This study examined the population dynamics, disease incidence, and effects on tomato yield of the false root-knot nematode (Nacobbus aberrans) under three control regimes in Mexico. At least three nematode generations occurred each crop season. Integrated control, which included fertilization, nematicide, and chicken manure, resulted in less crop damage and higher yields than technical control or the untreated check. Integrated control increased plant growth and yield by 31-53% compared to the other treatments. Yield loss was lowest under integrated control at 12%, compared to 29% for technical control and 83% for the untreated check. Integrated control improved commercial tomato production by 20-81% over the other treatments.
2. J. Cristóbal-Alejo et al.
further dissemination. Not knowing how to treat the dis-
ease, farmers often make improper use of nematicides or
other pesticides. Previous attempts have been made lo-
cally to control this disease on tomato, chilli pepper (Cap-
sicum annuum L.), and beans (Phaseolus vulgaris L.),
using nematicides, genetic resistance, manures, solarisa-
tion, and organic amendments (Zamudio, 1987; Silva,
1989; Gómez, 1991; Cid del Prado et al., 1997; Cristóbal-
Alejo et al., 2001a; Yáñez-Juárez et al., 2001; Franco-
Navarro et al., 2002). However, no specific guidelines
are available and the problem of controlling the nema-
tode has not been resolved. This is due partly to a lack
of basic local information about the biology of the nema-
tode, such as its population dynamics, ecology and epi-
demiology. Therefore, a study was made to investigate
the population densities and population fluctuations of N.
aberrans, the incidence of the disease that it causes, and
its effects on tomato, Lycopersicon esculentum Mill., cv.
Rio Grande, vigour and yield in field conditions when ap-
plying three different control schemes: integrated control
(IC, including fertilisation, nematicide and chicken ma-
nure), technical control (TC, based on local practices),
and a check treatment (AC, with no application of fer-
tiliser, nematicides or chicken manure). The study was
intended to identify the best control scheme, and to im-
prove the measures taken locally against the nematode,
as well as improving our understanding of the dynam-
ics of the relationship between the nematode and the
crop.
Materials and methods
ESTABLISHMENT OF THE EXPERIMENT
The experimental area (Tecamachalco, Mexico) is lo-
cated at latitude 18◦
53 32 north and longitude 97◦
44 22
west, at an elevation of 2012 m above sea level. Local
conditions include minimum and maximum average tem-
peratures of 3.5 and 29.5◦
C, and an average annual pre-
cipitation of 606 mm. The experiment was made on 1
ha of land, naturally infested with N. aberrans, during
the spring-summer season of 1999. The soil consisted of
48.8% sand, 22.0% silt and 29.24% clay, pH 7.5 and or-
ganic matter content 1.21%. The land was prepared for
planting the tomato crop by harrowing twice at right an-
gles, followed by ploughing, to even out distribution of the
nematode in the area occupied by the experiment. In or-
der to assess the spatial distribution of the nematode, soil
samples were taken to a depth of 20 cm in a systematic
zigzag pattern of ten cores (200-300 g each) from each
of a total of 12 plots of 6 × 12 m, thus providing a bulk
sample of ca 3 kg of soil per plot (McSorley, 1987). The
initial population density of N. aberrans in each plot was
estimated in a bio-assay. For this, two 1-month-old tomato
seedlings (cv. Rio Grande) were transplanted into 20 cm
diam. plastic pots filled with 2.5 kg of soil. After 45 days,
the plants were washed free of soil and the number of galls
on each counted. The number of galls ranged from 23 to
33 per plant, with no significant differences between ex-
perimental units (Tukey, P = 0.05). Thus, the distribution
of the inoculum in the soil was considered to be accept-
ably uniform. A second set of samples, taken in the same
way as the first but to a depth of 30 cm, allowed a soil
physico-chemical analysis to be made and the optimum
nutrient application required for the crop to reach a poten-
tial production of 30 tonnes ha−1
to be calculated (Etchev-
ers et al., 1994). From this analysis, the fertilisation for-
mula 210-88-00 (kg ha−1
N, P, K) was determined. The
nitrogen was added in three doses: at transplanting, and
at 45 and 75 days after transplanting (dat). Phosphorus
was added only at transplanting. The three management
schemes were established in a randomised block design
with four replications. Plots, consisting of six ridges (each
1 m wide by 12 m long), were planted with 1-month-old
tomato seedlings of cv. Rio Grande, of the Saladette type.
