33

AGRIVITA VOLUME 36 No. 1 FEBRUARY - 2014 ISSN : 0126-0537

STRUCTURE OF SOIL FOOD WEB IN SMALLHOLDER COCOA PLANTATION,

SOUTH KONAWE DISTRICT, SOUTHEAST SULAWESI, INDONESIA
1)* 2) 2)
Laode Muhammad Harjoni Kilowasid , Tati Suryati Syamsudin , Endah Sulystiawati and
3)
Fransiscus-Xaverius Susilo

1)
Department of Agrotechnology, Faculty of Agriculture, Halu Oleo University,
Jl. HEA Mokodompit 93231 Kendari, Southeast Sulawesi Indonesia,
2)
School of Life Science and Technology, Bandung Institute of Technology, West Java, Indonesia
3)
Department of Agrotechnology, Faculty of Agriculture, Lampung University, Bandar Lampung Indonesia
Corresponding author Phone:+62-401-3193596 Email: lohardjoni2@yahoo.co.id

Received: February 26, 2014 / Accepted: May 22, 2014

ABSTRACT (Berg et al., 2001; Holtkamp et al., 2011). Soil

organic matter and root are the primary energy
An understanding of the structure of the soil food source for microbes and soil fauna (Moore et al.,
web is critical in determining the practices of soil 2004; Petchey et al., 2010). Fraction of soil
fertility management based on the biological organic matter is labile organic fraction that can
processes in tropical agricultural regions. The be accessed by bacteria, fungi as well as
objectives of the study were to assess the saprophagous macro-arthropods, and recalcitrant
variation in trophic level biomass and to analyze organic fraction which is generally more
the dynamics of the energy channels on the accessible by fungi and saprophagous macro-
increasing age of cocoa plantation. The arthropods (Hunt et al., 1987; Coleman, 2008).
characteristics of soil food web structure in Energy and nutrients from soil organic
smallholder cocoa plantation aged 4, 5, 7, 10, matter supplied occupying at the higher trophic
and 16 years were analyzed. The results level can go through the channels of bacterial,
showed that only biomass at the third trophic fungal, and saprophagous macro-arthropods in
level increased with plantation age, but not for soil food web community (Susilo et al., 2004;
the biomass at the lower trophic levels. Biomass Moore et al., 2005; Bardgett and Wardle, 2010).
in all energy channels did not increased as well The process of nutrients in bacterial biomass
along with plantation age. We concluded that flowing into bacterivore up to the top predators is
variation in the soil food web structure was more known as bacterial energy channel, while the
influenced by biotic factors of macro-arthropods nutrients from fungal biomass flowing into the
group, such as facilitation, recolonization fungivora up to the top predators is known as
capabilities and accessibility in the soil habitat of fungal energy channel, and nutrients from root
smallholder cocoa plantation. biomass flowed by nematodes and root-feeding
insects up to the top predator is known as root
Keyword: biomass, biotic, energy channel, trophic energy channels (Moore and Hunt, 1988; Moore
level et al., 1988; Berg et al., 2001). Moreover,
nutrients flowing from saprophagous macro-
INTRODUCTION arthropods biomass to their consumer and finally
up to the top predator could be reffered as
The process of decomposition and saprophagous macro-arthropods energy
nitrogen mineralization involves trophic inter- channel in soil food web community.
action between soil fauna and microbes in soil Development stages of agricultural
food web (Schimel and Bennett, 2004; Osler and practices and succesional vegetation affect
Sommerkorn, 2007). Structures of soil food web energy channels in the soil food web. Generally,
are playing an important role in explaining the the factors causing changes in the energy flow
effect of changes in the composition and diversity will alter the quality and availability of organic
of species on the pathway in decomposition and substrates as a source of energy and nutrients
nitrogen mineralization by soil biota community for microbes and soil fauna (Loranger-Merciris et

