Advances in Agriculture and Biology (2022) 5(1): 27-34

RESEARCH PAPER

Survey and characterization of nematode populations affecting onion

and spinach crops in Karachi, Pakistan
Naveed Hameed1, Asmat Ullah1*, Zuama Khan2, Sumera Aslam3 and Amir Afzal4
1
National Nematological Research Center, University of Karachi, Karachi, 75270, Pakistan
2
Pir Mehr Ali Shah, Arid Agriculture University, Rawalpindi, Pakistan
3
Honeybee Research Institute (HBRI), National Agricultural Research Centre (NARC), Islamabad, Pakistan
4
Barani Agricultural Research Institute (BARI), Chakwal, Pakistan

*Corresponding author’s email: [email protected]

Received: 15 April 2022

Accepted: 11 July 2022

Key Message: This study conducted a comprehensive rate of multiplication. This research study conducted an
survey of nematode populations affecting onion and extensive survey of nematode populations affecting onion and
spinach crops in Karachi, Pakistan, identifying ten spinach crops in Karachi, Pakistan. Soil samples were
different genera of plant parasitic nematodes, including collected from farmers’ fields and the UBIT field at the
previously unreported species. The findings emphasize the University of Karachi. The survey identified a total of 10
critical need for effective management strategies to different genera of plant parasitic nematodes including
mitigate nematode-induced yield losses and ensure Longidorus elongatus, Hemicriconemoides communis,
sustainable agricultural practices in the region. Rotylenchulus reniformis, Hoplolaimus columbus, Bitylenchus
brevilineatus, Aphelenchus avenae, Pratylenchus coffeae,
Abstract Seinura spp., Filenchus spp., and Helicotylenchus spp., along
with free-living soil nematodes. Notably, some genera, such as
Vegetables are an important source of micronutrients, Longidorus elongatus, Bitylenchus brevilineatus,
which can help malnourished people throughout the world Rotylenchulus reniformis, Hemicriconemoides communis, and
and improve their health. In many countries, spinach and Seinura spp., were reported for the first time in onion and
Onion are popular vegetables that help to overcome spinach crops in Pakistan. The study also provided systematic
micronutrient deficiencies. Current technology and information, morphometric data, and illustrations of these
advances have greatly aided agricultural productivity, genera. The findings highlight the importance of understanding
while most of the producers have overlooked several and managing nematode populations in onion and spinach
critical aspects that might help to reduce yield losses. crops to ensure sustainable agricultural practices in Karachi,
Particularly, root-knot (Meloidogyne spp.) and cyst Pakistan. © 2022 The Author(s)
(Heterodera spp.) nematodes are thought to be among the
most significant plant pests on a variety of crop plants. Keywords: Diseases, Nematodes, Onion, Plant parasitic
They have a wide host range, a brief life cycle and a rapid nematodes, Spinach

Citation: Hameed, N., Ullah, A., Khan, Z., Aslam, S., & Afzal, A. (2022). Survey and characterization of nematode
populations affecting onion and spinach crops in Karachi, Pakistan. Advances in Agriculture and Biology, 5(1), 27-34.

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https://aabinternational.com/ Advances in Agriculture and Biology (2022) 5(1): 27-34

Introduction wilting, yellowing, and stunting as above-ground symptoms.

