HORTICULTURAL ENTOMOLOGY
Effects of Soil Moisture and Temperature on Reproduction and
Development of Twospotted Spider Mit (Acari: Tetranychidae)
in Strawberries
JEFFREY C. WHITE AND OSCAR E. 1I BURD)
Department i ... .... i. and Nematology, Natural Area Drive, University of Florida, Gainesville, FL 32611
J. Econ. Entomol. 98(1): 154-158 (2005)
ABSTRACT The effects of soil moisture and temperature on the reproduction of 1. :: .1 spider
mite, Tetranychus urticae Koch (Acari: Tetranychidae), were examined in laboratory and field tests
in strawberries, Fragaria X ananassa Duchesne, in Florida. Different soil moisture levels (low,
moderate, and high) were compared to determine how soil moisture affects the reproduction and
development of twospotted spider mite. In addition to soil moisture, i,:: ,. ... irrigation techniques
(drip versus drip/overhead) were compared to determine their effects on twospotted spider mite
reproduction as well as the incidence of angular leaf spot, Xanthonmonas fagaria Kennedy & King
disease. Similar studies were conducted to determine how different temperatures (18, 27, and 35C)
affect the reproduction and development of twospotted spider mites. In the laboratory, low soil
moisture as II as temperatures >27C promoted twospotted spider mite development. A similar
trend was observed in a field study with low soil moisture promoting twospotted spider mite
reproduction during the early season (11 November 8 December). Irrespective of moisture levels,
': i i ,. F X.Jfragaria was recorded in treatments with drip/overhead irrigation
systems compared with drip irrigation. Implications for management of soil moisture levels are
discussed with respect to the abundance of twospotted spider mite and X. fragaria in strawberries.
KEY WORDS soil moisture, temperature, twospotted spider mite, irrigation, strawberries
STRAWBERRIES ARE AN IMPORTANT small fruit crop in Flor-
ida with a farm gate value of $152 ..-.. 1: .... i:-
(National Agricultural Statistics Service 2004). Cur-
rent production is threatened by high populations of
twospotted spider mite, T . .. Koch, the
key arthropod pest during strawberry production sea-
son (Jepson et al. 1975, Hochmuth 1988). In the past,
twospotted spider mite has been controlled with sev-
eral applications of acaricides. However, high fecun-
dity and problems associated with resistance to acar-
icides (Trumble and Morse 1993) have made the
management of twospotted spider mite a major prob-
lem for strawberry growers in Florida.
Predatory mite releases, including / I,.* ,..". *
similis Athias-Henriot, have had moderate success in
suppressing twospotted spider mite activity,. .i:-
in southern Florida where rainfall patterns and tem-
peratures are more consistent than the northern re-
gions of the state (Decou 1994). However, growers in
northern Florida as :1 as other strawberry-produc-
ing areas in the southeast have not had much success
in managing twospotted spider mite populations with
augmentative releases of predatory mites (Liburd et
al 2003). Differences in environmental conditions be-
tween southern and northern Florida may account for
the high populations of twospotted spider mite i= .
recorded in north central Florida during the early
spring growing season when rainfall patterns and tem-
peratures are irregular. A better understanding of the
reproductive response of twospotted spider mite un-
der varying environmental conditions may help to
explain why strawberry growers in north central Flor-
ida and other areas of the southeast experience high
populations during the spring growing season.
Soil moisture and irrigation have been shown to
.-.. .. 1 mite feeding in almonds (Hoy 1985) as 11
as fruit size and yield in strawberries (Dwyer et al.
1987). Blatt (1984) evaluated irrigation and planting
methods to determine their effects on fruit size and
yield in strawberries. He found that application of
water before plants became water stressed signifi-
cantlyincreased the number -..I -. i ... 11
as overall marketable yield. Similarly, Dwyer et al.
(1987) monitored the response of 1-, 2-, and 3-yr-old
strawberry plants to irrigation schedules by using
three criteria: daily rainfall, leaf water potential, and
soil moisture. They found that all irrigated plots had
. _. i; :.,i higher yields compared with nonirrigated
strawberry plots. In addition, fruit weight was found to
be higher in all irrigated plots.
In addition to soil moisture, several studies have
documented the effects of temperatures on twospot-
ted spider mite reproduction (Ferro and Chapman
1979, Ho and Lo 1979). Ferro and Chapman (1979)
0022-0493 05/0154-0158504.00/0 c 2005 Entomological Society of America
WHITE AND LBURD: TWOSPOTTED SPIDER MITE RESPONSE
recorded a higher percentage of twospotted spider
mite egg hatch at 350C compared with a temperature
of 25C. Similarly, lo and Lo (1979) recorded lower
reproductive rates of twospotted spider mite in soy-
bean, Glcidne max (L.) Merr., at low temperatures
(<20C).
