107
Parasitic Nematodes associated with Tomatoe
Ubidia and Soria
p-ISSN 2477-9113
e-ISSN 2477-9148
REVISTA ECUATORIANA DE MEDICINA Y CIENCIAS BIOLOGICAS
Volumen 38. No. 2, Noviembre 2017
Parasitic Nematodes Associated with Tree Tomato
(Solanum betaceum Cav.) in the Ecuadorian Highlands
Nematodos parásitos asociados con tomate de árbol
(Solanum betaceum Cav.) en la sierra del Ecuador
Ubidia Vásquez P
1
, Soria C. A.
1*
1
Ponticia Universidad Católica del Ecuador. Facultad de Ciencias Exactas y Naturales. Escuela de Ciencias Bioló-
gicas. Laboratorio de Bioquímica. Av.12 de Octubre 1076 y Roca. Quito, Ecuador.
*casoria@puce.edu.ec; drcasp@hotmail.com
doi.org/10.26807/remcb.v38i2.549
Recibido 10-08-2017; Aceptado 6-09-2017
ABSTRACT.- A nematological survey was conducted in four tree tomato plantations (Solanum betaceum Cav.),
located in the Ecuadorian highlands. The purpose was to study the occurrence of parasitic nematodes associated with
this crop. A total of 64 soil and 34 root samples were processed and analyzed in duplicate, in which nematodes from
at least 12 genera in different population arrangements were found. Differences in soil conductivity measurements
were signicant, whereas pH was not. The most frequent genus was Meloidogyne spp., with a mean average of 363,5
nematodes per 100 g of soil sample, and 290,4 for 10 g of roots among the 64 and 34 soil and root samples collected
at all four locations. Pratylenchus spp. Followed, with a mean average of 146,3 and 97,4 per 100 g of soil and for
10 g of root samples, respectively. The occasional appearance of the nematode genus Hoplolaimus in 33 of the 64
soil samples (52%) is a signicant nding, since it is the rst report of this genus associated with tree tomato crops in
Ecuador. Around half of the total nematode population found in soil as well as in root samples (with a mean average
of 530 and 518, respectively) were from the saprophytic genera.
KEYWORDS: Ecuador, phytonematodes, population, Solanum betaceum, tree tomato.
RESUMEN.- Se realizó un estudio nematológico en cuatro plantaciones de tomate de árbol (Solanum betaceum Cav.),
situadas en los valles altos del Ecuador. El propósito de este estudio fue el de demostrar la incidencia de nemátodos
parásitos de estos cultivos. Un total de 64 muestras de suelo y 34 de raíces fueron procesados y analizados por dupli-
cado en los que se encontraron al menos 12 géneros de nemátodos distribuidos en poblaciones diferentes. Diferencias
en conductividad de los suelos fueron signicativas, mientras que las del pH no lo fueron. El género más frecuente fue
Meloidogyne spp. con un promedio de 363,5 por 100 g de suelo y 290,4 por 10 g de raíces en las 64 muestras de suelo
y 34 de raíces colectadas en cuatro diferentes localidades. Pratylenchus spp. fue la segunda población más frecuente
con un promedio de 146,3 y 97,4 individuos por 100 g de suelo y 10 g de raíces, respectivamente. La presencia del
género Hoplolaimus spp. en 33 de 64 muestras de suelo (52%) constituye un importante hallazgo de este género aso-
ciado con los cultivos de tomate en Ecuador. Alrededor de la mitad de la población total de nemátodos encontrados en
el suelo y raíces de este cultivo fueron del género saprofítico (un promedio de 530 y 518 individuos, respectivamente).
PALABRAS CLAVES: Ecuador, tonemátodos, población, Solanum betaceum, tomate de árbol.
Artículo científico
INTRODUCTION
Tree tomato, also known as “tamarillo”, “tomatillo”
or “tomate de árbol” is a solanaceaus plant, origi-
nally from the Latin American Andean region. It is
also found widely throughout tropical and subtro-
pical areas in New Zealand, Haiti, Mexico, Malay-
sia and Uganda (Moreno et al. 2007). It is a small,
half-woody tree reaching a height of 2 m. It has a
perennial vegetative life cycle, and fruit produc-
tion is continuous throughout the entire year. Pro-
duction begins 1-2 years after planting. Maximum
yield is reached at 4-5 years, but minor production
can occur up to 10 years (Amaya and Julca 2006).