Yields might be drastically decreased under some
In Pakistan, vegetables are cultivated continuously for the circumstances. Certain worm species do exhibit distinctive
fresh market. The location of planting can be doubled or symptoms or indicators; however, they will be covered in the
tripled due to warm summers and mild winters. section on particular nematodes. Nematodes frequently lower
Meloidogyne spp. is a serious parasite in many plants yields without exhibiting any signs that are visible above
affecting market production both in quality and quantity ground (Nicol et al., 2011).
(Nicol et al., 2011). M. incognita and M. javanica are types One of the major condiments that is used year-round in all
of two most prevalent root knot pathogenic nematode homes is the onion (Allium cepa L.). The young leaves and
species. These nematodes target a variety of crops both mature and immature bulbs can be eaten raw or added to
including fruits and vegetables (Anwar, 1989; Anwar et al., vegetable preparations (Lawande, 2012). Onions are used as a
2009). Root-knot nematodes, either alone or in condiment and in soups and sauces. According to recent
combination with other pathogens, significantly limit studies, eating onions may help avoid heart disease and other
vegetable crop yield in Pakistan (Khan et al., 2023). The conditions. Carbohydrates, calcium, and phosphorus are
indications of nematode feeding include rotting, abundant in onion bulbs. Allyl-propyl disulphide, a volatile oil,
deformities, lesions in the roots, and a decrease in plant is the cause of onion pungency. Over 9,000,000 acres
vitality (Enyiukwu et al., 2021). Crops have a small system (3,642,000 hectares) of onions are thought to be cultivated
of fruit and few root feeders which are damaged by root annually throughout the world. Approximately 170 nations
nematodes (Anwar & Javid, 2010). Plant vigor and yield grow onions for home consumption, and 8% of the world's
loss are caused by damage of root nematodes which production is exported. China is the largest country of the
decrease the crop capacity for take up of present water and world in onion production. China produced onion about
nutrition in soil (Trudgill, 1992). Losses of crops due to 20817295 MT in 2008. Other major producer countries of the
parasite plant nematodes are estimated to be seventy-eight world are India, USA, Egypt and Turkey respectively. In
billion dollars globally per year (Barker et al., 1998). It Pakistan Onion is cultivated on 129600 ha producing over 1.7
was estimated that plant-parasitic nematodes caused 11% million tons of onions (MINFA, 2008-09). A member of the
of the damage to 24 different vegetable crops of US Amaranthaceae family, spinach (Spinacia oleracea L.) is an
(Feldmesser et al., 1971). Vegetable plants are linked to edible flowering plant. It is indigenous to Asia's center and
density, population and frequency of parasite plant southwest regions. It is an annual plant that can reach a height
nematode. The majority of nematode species are thought to of up to 30 cm (occasionally biannual). In temperate climates,
be advantageous. They consume fungus, bacteria, and spinach can withstand the winter months. Microscopic
other aquatic or soil-dwelling creatures for food. While roundworms known as "plant parasitic nematodes" inhabit soil
some are classified as omnivores and may eat a variety of and plant tissues. The stem and bulb nematodes feed on the
foods, others are more selective about the kinds of meals stems, leaves, and bulbs of the plant that it inhabits. They can
they consume. Certain nematode species parasitize both survive for several years without water and can withstand
plants and animals (Maule & Curtis, 2011). desiccation. The juveniles of the second stage of root knot
Three traits are shared by plant-parasitic nematodes. nematodes are motile, while the other stages are stationary;
Initially, all of them are little, with adults measuring they reside within the roots. The soil is home to the stubby root
between 1/60th and 1/4th of an inch in length. Secondly, nematode, which feeds on roots.
they are obligatory plant parasites which mean that in order Growers utilize chemical pesticides, crop rotation, and soil
for them to proliferate and develop; they need to feed on additives extensively to control soil-borne infections, which
live plant tissues. Lastly, these nematodes have needle-like include worms that parasitize plants. Nematicides can be used
sucking mouthparts called stylets, which pierce plant cells to produce rapid and efficient worm management;
and withdraw their contents (Jones, 1961). While certain nevertheless, due to health and environmental concerns raised
plant-parasitic nematodes are primarily found in root or by their use and manufacture, several nematodes have been
leaf tissues, all of them are at least partially soil dwelling taken off the market (Thomason, 1987). The public's and
across their life cycle (Neher, 2010). There is the presence regulators' growing concern over the use of pesticides in our
of at least one plant-parasitic nematode for every plant food supply has sparked a renewed interest in the creation of
species. Approximately 95% of the reported species are ecologically nonthreatening, sustainable, and effective
nematodes, primarily plant-parasitic, predominantly alternatives. The utilization of natural enemies and host plant
feeding on roots (Kumar & Yadav, 2020). They inhabit resistance are two additional nematode management strategies
soil, residing either externally or internally within root that are currently being researched, however they can be very
tissues. The larvae of nematodes can feed on leaves. Plant- particular. It's critical to learn about the prevalence of
parasitic nematodes spread out in search of other plants or nematode species, their host range, damage thresholds, and
perish because to lay eggs and grow into an adult. Specific pathogenic potentials because crop resistance or predators that
secondary symptoms do not arise from feeding by plant- selectively target some nematode species while sparing others
parasitic nematodes. Nematode issues are hence frequently might seriously limit their efficacy. Data for vegetable crops
misdiagnosed. Typically, nematode infections cause cultivated in tunnels are nonexistent, despite recent findings in
Pakistan (Anwar & Akhtar, 1992; Anwar et al., 2009) on the
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association, distribution, and prevalence of plant parasitic the funnel after 48 hours and settled at the bottom. 100 cc of
nematodes on a variety of crops planted in field settings. the nematode-containing water was then poured into a beaker.
Thus, the purpose of this study was to examine the
occurrence, distribution, density, and prevalence of Nematodes isolation
nematode populations linked with spinach and onion crops
in Karachi, Pakistan, and to characterize and record these The aliquot obtained in the previous step was mixed with
data. water. After allowing it to settle, the majority of the
supernatant liquid was poured into a Petri dish. The contents of
Materials and Methods the Petri dish were rinsed with water and examined under a
stereomicroscope. Additional water was added to the beaker,
Collection and storage of samples thoroughly mixed, allowed to settle, and the liquid was
decanted again for further nematode inspection. This process
Random samples were taken from several locations at was repeated to ensure thorough removal of nematodes until
Karachi's onion and spinach farms. A scooping hand none were detected in the decanted liquid.
shovel was used to gather samples from the plant's
rhizosphere at a depth of 10 to 15 cm. Following mixing, Quantitative analysis
500 g of soil from each plant was put in a polythene bag,
knotted, and all the samples were immediately labeled with Under a stereomicroscope, nematodes were counted in an open
information about the location, the date of collection, counting chamber using just 5 ml of extracted solution by a
sample name, soil type, soil moisture and other relevant counter. The nematode counts per unit of soil were determined
data. Samples were collected at three different sites. In the by averaging three readings.
laboratory, samples were stored in a refrigerator at about 5
ºC until processed. Temporary mounts

