Agronomical management influence on the spatiotemporal progress of strawberry dry wilt in Michoacan, Mexico

Full text

Vol. 9(4), pp. 513-520, 23 January, 2014
DOI: 10.5897/AJAR2014.8488
ISSN 1991-637X ©2014 Academic Journals
http://www.academicjournals.org/AJAR
African Journal of Agricultural
Research
Full Length Research Paper
Agronomical management influence on the
spatiotemporal progress of strawberry dry wilt in
Michoacan, Mexico
Luis Fernando Ceja-Torres1*, Gustavo Mora-Aguilera2 and Antonio Mora-Aguilera2
1Instituto Politécnico Nacional, CIIDIR Unidad Michoacán, Departamento de Investigación, Jiquilpan, Michoacán,
C.P. 59510, México.
2Fitopatología, Colegio de Postgraduados, C.P. 56230. Montecillo, Estado de México.
Accepted 26 April, 2013
The spatiotemporal distribution of strawberry wilt, caused by Fusarium oxysporum, Phytophthora sp.,
Pythium aphanidermatum and Rhizoctonia fragariae, was studied with the aim to establish the effect of
some technological components of the strawberry crop cv. Camarosa (Fragaria x ananassa Duch.) and
sustain their use in an integral management of the disease. Epidemics were characterized in two
cropping seasons at three localities in Valle de Zamora, Michoacan, Mexico, in commercial plantations
with plastic mulch and drip irrigation (A+G), and non-mulch and gravity irrigation (T) on a 100 m2 area
per site. Temporal parameters were contrasting between both management techniques. A+G
plantations had significantly lower final incidence (Yf =12.8±5.6%) than T (22.5±5.9%) (p=0.05) and were
consistent with estimators of area of curve (ABCPEa and ABCPEe). The range of epidemic intensity
reduction induced by A+G was 22.21 to 76.7% day, which was reflected in lower apparent infection rates
(b-1=0.0015-0.0027, R2=0.92-0.99). Lloyd’s Index of Patchiness and Morisita Index (1.01 to 1.17) indicated
a slightly aggregated dispersion pattern. Autocorrelation and geostatistical analysis confirmed lower
aggregates in A+G (up to 5 plants) vs. T (8 plants), but an apparent higher mobility of inoculum in A+G
up to 6.5 m. Plastic mulch and drip irrigation are proposed as technological components of an eventual
integrated management program of dry wilt in Michoacan.
Key words: Epidemiology, plastic mulch, drip irrigation, strawberry dry wilt.
INTRODUCTION
Black root rot is a worldwide disease that limits the yield
of strawberry and is a serious and common problem that
has been reported and studied in mayor producing
countries such as Japan, Israel, South Africa, Italy, Spain
and the United States (Kohmoto et al., 1981; Yigal et al.,
1981; Wing et al., 1994; Botha et al., 2003; Manici et al.,
2005; Avilés et al., 2008; Ellis, 2008). Despite its
significance, the etiology of black root rot has not yet
been fully resolved, and appears to vary according to the
site on which it occurs (Botha et al., 2003). In Mexico,
strawberry black root rot is commonly known as
strawberry dry wilt, caused by the complex F. oxysporum,
Phytophthora sp., Pythium aphanidermatum and
Rhizoctonia fragariae (Ceja-Torres et al., 2008), and
reaches incidences of 40 to 80% of the major strawberry
producing states in Mexico (Mendoza and Romero, 1989;
Castro and Dávalos, 1990). The development of effective
strategies for disease management is limited due to the
*Corresponding author. E-mail: lfceja@colpos.mx. Tel: 01 (353) 53 30083. Fax: 01 (353) 53 30218.

514 Afr. J. Agric. Res.
success of methyl bromide as a soil sterilant, currently
restricted. In addition, the management includes cultivar
selection, use of certified planting stock, replacement of
plants annually, biological control, rotation crops, soil
fumigation prior to planting, soil solarization and use of
systemic fungicides during the crop cycle (Yigal et al.,
1981; Yuen et al., 1991; Elmer and LaMondia, 1999;
Benlioğlu et al., 2005). Moreover, the use of new
production technologies such as plastic mulch and drip
irrigation influence on the population structure of
microorganisms associated with the disease by modifying
the soil microenvironment. Therefore, it is important to
sustain recent etiological studies of the dry wilt and have
a to better knowledge of the development of disease over
time and space for identifying options for management of
soil-borne diseases (Gilligan, 2002), with additional work
to determine the influence of agricultural practices, with
emphasis on land cover and irrigation system, and on the
spatiotemporal behavior of the disease in order to design
management strategies that enhance the possible
suppressive effects of conventional crop technologies.
