 (range 2.5 to 7.4)

Discussion different species in the same habitat had their own
The physicochemical properties of soil in the niche (Judas, 1992). The results of investigations
sugarcane and maize with nearly neutral pH and indicated that a period of several years was needed for
more than 1% organic matter (OM), are best suitable settlements of earthworms in cropland due to the
for productivity and earthworms abundance in disturbing factors, tilling, harvesting, fertilization and
contrast to acidic pH (Nakamura, 1998). OM and the use of pesticides, even under favourable conditions, in
quantity of water are the key limiting factors that are contrast a co relationship between total OM and
sufficient near the channels (Aina, 1984). Therefore, abundance of earthworms (Blancart et al., 2004;
the presence of different species earthworms with Nakamura et al., 2003; Rehman et al., 2000; Whalen,
different niches is obvious, according the water 2004; Rossi et al., 2006).
moisture availability. In case of OM, the litter was
more important than OM and different species In the present study, eighteen species (Table 1) have
preferred different decomposing stage of it as been reported on the bases of morphological

79 Jalal et al.

Int. J. Biosci. 2014

characteristics. Monthly samples showed that P. and hot months of summer (May and June) (Pelosi et
posthuma was the most abundant species throughout al., 2009). Therefore in this study, the harsh
the years except in the months of February. This gab condition of winter and summer seasons seems to be
was filled two species, Aporrectodea calliginosa and limiting factors for various earthworm species. Only a
Eutypheous woltoni as earthworms activity in the few specimens of P. posthuma and its close associate
tropics was limited to certain season (Gates, 1961). P. hawayana were found to penetrate to two feet
Most of the species were absent in the cold and dry deep in the soil in the winter along R. Bishambari
months of winter (December, January and February) and D. pygmaea.

Table 4. Casts diameter of Pheretima species (n=50) harbor from the orchards.

Parameter Adults (mm) adult/immature (mm) Immature (mm)

Minimum 3.0 0.5 0.5
Maximum 11.6 8.25 7.7
Average 10.5 7.27 5.9

The number of species in a given earthworm rosea, A. chlorotica) might be dominant in the center
community which is the simplest measure of species of fields in order to resist field practices (Smith et al.,
diversity, was ranging from 1-18 species. The 2008). The second main reason, small size species
Shannon Diversity Index indicated that the (Ramiella bishambari, Dendrobaena pygmaea etc.)
submission of the four selected orchards were highly were mostly present the center of the fields in the cold
diversified (H= 81. 85) as compared to the selectively and dry months of November through February as
selected orchards. The comparison between the fields permits (ploughing/ field practices) let not
orchards indicated Berri orchards is highly diversified adversely damaged (Lagerlof et al., 2002) irrespective
(38.75) leading to Mango and Orange orchards (26.4, to fields provided all the resources necessary for the
24.93), except Guava Orchards (15.61). Most survival of the species.
earthworm communities contain three to six species
indicating the influence of the characteristics of soil, A strong linear correlation existed between climatic
climatic conditions, organic resources of the locality factors, number of casts, number of burrows and
and the history of land use as well as soil disturbance earthworms population. Rainfall, temperature and
etc. (Edwards and Bohlen, 1996; Whalen et al., 1998; wetness, having profound linear correlation with the
Pelosi et al., 2009). Therefore, proper wetness and increase of earthworm (p = 0.01 as well p = 0.05),
optimum temperature (25 – 35 °C) conditions was although the relative humidity having inverse linear
favourable factors to enhance the population size of correlation. Rainfall significantly influenced the
earthworms. earthworm population (p = 0.05) which is indicated
in the months of April and May. The primary
Mostly, species were present near the water channels production and stability plays the key role in
under the shadow of tall trees as inside the fields agroecosystem maintenance and earthworms played
where adverse environmental factors, crop rotation, an indispensable role in mediating some biophysical
ploughing, limited and are suitable for the survival of processes for the primary production in the paddy
the earthworms (Lagerlof et al., 2002), in accordance fields (Changuo et al., 2006). It is also prove in some
that earthworms were most abundant in non-arable agroecosystem, earthworms play vital role in the
and undisturbed parts of the fields than that of growth of plants under favourable environmental
ploughed ones (Ivask et al., 2007; Smith et al., 2008). conditions (Eriksen-Hamel and Whalen, 2007).
This is might be the one main reason for the absence
of the earthworms in the center of the orchards, while The fresh casts (8 h, 12, 24, 48, 72 h) sample had no
endogeic earthworms (Aporrectodea caliginosa, A. significant influence on aggregate stability which is

80 Jalal et al.

Int. J. Biosci. 2014

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