The IC treatment consisted of application of the calcu-
lated dose of fertiliser as described before; ethoprop gel
(68% Mocap®
) was applied at 7 kg active substance (a.s.)
ha−1
in a band 10 cm from the plants, after a light irriga-
tion, at transplanting and 20 dat; and 10 ton ha−1
of ho-
mogenised, matured (i.e., allowed to stand for 12 months
before use) chicken manure was applied in a band at the
base of the furrow 30 days before transplanting. The lat-
ter supplemented chemical fertilisation and improved soil
structure and may bring about a nematode suppressive ef-
fect (Mankau, 1962, 1963; Handelsman & Stabb, 1996).
The TC scheme consisted of the best local practices and
included use of fertiliser (150, 100 and 100 kg ha−1
of N,
P, K, respectively) and 1 l ha−1
of carbofuran 27.5% (Fu-
radan 300 T®
) applied to plants at 15, 30 and 60 dat. For
the check treatment (AC), no nematicides and no chem-
ical or organic fertilisers were used as crops are some-
times grown under these conditions in this area, and such
a treatment would provide a clear demonstration of the
benefits of nematode management strategies under such
conditions. Cultural practices and control of other pests
and pathogens were carried out according to conventional
local methods for all three management strategies.
728 Nematology
3. Epidemiology and control of Nacobbus aberrans on tomato
CROP VIGOUR AND PRODUCTION AND NEMATODE
COUNTS
Every 10 days for 15 weeks, four plants were taken
from the outer rows of each plot. A single randomly
selected plant from the four that were taken was used
to determine the population density of nematodes in
the roots. After roots had been washed, cut into 1 cm
sections and thoroughly mixed, a 1 g subsample per
plant was blended and the third- (J3) and fourth-stage
juveniles (J4) and the obese females within it were
counted. Determination and counting of the stages of
the nematode were made at a magnificaction of 40×
using a stereomicroscope. The numbers of galls per plant
were counted and the data used as an estimate of disease
incidence through the crop season (McSorley, 1987). At
the same time as taking plant samples, soil samples
consisting of ten cores were taken midway between plants
from the outer rows to a depth of 20-30 cm (totalling
500 g of soil/replicate). The procedures described by
Ayoub (1980) were employed to extract the nematodes
from soil and roots. The sieving flotation-centrifugation
technique was used to extract second-stage juveniles (J2),
J3 and J4 from 200 ml of soil per sample (using sieves of
meshes 212, 106, 53 and 30 µm). Soil temperature was
measured at a depth of 20 cm during the development of
the crop using Tiny Talk Temperature Loggers®
(Gemini,
Chichester, UK) (Manzanilla-López, 1997).
Fifteen plants, selected at random from the two cen-
tral rows of each plot at harvest time, were used to esti-
mate crop vigour and yield by measuring the following
variables: plant height, foliage dry weight, stem diame-
ter, total production, and commercial production. The data
were subjected to analyses of variance and comparison of
means using Tukey’s HSD test (P = 0.05; Steel & Torrie,
1986).
EPIDEMIC CHARACTERISATION AND STATISTICAL
ANALYSIS
The numbers of galls per plant and of obese females per
g of root that were estimated every 10 days were used to
model the disease progress curve and population density
over time. The area under the disease progress curve
(AUDPC) was calculated using the trapezoidal integration
method (Campbell & Madden, 1990), and the rate of
apparent infection was estimated as the b−1
parameter
of the Weibull model, in which Y(disease incidence) =
1 − e{−(t/b)c
}, where e is the base of natural logarithms,
t is the time measured in days, b is the reciprocal of the
rate of disease increase, and c is an index determined
by the shape of the curve (Pennypeker et al., 1980;
Thal et al., 1984). The AUDPC and b−1
parameter were
used as estimators of epidemic intensity based on the
number of galls per plant. In both cases, the estimators
were obtained using SAS procedures (Anon., 1988). For
the b−1
parameter, a non-linear procedure (NLIN) and
Dudd algorithms were used. The AUDPC and b−1
were
also calculated based on the population curves of obese
females (density per g of root). The numbers of galls per
plant evaluated at the last commercial harvest were used to
estimate the final disease incidence (Yf ). The parameters
AUDPC, b−1
and Yf were subjected to analysis of
variance followed by a multiple comparison of means
using Tukey’s HSD test (P = 0.05).