Extraction of nematodes For qualitative analysis, observations were done on temporary

mounts with the use of stereomicroscope. Temporary mounts
In order to identify and count the nematodes in a sample, were prepared for immediate examination. The suspension was
they were separated from the soil or plant material. There allowed to settle for at least two hours. The surplus supernatant
are numerous ways of separating nematode from soil, and water was drained off, and the remaining concentrated contents
all have advantages and disadvantages. The method were placed to a hollow block for observation under a stereo
employed in this experiment is Cobb’s sieving method and microscope. Three droplets of nematode suspension were put
modified Bearmann’s funnel method. on a glass slide measuring 3 × 1 inch. The slide was placed
over a heated plate to effectively kill the nematodes and
Sieving preserve their proper shape, ensuring not to overheat them.
Cover slips were then placed over the drops on the slide and
For analysis, the roots were carefully taken out of the sealed with Zut. Each slide was carefully labeled for
ground. The leftover dirt was well-combined. The samples identification.
were subjected to the Bearmann funnel procedure (Cobb,
1915; Bearmann, 1917) which involved screening and Qualitative analysis
decantation techniques to isolate and process the
nematodes. After adding roughly 500 g of soil to a plastic On temporary mounts, observations were made up to the
bucket and giving it a good shake to create a uniform general level for the qualitative analysis.
suspension, the mixture was left to settle for about two
minutes. Nematodes which are still afloat in the water Killing, fixing and dehydration
while the heavier soil particles have sank to the bottom.
The suspension was gradually passed through a series of To obtain good specimens for taxonomic studies, nematodes
36, 100, and 350 mesh sieves; to prevent clogging, the were killed by placing the watch glass containing nematodes
sieves were manually tapped on a regular basis. A mild jet on the hot plate for a few seconds just enough to kill the
of water was then used to wash the residues on the sieve, nematodes. Care was taken to avoid overheating. The water
36 for roots examination and 100 for cyst. After that, 350 was drawn out with the help of a fine dropper and nematodes
mesh sieves were used to filter the water suspension that were fixed in T.A.F. fixative left to soak for a minimum of 24
contained nematodes shaped like eels. Then, using a funnel hours. These were then washed with the distilled water 3 times
with a rubber tube and a clam at the bottom, the nematode and then these were transferred to 1.25% glycerin for
suspension was poured over a piece of tissue paper that dehydration. The glycerin solution was used to keep the
was fastened to a perforated plastic sheet. The bottom of nematodes alive until the remaining ingredients vanished and
tissue paper was in contact with the water within the only glycerin remained. Finally, the prepared specimens were
funnel. The nematodes wriggled out into the clear water in kept in an incubator at 35 degrees Celsius for five to six days.

