Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

Iranian (Iranica) Journal of Energy & Environment

Journal Homepage: [Link]
IJEE an official peer review journal of Babol Noshirvani University of Technology, ISSN:2079-2115

Growth Performance of Varieties of Bean (Phaseolus vulgaris) Seedlings in

Earthworm-Bioturbated Soil and Crab-Bioturbated Soil

E. O. Dada*, F. A. Oke, Y. O. Balogun

Department of Cell Biology and Genetics, Faculty of Science, University of Lagos (Institution), Akoka, Yaba, Lagos, Nigeria

PAPER INFO A B S T R A C T

Paper history: Earthworms and crabs are known to influence the physicochemical state of their respective soil
Received 08 September 2022 habitats through their bioturbation actions. While earthworm-bioturbated soils have been well
Accepted in revised form 06 November 2022 documented to positively affect plant growth, not much is known about the effects of crab-
bioturbated soil on plant growth. In this study, we compared the growth performance of four
Keywords: varieties of Phaseolus vulgaris (bean) seedlings in earthworm-bioturbated soil, crab-bioturbated
Bioturbation soil, and unbioturbated soil collected within the same proximity of a wetland habitat. Seeds of
Plant growth Phaseolus vulgaris were planted in replicates in each soil type, and allowed to grow for 15 days.
Plant hormones Physical growth was measured using a metre rule. Biochemical growth parameters were
Vermicasts measured using standard procedures. The differences in stipule length of bean seedlings grown
in all the soil types were generally not significant (p > 0.05). However, seedlings grown in
earthworm-bioturbated soil and crab-boturbated soil recorded significantly higher (p < 0.05)
stipule weight, relative to those grown in unbioturbated soil. Bean seedlings grown in
earthworm-bioturbated soil recorded the highest and significant (p < 0.01) concentrations of
chlorophyll, total sugar, starch, nitrogen, and crude protein, relative to those grown in crab-
bioturbated and unbioturbated soils. This was followed by seedlings grown in crab-bioturbated
soil which recorded significantly higher (p < 0.01) concentrations of these biochemical
parameters, relative to those grown in unbioturbated soil. The significantly higher biochemical
and marginally better physiological growth recorded for seedlings in bioturbated soils indicate
that earthworms and crabs both contribute significantly to wetland productivity, through their
bioturbatiion activities.
doi: 10.5829/ijee.2023.14.01.05

INTRODUCTION1 documented, such that earthworms are figuratively

referred to as ‘friends of farmers’ [4, 5]. Earthworms are
Bioturbation is a biological reworking and remixing of so much considered important to soil health and quality
soil sediments by the activities of plants and animals. that their presence has become a major yardstick for
Bioturbation activities by living organisms, especially determining the fertility of soil. Earthworms impact soil
burrowing animals, are a powerful driver of nutrients and quality and contribute to plant growth and crop yield
carbon cycling across soil sediments and layers. through their bioturbation activities of burrowing,
Bioturbation significantly impacts soil quality, nutrients feeding, foraging, and hormone and enzyme secretions.
availability, and other ecosystem services [1]. Plants, Burrowing, feeding and casting are a three-in-one soil-
especially trees, may also bioturbate the soil through their impacting bioturbation process of many earthworm
rooting and falling actions [2, 3]. species. During feeding, earthworms eat through the soil
The contributions of earthworms to soil nutrient or soil organic matter, creating burrows in the process. As
enrichment, plant growth, and crop productivity have, for the soil and organic matter passes through the alimentary
long, been significantly appreciated, researched, and canal of the earthworm, they are ground and mixed with

* Corresponding Author Email: eodada@[Link] (E. O. Dada)

Please cite this article as: E. O. Dada, F. A. Oke, Y. O. Balogun, 2023. Growth Performance of Varieties of Bean (Phaseolus vulgaris) Seedlings in
Earthworm-Bioturbated Soil and Crab-Bioturbated Soil, Iranian (Iranica) Journal of Energy and Environment, 14(1), pp. 38-45.
Doi: 10.5829/ijee.2023.14.01.05
 E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