PRODUCTION LOSS MODELS
Models were built using a multiple regression of the
form: Y = b0 + b1x1 + b2x2 + b3x3 + bnxn, where
Y is the commercial yield (i.e., fruit of marketable
quality), b0 is the intercept parameter or ‘theoretical
production’ sensu Zadoks and Schein (1979), and b1
to bn are parameters that estimate the effect of gall
incidence on fruit production measured at different stages
of crop phenology. Gall incidence, x1−n, was measured
on different dates, beginning 10 days after transplanting
and continuing up to the last harvest. By reference to the
degree of galling of the plants in the AC treatment, the
relative percentage incidence of galling in each treatment
on each date was calculated and also used to estimate
model parameters.
A multiple point model (Madden, 1983; Teng, 1984;
Campbell & Madden, 1990) was constructed using gall
incidence during crop growth to estimate epidemic inten-
sity at specific stages of crop phenology (Duncan & Fer-
ris, 1983; Noling, 1987). A matrix of 12 observations, the
result of averaging the disease incidence and yield of 15
plants per plot, was used to build the model, which con-
sisted of the commercial (i.e., marketable) yield as the
dependent variable (Y) and ten incidence measurements
over time as independent variables (x1−10) per treatment
and replicate. Percentage data were transformed for nor-
mality by taking the arc-sin of the square root (Steel &
Torrie, 1986). The Stepwise method of the GLM (gener-
alised linear model) procedure of SAS (1988) was used
to adjust the models, selecting those that satisfied a rel-
atively high R2
, and also based on the general signifi-
cance of the model and where the number of parame-
Vol. 8(5), 2006 729
4. J. Cristóbal-Alejo et al.
Fig. 1. Population densities of juveniles of Nacobbus aberrans on tomato (Lycopersicon esculentum cv. Rio Grande) under three control
schemes. A: Second-stage juveniles (J2) per 200 ml of soil; B: Third- and fourth-stage juveniles (J3 and J4) per 200 ml of soil. IC =
Integrated Control, TC = Technical Control, AC = Check.
ters (p) gave a Cp-Mallow ≈ p, which gives the model
good stability when used predictively (Freund & Littell,
1991).
Results
POPULATION DENSITY
The population density of the nematodes in the soil
and roots fluctuated during the cultivation cycle in all of
the treatments (Figs 1, 2). Three overlapping generations
of N. aberrans can be identified through the cultivation
cycle. These correspond approximately to the periods
0-60, 60-100, and 100-130 dat, periods that show different
peaks of juveniles in soil and roots (Figs 1A, B; 2A) and
obese females in roots (Fig. 2B). Although some J3 and
J4 were detected in soil as early as the first day after
transplanting the crop, the J2 numbers peaked at 20, 75, 95
and 115 dat (Fig. 1A), while the J3 and J4 numbers peaked
at 20, 80 and 100 dat (Fig. 1B). Blended root samples
showed that the J3 and J4 were abundant (>100 g−1
root) in the AC at 20 dat (Fig. 2A). Population peaks of
obese females (Fig. 2B) occurred at 30, 70-80 and 110
dat. All of the treatments showed a decrease in numbers
of nematodes in soil and roots at the end of crop growth
(Figs 1, 2).
CHARACTERISATION OF EPIDEMICS
The general trend was of peaks in the numbers of obese
females and galls starting at 20 dat (Figs 2B; 3). The final
phases of the first and second generations of the nematode
population produced increments at 70 and 90 dat. These
peaks, particularly for the numbers of galls, were lower in
the IC (Fig. 3).
The b−1
parameter of the Weibull disease progress
model explained at least 94% of the experimental varia-
tion during 0-50 dat (Table 1). The fit for the complete
disease cycle (110 dat) was poor (r2
0.62) because
730 Nematology
5. Epidemiology and control of Nacobbus aberrans on tomato
Fig. 2. Nacobbus aberrans population densities on tomato roots (Lycopersicon esculentum cv. Rio Grande) under three control schemes.