This research has been established for this purpose and
under the assumption that attributes of intensity of
epidemics and pathogen dispersal patterns are strongly
influenced by the mulch and the drip irrigation.
MATERIALS AND METHODS
Field experiments
This research was carried out during the 2003-04 and 2004-05 crop
cycles in three localities of the Valley of Zamora, Michoacan,
Mexico: Ario de Rayón, Tamándaro and Villafuerte. In each locality
two commercial plots of 2 ha were chosen for the variety
Camarosa; one with plastic mulch and drip irrigation (A+G) and the
other with non-mulch soil with gravity irrigation (T). In all cases, the
soil was clay. The density was 90 thousand plants per ha set out in
zig-zag, double row manner, every 18 cm. The monthly average
temperature of the study area was obtained from the Irrigation
District 061, Zamora, Michoacan.
Evaluation of the disease
In an area of 100 m2 (10×10 m) by commercial plot, incidence of
wilt plants was recorded monthly from September to January during
the crop growth and biweekly from February to May, during
flowering and fructification. A plant was considered diseased if it
exhibited wilting and gradual death. The spatial location of the
plants was recorded using field maps.
Temporal analysis
Epidemics in each of the three regions were characterized by the
model of simplified Weibull distribution with two parameters (b and
c) (Pennypacker et al., 1980; Thal et al., 1984): Y = 1-e-(t/b)c, t>0;
where Y = incidence ratio, t = time in days after planting, b =
parameter estimator of the epidemic rate in its inverse form, and c =
parameter of the curve shape. Additionally, the intensity of
epidemics was estimated by calculating the absolute area under the
disease progress curve (AUDPCa) by the trapezoidal integration
method: AUDPCa = Σ1n-i [(Yi + Yi +1) / 2] (t i +1 - ti), where: Yi =
proportion of disease in the i-th evaluation, ti = time at the i-th
observation, n = number of evaluations (Campbell and Madden,
1990; Jeger and Viljanen-Rollinson, 2001). The parameter
AUDPCa) was standardized (AUDPEe) by dividing its value
between the time of duration of the epidemics. The relative
reduction of area (AUDPEr) in percentage was calculated in relation
to AUDPCa of plantations T (AUDPEaT) by location and crop cycle
(100-[AUDPCa /AUDPEaT] [100]). Confidence intervals with p =
0.05 and t test were applied for comparison of intensity parameters
of epidemics. All data were analyzed with the Statistical Analysis
System (SAS) ver. 6.10 (SAS Institute, Cary, NC) (Jesus Junior et
al., 2004).
Spatial analysis
The optimum quadrant sizes of (OQS) to calculate indices of
aggregation were obtained by the Greig-Smith method (Campbell
and Madden, 1990) in blocks 1, 2, 4, 8, 16, 32, 128 and 256 plants
with software, MorLloyd version 1.0® MS EXCEL (Rivas and Mora-
Aguilera, 2011. Unpublished). The spatial pattern of strawberry dry
wilt was determined with Lloyd´s Index of Patchiness (LIP) and
Morisita Index (Iδ) (Campbell and Noe, 1985). LIP = m + [(V / m) -1]
/ m, where m = average number of diseased plants per quadrant,
and V = variance. Iδ = n[∑(y)2 - ∑y]/(∑y)2 - ∑y; where: n= total
number of quadrants, and y = number of diseased plants per
quadrant. Criteria to determine the spatial pattern with these
indexes were: 1 = at random, >1 = aggregate and <1 = uniform.
The patterns of proximity and spatial dependency of diseased
plants were defined by autocorrelation analysis, with the LCOR2®
program (Gottwald et al., 1992), and the geostatistical GEO-EAS
1.2.1 software; to determine the spatial dependency in a row
(isotropy) and in any direction (anisotropy).