digestive enzymes and microorganisms, and are experimental container and evaluated for the growth
eventually egested as vermicasts. Earthworm casts or performance.
vermicasts have been found to be richer in plant growth-
promoting hormones and microorganisms, than their Determination of physical and biochemical growth of
surrounding soil [4, 6, 7]. bean seedlings
Similarly, burrowing crabs have been identified as Physical growth parameters of seedlings, namely stipule
one of the most essential macroinvertebrates in many length and stipule weight were measured using a metre
marshy wetlands, where they are often present in large rule and weighing balance, respectively. To measure
numbers [5, 8, 9]. The burrowing and feeding activities of biochemical growth, bean seedling tissues were
these crabs have been found to influence many wetland homogenized using a mortar and pestle. Homogenized
ecosystem functions, including carbon transformation, samples were thereafter analyzed for chlorophyll a,
nutrients cycling, and sediments remixing [3, 10, 11]. chlorophyll b and total chlorophyll, starch, total sugar,
Although, studies on the potential of crab-bioturbated soil protein, total nitrogen, using the procedures adapted from
as a plant growing medium are scarcely found, researches the Association of Official Analytical Chemists [14], as
conducted to examine the quality of crab-bioturbated soil briefly described hereunder.
have suggested that they would serve as good plant-
growing medium [12, 13]. Crab burrows can selectively Chlorophyll a, b and total chlorophyll
trap sediments that have high organic matter To determine chlorophyll a, chlorophyll b, and total
concentrations, finer grain size and low density, which chlorophyll, fresh leaf samples were weighed, put
can increase nutrient availability and thus, promote the separately in 80 % N/V acetone (15 ml for each gram) and
growth of plant and beneficial microorganisms [12, 13]. homogenized with the Phillip type harmonizer at 1000
In our previous work [3], we carried out rpm for one minute. Thereafter, 0.5 g of pure sand, plus
physicochemical and microbial analysis of earthworm- 1.0 g of anhydrous sulphate was added to the sample. The
bioturbated soil and crab-bioturbated soil collected from homogenate was filtered through a two-layered
a wetland habitat and reported improved qualities in the cheesecloth and centrifuged using the Signs centrifuge, at
two soil types, relative to unbioturbated soil. In this 2500 rpm for ten minutes. The supernatant was separated,
study however, we aimed to compare the growth and the absorbance were read at spectrophotometer.
performance of four varieties of Phaseolus vulgaris Chlorophyll a was read at wavelength 663 nm and 645
(bean) seedlings in earthworm-bioturbated soil and crab- nm, while chlorophyll b was read at 645 nm and 663 nm
bioturbated soil, collected from the same proximity of a [15, 16], Chlorophyll a, chlorophyll b, and total
wetland habitat. chlorophyll were calculated as indicated below.
Chlorophyll a (Chl a) = 12.7A663) – 2.69 (A645) (1)
MATERIALS AND METHODS
Chlorophyll b (Chl b) =
(2)
Sample collection and experimental design 22.9 (A645) – 4.68 (A663)
The present study was conducted in the main campus of
the University of Lagos, Nigeria, on longitude 3° 24' E Total chlorophyll = (Chl a + Chl b) (3)
and latitude 6° 30' N. The location is a marshy wetland,
in which earthworms and crabs are always active,
especially in the rainy season. Three soil samples Total nitrogen and crude protein
[earthworm-bioturbated soil (earthworm casts), crab- The crude protein of each sample was determined using
bioturbated soil (dug-out soil), and unbioturbated soil the Kjeldahl nitrogen method. Two grams of each sample
(undisturbed soil)] were collected within a radius of one with two tablets of digestion catalyst were subjected to
meter (1m). Twelve plastic containers were obtained and reaction with 15ml sulphuric in a Kjeldahl tube. The tubes
divided into three groups (four per group). The first, were set up in a digestion block heater (370 oC) until a
second, and third groups of plastic containers were filled clear green colour was obtained. The organic nitrogen in
with earthworm-bioturbated soil, crab-bioturbated, and the sample was converted to ammonium sulphate. The
unbioturbated soil, respectively. Each container was filled digest was cooled to room temperature and diluted to
with 500 mg soil, to three-quarter capacity. 100ml with distilled water, which was further distilled in
Four varieties of Phaseolus vulgaris (Ife Brown, an alkaline condition of 40% sodium hydroxide. The
Oloyin, White Bean, Olo), purchased from an open liberated ammonium hydroxide was trapped in a 2% boric
market in Lagos state, Nigeria were used for the acid solution and titrated against a 0.1 N hydrochloric
experiment. Five seeds of each variety of bean seeds were acid solution [1, 17, 18]. Total nitrogen was then
sown in each soil type. Each experimental container was calculated using the following formula:
irrigated weekly with distilled water. After 15 days, 𝑇𝑜𝑡𝑎𝑙 𝑁𝑖𝑡𝑟𝑜𝑔𝑒𝑛 =
1.4𝑉∗𝑁
𝑊
(4)
three seedlings were randomly harvested from each