Accredited SK No.: 81/DIKTI/Kep/2011

http://dx.doi.org/10.17503/Agrivita-2014-36-1-p033-047
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Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

al., 2008). Didden et al. (1994) found the pattern changes in the structures of soil food
biomass of fungivore soil fauna more dominant web with age of small-holder cocoa plantation is
than bacterivore soil fauna biomass in still rare. The objectives of the study are to
agricultural systems minimized in soil tillage, use assess the variation in biomass of trophic level
of inorganic fertilizers, and biocides. The and to analyze the dynamics of the energy
biomass ratio of fungi to bacteria, biomass ratio channels in the soil food web among ages of
of fungal energy channels to bacterial energy small-holder cocoa plantation.
channels, and biomass ratio of bacterivore to
fungivore in the former agricultural land was MATERIALS AND METHODS
lower than that of the natural forest land
(Holtkamp et al., 2008). Root biomass does not Study Site
only contribute to soil organic matter content The study was conducted in Konda and
(Hertel et al., 2009), but it also serves as carbon Mowila sub-District, South Konawe District,
and nutrient source for soil fauna. Biomass of South East Sulawesi in smallholder cocoa
root-feeding nematodes tend to decrease with plantation aged 4 years (040 08’ 33.2’’S; 122
age of vegetation (Holtkamp et al., 2008), for it is 031’ 01.7’’E), 5 years (040 08’ 50.5’’S; 122 030’
allegedly associated with increased 41.04’’E), 7 years (040 08’ 44.4’’S; 122 030’
concentrations of defense compounds (i.e. 47.7’’E), 10 years (040 08’ 34.4’’S; 122 031’
terpenoids) in root tissues, so it is not easily 40.5’’E), and 16 years (040 07’ 04.9’’S; 1220 15’
accessed by groups of nematodes and insects 02.8’’E). The average of rainfall was 175.58 mm
-1 0
(Bonkowski et al., 2009). The quality of root month and air temperature was 26.74 C. The
tissues not only affects the abundance of root- topography of the research area was
feeding nematodes (Marhaning et al., 2009; categorized as flat with the slope class of 0-3%.
Viketoft et al. 2009), but also the abundance of Soil type was categorized as a sub-group
root-feeding insects and saprophagous macro- Dystrudept Typical, coarse clay, Isohypertermic.
arthropods (Doblas - Miranda, 2009). The location description of every plantation was
An understanding of the dynamics of the described in Kilowasid et al. (2012) and the soil
energy channels in the soil food web is critical in characteristics in the Kilowasid et al. (2013).
determining the regulation of agricultural soil
fertility management practices based on Sample Collection of Soil Organic Fraction,
biological processes in tropical environment Root and Soil Organisms
(Swift, 1997). However, studies related to the Organic fraction of the soil, roots,
dynamics of the soil food web structure in the microbes and soil fauna were put on a square of
2
tropical agroecosystem, especially in 2500 m (50 mx 50 m) on each cocoa plantation.
smallholder cocoa plantation are still neglected. All samples were taken from each site with 15
Indonesia was in the world’s third rank, and it cm in soil depth using stainless steel cylinders.
was in the first rank in Asia-Pacific as cocoa The samples for analysis of soil organic fractions
bean producer (ICCO, 2010). In this region, were collected on August 15, 2010 using soil
approximately 94 % of the total area of cocoa cores with a 7.4 cm-in-diameter cylinder on each
plantations was managed by small farmers corner of the square of each place. Samples of
(Directorate General of Estate, Agricultural active roots, microbes, protozoa, nematodes,
Ministry RI, 2012). By some researchers was acari, collembola, enchytraeids and soil macro-
proposed a small-holder cocoa plantation as fauna were collected five times over a period of
management land system suitable for the soil a year on August 1, 2009, 21 November 2009,
biodiversity conservation (Delabie et al., 2007; January 26, 2010, 22 April 2010, and June 13,
Moco et al., 2009). 2010. Each time the sampling was constructed
The studies related to the dynamic of soil of four sub - squares (each sub - sized 0.5mx
biota community structures was still focused on 0.5m square) were placed between the cocoa
composition and diversity of soil fauna crop in the size of 3m x 3m, and the distance
community from different managemen system between the sub - sqaures to 10 m in each
and different age of cocoa plantation (Moco et square at each place (for more details of the
al., 2009; Kilowasid et al., 2012; Kilowasid et al., sampling design see Kilowasid et al., 2012 and
2013). Meanwhile, up to now the study how the Kilowasid et al., 2013). At every time point in
 35