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Monitoring and sealing lucida mounted to a compound microscope. The De Mans

(1884) formula was employed to denote the dimension of the
On the glass slide's middle, five to ten nematodes were put nematode.
in a state of pure dehydration. Around the drop, three or
four tiny lumps of paraffin wax with a 19 mm diameter Photography of eel nematodes
were inserted, and a cover slip was placed on top of the
wax lumps. After that, the slide was slowly heated to melt For light microscopy (LM), the fixed nematodes were
the wax, filling the area between the coverslips and the processed following the methods outlined by Hopper (1970)
slides. To ensure that the specimens were not under any and Golden (1978). Photomicrographs of eel worms, male,
pressure, glass-wool supports the same size as nematodes female, and juvenile were taken using an automated camera
were always employed. Zut-adhesive was finally used to mounted to a compound microscope equipped with an
seal the cover slips and properly labeled as well. interference contrast system.

Roots examination Results

The roots were inspected for endoparasitic nematodes; Survey
roots were carefully cleaned and sliced into 2-3 cm length
sections. The roots were examined under stereomicroscope A survey of onion and spinach field was conducted in Karachi.
and stained with 0.03% cotton blue lacto phenol. Out of 15 samples, 6 samples were taken from the onion fields
of Allah Baksh Farm, Gadap Town, and 9 samples were
Humid chamber gathered from the UBIT field located at Karachi University.
The samples were taken from the infected & healthy plant
To ensure convenience and prevent the loss of nematodes roots. Frequently occurring nematodes such as
during temporary mounting, slides were placed inside a Helicotylenchus, Longidorus, Pratylenchus, Bitylenchus,
humid chamber stored in a refrigerator to prevent Rotylenchulus, Aphelenchus, Hoplolaimus,
desiccation. Humid chamber was made by using Petri dish Hemicriconemoides, Filenchus and Seinura are given in
with its cover, 3-4 folds of tissue papers were placed, and Tables 1 and 2.
the tissue layer were wet with distilled water, then the
temporary mount was placed over the slide, covered with Quantitative analysis
Petri dish lid, and then stored in the fridge. When the
qualitative analysis of each slide was completed, Table 1 consists of a total of 15 samples. Each sample has
nematodes were carefully picked off the slide. three sub samples taken randomly from the main sample.
Different number of nematodes were found in sub samples
Measurements and drawing including free living and plant parasitic nematodes. The details
of each sample is mentioned below:
All measurements were done using an ocular micrometer
and drawings. The images were created with a camera

Table 1 Quantitative analysis of nematode populations in soil samples

Sample Number Calculation Mean

1. 10

2. 21

3. 49

4. 83

5. 19

6. 36

7. 60

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8. 41

9. 38

10. 44

11. 22

12. 35

13. 49

14. 22

15. 28

Nematode population of onion and spinach

After further detail analysis of each sample, plant parasitic in the sample and found various genera of plant parasitic
and free-living nematodes were isolated from one another nematodes. In each sample as mentioned below:

Table 2 Nematode population analysis in onion and spinach samples

No. of Nematode genera that

Sample # free- living No. of PPN parasitize plants Number of genera
nematodes
Longidorous 04
1. 40 10
Pratylenchus 06
Longidorous 01
2. 42 03
Tylenchus 02
Tylenchorhynchus 02
3. 57 05 Pratylenchus 01
Helicotylenchus 02
4. 70 01 Filenchus 01
Pratylenchus 03
5. 28 05 Helicotylenchus 01
Longidorous 01
Filenchus 04
6. 30 08 Pratylenchus 02
Longidorous (100 mesh) 02
Pratylenchus 03
7. 18 05
Hoplolaimus 02
Pratylenchus 04
Longidorous (100 mesh) 02
8. 18 10
Aphilenchus 02
Helicotylenchus 02
Pratylenchus 12
9. 33 15
Longidorous 03
Aphilenchus 05
10. 65 20 Helicotylenchus 12
Filenchus 03
Pratylenchus 3
11. 50 13
Helicotylenchus 10
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Helicotylenchus 23
12. 38 28
Hoplolaimus 05
Helicotylenchus 09
13. 47 13 Pratylenchus 02
Filenchus 02
14. 45 00 No 00
Helicotylenchus 12
15. 20 18
Filenchus 06