39
 E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

where, V is acid used in titration (ml), N stand for The concentration of starch was then determined by
normality of standard acid and W is the weight of multiplying the obtained value by 0.9; converting the
sample (g). glucose value to starch content [20, 21].
The crude protein was then calculated from the total
nitrogen in the sample using the conversion factor 6.25, Statistical analysis of data
based on the premise that the average protein contains The data generated from the measurement of physical
about 16% nitrogen [14]. growth and laboratory analysis of biochemical parameters
were subjected to Analysis of Variance (ANOVA). Mean
Total soluble soluble sugar and starch content differences were separated using Duncan Multiple Range
Total sugars and starch were estimated according to the Test, at 5% level of significance (p < 0.05). All analyses
anthrone-sulphuric acid reported by Sung et al. [19], with were done using IBM SPSS v 26 (IBM Corporation, New
slight modification. Homogenized sample extract (0.1ml) York).
was pipetted into duplicate test tubes and 0.9 ml of
distilled water was added. The test tube contents were
further diluted by taking 0.1 ml from each of the tubes, Results
and adding 0.9 ml distilled water (making 1% extract
solution), which was also made in triplicates. A blank was Stipule length and stipule weight of Phaseolus vulgaris
prepared using 1ml of distilled water. Four millilitres seedlings grown in earthworm-bioturbated, crab-
(4ml) of Anthrone reagent (0.2% anthrone in bioturbated, and unbioturbated soils
concentrated H2SO4) was added to each of the test tubes. The stipule length and stipule weight of Phaseolus
The tubes were shaken and left in boiling water for ten vulgaris seedlings grown in crab-bioturbated, earthworm-
minutes. The tubes were cooled under tap water and the bioturbated and unbioturbated soils are presented in Table
optical density was read using 620nm wavelengths. The 1. The differences in stipule length of bean seedlings
concentration of total soluble sugar was calculated, using grown in all the soil types were generally not significant
the concentration factor 1.0 mg/ml glucose as standard, (p > 0.05). The stipule weight of Olo and oloyin varieties
with the formula: of Phaseolus vulgaris grown in earthworm-bioturbated
𝑆𝑡𝑑.𝑐𝑜𝑛𝑐 𝑠𝑎𝑚𝑝𝑙𝑒 𝑎𝑏𝑠. 𝑥 100 soil (Olo: 5.57±1.01 g; Oloyin: 5.83±0.29 g) and crab-
Total sugar = 𝑥 (5)
𝑆𝑡𝑑. 𝑎𝑏𝑠. 𝑤𝑒𝑖𝑔ℎ𝑡 𝑜𝑓 𝑠𝑎𝑚𝑝𝑙𝑒 boturbated soil (Olo: 4.83±0.29 g; Oloyin: 5.00±0.50 g)
where, were significantly higher (p < 0.05), relative to those
Std. abs. = Standard absorbance, and grown in unbioturbated soil. Both stipule lengths and
Sample abs. = Sample absorbance. weights of the White bean variety showed no significant

Table 1. Stipule length and stipule weight of Phaseolus vulgaris seedlings grown in earthworm-bioturbated, crab-bioturbated and
unbioturbated soils
Stipule length and stipule weight of varieties of bean seedlings
Stipule length (cm)
Soil type Ife brown Olo Oloyin White bean
a a a
Unbioturbated soil 10.00 ± 1.00 10.17 ± 0.29 10.57 ± 0.51 10.17 ± 1.04 a
Crab-bioturbated soil 10.93 ± 0.12 a 10.90 ± 0.17 a 11.50 ± 0.50 a 11.23 ± 0.64 a
a a a
Earthworm-bioturbated soil 10.00 ± 0.50 11.06 ± 1.51 11.67 ± 0.58 11.67 ± 1.41 a
F value 2.27ns 1.93 ns 3.73 ns 2.08 ns
Stipule weight (g)
Soil type Ife brown Olo Oloyin White bean
b b b
Control (Unbioturbated soil) 4.07 ± 0.81 3.83 ± 0.29 4.37 ± 0.71 4.33 ± 1.26 a
Crab-bioturbated soil 5.20 ± 0.61 a 4.83 ± 0.29 ab 5.00 ± 0.50 ab 5.17 ± 0.58 a
Earthworm-bioturbated soil 4.83 ± 0.76 b 5.57 ± 1.01a 5.83 ± 0.29 a 5.50 ± 0.87 a
ns * *
F value 1.862 5.77 5.82 1.29ns
Different letters: statistically significant
*
Signoficant at P< 0.05
**
Significant at P < 0.01
ns
Not significant