Our hypothesis is that in addition to fruit size and
marketable yields, soil moisture and temperature af-
feet the reproduction and development of twospotted
spider mite as well as the incidence of diseases in
strawberries. Our research goals were to study envi-
ronmental conditions; specifically soil moisture and
temperature, to determine how these factors influ-
ence the reproduction and development of twospot-
ted spider mite. Effects of soil moisture and temper-
ature were examined in the laboratory in a controlled
environment and then in the field under varying con-
ditions. Furthermore, irrigation systems were studied
in the field to determine how watering techniques
(drip versus overhead irrigation) may affect growth
and reproduction of twospotted spider mite and the
incidence of angular leaf spot, Xanthomonioas agaria
Kennedy & King disease.
Materials and Methods
Laboratory. Laboratory experiments were con-
ducted at the University of Florida Fruit and Vege-
table Integrated Pest Managemen (i 1 ) I) laboratory
in ( ..... :. FL.
SoilMoisture. Twelve potted Charlie'straw-
berry plants were randomly selected from our green-
house nursery stock. Plants were pruned to six leaf-
trifoliates and placed into 20-cr pot saucers before
they were examined using a 2X circular illuminated
magnifier (Cole Farmer, Vernon Hills, IL) to ensure
that all plants were free from mites. Soil moisture
levels in each pot were tested using a 9-in. soil mois-
ture meter tensiometerr) (Lincoln Irrigation Com-
pany, Lincoln, NE), which measures moisture levels
and translates the results to a scale of 0-10 (with 0
being completely dry soil and 10 being entirely satu-
rated). The soil containing potted plants was then
.11 I to air-dry to conform to the required soil
moisture levels according to each experimental treat-
ment.
Three treatments were evaluated: 1) alow soil mois-
ture (representing 1 3 on the soil moisture neter), 2)
a moderate soil moisture ([control] 4-6 on the soil
moisture meter), and 3) a high soil moisture (7-9 on
the soil moisture meter), i ..I .-.... -I design was a
completely randomized block with four replicates per
treatment. Ten twospotted spider mite (adults) were
placed onto each plant subjected to the various soil
moisture treatments (low, moderate, and high mois-
ture levels). The duration of the experiment was 9 d.
Temperature. Three environmental rearing cham-
bers (Percival Environmental Chambers, Boone, IA)
were used for this experiment. Each charrber was set
for aphotoperiod of 16:8 (L:D) h with 70% RH. During
the 8-h dark period, the temperature was set at 15C
in all rearing chambers. Three treatments were eval-
uated: 1) a low daytime temperature 180C, 2) a mod-
erate daytime temperature 27C (control), and 3) a
high daytime temperature 35C.
By using a similar protocol described for the soil
moisture experiment, 12 plants were selected at ran-
domr from the greenhouse and screened using a 2X
circular illuminated magnifier to ensure that plants
were mite free. Each plant was pruned to six leaf-
trifoliate, and 10 twospotted spider mites were placed
onto each plant. Experimental design was completely
randomized block with four replicates. The experi-
ment ran for 9 d.
Sampling. Every third day, all mites (motiles) and
unhatched eggs on each plant in both soil moisture and
temperature experiments were counted using a 40X
..1;. : 1. stereomicroscope. All twospotted spider
mite life stages (excluding eggs) were lumped and
referred to as motiles.
S; ; 1. .Data from the soil moisture and
temperature experiments were analyzed using re-
peated measures analysis of variance (ANOVA) with
mean separation using least significant differences
(LSDs) to show treatment differences (PROC
MIXED, SAS Institute 2002). Data were considered
significant when P values were < 0.05.
Field Trial. The field experiment was located at the
University of Florida, Plant Science Research and Ed-
ucation Unit, in Citra, F. Charlie' strawberry
transplant ts were planted in to 24 plots on the 7 October
2002, and the experiment was continued until 15 April
2003. Plot size was 7.3 by 6 m with a 10-m buffer
between each plot. Rows were 1.2 m in width, and
plants were spaced -30 cm apart. Approximately 240
plants were planted in each plot. Overhead sprinklers
were installed on all plots for frost protection (when
needed).