Spinach reaction to cyst nematode H. schachtii schachtii (Rf = 1.11 - 4.95), whilst 'Pacific' was moderately
susceptible. Swiss chard 'Balady' and 'Ford Hook' exhibited
Results from 2019 trials were comparable to those from sensitive reactivity to H. schachtii (Rf = 1.12 - 3.93).
2020. Table 3 shows how the examined spinach responded Nematode infection caused considerable declines in shoot and
to infection by H. schachtii. Spinach 'Balady', 'Barkly', root dry weights in sensitive and highly susceptible spinach.
'Orient', and 'Solanicy' were very susceptible to H.

Table 3 Spinach reaction to cyst nematode H. schachtii during the year 2019 and 2020
Year 2019 Year 2020
Plants type Number of the pots Rf(x) Number of pots Rf(x)
Balady 79 5 73 5
spinach
Barkly 19 1.2 18 1.2
spinach
Orient 31 2 29 2
spinach
Salonicy 25 2 24 1.5
spinach
Pacific 13 1 14 1
spinach

Discussion Helicotylenchus spp., along with free-living soil nematodes.

Notably, some genera, such as Longidorus elongatus,
Vegetables are vital sources of micronutrients that can Bitylenchus brevilineatus, Rotylenchulus reniformis,
significantly benefit undernourished populations globally, Hemicriconemoides communis, and Seinura spp., were
enhancing overall health. Spinach, a widely consumed reported for the first time in onion and spinach crops in
vegetable, is particularly rich in various micronutrients and Pakistan.
helps address micronutrient deficiencies (Hedges & Lister, The study provided detailed information, morphometric
2007). However, vegetable yields are often compromised data, and illustrations of these genera, emphasizing the
by pests and diseases (Wilson, 2014). Spinach, in importance of understanding and managing nematode
particular, is highly susceptible to nematode infestations populations in onion and spinach crops to promote sustainable
(Premachandra & Gowen, 2015). Despite advancements in agricultural practices in Karachi. Crop rotation is commonly
agricultural technology improving productivity, many practiced, where onion and spinach are rotated with non-host
producers have neglected essential measures to mitigate crops, such as legumes or cereals to disturb the nematode's life
yield losses. Root-knot (Meloidogyne spp.) and cyst cycle (Bahadur, 2021). Additionally, the use of resistant
(Heterodera spp.) nematodes are among the most varieties that show tolerance or resistance to nematodes is an
significant plant pests affecting a wide range of crops effective approach (Starr & Mercer, 2009). Soil polarization, a
(Mandal et al., 2021). These nematodes can spread through technique that involves covering the soil with transparent
contaminated planting materials and seeds, persist in soil plastic to increase soil temperature and kill nematodes, has
for extended periods, and exhibit a broad host range, short shown promise in managing nematode populations. However,
life cycle, and rapid reproduction rate. Research study the success of soil polarization depends on factors such as
conducted an extensive survey of nematode populations duration, timing, and soil moisture (Riga et al., 2020).
affecting onion and spinach crops. The survey identified 10 Chemical nematicides have been used in the past, their
different genera of plant parasitic nematodes, including usage is being more limited owing to environmental concerns
Longidorus elongatus, Hemicriconemoides communis, and regulations (Chen et al., 2020). Integrated pest
Rotylenchulus reniformis, Hoplolaimus columbus, management (IPM) practices, including cultural practices, such
Bitylenchus brevilineatus, Aphelenchus avenae, as field sanitation, using clean planting material, and
Pratylenchus coffeae, Seinura spp., Filenchus spp., and maintaining optimal soil fertility and moisture levels, are
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gaining popularity as sustainable alternatives to chemical schachtii J2/kg of soil (Olthof et al., 1974). The examined
control (Duncan & Noling, 1998). The findings of this spinach was either moderately sensitive or moderately resistant
study show that plant parasitic nematodes are widely to this nematode, except for spinach 'Balady'. Infection with H.
dispersed on vegetable crops grown beneath tunnels in trifolii considerably lowered the shoot and root dry weights of
Punjab. This information on nematode incidence on sensitive spinach. The current findings suggest that H. trifolii