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REMCB 38 (2): 107-118, 2017
Tree tomatoes grow in both warm and cold areas
between 1000-3000 m above sea level. The opti-
mal habitat temperature is 16-19°C; high humidity
is not a factor. Soil requirements include pH values
between 5,6 and 7,7; mostly sandy soil, and the pre-
sence of organic matter (Cadena 2001).
The fruit contains high levels of vitamins A,
B, C and E; it is also a good source of cal-
cium, iron and phosphorus, as well as antioxi-
dants found in carotenes, pectins, polyphe-
nols, proteins and bers (PAVUC 2008).
In Ecuador, tree tomato production is located
mainly on small farms in the Andean highlands,
especially in the provinces of Imbabura, Tungura-
hua, Chimborazo, Azuay and Pichincha (Cadena
2001). The crop constitutes an important econo-
mic activity for indigenous low-income farmers.
Its production has been directed towards satisfying
the needs of local markets; however, since 2005,
part of the yield has been redirected to interna-
tional markets such as the United States, Canada,
Spain and other European countries (CICO 2006).
There are six commercially relevant varieties of tree
tomatoes: Yellow or “Incan Gold” which is prefe-
rred by the industry for its taste, size and durability
in shipment and transportation; Purple or “Purple
Red”, which is the market’s second choice; Black or
“Heights Tomato”; Pointy Tree Tomato; Round Tree
Tomato, and Giant Yellow. All of these varieties are
reported to be attacked by plant soil and root parasi-
tic nematodes to an unequal degree (Cadena 2001).
In crop production it is estimated that nearly
20 % of the harvest worldwide is lost annually
due to nematodes and related diseases. This va-
lue is greatly underestimated, however, since in-
fections are often confused with nutritional or
water deciencies or other plant diseases; 40%
might be a closer approximation (Ríos 2006).
The identication of nematodes in the tree tomato
is essential for the diagnosis of their impact on pro-
duction, so as to evaluate crop losses due to these
parasites and establish adequate pest management
programs (Solano et al. 2014; Khan et al. 2011), in
order to improve the quality and quantity of the har-
vest. There is little information available on nemato-
des associated with tree tomatoes in other similar re-
gions (Ramirez et al. 2015; Prohens and Nuez 2005).
The purpose of this study was to determine
the incidence of root and soil nematode infec-
tion associated with tree tomato farms located
in the Pichincha province of Ecuador, including
pH and soil conductivity measured during the
time of the study. Existing methods for nema-
tode analysis were adapted to our facilities in
order to record and process the data collected.
MATERIALS AND METHODS
This study was conducted in four yellow tree to-
mato plantations in areas close to 2200 m al-
titude, near the towns of Puembo, Yaruquí and
Checa: Daniela Verónica, 1 ha (Location 1:
78º21’15.78’’W; 0º10’30.06’’S); Los Guabos, 1.5
ha (Location 2: 78º19’30.78’’W; 0º9’23.01’’S);
Santa María, 2 ha (Location 3: 78º19’30.78’’W;
0º9’23.01’’S); Santa Rita, 0.7 ha (Location
4: 78º18’52.83’’W; 0º7’42.09’’S) (Figure 1) |
Figura 1.- Location map of the 4 study points close to the towns of Puembo, Yaruquí and Checa in Pichincha, pro-
vince of Ecuador.
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Parasitic Nematodes associated with Tomatoe
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All of these plantations were between 15-27 mon-
ths old. The study was conducted from April to July
of 2008. Sixty-four soil samples were collected, ta-
king one sample weekly from each of the four loca
tions; thirty-four root samples were also collected.
Soil pH and conductivity were measured wee-
kly for 16 weeks at all four locations, by mixing
a 10 g soil sample in 100 ml of distilled Milli Q
water, using a Metler Toledo® SevenEasy pH-me-
ter and conductivity that was calibrated prior to
each measurement. The 10 g sample was taken
out of a pool of mixed 1 kg sample collected every
week from ve random 20 cm deep soil sam-
ples (200 g each) from each of the four locations
.
Each soil sample was obtained using small steel
shovel a distance of 20 cm from each plant’s step
and at a depth of 20 cm. The sampling surface was
previously cleaned of organic and inorganic debris.