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

each sub-sample was taken for analysis of soil active amoebae in soil suspensions (1:10) in a
microbes and protozoa using a stainless steel petri dish was counted under an inverted phase
cylinder of 7.4 cm in inner diameter. Soil sample contrast microscope magnified 200 times,
for analysis of microbial analysis, protozoa, following the procedure of Adl et al. (2008).
enchytraeid, nematodes and soil mesofauna Individuals of flagellates were converted to
3
was put in different zipper packs, and each was biovolume with a convertion factors of 50μm
placed in a cool box and transported to the per flagellates (Stout and Heal, 1967). For
3
laboratory. amoeba, the 400 μm convention factor per
amoeba was used (Ekelund et al., 2001), and
Determination of Soil Organic Fraction and biomass of flagellates and amoeba were
-13
Root Biomass calculated with this assumption: 1.1 x 10 g C
-3
Fraction of labile soil organic matter and μm (Adl et al., 2008).
recalcitrant were extracted following the acid Free nematodes were extracted from soil
hydrolysis two-step procedure with H2SO4 as using a modified technique of Funnel Baerman
solvent extraction (Rovira and Vallejo, 2002; (Kilowasid et al., 2013). Nematode individuals
Rovira and Vallejo, 2007; Belay-Tedla et al., were counted under a dissecting microscope
2009). Separation of active roots from the soil and a minimum of 100 individuals were identified
following the procedure is described in Kilowasid up to family level under a light microscope,
et al. (2013). Fresh root was dried at a magnified 400 times. Every family was allocated
0
temperature of 70 C for 48 hours (Munoz and to the feeding type grouping as in Yeates et al.
Beer, 2001). After the dry weight was weighed, (1993). Every nematode was converted to wet
then the root was smoothed using a blender to weight using a conversion factor value by Ferris
analyze the C root tissue. (2010). The wet weight was converted to dry
weight using the ratio dry weight: wet weight
Analysis of Soil Organism Biomass was 0.21 (Yeates, 1979) and 50% carbon
The biomass of each soil organism group content of dry weight (Beare et al., 1992).
was expressed in kg C/ha/15 cm in soil depth. Soil meso-fauna including Acari (mites),
The number of bacteria in the soil samples was Collembola and adult Diptera were extracted
estimated, following the procedure by Trolldenier from soil using a Berleses Tullgren technique at
0
(1996). Cell number of soil bacteria stained with 38- 40 C room temperature for five days. Each
acridine orange on a microscope slide was soil meso-fauna was preserved in 70% alcohol
counted under epifluorescence microscope and counted under a dissecting microscope.
which was magnified 500 times, and as many as Acari, Collembola, and Diptera, which had been
20 fields of view were obtained. The number of cleaned and mounted, were identified up to
bacteria was then converted into biovolume morphospecies level. Individuals of Acari were
3 -1
using a factor of 0.5236 μm cell (Klein and converted to biomass using a conversion factor
Paschke, 2000). The biovolume of bacteria was of carbon content of dry weigth from each group.
-1
changed into bacterial biomass using a Oribatida was 2.39 μg C individual ,
-13 -3 -1
conversion factor (3.20 x 10 g C μm ) Mesostigmata 3.47 μg C individual ,
-1
(Bakken and Olsen 1985). Soil fungal biomass Prostigmata 0.45 μg C individual (Beare et al.,
-1
was estimated with an approach of fluorescein 1992) and Astigmata 0.26 μg C individual
diacetate hydrolysis method, following the (Persson and Lohm, 1977; Berg et al., 1998).
procedures explained by Green et al. (2006). Diptera and Collembola biomass having been
Fluorescein content in the soil was converted to preserved in 70% alcohol were estimated using
fungal biomass with a regression model reported the relationship between dry weight and body
by Gaspar et al. (2001), and 40% carbon length based on the formula from Ganihar
content of fungal biomass (van Veen and Paul, (1997) and 50% carbon content of dry weight
1979). (Bezemer et al. 2010).
The number of active flagellates was Enchytraeid was extracted using a
estimated from 15 µl soil suspension (1:5) in a modified Baerman funnel extractor under room
0
hemocytometer chamber and counted under the temperature of 38 - 40 C for five days, and the
objective lens light microscope at a individuals were counted under a dissecting
magnification of 400 times, while the number of microscope. Dry weigth of enchytraeid was
36