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 E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

difference, across the three soil types. Olo seedlings in unbioturbated soil (19.93±2.39mg/g). The same pattern
earhtworm-bioturbated soil recorded significantly higher was observed for chlorophyll a of White bean; there was
(p < 0.05) weight (5.57 ± 1.01mg/g) than those in no significant difference between the pigments in crab-
unbioturbated soil (3.83 ± 0.29mg/g). Oloyin seedlings in bioturbated soil (29.11±1.66mg/g) and earthworm-
earthworm-bioturbated soil had significantly higer (p < bioturbated soil (30.64±0.42mg/g). However, they were
0.05) weight (5.83 ± 0.29mg/g) than the seedlings in both significantly higher (p < 0.05) than those in
unbioturbated soil (4.37 ± 0.71mg/g). unbioturbated soil (21.61±1.91mg/g). Total chlorophyll
in White bean seedlings grown in crab-bioturbated soil
Chlorophyll a, b and total chlorophyll of Phaseolus (42.64±1.50mg/g) and earthworm-bioturbated soil
vulgaris seedlings grown in earthworm bioturbated, (42.16±0.57mg/g) showed no significant deifference, but
crab-bioturbated, and unbioturbated soils were both significantly higher (p < 0.05) than the total
Phaseolus vulgaris grown in bioturbated soil recorded chlorophyll in White bean grown in unbioturbated soil
significantly higher Chlorophyll a, b and total (34.50±3.11mg/g).
chlorophyll, relative to those grown in unbioturbated soil.
Seedlings grown in earthworm–bioturbated soil recorded Total soluble sugar, starch, nitrogen, and protein in
the highest chlorophyll a, b and total chlorophyll, Phaseolus vulgaris seedlings grown in earthworm
followed by those grown in crab-bioturbated soil. bioturbated, crab-bioturbated, and unbioturbated
Seedlings grown in unbioturbated soil recorded the least soils
of these parameters (Table 2). The chlorophyll b in White Bean seedlings grown in earthworm-bioturbated soil
bean and Oloyoin seedlings showed no significant recorded the highest and significant (p < 0.01)
difference (p > 0.05), across the three soils. The concentrations of total soluble sugar, starch, nitrogen, and
difference observed between the chlorophyll a of Oloyin crude protein, relative to those grown in crab-bioturbated
seedlings grwon in crab-bioturbated soil and unbioturbated soils. Similarly, seedlings grown in
(29.11±1.66mg/g) and those grown in earthworm- crab-bioturbated soil recorded significantly higher (p <
bioturbated soil (29.00±1.84mg/g) was not significant (p 0.01) concentrations of these biochemical parameters,
> 0.05). However, they were both significantly higher relative to those grown in unbioturbated soil (p < 0.01)
than chlorophyll a in Oloyin seedling grown in (Table 3).

Table 2. Chlorophyll a, b and total chlorophyll of Phaseolus vulgaris seedlings grown in earthworm bioturbated, crab-bioturbated, and
unbioturbated soils
Chlorophyll a, b and total chlorophyll in varieties of bean seedlings
Chlorophyll a (mg/g)
Soil type Ife brown Olo Oloyin White bean
Unbioturbated soil 19.84±1.73 c 22.71±1.26 c 19.93±2.39b 21.61±1.91b
b b a
Crab-bioturbated soil 29.56±1.79 28.08±1.26 29.11±1.66 30.44±1.16a
Earthworm-bioturbated soil 31.33±1.07 a 30.45±0.74 a 29.00±1.84a 30.64±0.42a
F value 141.10** 113.70** 625.04** 138.94**
Chlorophyll b (mg/g)
b
Unbioturbated soil 16.32±0.67 16.05±0.52b 14.52±0.22a 12.89±2.13a
Crab-bioturbated soil 19.59±0.71a 15.96±0.84b 15.27±0.93a 12.61±1.11a
a a a
Earthworm-bioturbated soil 20.10±1.04 17.33±0.96 14.53±2.33 11.51±0.27a
F value 55.52** 8.33** 0.781ns 2.43*
Total chlorophyll (mg/g)
b
Unbioturbated soil 36.14±3.36 37.64±3.05c 34.45±2.54c 34.50±3.11b
Crab-bioturbated soil 50.05±2.91a 44.04±2.08b 44.39±2.26b 42.64±1.50a
Earthworm-bioturbated soil 51.42±2.01a 47.78±1.48a 43.46±3.97a 42.16±0.57a
** ** **
F value 109.63 44.68 29.62 46.04**
Different letters: statistically significant
*
Signoficant at P< 0.05
**
Significant at P < 0.01
ns
Not significant