Soil samples were taken from the around the secon-
dary and tertiary roots. Approximately 200 g of soil
were collected from each of ve randomly selected
plants. These soil samples were mixed together to
obtain a sample of approximately 1 kg for each ve
plant group selected, which collectively represen-
ted one sample out of the 64 soil samples studied.
Root samples were collected from randomly selec-
ted and subsequently labeled plants, at the same
distance and depth as described above, using a kni-
fe disinfected with alcohol to cut exposed secon-
dary and tertiary roots. Once the root samples were
taken, the soil was quickly replaced to cover the
exposed roots. Approximately 5 g of tertiary-only
roots were collected from each of the ve different
randomly selected plants. These were then mixed
together in order to obtain a 25 g root sample, re-
presenting one out of the 34 samples analyzed:
eight samples each from locations 2 and 4, and
nine each for locations 1 and 3 (farmers allowed
only these numbers of samples to be taken).
All soil and root samples were labeled accordin-
gly, transported to our laboratory in individual,
hermetically sealed plastic bags, stored at room
temperature (± 20°C) in a dark, dry environment,
and then processed and analyzed the day following
collection using a modication of the Cobb (1918)
sieving and decanting technique, which has been
standardized in accordance with our laboratory
facilities. The original methodology has been des-
cribed by Townshead (1962) and Thorne (1961).
Samples were collected on a single basis either from
a given place or from an individual plant sample.
One hundred grams of soil were processed
from each thoroughly mixed 1 kg soil sample.
These 100 g of soil were stirred vigorously into 1
l of tap water for two minutes and were allowed to
settle for 30 seconds. Leaving the sediment for a
second wash treatment, the liquid phase was com-
pletely ltered through a 150 mesh (106 μm) sieve
over a 350 mesh (45 μm) sieve that was inclined
to 45º. While the liquid phase passed through the
sieves, approximately 1 g of small soil particles, in-
cluding the nematodes, remained on the 350 mesh
sieve; this last sieve was turned over and was then
washed with portions of tap water over wet lter
paper (Whatman No.1) so as to retain the remaining
soil particles while allowing the nematodes to pass
through and be collected in a small plastic container.
Filtration lasted for two days and small volumes
of water were added continuously to avoid l-
ter paper desiccation while assuring maximum
nematode retention. In order to maximize the
number of nematodes collectable from each sam-
ple, an extra 1 L of tap water was added to the
rst sediment which was stirred, decanted and
ltered again as previously described; the volu-
me of these last two ltrates, containing the ne-
matodes, was adjusted to 100 ml with tap water.
Each 25 g root sample was washed with running tap
water and gently blotted with a paper towel. Ten
grams of roots were randomly selected from each
sample and cut in smaller pieces (± 1cm length).
The roots were gently macerated and mixed homo-
geneously for 15 seconds in 100 ml of tap water
using a blender at maximum speed. This mix was
decanted and washed through the 150 mesh sieve
over the 350 mesh sieve; both lters were inclined at
45º. Water was allowed to pass entirely through the
sieves while the small pieces of roots, debris and ne-
matodes remained on the sieves. Both sieves were
turned over, then washed with tap water over soaked
lter paper (Whatman No.1) in order to retain the
nal debris, allowing the nematodes to pass throu-
gh and be collected into a small plastic container.
Filtration lasted two days and small volumes of
water were added continuously to avoid lter
paper desiccation while assuring maximum ne-
matode recovery. The volume of this nal ltra-
te containing the nematodes was adjusted to 100
ml with tap water; each of the 64 soil and the 34
root samples was processed and analyzed twice
as two subsamples, and the results were reported
as the mean of the two counts in order to minimi-
ze errors in nematode counting and identication.
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REMCB 38 (2): 107-118, 2017
A 10 ml sample of each ltrate was placed in a sma-
ll Petri dish to be studied under a microscope. Ne-
matode identication and counting were done using
only the live specimens found in each sample. Due
to degradation processes that could alter the results,
dead nematodes were not included in the counting
or identication. The quantity of nematodes found
in each 10 ml sample was multiplied by 10, and
reported as the number of nematodes found in the
100 g soil sample or in the 10 g of processed roots.
Nematodes were identied with an inverted micros-
cope (ZEISS® Telaval 3) at 5x. Identication of ge-
nera was possible with the aid of several taxonomic
keys found in Tiwari et al. (2001), Nickle (1991),
Eisenback et al. (1981), Tarjan (1973) and Golden
(1971). Photos were taken with a Canon Powers-
hot® A540 camera with a 4x zoom positioned over
the microscope optic lens at 5x optics and a 4x zoom.