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

estimated using an average of 0.031 mg dry Diagram of Soil Food Web

weight per individual (Persson and Lohm, 1977) The diagram of the soil food web was
and 50% carbon content of dry weight (Bezemer constructed by grouping soil organism taxa
et al., 2010). based on the similarity in their prey, predator,
Soil macrofauna from soil was removed growth rate and survival rate (Moore et al., 1988;
using a hand sorting techniques, and the Moore, 1994; Sugihara et al., 1997).
specimens preserved in alcohol 70% were Construction of the soil food web in this study
identified up to morphospecies. Dry weight of was developed from a generic soil food web for
each taxon of macrofauna was estimated using tropical agricultural proposed by Susilo et al.
allometric equation between dry weight and (2004). The generic soil food web model
body length of specimens that had been combined with the latest knowledge about the
preserved in 70% alcohol (Collins, 1991; feeding habit of functional groups in soil food
Ganihar 1997; Sabo et al. 2002; Gruner 2003; webs from a number of ecosystem types and
Brady and Noske, 2006; Höfer and Ott., 2009) climates was previously described by some
and carbon content assumed 50% of dry weight authors (i.e. Berg et al., 2001; Schröter et al.,
for each taxa (Bezemer et al. 2010). 2003; Holtkamp et al., 2008; Bezemer et al.,
2010). The soil food webs for smallholder cocoa
plantation is described in the following diagram
(for more details see Kilowasid, 2012)

Figure 1. Diagram of soil food web in smallholder cocoa plantation. Box indicates trophic group, an arrow
indicates direct of energy flow. TL shows trophic level
 37

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

Analysis of Characteristics of Soil Food Web trophic group within the respective trophic levels
Structure (Holtkamp et al. 2008).