RESULTS AND DISCUSSION
Temporal analysis
Disease onset was delayed until 45 days after planting
with an initial incidence less than 1% (Y0) regardless the
agronomic management (Figure 1A to F). However,
management significantly influenced the further progress
of the disease (Tables 1 and 2). The incidence of the dry
wilt increased between 213 and 228 days after planting,
being higher in the gravity irrigation system without mulch
(T). The flexibility of the Weibull model (Thal et al., 1984)
allowed describing the epidemic progress of the
strawberry dry wilt with determination coefficients of 0.92
to 0.99 and from 0.97 to 0.99 in the first and second
production cycles, respectively. With the exception of
Tamándaro and Ario de Rayón in the 2004-05 cycles, the
estimator of the epidemic rate (1/b) was lower in A+G.
However, only statistical differences (p=0.05) were found
in Tamándaro and between this with the T values of
Villafuerte and Ario de Rayón (2003-04 cycle) and
between Villafuerte (A+G) and Tamándaro (T) (2004-05
cycle) (Table 1). The mechanism of dispersal of the
primary inoculum in soil can have large impacts on
disease onset, progress, and final incidence (Sujkowski
et al., 2000), in this study the shape of the epidemic
curve (c) in all cases was sigmoidal asymptotic, typical of

Ceja-Torres et al. 515
Figure 1. Curves of the temporal progress accumulated of strawberry dry wilt in plantations with plastic mulch and drip
irrigation (A+G) and non-mulch and gravity irrigation (T), in the Valley of Zamora, Michoacan, Mexico (A, C and E 2003-04
cycle; B, D and F 2004-05 cycle).
low-level epidemics with limited inoculum dispersal. In
this case, statistical differences were also detected
between the curve shapes being clearer between
Tamándaro (A+G) and the other localities in both cycles.
Although the intensity of disease was generally lower in
A+G, Weibull analytical results were not fully consistent
with the graphical inspection of the curves where less
epidemic intensity was detected in A+G (Figure 1B to F).
Final incidence (Yf) in the 2003-04 cycle ranged from 7.8
to 14.5% (11.8 ± 3.5%) in plantations A+G and 13.1 to
27% (21.7 ± 7.1%) in T, and in the 2004-05 cycle, 10.8 to
16.4% (13.8 ± 2.8) and from 18.2 to 28.2% (24.1 ± 5.3%)
in the same order (Table 2). The significance of mean
differences in the first and second cycles was 11.6 and

516 Afr. J. Agric. Res.
Table 1. Description of 12 epidemics of strawberry dry wilt by the Weilbull model for the 2003-04 and 2004-
05 cycles in the Valley of Zamora, Michoacan, Mexico.
Locality (management)
Model
Y= 1-e-(t/b)c
R2
Interval of confidence (95%)*
b
c
2003-2004 cycle
Ario de Rayón (A+G)
Y= 1-e(t/426.6)3.99
0.97
381-472a
3.22-4.77a
Ario de Rayón (T)
Y= 1-e(t/410.4)4.84
0.99
395-426a
4.47-5.21a
Tamándaro (A+G)
Y= 1-e(t/653.0)2.16
0.97
516-790b
1.72-2.60b
Tamándaro (T)
Y= 1-e(t/397.0)3.41
0.96
352-442a
2.64-4.19a
Villafuerte(A+G)
Y= 1-e(t/459.0)4.69
0.92
361-558ab
3.01-6.37a
Villafuerte (T)
Y= 1-e(t/366.1)3.67
0.96
331-402a
2.82-4.51a
2004-2005 cycle
Ario de Rayón (A+G)
Y= 1-e(t/374.6)5.26
0.98
348-401ab
4.31-6.21bc
Ario de Rayón (T)
Y= 1-e(t/386.9)3.24
0.99
305-409ab
2.86-3.61a
Tamándaro (A+G)
Y= 1-e(t/355.0)6.99
0.97
323-378a
5.59-8.39c
Tamándaro (T)
Y= 1-e(t/362.6)4.07
0.98
338-387a
3.38-4.75ab
Villafuerte(A+G)
Y= 1-e(t/435.8)4.68
0.98
397-475b
3.92-5.44b
Villafuerte (T)
Y= 1-e(t/375.1)5.06
0.97
341-409ab
3.91-6.20bc
b, Estimator of the apparent infection rate in its inverse form (1/b); c, estimator of the curve shape. *Values of
same parameter for each crop cycle, with different letter are statistically different (p = 0.05%).