The SPSS® statistical program was used to or-
ganize and analyze data collected. Original data
were transformed into Log x+1 to avoid statistical
errors. The statistical model used to analyze the-
se data was an ANCOVA for soil samples (in or-
der to compare nematode quantities with pH and
conductivity measures) and a RBD ANOVA for
root samples (since neither pH nor conductivi-
ty measurements were carried out on roots). The
frequency of each genera in each location was
calculated as the number of samples containing a
nematode specie divided by the number of sam-
ples collected, multiplied by 100 (Barker 1985).
RESULTS
Soil samples from location 1 showed an average, acid,
pH of 6,7; alkaline pH 7,4 in location 2; pH 7,2 in lo-
cation 3 and neutral pH 7 in the soils from location 4
(Figure 2)
ANCOVA in DBCA analysis showed that the soil
pH measurements were not signicant with res-
pect to the quantity of total soil nematodes found
at each of the four locations (p=0,675; H
0
= 0,93).
Soil conductivity was found to be signi-
Figure 2.- Weekly soil pH (A) and conductivity (B) measurements of each sample collected in all four studied locations
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REVISTA ECUATORIANA DE MEDICINA Y CIENCIAS BIOLOGICAS
Parasitic Nematodes associated with Tomatoe
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cant as a parameter that could affect the total
number of nematodes found at each location
(p=0,081; H
1
=0,05). The mean average soil con-
ductivity among all samples was 1,14 mSiem/
cm. In location 1, the mean conductivity among
the samples collected was 1,75 mSiem/cm; a low
0,54 mSiem/cm in location 2; 0,88 mSiem/cm
in location 3; and 1,36 mSiem/cm in location 4.
Nematodes were found in the soil and in roots
of tree tomatoes at the four locations. The nema-
todes found represented at least 12 genera in 10
families of the Tylenchida order; the remaining
2 (Aphelencoides and Aphelenchus) belonged to
one of two families in the Aphelenchida order;
others that could not be identied were grouped
as “other genera”. Means and frequencies of these
nematodes are reported (Table 1 and 2) and were
calculated without any Log x+1 transformation.
Species diversity was similar at all four locations and
within soil and roots. The smallest nematode was
Meloidogyne spp. (250 um) found with other larger
genera such as Pratylenchus spp., Aphelenchus spp.
and Criconemella spp. (Figure 3) which measured
400 to 500 μm in length; the largest phytoparasite was
Hoplolaimus spp., which measured more than 1000
μm (Figure 4)
Meloidogyne spp. was the most numerous and fre-
quent parasite found ( = 364) per soil sample in all
four locations. Pratylenchus spp. showed a mean
Table 1. Frecuency and mean density of tomato tree nematodes found in 100 g soil samples: 16 samples taken from each of the
four locations. Results were calculated from the original data without any log x+1 transformation.
Genera Frecuency Mean Frecuency Mean Frecuency Mean Frecuency Mean
Aphelenchoides 75 8 89 16 100 18 100 33
Aphelenchus 88 6 89 16 89 12 75 8
Criconemella 38 4 78 11 44 3 38 6
Helicotylenchus 100 52 100 72 100 52 100 61
Heterodera 75 8 89 15 89 22 88 26
Haplolaimus 0 0 0 0 0 0 0 0
Meloidogyne 100 175 100 212 100 356 100 479
Paratylenchus 100 21 100 22 89 25 100 29
Pratylenchus 100 59 100 93 100 114 100 124
Radopholus 100 28 100 37 100 21 75 16
Rotylenchus 88 19 100 23 100 26 100 24
Tylenchus 75 10 100 23 89 22 100 31
Otros géneros 88 21 100 18 100 24 100 32
Saprófitos 100 167 100 241 100 496 100 1170
Frecuency is the result of dividing the number of the samples with a given nematode for the total number of samples analyzed in a given location,
times 100.
Table 2.- Frecuency and mean density of tomato tree nematodes found in 10 g root samples: 9 samples taken from locations 1 and 3, and 8 samples
from 2 and 4. Results were calculated from the original data without any log x+1 transformation.