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 E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

Table 3. Total soluble sugar, starch, nitrogen, and protein in Phaseolus vulgaris seedlings grown in earthworm bioturbated, crab-
bioturbated, and unbioturbated soils
Total soluble sugar, starch, nitrogen, and protein in varieties of bean seedlings
Total soluble sugar (mg/g)
Soil type Ife brown Olo Oloyin White bean
c c c
Unbioturbated soil 54.76±1.60 53.96±1.20 56.46±0.77 57.97±0.69c
Crab-bioturbated soil 64.05±0.95b 60.81± 0.86b 61.30± 0.81b 62.12± 2.15b
Earthworm-bioturbated soil 65.71± 0.51a 63.87± 0.63a 66.12± 0.62a 66.52± 0.87a
F value 253.41** 246.70** 382.35** 83.96**
Starch (mg/g)
Unbioturbated soil 34.75±0.97c 35.75± 0.33c 35.35± 0.10c 35.79± 0.19c
b b b
Crab-bioturbated soil 36.49±0.20 36.82±0.46 37.19±0.27 37.83± 0.23b
Earthworm-bioturbated soil 38.71± 0.22a 38.61± 0.21a 39.19± 0.26a 39.30± 0.08a
F value 103.83** 55.14** 658.32** 866.99**
Nitrogen (mg/g)
c
Unbioturbated soil 3.47± 0.07 3.22± 0.06c 3.34± 0.04c 3.23± 0.02c
Crab-bioturbated soil 3.99± 0.08b 3.84± 0.07b 3.88± 0.11b 4.02± 0.05b
a a a
Earthworm-bioturbated soil 4.48± 0.10 4.27± 0.08 4.32± 0.04 4.46± 0.04a
F value 316.54** 551.43** 430.43** 2355.66**
Protein (mg/g)
c
Unbioturbated soil 21.69± 0.47 20.14± 0.35c 20.83± 0.35c 20.23± 0.12c
Crab-bioturbated soil 24.96± 0.49b 23.99± 0.42b 24.21± 0.63b 25.10± 0.29b
Earthworm-bioturbated soil 27.93± 0.58a 26.70± 0.49a 27.02± 0.24a 27.81± 0.26a
** ** **
F value 332.75 555.31 451.08 2360.64**
Different letters: statistically significant
*
Signoficant at P< 0.05
**
Significant at P < 0.01
ns
Not significant

DISCUSSION with crab-bioturbated soil [9, 11]. These qualities can be

related to the better growth performance of seedling
In this study, seedlings performance in earthworm- grown in bioturbated soil.
bioturbated and crab-bioturbated soils, in comparison The chlorophyll content of a plant is directly related
with unbioturbated soil, show significant improvements to the amounts of soil nutrients availabe for the plant’s
in all the measured biochemical and physiological growth absorbtion, as these nutrients serve as building blocks for
parameters, expect for stipule weight whose difference the plant tissues [24, 25]. Therefore, the observed
was only marginal. The improved seedling growth in increase in chlorophyll content of P. vulgaris seedings
earthworm-bioturbated soil readily corroborates many grown in bioturbated soils can be linked to the relatively
previous studies including Tomati et al. [22] and Xaio et abundanrt nutrients in the soils [3]. Total soluble sugar,
al. [23] who reported improved growth of Raphanus starch, nitrogen and protein are essentially photosynthetic
sativus and Brassica rapa respectively, in earthworm products; hence, the higher concentrations recorded for
casts. Both earthworm-bioturbated and crab-bioturbated these products in seedlings grown in bioturbated soil can
soils are known to possess improved physicochemical be associated with their elevated levels of chlorophyll,
qualities that can potentially promote plant growth and which must have conferred on them, improved
development. Earthworm-bioturbated soils are photosynthesis efficiency. Similarly, the significantly and
characterized by decreased bulk density and increased marginally higher stipule weight and stipule length
soil water content, organic matter, soil organic and respectively, recorded for seedlingsown in bioturbated
inorganic carbon, nitrogen, phosphorus and beneficial soils are complimentary to the observed increased
microorganisms [4, 6]. These qualities are also associated biochemical growth and chlorophyll efficiency. The