Table 2. Absolute, relative and standardized AUDPE, Yf y b-1 (Weibull) of 12 cumulative progress curves of
strawberry dry wilt for the 2003-04 and 2004-05 cycles in the Valley of Zamora, Michoacan, Mexico.
Locality
Management
AUDPEa
AUDPEr
AUDPEe
Yf
b-1
2003-2004 cycle
Ario de Rayón
A+G
7.58
-30.69
0.033
14.5
0.0023
Ario de Rayón
T
5.80
0.00
0.025
13.1
0.0024
Tamándaro
A+G
11.35
22.21
0.050
13.1
0.0015
Tamándaro
T
14.59
0.00
0.064
22.8
0.0025
Villafuerte
A+G
3.84
76.63
0.028
7.8
0.0022
Villafuerte
T
16.43
0.00
0.072
27.0
0.0027
2004-2005 cycle
Ario de Rayón
A+G
8.59
57.14
0.038
16.4
0.0027
Ario de Rayón
T
20.04
0.00
0.088
28.2
0.0026
Tamándaro
A+G
5.89
64.96
0.026
14.3
0.0028
Tamándaro
T
16.81
0.00
0.073
26.0
0.0028
Villafuerte
A+G
5.74
42.94
0.025
10.8
0.0023
Villafuerte
T
10.06
0.00
0.044
18.2
0.0027
A+G, Plastic mulch with drip irrigation; T, non-mulch and gravity irrigation.
0.05%, respectively. Weibull failure to reflect these trends
could be due to the extension of the lower asymptote
which was due to the delay that A+G caused in the
increase of the epidemics. Another alternative analytical
unaffected by the asymptotic factor was AUDPE. Lower
values of AUDPEa and AUDPEe were obtained with the
operation A+G except in the 2003-04 cycle in Ario de
Rayón which was consistent with the values of Yf (Table
2). The Weibull rate parameter (b-1) was significantly
correlated with AUDPEa but with low accuracy (r2=0.58)
confirming its limited ability to describe in the context of
this work. The reduction range of epidemic intensity of
A+G on T was 22.1 to 76.6% and 42.1 to 64.9% in 2003-
04 and 2004-05 cycles, respectively, which demonstrates
the strong suppressive effect of the combination of plastic
mulch with drip irrigation (Table 2). There were no

Ceja-Torres et al. 517
Table 3. Spatial pattern of strawberry dry wilt with different crop management for the 2003-04 and 2004-05 cycles
in the Valley of Zamora, Michoacan, Mexico.
Locality (management)
Optimum quadrant size
LIP
Morisita Index
Spatial pattern
2003-04 cycle
Ario de Rayón (A+G)
128
1.09
1.07
Aggregate
Ario de Rayón (T)
128
1.02
1.01
Aggregate
Tamándaro (A+G)
128
1.02
1.02
Aggregate
Tamándaro (T)
128
0.99
0.99
Uniform
Villafuerte (A+G)
128
1.14
1.12
Aggregate
Villafuerte (T)
128
1.07
1.05
Aggregate
2004-05 cycle
Ario de Rayón (A+G)
32
0.94
0.96
Uniform
Ario de Rayón (T)
32
1.09
1.06
Aggregate
Tamándaro (A+G)
32
1.17
1.10
Aggregate
Tamándaro (T)
32
0.98
0.98
Uniform
Villafuerte (A+G)
16
1.01
1.01
Aggregate
Villafuerte (T)
32
1.05
1.04
Aggregate
differences between cycles with no parameters (p = 0.05)
suggesting that the increase of inoculum required longer
periods of time, typical of soil organisms (Michreff et al.,
2005).