1 Daniela Verónica
2 Los Guabos
3 Santa María
4 Santa Rita
occurrence of 146 and 106 for Helicotylenchus
spp. Other parasites such as Aphelenchoides spp.,
Aphelenchus spp., Paratylenchus spp., Radopho-
lus spp., Rotylenchus spp., Heterodera spp. and
Tylenchus spp. were found in small num-
bers, around 20 each in all four locations.
Others, such as Criconemella spp., were de-
tected in even smaller numbers ( =7,6).
The occasional appearance of Hoplolaimus spp.
was observed in 33 of the 64 soil samples analyzed
( = 7,1). About 50% of the total nematodes counted
were saprophytes (700-1000 μm long) from several
unidentied genera. Other less damaging nematodes,
such as Rotylenchoides spp., Dorilaymus spp. and
Radopholoides spp., reported as other genera, were
also found, but their total mean number was
x
= 26,1.
Numbers of nematodes found in soil samples from
the four different locations (Figure 5) were similar
at locations 1 and 2, with larger numbers in location
3, and at even greater quantities in location 4, where
each of the two largest peaks represented maximum
numbers of Meloidogyne spp. and saprophytes.
With the exception of Hoplolaimus spp., all ge-
nera encountered in soil samples were also found
in roots. Meloidogyne spp., Pratylenchus spp.
and Helicotylenchus spp. were also the most fre-
quent nematodes associated with the root system
(
x
= 290,4;
x
= 97,4 and
x
= 56,8 respectively).
x
x
x
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REMCB 38 (2): 107-118, 2017
The absence of Hoplolaimus spp. in all root samples,
together with a decrease in numbers of Radopholus
spp. and Rotylenchus spp., was also evident. Other
less damaging phytoparasitic nematodes, such as
Rotylenchoides spp. and Radopholoides spp., repor-
ted as one group, were also found in smaller numbers
( = 23,7). The number of saprophytes (45,8 % of
the total number of nematodes observed) was greater
than that of any of the phytoparasites encountered.
The number of nematodes found in root sam-
ples was also compared between the four diffe-
rent locations (Figure 6) Roots from plants at
locations 1, 2, and 3, showed similar numbers
of parasites. Location 4 had higher numbers of
Meloidogyne spp., and saprophytes were even higher.
The original data from soil and root samples were
transformed to Log x+1 due to the presence of some
data with zero values. Results showed highly sig-
nicant differences within and among genera and
samples (p=0.00 in both categories). Highly sig-
nicant differences were also found in the number
of nematodes reported for each location (p=0.00).
These differences were a result of the larger num-
ber of saprophytes and Meloidogyne spp reported
at location 4 in both root and soil samples, and
also, to a lesser degree, to the amount of other pa-
rasitic nematodes found in each distinct location.
In accordance with similarities found between the
averages of each genus, it was possible to create
frequent genera that could be separated into ei-
Figure 3 - Some of the nematodes found in soil and roots of tree tomato (Solanum betaceum Cav.): a) Criconemella
spp., b) Meloidogyne spp., c) Aphelenchus spp., d) Helicotylenchus spp
Table 2.- Frecuency and mean density of tomato tree nematodes found in 10 g root samples: 9 samples taken from locations 1 and
3, and 8 samples from 2 and 4. Results were calculated from the original data without any log x+1 transformation.
Genera Frecuency Mean Frecuency Mean Frecuency Mean Frecuency Mean
Aphelenchoides 86 14 81 10 94 17 100 26
Aphelenchus 94 18 81 16 81 22 81 14
Criconemella 75 8 69 8 81 9 50 6
Helicotylenchus 100 107 100 109 100 106 100 102
Heterodera 75 14 86 17 100 22 100 25
Haplolaimus 31 4 69 7 56 8 50 10
Meloidogyne 100 215 100 323 100 416 100 506
Paratylenchus 81 12 94 15 86 14 100 25
Pratylenchus 100 107 100 158 100 133 100 187
Radopholus 86 17 94 23 86 23 94 28
Rotylenchus 75 16 94 20 94 24 100 24
Tylenchus 56 7 86 18 81 15 86 26
Otros géneros 86 16 86 24 100 29 100 34
Saprófitos 100 260 100 298 100 499 100 900
Frecuency is the result of dividing the number of the samples with a given nematode for the total number of samples analyzed in a given location,
times 100.