Experimental design was a completely randomized
block with four replicates. Six treatments (watering
program) were evaluated. The program for each treat-
ment was split into two 15-rnin watering cycles at 730
and 1000 hours, during the specific days when the
treatment was administered. Treatments included 1)
watering every day by using drip irrigation (high mois-
ture level), 2) watering every day by using drip and
overhead irrigation (high moisture level), 3) watering
every other day by using drip irrigation ([moderate]
control), 4) watering every other day by using drip
and overhead irrigation ( [moderate] control), 5) wa-
tering every third day by using drip irrigation (low
moisture level), and 6) watering every third day by
using drip and overhead irrigation (low moisture
level). The duration of this experiment was from 7
October 2002 to 3 April 2003.
i ... a Twenty leaves were collected randomly
in each plot (80 leaves per treatment). Leaves were
i: I from the lower strata of the plant and ex-
amined for twospotted spider mite under a 40x ste-
reomicroscope. Similar to the laboratory experiment,
all twospotted ...1. ....::. life stages (excluding eggs)
were lumped together and referred to as motiles. The
number of motiles and eggs were counted and re-
corded.
February 2005
JOURNAL OF ECONOMIC ENTOMOLOGY
Table 1. Mean SEM twospotted spider mite egg and motile populations on strawberries grown under different soil moisture levels
in the greenhouse
Days after initial twospotted spider mite transfer
Treatment 3 d 6 d 9 d
Eggs Motiles Eggs Motiles Eggs Motiles
Low soil moisture 451.5 69.2a 27.3 5.7ab 454.0 138.2a 375.8 10.8a 953.0 2875a 487.5 990a
Moderate soil moisture 490.3 67.4a 7.3 3.3a 215.8 56.6a 202.5 66.4a 863.0 1 36.9a 524.8 112.6a
Ihgh soil moisture 195.5 12.8b 16.8 1.3b 87.0 23.3b 89.5 48.4b 260.0 63.b 147.3 + 15.4b
Means followed by the same letter are not significantly different (P = 0.05, LSD test).
For 3 d eggs. F 17.8; df 2, 6; P < 0.01; for 3 d motiles, F 5.3; df 2 6; P 0.05; for 6 d eggs, F 6.2; df 2 6: P 0.04; for 6 d
motiles, F = 4.4; df = 2, 6: P = 0.07; for 9 d eggs, F = 6.0; df = 2, 6; P = 0.04; and for 9 d motiles, F = 12.8; df = 2, 6; P < 0.01.
a Low soil moisture represents 1-3 on the soil moisture meter, 4-6 for moderate soil moisture, and 7-9 for high soil moisture.
At the end of the season, 20 plants in each plot were
chosen randomly and examined for angular leaf spot.
We used two parameters to determine the presence of
the disease. First, if >5% of the upper surface of the
leavesoneach 1i ... 1 .-1. .. .1-1. i brown
necrotic spots, the plant was diagnosed as having an-
gular leaf spot. Second, if water-soaked areas were
present on >5% of the lower surface of the leaves on
each plant, it was diagnosed as displaying angular leaf
spot. Positive identification of angular leaf spot was
determined by Richard E. Cullen (Plant Disease
Clinic, University of Florida, ( n-.. i FL). Plants
selected from the various treatments were classified
into two categories: 1) presence of disease and 2)
absence of disease.
Statistical Analysis. Because the production season
for this experiment lasted for >6 tro, data were ini-
,. ,i pooled to determine .. I trends and then
separated into three categories: early (11 Novem-
ber 8 December), mid (22 February-11 March), and
late (18 March 15 April) season to follow the trends
throughout the season.
Poisson Regression with PROC GENMOD (SAS
Institute 2002) was used to determine the effects of
drip versus drip/overhead irrigation on populations of
twospotted spider mite. Data were considered signif-
icant when the P values were <0.05. Binomial coef-
ficients were used to estimate disease incidence.
Results
Laboratory. Soil Moisture. There were significantly
higher numbers of twospotted spider mite eggs in the
low and moderate soil moisture treatments compared
with the high soil moisture treatment after 3, 6, and 9 d
(Table 1). OG :11 the low soil moisture treatment
averaged 2.3, 5.2, and 3.6 times as many eggs compared
with the high soil moisture treatment for 3, 6, and 9 d,
respectively. Similarly, there were significantly higher
populations of twospotted spider mite motiles in the
low and moderate soil moisture treatments compared
with the high soil moisture treatment after 6 and 9 d
(Table 1). Treatments were significant over time for
both the eggs (F = 10.2; df = 6, 18; P < 0.01) and
motiles (F = 5.1; df = 6, 18; P < 0.01).
Temperature. There were significantly higher pop-
ulations of twospotted spider mite eggs in the high
temperature (35C) treatment compared with the low
temperature (180C) treatment after 3, 6, and 9 d (Ta-
ble 2). After 9 d, twospotted spider mite egg numbers
at all three temperatures (low, moderate, and high)
were significantly different. Similarly, significantly
higher populations of twospotted spider mite motiles
were recorded in the high temperature treatment
compared with the low temperature treatment after 6
and 9 d, respectively (Table 2). Significantly different
numbers of twospotted spider mite motiles were
present in all three temperature treatments after 6 and
9 d. Treatments were significant over time for both the
eggs (F = 16.7: df = 6,18; P < 0.01) and motiles (F =
2.8; df = 6, 18; P = 0.04).