Trophic level Energy Channel

Labile organic fraction, organic fraction Energy channels of root, bacteria, fungi,
recalcitrant and the root were the primary energy and saprophagous micro-arthropods were
sources of functional groups in soil food web quantified by summing the biomass of all trophic
and set occupied at the basal trophic and groups that obtained energy from each channel.
refered as zero trophic levels (Rooney et al., A trophic group gained more energy from the
2006; Holtkamp et al., 2008). Trophic position of primary sources contributed to more than one
each predator is determined using the following channel of energy. The roots were assumed to
formula (Williams and Martinez, 2004; Rooney contribute over the energy channels through the
et al., 2006): root-eating nematodes and herbivorous macro-
n arthropod. Labile organic fraction contributed fully
TL j  1   p ij x TLi to channel the energy that flows through bacteria,
i 1 saprophagus macro-arthropods, enchytraeidae,
where TLj is the trophic level of the higher order and milipedes. Labile and recalcitrant organic
predator trophic position, TLi is trophic level of fraction contributed equally to the energy
the prey, n is the number of prey consumed by channels in fungi, saprophagous macro-
the predator, pij is the dependent feeding arthropods, termites, earthworms and milipedes.
preference of predator j on prey i. Contributions of another group to each energy
The dependent feeding preference of channel were calculated using the feeding
predator j on prey i (pij) was calculated with preference rate. Before the feeding preference
formula by Hunt et al. (1987): rate was calculated, biomass group at every
w ij B i trophic level was standardized with the way each
p ij  n trophic group of biomass was divided by the total
 w ij Bi
i 1
biomass from all groups which constituted the soil
food web community multiplied by 100. Based on
the standardized biomass, later the contribution
Where, wij is a weighing factor, n is the index for of each group in the energy channel was
summation over all (n) trophic groups on which j calculated with the procedure from Holtkamp et
prayed, Bi is the biomass of prey i. al. (2008).
Generally, feeding preferences of top
predators on certain prey types in the soil food Statistical Analysis
web modeling used dietary data on estimated To detect differences of biomass in trophic
percentage of each functional group (flagellates, level and energy channels from the soil food web
amoebae, nematodes, acari, Collembola, among different ages of cocoa plantations,
enchytraeids and earthworms) following de univariate analysis of variance with least significant
Ruiter et al. (1994) and Didden et al. (1994). differences (LSD) post hoc test was applied. The
Meanwhile, feeding preference data for other assumption of normality was tested using the
soil macro-invertebrates for the soil food web Shapiro-Wilk and the assumption of homogeneity
modeling has not been published (Holtkamp et of variance between groups was tested with
al., 2011). To overcome the limitation of the data Levene's test. To detect the changing trend of
availability related to dietary percentage for every trophic level biomass and energy channel
macro-invertebrates functional groups to biomass along the age of cocoa plantation, linear
determine the feeding preference weight of a regression analysis was employed.
predator on prey particular types, the weighting
factor (wij) used was 1, which is based on the RESULTS AND DISCUSSION
consideration that consumption depends on the
relative abundance of prey predator (Berg et al., Biomass of trophic level
2001). Every trophic level biomass was Fraction of soil organic and roots were
calculated by summing the biomass from each placed at the trophic level 0 in diagram of soil
38