Table 1. Frecuency and mean density of tomato tree nematodes found in 100 g soil samples: 16 samples taken from each of the four locations.
Results were calculated from the original data without any log x+1 transformation.
1 Daniela Verónica
2 Los Guabos
3 Santa María
4 Santa Rita
x
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Figure 4. A male from the genus Hoplolaimus found in
soil samples from tree tomato (Solanum betaceum Cav.).
ther soil nematodes (Figure 7) or root nematodes
(Figure 8) as the following subgroups: 1.
Helicotylenchus spp. and Pratylenchus spp.; 2.
Meloidogyne spp; 3. Saprophytes; and 4. other ne-
matodes. The variation coefcient for this statistical
soil analysis was 31% and 33 % for the root samples;
percentages accepted for this type of eld work.
Figure 5.- Comparison of the mean number of nematodes found in soil samples (100 g) from tree tomato (Solanum
betaceum Cav.) in 4 dierent locations.
DISCUSSION
Parasitic nematode infections in the roots of tree
tomatoes and in surrounding soil samples at four
different locations were studied and found to host
similar genera. The population density of each
genera in both the soil and the roots was statisti-
cally different. The processed soil sample wei-
ghed 10 times that of a root sample, and the re-
sults clearly indicated the importance of nematode
proximity to roots in accordance to nourishment,
invasion and survival needs. Furthermore, De
Waele et al. (2006) reports that the host suitabili-
ty for a given plant based on nematodes per root
system and nematodes per root unit can differ.
The results also showed a large root and soil po-
pulation of Meloidogyne spp., Helicotylenchus spp.
and Pratylenchus spp. with a clear predominance of
Meloidogyne parasites in soil and root samples at all
four locations; other studies (Ramirez et al. 2015)
also found similar results in similar crops. Our re-
sults indicated that this nematode has adapted to
crops such as tree tomatoes and is capable of existing
in close relationship within root nodula, or freely in
the soil. This latter habitat is an important means of
rapid and continuous dissemination of second-stage
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REMCB 38 (2): 107-118, 2017
thin and long free-living juvenile parasites in crops,
while eggs and nodules are secluded spaces for para-
site development and reproduction in plant tissues,
including dissemination over the time (Soria 2009).
The pathological damage that Meloidogyne spp. can
cause (Baicheva et al. 2002) is in association with
the common root gall. The nodule may interrupt the
ow of nutrients within the plant, and the root da-
mage caused by the digestive enzymes will contri-
bute to the development of plant diseases associa-
ted with invasive bacteria, fungi or viruses (Haseeb
et al. 2005). Therefore, in association with tree
tomato crops, Meloidogyne spp., constitutes ano-
ther suitable model for the study of nematode pest
management and applied phytopathology research.
The low numbers of the other phytonemato-
des (Aphelenchoides spp., Aphelenchus spp.,
Paratylenchus spp., Radopholus spp., Rotylenchus
spp., and Tylenchus spp.) or others with even sma-
ller populations (Criconemella spp., Hoplolaimus
spp. or those grouped as “other genera”) found in
this study may indicate their ability to coexist as
internal and external plant parasites. The number
of nematodes are not necessarily to be taken as
an absolute indication of high or low infestations,
perhaps due to differences in isolation techniques
according to size and motility nematode habits. It
may also indicate the different life cycles for each
genera that may take place in the soil or in root tis-
sues, which should be taken under consideration
when implementing control strategies. These are
good reasons to choose an appropriate standar-
dized isolation technique (McSorley and Parra-
do 1981), and an extended sampling to study at
least two generations of nematodes (Barker 1985).
Hoplolaimus spp. is a very large nematode usually
reported in turf or other kinds of grasses; damage
to the crop may appear as yellowing patches across
the eld, sometimes confused with being caused by
nutritional deciency or drought (Tiwari et al. 2001;
Mateille 1994; Rhoades 1986). Small tertiary roots
are most affected by this parasite, since their growth
and function are notably diminished (Nickle 1991).
The presence of Hoplolaimus spp. represents ne-
matological diversity in the tree tomato. While its
numbers were small, and it was found only in soil
surrounding the roots, its presence suggests the pos-
sibility of established relationships with tree tomato
plantations. The low numbers found in the soil need
to be conrmed. Hoplolaimus spp. is the largest and
probably the most massive of the phytoparasitic ne-
matodes found, and it may very well be that it was
decanted together with soil particles or possibly tra-
pped on the last sieve or on the lter paper prior to
analysis; it thus may be more abundant than we ob-
served. In contrast, Meloidogyne spp. was the most
numerous and frequently found parasite in this study,
probably because the collection technique may fa-
vor small parasites (McSorley and Parrado 1981).