The temporal analysis of dry wilt showed that the A+G
management affected the efficiency of fungal and
pseudofungi inoculum associated with the disease,
leading to a lower intensity of epidemics, but not total
elimination capacity. The increase in incidence in all
cases coincided generally with fructification and average
room temperature during this period between 19 and
25.5°C, range biasing the expression of pathogens
associated with diseases of root diseases in part by the
increase of the transpiration rate combined with the
productive stress of the plants (Michereff et al., 2005). In
Australia Fusarium oxysporum and binucleate
Rhizoctonia particulary AG-A, caused severe disease on
root and crowns, resulting in the eventual death of plants,
still severely retarded the growth and development at
27°C, but Macrophomina phaseolina was most virulent
and caused most severe disease at 32°C (Xiangling et
al., 2011), this last pathogen has not been reported in
Mexico. Although soil temperature was not measured,
plastic mulch can increase temperature from 3 to 7°C and
drastically change the soil moisture (Mbagwu, 1991;
Schmidt and Worthington, 1998), which could explain the
reduced efficiency of inoculum in the initial phase of the
epidemics, as evidenced by the prolongation of the initial
asymptote A+G. It is shown that these factors
differentially affect the pathogenicity of microorganisms
(Pinkerton et al., 2002; Michereff et al., 2005). For
example, Phytophthora capsici was more aggressive in
Capsicum annuum and caused a higher incidence of
wilting than Rhizoctonia solani due to soil temperature
(20 to 22°C) and humidity at field capacity not optimal for
this fungus (Vázquez-López et al., 2009). Previous
studies with strawberry dry wilt indicate that this disease
increases in poorly drained clay soils (Castro and
Dávalos, 1990; Mendoza, 1992), which was characteristic
of plots under study. In a subsequent regional study it
was confirmed that the distribution and prevalence of
fungi and pseudofungi causing of strawberry dry wilt was
influenced by soil texture and other factors such as the
level of organic matter (Ceja-Torres et al., 2008).
Spatial analysis
Optimum quadrant size (TOC) for use in the calculation
of Lloyd’s Index of Patchiness (LIP) and Morisita Index
(Iδ) was 120 plants in 2003-04 and 32 plants in 2004-05
from a matrix of data of 40 × 20 in the first crop cycle and
20 × 20 in the second crop cycle (Table 3). Exploratory
maps were obtained using SURFER 4.0® (Figure 2) and
the LIP indices of 1.01 to 1.17 and Iδ of 1.01 to 1.12,
indicated that dry wilt of strawberry had a pattern of
slightly aggregated dispersion in 75% of the plantations
studied predominantly at A+G (83.3%) (Table 3). This is
because the values of these indices were slightly higher
than one, indicating weak aggregation, which verifies
previous observations regarding the distribution of the
disease in patches (Téliz et al., 1986). Only two
plantations with gravity irrigation and one with drip
irrigation, showed a trend toward a uniform pattern of
disease (LIP and Iδ of 0.94 to 0.99) (Table 3). These
results suggest that the distribution pattern of the
inoculum is influenced by the plantations management in
addition to biological attributes inherent in the aggregate
behavior of some pathogens due to the effect of
rhizosphere (Mora-Aguilera et al., 1990) and to

518 Afr. J. Agric. Res.
Figure 2. Spatial behavior of strawberry dry wilt into quadrants of 100 m2 (10 ×
10 m) in Tamándaro (A and B 2003-04 cycle, C and D 2004-05 cycle).
Plantations with plastic mulch and drip irrigation (A+G) left, and non-mulch and
gravity irrigation (T) right.
competition for sites of infection between individuals
which can result in consistent patterns of damage
(Ludwig and Reynolds, 1988).
Autocorrelation analysis confirmed the spatial effect of
management and allowed to estimate attributes of
distance and directionality of dispersal. The greatest
dispersion in aggregates (continuous dependence) and
sub-aggregates (discontinuous dependence), it is
generally found in Ario de Rayón and Tamándaro in both
crop cycles. In Villafuerte only sub-aggregates were
found (Table 4).