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

food web (Figure 1). In chronosequence shows that the biomass of centipedes, milipedes
approach it was often hypothesized that and diplura on cocoa plantation aged 5 years
biomass at trophic level 0 of soil food web was the lowest, while biomass of centipedes and
tended to increase linearly with age of Diplura at the plantation aged 10 years and
vegetation (Holtkamp et al., 2008). In this study, milipedes at the plantation aged 16 years was
biomass at the trophic level 0 did not show a the highest. Biomass of ants, all groups of
linear increase with age of cocoa plantation (p = micro-arthropods and flagellates between age of
0.073; R2 = 0.168). The content of each soil cocoa plantation were not significantly different.
organic fraction in all cocoa plantations was Biomass of amoeba in cocoa plantation aged 5
relatively the same (Table 1). These results years was the highest and in the aged 16 years
were similar to findings by Smiley and Kroschel it was the lowest. Biomass of omnivorous,
(2009), where the soil organic carbon content bacterivorous and fungivorous nematodes at the
did not change significantly along the age of plantation aged 4 years was the highest.
smallholder cocoa plantation. Biomass at the Biomass of bacterivorous and fungivorous
trophic level 0 was composed the fraction of soil nematode in cocoa plantation aged 5 years and
organic matter plus root biomass. Biomass at omnivorous nematode in cocoa plantation aged
the trophic level 0 in cocoa plantation aged 16 16 years was the lowest.
years was lowest (LSD> 0.05) compared with Biomass at trophic level 3 consisted of
that of 5 years, but the differences were not biomass from predacious Coleoptera, macro-
significant compared to the biomass in other Arachnida, Acari predaceous, Acari
cocoa plantation (Figure 2A). Biomass of root nematofagus (uropodina) and pretadecous
was signicantly different between the ages of nematode (Figure 1) showing a tendency to
cocoa plantations (Table 2). Biomass of root in increase linearly with age of cacao plantation (p
2
the plantation aged 4 to 5 years increased = 0.437; R = 0.034). Biomass at the trophic
significantly (p <0.05), and active root biomass level 3 on cocoa plantation aged 4 years was
after the cocoa plantation aged 5 years tended the lowest, while the biomass at the trophic level
to reduce with age of the cocoa plantation. This 3 on cocoa plantation aged 16 years was the
pattern of reduction in root biomass is similar to highest (Figure 2D). It is presented in Table 2
the findings of Smiley and Kroschel (2008) on that biomass of macro-arachnids and
the pattern of changing biomass of cocoa root in predaceous coleoptera in cacao plantation aged
Napu, Central Sulawesi. Although biomass of 5 years was the lowest, while biomass of
root between cocoa plantations differed predaceous coleoptera and macro-arachnids in
significantly, but its influence could not change plantation aged 16 years was the highest.
the contribution effect of the soil organic fraction Biomass of predaceous acari in cocoa plantation
to biomass at the trophic level 0 with age of the aged 5 years was higher than biomass of
cocoa plantation. predaceous acari in other plantations, while
Biomass at the trophic level 1 consisted biomass of nematophagous acari in all cocoa
biomass of saprophagous macro-arthropods, plantations was similar. Biomass of predaceous
herbivorous macro-arthropods, termites, nematode in cocoa plantation aged 5 years was
earthworms, Enchytraeidae, bacteria, fungi and the highest, and its biomass in cocoa plantation
root-feeding nematodes (Figure 1). Biomass at aged 4 years was the lowest. Biomass of
the trophic level 1 (Figure 2B) did not show a predaceous nematodes in cocoa plantation aged
2
significant increase (p = 0.925; R = 0.001). 4 and 5 years were not significantly different
Biomass with trophic level 2 was composed of from those of cocoa plantation aged 7, 10, and
centipedes, milipedes, Diplura, ants, flagellates, 16 years. These facts showed that the group of
amoeba, prostigmatid mites, oribatid mites, saprophagous, herbivorous or omnivorous
Collembola, omnivorous, bacterivorous, and macro-arthropods influenced biomass of other
fungivorous nematodes (Figure 1) also showed functional groups in soil food web communities,
no significant increase with age of cocoa so that in this study it was showed that the
2
plantation ( p = 0.120 ; R = 0.129 ). Biomass at biomass of trophic levels had no tendency to
the trophic level 2 on plantation aged 5 years decline or increase linearly with age of cocoa
was the lowest, and on the plantation aged 10 plantation. Thus, the results achieved in this
years was the highest (Figure 2C). Table 2 study are linear with what was reported by
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Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

Susilo et al. (2004) that the prediction of an Biomass of Energy Channel

increase or decrease in abundance of functional The biomass of root energy channels did
groups in the soil biota community should be not show a linear increase with age of cocoa
2
seen as a "random walk" because the plantation (R = 0.014 p = 0.624). A similar
accessibility and the recolonisation from some pattern was also shown by the biomass in fungal
taxa of macro-arthropods, such as ants, energy channels (R2 = 0.120 p = 0.134),
2
Coleoptera, Diptera, Centipedes, and bacterial energy channel (R = 0.006 p = 0747),
Dermaptera (Wallwork, 1970) are playing an and saprophagous macro-arthropod energy
2
important role in controlling the abundance channels (R = 0.130 p = 0.119).
within trophic levels (Hubbell, 2001).

Figure 2. Biomass from: (A) trophic level 0 (TL 0); (B) trophic level 1 (TL 1); (C) trophic level 2 (TL 2); (D)
trophic level 3 (TL 3) in soil food web at small-holder cocoa plantation aged 4, 5, 7, 10, and 16
years. Different letters above the bars indicate significant difference between age of small-
holder cocoa plantation at the p <0.05 level.
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Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

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Laode Muhammad Harjoni Kilowasid et al.: Structure Of Soil Food Web In Smallholder Cocoa ......................