Figure 6.- Comparison of the mean number of nematodes found in root samples (10 g) from tree tomato (Solanum
betaceum Cav.) in 4 dierent locations.
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Parasitic Nematodes associated with Tomatoe
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Figure 7.- Results of the Tukey test with signicant levels of 0,05 on the means of all genera found in the 64 soil sam-
ples collected and analyzed on the 4 locations of tree tomato plantations. Data was grouped as 4 signicantly dierent
subsets.
The occurrence of a large saprophytic nematode
population associated with soil and roots constitu-
tes a for soil quality reference. Usually, a relatively
high number of saprophytes suggest that there is
enough organic matter in the soil for the plant to
grow adequately (Nickle 1991) and for free living
nonpathogenic saprophytes to closely coexist with
terciary roots. Ecological competition with phyto-
parasitic nematodes, not for food, but for space, is
also of great importance for the saprophyte balance
in soil; particularly in external root tissues where
nematodes were found to contribute to the proces-
sing of organic molecules that specially modied
soil niche conductivity. While the genera found
are the same in all four locations, note should also
be made of the heterogeneity of nematodes in rela-
tion to the signicant differences in numbers and
frequencies found among genera and locations, in
spite of the similarities in pH measurements and
the differences in soil conductivity. Particular note
should be made of location 1, where conductivity
was signicantly higher than in other locations, but
parasites were less numerous than those in location
4, where conductivity was around 0,3 mSiem/cm
lower than in location 1. Increased conductivity as
a result of sodium or related salts added as fertili-
zers or released by saprophytic organic debri pro-
cessing lowered the nematode population. This is
perhaps due to unfriendly environment for metabo-
lic exchange, which includes altered parasite cellu-
lar osmotic pressure. These factors may also help
to explain the natural grouping in repetitive fre-
quencies for each genus in each of the four farms.
These small plantations were located close to
one another at approximately the same altitude,
and were exposed to similar weather conditions;
however, frequencies encountered are direct-
ly proportional to differences in organic matter
and conductivity, the presence of certain fungi or
bacteria acting as bio-controllers (Sauddin et al.
2015), and neighboring nematode contamination.
The number of nematodes found in soil is di-
fferent than those reported for roots. This result
might be explained both by differences in the
quantity of sample processed as well as by the as-
sociation of certain nematodes with roots in pre-
ference to the soil. It could likewise indicate the
comparative number of nematodes that actually pe-
netrate the root tissue during part of their life cycle
(Meloidogyne spp.), in relation to the number of ne-
matodes that remain outside, which may feed on the
exterior byproducts of roots while moving to other re-
sources in order to minimize ecological competition.
116
REMCB 38 (2): 107-118, 2017
In view of these results, it is possible that new
and improved soil, crops, and pest manage-
ment techniques are needed in order to increase
yields and crop quality as well as to ensure suc-
cessful and competitive large scale production
of tree tomatoes in Ecuador and in other regions.
ACKOWLEDGEMENTS
The authors wish to acknowledge the Pontical
Catholic University of Ecuador -PUCE, where
this research was conducted and nanced; Julio
Sánchez (PUCE) for his help with data analysis,
Franklin Vásconez from SESA (Servicio Ecuato-
riano de Sanidad Agropecuaria [Ecuadorian Agri-
cultural Health Service]) and Jorge Revelo from
INIAP (Instituto Nacional Autónomo de Investi-
gaciones Agropecuarias [National Autonomous
Institute of Agricultural Research]) for their help
with nematode identication. Thanks to Dr. Darrell
Stokes (Emory University) for reviewing this arti-
cle, to Rafael Narváez, Dr. Óscar Pérez, and Juan
Pablo Almeida (PUCE) for their help in various
aspects of this study, and to Rodrigo Cabrera, Ro-
berto Sánchez, María Eugenia Arcos and Enrique
Gutierrez for allowing the gathering of soil and
root samples from their tree tomato plantations.
We thank the Carlos Andrade Mari Hos-
pital Bacteriology Laboratory for kind-
ly providing the isolates for this study.
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