Confirmation of aggregates within and between rows
was of order 1, with exception of Tamándaro with order 2,
which implied small patches of diseased plants. The sub-
aggregates were in the range of order 2 to 20 with higher
dominance within the row. The epidemic intensity level
was not associated with a specific spatial pattern possibly
by Yf less than 23% (Table 2 and Figure 1). With regard
to the management, higher aggregation was found in T
plantations; with patterns of 1 to 5 diseased plants, by

Ceja-Torres et al. 519
Table 4. Spatial self-correlation to determine spatial dependence of strawberry dry wilt with two irrigation
technologies and three locations of Valle de Zamora, Michoacan, Mexico.
Location (management)
Spatial dependence
Within rows
Between rows
GG
2003-04 cycle
Ario de Rayón (A+G)
C1**, D5*, 11** and 20*
C1**
+
Ario de Rayón (T)
C1*, D7** and 15**
-
+
Tamandaro (A+G)
D8* and 14**
D6*
+
Tamandaro (T)
C2*, D19*
C1**, D13* and 16*
+
Villafuerte (A+G)
D3*
D10**
+
Villafuerte (T)
D2*, 7* and 15**
D2*
-
2004-05 cycle
Ario de Rayón (A+G)
C1*, D7* and 27*
-
+
Ario de Rayón (T)
D2*, 3**, 4**, 5** and 14*
C1**, D7*, 8**, 15** and 17**
+
Tamandaro (A+G)
C1**, D16**
D2**, 4*
-
Tamandaro (T)
C1**
C1**, D3**, 7** and 10*
+
Villafuerte (A+G)
D8** and 18*
D2* and 12*
-
Villafuerte (T)
D12**
D2* and 7**
+
GG, Continuous general gradient (aggregated); C, continuous dependence; D, discontinuous dependence. The
number indicates the “order” of the dependence.
autocorrelation and 1 to 8 plants with geostatistics while
in A+G were 1 to 3 and 1 to 5 plants by the respective
analysis, which made it possible to visualize patterns of
spatial dependence in different directions (Nelson et al.,
1999). The dominant sub-aggregates were formed up to
4.5 and 6.5 m in plots T and A+G, respectively.
Remarkably, A+G had the smallest aggregates, but the
restrictive space could explain the highest displacement
of the inoculum within the row. This level of dispersal is
consistent with root pathogens, because it depends on
the spatial pattern of host population, especially when
disease transmission requires contact between healthy
and susceptible tissues, that is, root to root (Sujkowski et
al., 2000; Willocquet et al., 2000) and the airborne
pathogens have a less restrictive dispersion. Since 2006,
Fusarium wilt of strawberry has increased in incidence
and severity in California, USA. Initial problems in 2006
consisted of multiple small patches (2 to 4 beds wide × 3
to 10 m long) of diseased plants; in these patches
disease incidence could range from 80 to 100%. By
2009, in some fields, the disease affected large sections
that ran the length of the field (Koike et al., 2009).
Moreover, the existence of spatial dependencies
presupposes the action of a common inoculum source
(primary source of infection). This may be valid for a
single pathogen-host association. Strawberry dry wilt is
caused by a complex of pathogens which involves
various sources of inoculum and roles of primary and
secondary infection, originating from soil-borne inoculum
and diseased plants, respectively (Willocquet et al., 2007;
Ellis, 2008; Xiangling et al., 2011). Hence the
interpretation of spatial dependencies cannot be via a
conventional method without considering other effects
such as competition and aggression.
Conclusions
The commercial applications of plastic mulch and drip
irrigation (A+G) for the purpose of productivity of
strawberry crops in the Zamora Valley were effective in
reducing inoculum potential of organisms associated with
dry wilt, although these did not induce a total suppressive
action. Spatiotemporal studies in two production cycles
and three localities selected for high inductance to the
disease confirmed in all parameters used (yf, AUDPCa,
AUDPEr, AUDPEe, b-1) the lowest epidemic intensity in
plantations A+G with reductions in the range of 22.2 to
76.6%. Similarly, the indexes and spatial statistical
analysis showed lower aggregates in A+G (up to 5
plants) but found an apparent increased dispersiveness
along the row, possibly as a result of its plastic enclosure
(up to 6.5 m). The plastic mulch and drip irrigation should
be adopted in a program of integrated management of
dry wilt. Future studies may be aimed to optimize these
technologies with respect to the suppressive ability of the
organisms associated with the disease.
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