A: Third- (J3) and fourth- (J4) stage juveniles per g of root; B: Obese females per g of root. IC = Integrated Control, TC = Technical
Control, AC = Check.
of the peaks of damage mentioned above (Table 1). In
addition, the AUDPC and Yf were calculated, so allow-
ing us to define the intensity of the epidemics for the
whole cultivation cycle. The IC treatment showed a less
intense epidemic than the other treatments according to
all of the models (P = 0.05), whilst the AC treatment
had the highest epidemic intensity (Table 2). The AUDPC
for the numbers of obese females/g of root also showed
that IC allowed nematode development but that this treat-
ment achieved the greatest degree of control (P = 0.05)
(Table 2).
EFFECTS OF TREATMENTS ON VIGOUR AND CROP
PRODUCTION
The beneficial effects of IC resulted in greater plant
vigour throughout crop development as estimated from
plant height, foliage dry weight, and stem diameter (P =
0.01) (Fig. 4). In reducing epidemic intensity, the IC
treatment increased plant height by 41 and 49.6%, foliage
dry weight by 36.9 and 53.1%, and stem diameter by
31.1 and 41% with respect to the TC and AC treatments,
respectively. TC exceeded AC in plant height and foliage
dry weight, but not in stem diameter (P = 0.05) (Fig. 4).
Similar total yields were obtained in treatments IC and
TC, which exceeded AC by 78.7 and 74.7%, respectively
(P = 0.05) (Fig. 5). However, marketable production
in IC exceeded that in TC and AC by 33.9 and 82.0%,
respectively, and TC exceeded AC by 72.8%.
PRODUCTION LOSS MODELS
The best multiple point model for calculating commer-
cial production loss caused by N. aberrans on the tomato
cv. Rio Grande, was Y = 15.505 − 0.045 × 4 − 0.045 ×
5 − 0.024 × 6, which had an R2
of 0.83 (P < 0.05) and a
Vol. 8(5), 2006 731
6. J. Cristóbal-Alejo et al.
Fig. 3. Partial temporal progress curves of disease on tomato, Lycopersicon esculentum cv. Rio Grande (up to 50 days after
transplanting), caused by Nacobbus aberrans (values are means of four replicates per treatment). IC = Integrated Control, TC =
Technical Control, AC = Check.
Table 1. Nacobbus aberrans epidemics on tomato (Lycopersicon esculentum cv. Rio Grande) under three different control schemes.
Coefficient of determination (r2), mean square of error (MSE) and apparent infection rate (b−1) values for partial epidemics (50 days
after transplanting) and complete epidemics (110 days after transplanting) as estimated by the Weibull model.
Treatment Replicate Weibull model
50 days after transplanting 110 days after transplanting
r2 MSE b−1 r2 MSE b−1
IC 1 0.97 0.004 0.025 0.40 0.098 0.052
2 0.97 0.010 0.043 0.54 0.070 0.045
3 0.94 0.018 0.050 0.31 0.114 0.050
4 0.96 0.011 0.039 0.42 0.094 0.049
TC 1 0.99 0.000 0.096 0.45 0.082 0.096
2 0.95 0.014 0.077 0.30 0.101 0.061
3 0.95 0.012 0.079 0.49 0.068 0.068
4 0.96 0.009 0.084 0.41 0.083 0.075
AC 1 0.97 0.008 0.080 0.62 0.049 0.078
2 0.97 0.010 0.084 0.46 0.086 0.049
3 0.96 0.009 0.083 0.31 0.090 0.060
4 o.97 0.009 0.082 0.46 0.075 0.062
IC = Integrated Control; TC = Technical Control; AC = Check; r2 = coefficient of determination; MSE = mean square of error
(variance) of the estimated apparent infection rate; b−1 = progress of apparent infection rate obtained from the reciprocal of the b
parameter of the Weibull model.
732 Nematology
7. Epidemiology and control of Nacobbus aberrans on tomato
Table 2. Effect of control schemes on three parameters of the temporal progress of disease on tomato (Lycopersicon esculentum cv. Rio
Grande) caused by Nacobbus aberrans in Tecamachalco (Mexico).