vegetable crops will assist producers in planning and infection has harmful effects on the tested spinach. Infection
implementing nematode management measures to reduce with H. schachtii clearly caused higher damage to the dry
nematode populations below threshold levels. This study weight of infected spinach shoots and roots. Furthermore, it
also found that the prevalence of several economically was noticed that on the examined cultivars with the name
significant plant-parasitic nematodes relates to Punjab 'Balady' of spinach, H. schachtii showed high reproduction
vegetable plants, particularly those in tunnels where rates (Rf = 4-8) as opposed to H. trifolii (Rf = 2-2.2). The
replanting is typically done on a quick cycle. This study current study also demonstrated that both H. schachtii and H.
further reveals that the scale of the nematode problem in trifolii have high damage potential and reproductive capacities
tunnel planted crops deserves careful consideration to on susceptible and highly susceptible spinach. The study of
handle through the adoption of appropriate worm control determining the host reaction of certain spinach cultivars to H.
measures. schactii and H. trifolii concluded that resistance to these
The harm produced by root-knot nematodes, nematodes is significant and can be useful to incorporate in
Meloidogyne species, to diverse crops is determined by breeding programs when planning cyst nematode control
species or physiological race, as well as the size of measures. More study is needed to generate resistant or
nematode population densities in soil at planting time tolerant varieties of these food crops.
(Anwar & Mckenry, 2010). To ensure improved crop
performance, plant growers primarily want information on Conclusion
the pre-planting (initial) nematode population densities in
soil prior to establishing their crops. Furthermore, crop The occurrence and distribution of nematodes in onion and
response to changing initial infective juvenile (IJ) densities spinach fields at Karachi pose a significant concern for crop
of Meloidogyne nematodes is critical for implementing production. Nematodes are microscopic worms that can cause
control actions ahead of time to reduce yield losses. The detrimental effects on plant health and yield. The common
results of this study revealed that the variance in growth nematode species at Karachi affecting onion and spinach crops
and root infection of spinach plants in response to a range are root-knot nematodes (Meloidogyne species), lesion
of initial population densities of M. incognita. The nematodes (Pratylenchus species), and dagger nematodes
response of growth to various nematode inocula was (Xiphinema species). The nematodes can infest the root
assessed using four parameters: shoot and root length, systems of onion and spinach plants, leading to inhibited
shoot and root weight. Meloidogyne nematode root growth, staining leaves, wilted plant leaves, and reduced plant
infestations are frequently examined using the gall index, vigor. The warm and humid climate of Karachi provides
which is a measure of the number of galls per root system. favorable conditions for nematode reproduction and spread,
However, such a measure does not offer an accurate making nematode infestation a recurrent problem for farmers.
assessment, owing to the fact that gall size fluctuates with Despite these management efforts, nematodes continue to be a
the density of nematodes in the root tissue of the plant persistent challenge in onion and spinach fields in Karachi.
species that they infected (Eisenback & Triantaphyllou, Continued research, extension services, and farmer education
1991). Previous studies found that the galls formed by M. are crucial for developing effective and sustainable nematode
incognita on spinach roots varied in size (Di Vito et al., management strategies. Collaborative efforts between
2004). researchers, agricultural experts, and farmers are necessary to
This study found that the majority of the address the occurrence and distribution of nematodes in onion
chenopodiaceous plant cultivars evaluated were both and spinach fields, ensuring the long-term productivity and
sensitive and suitable hosts for H. schachtii. The findings sustainability of these crops in Karachi.
complement previous research suggesting that H. schachtii
may infect and proliferate on certain cabbage, cauliflower,
and turnip cultivars (Ibrahim et al., 2013). Heterodera References
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