40
Table 1. Biomass of functional group in different age of smallholder cocoa plantation (kg C/ha/ 15 cm, soil depth)
Age of smallholder cocoa plantation (years)
Functional Group
4 5 7 10 16
Labile organic fraction 23051.14±859.5a 21686.85±1639.01a 22326.86±1346.47a 24082.16±4473.27a 20976.41±3998.72a
Recalcitrant organic fraction 12559.28±2486.99a 16368.41±4016.37a 15192.11±2383.52a 13392.26±4774.42a 8137.99±696.77a
Root 771.34±59.91a 2115.38±245.45b 1974.31±253.15b 1738.86±214.94b 1571.13±255.44b
Microbe:
Bacteria 8.79±1.32a 9.08±0.56a 8.23±0.99a 8.57±0.88a 7.12±0.66a
Fungi 395.65±23.49a 393.14±9.69a 421.98±20.03a 423.14±9.93a 395.58±19.62a
Protozoa:
Flagellata 0.25±0.06a 0.30±0.09a 0.32±0.05a 0.26±0.06a 0.35±0.05a
Amoebae 0.16±0.02ab 0.23±0.05b 0.21±0.04ab 0.25±0.03b 0.13±0.01a
Microarthropods:
Collembola 2.80±1.88a 6.36±2.28a 4.49±1.55a 4.02±1.32a 2.01±0.94a
Predaceous mites 0.0212±0.0152a 0.0542±0.0144b 0.0123±0.0069a 0.0212±0.0079a 0.0191±0.0080a
Nematophagous mites 0.0088±0.0088a 0.0088±0.0088a 0.0177±0.0125a 0.0133±0.0085a 0.0044±0.0044a
Oribatid mites 0.0091±0.0058a 0.0061±0.0061a 0.0122±0.0050a 0.0122±0.0050a 0.0061±0.0035a
Prostigmatid mites 0.0034±0.0011a 0.0046±0.0019a 0.0017±0.0017a 0.0057±0.0011a 0.0046±0.0016a
Nematodes:
Predators 0.4716±0.0580a 0.9598±0.0695b 0.7227±0.1101ab 0.7524±0.0832ab 0.7517±0.0564ab
Omnivores 0.4075±0.0751b 0.0013±0.0003ab 0.0089±0.0028b 0.0012±0.0001ab 0.0000±0.0000a
Bakterivores 0.2543±0.0231b 0.0775±0.0073a 0.2144±0.0314ab 0.1879±0.0103ab 0.1428±0.0151ab
Fungivores 0.0121±0.0025c 0.0000±0.0000a 0.0043±0.0009bc 0.0006±0.0000abc 0.0002±0.0000ab
Herbivores 0.1978±0.0125ab 0.3444±0.0762b 0.0543±0.0087ab 0.3749±0.0773b 0.0142±0.0027a
Macroarthropods:
Macro-Arachnida 0.012±0.003a 0.00±0.00a 0.046±0.018ab 0.077±0.037ab 0.163±0.083b
Centipedes 1.68±1.68a 4.14±2.41a 25.31±9.40b 46.37±23.89b 3.44±3.05a
Predaceous Coleoptera 1.67±1.14ab 0.13±0.06a 0.92±0.80ab 1.87±1.57ab 14.68±12.99b
Saprophagous 0.28±0.09a 0.17±0.08a 0.64±0.25ab 0.91±0.19b 0.62±0.17ab
Milipedes 0.00±0.00a 0.00±0.00a 7.92±6.80ab 3.67±2.24ab 10.20±5.67b
Diplura 0.335±0.335a 0.00±0.00a 0.821±0.314ab 3.617±1.222b 1.210±1.004ab
Herbivores 9.03±6.00a 1.40±1.38a 0.40±0.37a 7.59±5.39a 5.84±3.00a
Ants 37.39±20.45a 2.96±1.82a 18.56±11.32a 3.65±1.92a 21.08±15.45a
Termites 0.00±0.00a 0.00±0.00a 0.00±0.00a 0.083±0.050a 0.004±0.004a
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Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