Disease parameter Number of galls per plant Females per g of root
IC TC AC IC TC AC
Yf (%) 64.0 b 71.0 a 71.0 a – – –
b−1 0.039 b 0.085 a 0.083 a – – –
AUDPC 1525 b 2830 a 3263 a 1282 c 2733 b 3220 a
Yf = Final incidence (110 days after transplanting); b−1 = rate of apparent infection (reciprocal of the b parameter of the Weibull
model) 50 days after transplanting; AUDPC = area below the disease progress curve 110 days after transplanting; IC = Integrated
Control; TC = Technical Control; AC = Check.
Note: numbers with the same letters in the same row are not significantly different (Tukey, P = 0.05).
Fig. 4. Tomato (Lycopersicon esculentum cv. Rio Grande) vigour estimates under three control schemes for Nacobbus aberrans. IC =
Integrated Control, TC = Technical Control, AC = Check. Bars with the same letter are not significantly different (Tukey, P = 0.05).
Cp of Mallow of 6.38. In this model, Y corresponds to the
estimated production and ×4, ×5, and ×6 represent the
estimates of damage (i.e., degree of galling) caused by the
nematode at 40, 50, and 60 dat, coinciding with the pheno-
logical periods of flowering, fruit initiation, and fruit set,
respectively (Fig. 3). From this model, the theoretical pro-
duction (sensu Zadoks & Schein, 1979) was estimated, for
a damage level equal to zero, at 1.03 kg plant−1
. From this
estimate and with a sowing density of 20 000 plants ha−1
,
a theoretically achievable yield of 20 673 kg ha−1
was cal-
culated.
The experimental treatments produced average total
yields of 0.991 kg plant−1
(18 253 kg ha−1
), 0.729 kg
plant−1
(14 593 kg ha−1
) and 0.174 kg plant−1
(3497 kg
ha−1
) in IC, TC and AC, respectively. Thus, the estimated
production losses on tomato caused by N. aberrans, cal-
culated from the theoretical maximum possible produc-
tion and the average production achieved with the dif-
ferent treatments, were 0.121 kg plant−1
(2420 kg ha−1
)
with IC, 0.304 kg plant−1
(6080 kg ha−1
) with TC and
0.858 kg plant−1
(17 176 kg ha−1
) with AC, which corre-
spond to 11.7, 29.4 and 83.1%, respectively.
Discussion
There are few studies of disease progress and yield loss
caused by N. aberrans (Manzanilla-López et al., 2002).
Otazú et al. (1985) determined the progress curve of N.
Vol. 8(5), 2006 733
8. J. Cristóbal-Alejo et al.
Fig. 5. Effects of three different systems of management of Nacobbus aberrans on the production of tomato cv. Rio Grande. IC =
Integrated Control, TC = Technical Control, AC = Check. Bars with the same letters are not statistically different (Tukey, α = 0.05).
aberrans infection on potato during the growing season.
However, the present work is the first report of the use
of epidemiological models and management schemes to
estimate production losses due to N. aberrans on tomato
crops under field conditions. Others have made estimates
based on different treatments under glasshouse conditions
(Costilla & Gómez, 1981) or on the traditional criteria
of chemical control based mainly on different dosages
of nematicides and intensity of control (Zamudio, 1987;
Franco et al., 1993a, b). The critical period for controlling
the nematode is during its first generation (0-60 dat),
and the damage in our experiment was estimated best by
measuring the damage caused by N. aberrans between 40
and 50 dat, i.e., when the crop is at the stage of flowering
and fruit initiation.
The decrease in numbers of nematodes in soil and
roots at the end of crop growth found in all treatments
is a behaviour already reported by Gómez (1991) and
Cid del Prado et al. (1996a). This phenomenon seemed
to be due to the decline of the crop, the consequent
disintegration of the roots, and the invasion of secondary
disease organisms, such that less nutritious tissue was
available for the nematodes. The first peak of obese
females corresponded to the inoculum of J3 and J4 and
immature females already present in the field before
the crop was transplanted and responsible for the galls
that developed on the plants in the bio-assay. Figure
1B clearly shows the presence of J3 and J4 in the soil
at transplanting, a feature reported previously for this
pathosystem (Manzanilla-López, 1997).