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 E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023

stipule growth-promoting potential of bioturbated is of biotubated soil is not only remarkable, but calls for
remarkable importance because it contributes research attention.
substantially to primary productivity in plants. It is on
record that stipules can contribute as much as 30% to
plant photosynthesis, which is occasionally more than the AKNOWLEDGEMENT
contribution of leaves [26]. Stipule growth also
determines the flowering time of a plant, an indicator of This research received no specific grant from any funding
plant pod production [27]. In other words, stipule growth agency in the public, commercial, or not-for-profit
substantially determines seed production. sectors.
The higher growth performance recorded for
seedlings grown in earthworm-bioturbated soil, relative
to those grown in crab-bioturbated soil is a reflection of CONFLICT OF INTREST
the long-known positive impact of earthworms to soil
improvement and crop production. It is also in tandem The authors declare that there was no conflict of interest
with our earlier work [3]. where we compared the related to this article.
physicochemical and biochemical qualities of
earthworm-bioturbated soil and crab-bioturbated soil and
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 ‫‪E. O. Dada et al. / Iranian (Iranica) Journal of Energy and Environment 14(1): 38-45, 2023‬‬

‫‪Persian Abstract‬‬
‫چکیده‬
‫کرمهای خاکی و خرچنگها بهعنوان تأثیرگذار بر وضعیت فیزیکوشیمیایی زیستگاههای خاکی مربوطه خود از طریق اقدامات بیوتورباسیون خود شناخته شدهاند‪ .‬در حالی که‬
‫خاکهای بیوتورباته شده با کرم خاکی بهخوبی مستند شدهاند که بر رشد گیاه تأثیر مثبت میگذارند‪ ،‬اطالعات زیادی در مورد اثرات خاکهای بیوتورباته شده با خرچنگ بر‬
‫رشد گیاه شناخته نشده است‪ .‬در این مطالعه‪ ،‬ما عملکرد رشد چهار گونه از نهالهای (‪ )Phaseolus vulgaris‬لوبیا را در خاک با کرمهای خاکی‪ ،‬خاک بیوتورباته شده با‬
‫خرچنگ‪ ،‬و خاک بدون توربوتی که در همان مجاورت یک زیستگاه تاالب جمعآوری شدهاند‪ ،‬مقایسه کردیم‪ .‬بذر ‪ Phaseolus vulgaris‬به صورت تکرار در هر نوع خاک‬
‫کاشته شد و به مدت ‪ 15‬روز رشد کرد‪ .‬رشد فیزیکی با استفاده از قانون متر اندازه گیری شد‪ .‬پارامترهای رشد بیوشیمیایی با استفاده از روش های استاندارد اندازه گیری شد‪.‬‬
‫تفاوت در طول نهال لوبیا رشد یافته در تمام انواع خاک به طور کلی معنی دار نبود (‪ .)p < 0/05‬با این حال‪ ،‬نهالهای رشد یافته در خاک با کرمهای خاکی و خاک خرچنگ‬
‫بوتهشده به طور قابلتوجهی باالتر (‪ )p > 0/05‬وزن ‪ ،stipule‬نسبت به کسانی که در خاک ‪ unbioturbated‬رشد کردهاند‪ ،‬ثبت کردند‪ .‬نهالهای لوبیا رشد کرده در خاک‬
‫بیوتورباته شده با کرم خاکی‪ ،‬باالترین و معنیدارترین (‪ )p > 0/01‬غلظت کلروفیل‪ ،‬قند کل‪ ،‬نشاسته‪ ،‬نیتروژن و پروتئین خام را نسبت به آنهایی که در خاکهای خرچنگ و‬
‫اردهای نشده رشد میکنند‪ ،‬ثبت کردند‪ .‬این توسط نهال رشد کرده در خاک خرچنگ ‪ bioturbated‬که به طور قابل توجهی باالتر (‪ )p > 0/01‬غلظت این پارامترهای‬
‫بیوشیمیایی‪ ،‬نسبت به کسانی که در خاک ‪ unbioturbated‬رشد ثبت شده است‪ .‬رشد بیوشیمیایی و فیزیولوژیکی به طور قابل توجهی باالتر ثبت شده برای نهالها در‬
‫خاکهای بیوتوربیت شده نشان میدهد که کرمهای خاکی و خرچنگها هر دو از طریق فعالیت های بیوتوربایی خود به طور قابل توجهی به بهرهوری تاالب کمک میکنند‪.‬‬

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