..................................
Laode Muhammad Harjoni Kilowasid et al.: Structure Of Soil Food Web In Smallholder Cocoa ......................
Table 1 (Continued)
Age of smallholder cocoa plantation (years)
Functional Group
4 5 7 10 16
Oligochaeta:
Earthworms 0.123±0.036a 0.062±0.033a 0.205±0.054abc 0.375±0.133c 0.095±0.026ab
Enchytraeids 0.614±0.217ab 0.242±0.108a 0.413±0.137ab 1.103±0.538b 0.271±0.142ab
Remarks: Numbers followed by different letter within a column indicate significant difference in functional group biomass (n = 20, mean±standard error)
between the cocoa plantations at p < 0.05 level

41
42

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

Figure 3. Standarised biomass (*) of (A) root energy channel, (B) fungal energy channel, (C) bacterial
energy channel, and (D) saprophagous macro-arthropods energy channel in small-holder cocoa
plantation aged 4, 5, 7, 10, and 16 years (n = 20, mean±standar error). Different letters placed
above the bars indicate significant difference between ages of cocoa plantation at p < 0.05

Biomass in root energy channels in cocoa Biomass in energy channels of fungi,

plantation aged 4 years was lower than that of bacteria or saprophagous macro-arthropods
cocoa plantation aged 5, 7, 10 and 16 years between ages of cocoa plantation was not
(Figure 3A). In this research, it was found that significantly different (Figure 3B, 3C, and 3D). This
the pattern of changing biomass in root energy may be related to soil organic contents among
channels followed the pattern of changes in root cocoa plantations which were relatively similar
biomass. A possible explanation on the pattern (Table 2). Similarly, other indicators from changes
form biomass of root energy channels may be of the structure of soil food webs which consisted
related to the dynamics of root defense on biomass ratio of fungal energy channels to
mechanism against soil fauna feeding on root bacterial energy channels and biomass ratio of
(Bonkowsky et al., 2009). saprophagous macro-arthropods energy channels
to fungal energy channels between cocoa
 43

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

plantation age were not significantly different recalcitrant organic fraction to labile organic
(Figure 4C and 4D). in other words, the structuring fraction, biomass ratio of fungi to bacteria,
in soil food web communities was influenced by biomass ratio of fungal energy channels to
combination of soil organic matter availabilty and bacterial energy channel (FB ratio), or the
biotic factors, such as facilitation, competition and biomass ratio of saprophagous macro-arthropod
predation.. energy channels to fungal energy channels
Variation in energy channels indicated by between cocoa plantations were not significantly
the ratio of the organic fraction, the biomass ratio different (Figure 4A, 4B, 4C, and 4D). The
of fungi to bacteria, and the biomass ratio of proportion of recalcitrant organic fraction was
energy channels was generally used to analyze slightly lower than labile organic fractions in all
changes in soil food web structure (Holtkamp et cocoa plantations (Figure 4A).
al., 2008). The results showed that the ratio of

Figure 4. (A) ratio of recalcitrant organic fraction to labile organic fraction, (B) biomass ratio of fungi to bacteria,
(C) biomass ratio of fungi enegy channel to bacterial energy channel, and (D) biomass ratio of
saprophagous macro-arthropods energy channel to fungal energy channel in small-holder cocoa
plantation aged 4, 5, 7, 10, and 16 years. Values followed by the same letters placed above the bars
indicate no significant difference between ages of cocoa plantation at p > 0.05
44

Laode Muhammad Harjoni Kilowasid et al.: Structure of Soil Food Web in Smallholder Cocoa ......................................

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