More generations may occur immediately if alternative
crop hosts or weeds follow a tomato crop (Cid del Prado
et al., 1996b, 1997). Also, it has been observed that
the nematode is able to survive without any host for
at least one year under field conditions as J3 and J4
(Cristóbal-Alejo et al., 2001b). These two stages can
tolerate gradual dehydration over 15-30 days (Manzanilla-
López & Pérez-Vera, 1999) and host absence for up to
a year (Manzanilla-López, unpubl.) better than other life
stages. This may explain why, at the time of transplanting,
only J3 and J4 (4-6 nematodes/200 ml) were found in the
soil (Fig. 1B), despite efforts to recover J2 through sieving
techniques. Thus, from the present work, it seems that J3
and J4 represent the main inoculum for the progress of
epidemics, and this is the first report that demonstrates the
importance of these juvenile stages under field conditions.
These stages must, therefore, be the principal target for the
purposes of achieving an effective control of crop damage
and management of the nematode.
The chemical control in IC at the begining of the crop
season was presumably the cause of the lowered peak in
numbers of J2 (Fig. 1A), thereby reducing the impact of
the initial inoculum of the nematode and helping to reduce
the numbers of the first generation of obese females (Figs
2B; 3).
734 Nematology
9. Epidemiology and control of Nacobbus aberrans on tomato
The overall beneficial effects of IC must have been due
to the two main components (i.e., nematicides and fertilis-
ers, both chemical and organic), which influence the ef-
fective initial inoculum (estimated through Y0) by reduc-
ing nematode densities and also improve host nutrition.
Later, IC also reduced the values of the epidemic intensity
parameters (AUDPC, b−1
, and Yf ). The positive effects
of addition of chicken manure might be at least partly
due to their restrictive effect on nematode development
(Rodríguez-Kábana, 1986; Zavaleta-Mejía, 1986). How-
ever, as with other types of amendment, it is important to
study the effects of the amendment on various physico-
chemical processes in the soil and on soil pH (Etchevers
et al., 1989). Its effects on nematode antagonistic organ-
isms (Mankau, 1962, 1963; Wallace, 1983) and the opti-
mum period of application could also be important. The
application of nematicide in this experiment, especially
at the time of transplanting, did reduce the initial inocu-
lum, but it would be informative to study the frequency of
application, dose, and alternative chemical products, and
to make cost-benefit analyses, to determine the most ef-
fective strategy (Chew, 1995; Barker & Koenning, 1998;
Yáñez et al., 2001).
Conclusions
Epidemiological models to assess disease progress have
been built for few species of plant-parasitic nematodes.
This is partly due to the lack of studies that include
data on nematode population dynamics related to crop
phenology, and this is especially true for Nacobbus. In
the present study, information has been generated on the
population dynamics of N. aberrans on tomato plants
under field conditions in a comparison of treatments
designed to increase production and to reduce the effect
of the nematode on yield. At least three generations
of N. aberrans seemed to occur through the cropping
season and J3 and J4 were the main inoculum for the
progress of epidemics. The critical period for controlling
the nematode is probably during the first generation
(0-60 dat).
The epidemiological models for the disease caused
by the nematode on tomato crops, revealed that the
number of galls per plant and females per g of root
through the crop season were the most practical and
suitable variables for definition of the area under a
disease progress curve (AUDPC). The variables b−1
(Weibull’s apparent infection rate), AUDPC and Yf (final
disease incidence) indicated less crop damage under
the IC scheme than under the other two schemes (TC
and AC) (P = 0.05). However, comparison with AC
also showed that chemical control only reduces the
numbers of nematodes for a short period without exerting
permanent control. Therefore, this could still permit a
major loss in production but, by using the additional
measures included in IC, such large losses are avoided,
thus diminishing the impact of the disease (Chávez,
1995; Chew, 1995; Cid del Prado et al., 1997). The
epidemiological approach used in the present study helped
to assess the impact of the different control practices and
their potential for increasing production and reducing the
nematode population in infested soils. The results should
help in planning and implementing improved control
strategies. The IC programme would allow the disease to
be managed in a sustainable production system and to
increase crop yield (Téliz, 1992) in infested soils, thus
reducing the area of land abandoned by small farmers
because of infestation of the soil by N. aberrans and the
consequent poor crop yields.
Acknowledgements
The first author thanks CONACYT (Mexico) for finan-
cial support through the development of the research, and
Manuel Rodríguez, the cooperating farmer. Rothamsted
Research receives grant-aided support from the Biotech-
nology and Biological Sciences Research Council of the
United Kingdom.
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