Field Trial. Comparison of different moisture levels
under drip irrigation revealed that there were signif-
icantly higher populations of twospotted spider mite
in low soil moisture plots compared with high soil
moisture plots during the early season (11 Novem-
ber-8 December; Fig. 1). There were no significant
differences in the population of twospotted spider
mite among soil moisture treatments during mid- and
late seasons for drip and drip/overhead irrigation.
Table 2. Mean SEM twospotted spider mite egg and motile populations on strawberries grown at different temperatures
Days after initial twospotted spider mite transfer
Treatment 3 d 6 d 9 d
Eggs Motiles Eggs Motiles Eggs Motiles
Low temp (18C) 25.5 8.3b 6.3 1.7a 41.0 5.3b 6,8 2.5c 43.0 1 10.1c 4.8 1.8c
Moderate temp (27C) 70.3 1 13.6a 10.5 1.9a 152.8 34.4a 40.8 14.4b 99.0 1 2.2b 913 164b
High temp (35C) 1150 12.4a 8.5 0.9a 149.3 1 29.0a 137.5 22.2a 203.0 1 32.3a 204.3 362a
Means followed by the same letter are not significantly different (P = 0.05, LSD test).
For 3 d eggs, F 10.9; df 2, 6; P 0.01; for 3 d motiles, F 1.9; df 2,6; P 0.24; for 6 d eggs, F 8.6; df 2, 6; P 0.02; for 6 d motiles,
F = 319; df = 2 6;P <0.01; for 9 d eggs, F = 17.4; df 2, 6; P = <0.01 and for 9 d motiles, F = 684: df = 2, 6; P = <0.01
Vol. 98, no. 1
WHITE AND LIBURD: TWOSPOTTED SPIDER MITE RESPONSE
6
S5 -
4-
C+
0
N
a
0
I3-
t
0
Low Moderate High
Treatment
Fig. 1. Comparison of low, moderate and high soil moistures under drip irrigation during the early season (11 November 8
December) by using X analysis (X = 4.84; df = 1, 18; P = 0.03). Vertical bars represent mean SEM. Poisson regression
SAS version 9.0 with PROC GENMOD to estimate parameters (SAS Institute 2002).
Comparison of drip versus drip/overhead irrigation
across all treatments indicated that there was a sig-
nificantly higher population of twospotted spider mite
motiles under drip/overhead irrigation during the
early and late season (18 March-15 April) as well as
over the course of the entire season (Table 3). Overall,
the drip/overhead irrigation treatments averaged 5.1,
6.2, and 5.5 times as many twospotted spider mite
motiles compared with drip irrigation treatments in
the early, late, and entire season, respectively. Finally,
the probability of getting symptoms of angular leaf
spot for treatments with drip/overhead was 80% in
contrast with only a 30% probability for treatments
with drip irrigation.
Discussion
Our results demonstrate that low soil moisture and
high temperature increase twospotted spider mite re-
production in strawberries, with nearly 3 times as
Table 3. Effects of drip versus drip/overhead irrigation on
populations of twospotted spider mite motiles on strawberries
Mean I SEM no. of
twospotted spider mite
Season motiles/20 leaves X value P
Drip Drip/overhead
Early 0.4 1 0.3 2.3 1 1.7 8.63 0.0033
Mid 4.7 2.1 13.6 1 7.9 0.70 0.4032
Late 17.8 7.0 110.1 41.8 7.74 0.0054
Entire 7.7 2.6 42.0 15.6 5.64 0.0175
Poisson regression SAS version 9.0 with PROC GENMOD to esti-
mate parameters (SAS Institute 2002).
many eggs and motiles on plants exposed to low or
moderate soil moistures compared with high soil mois-
ture. Similar results were recorded for plants exposed
to high temperatures (35C) when they were 4 times
as many twospotted spider mite motiles as opposed to
plants exposed to lower temperatures (180C). The
mechanisms) of temperature and soil moisture ef-
fects on twospotted spider mite physiology is un-
known at present and requires further research. How-
ever, previous work has shown that when plants
(soybean) are deprived of water, the sugars inside the
leaves become more concentrated (White 1984), in-
creasing the feeding of twospotted spider mite and
promoting outbreaks (English-Loeb 1989). Another
possibility is that when soil moisture is a limiting fac-
tor, more water is retained in the leaves of plants,
which decreases the humidity around the leaves. This
limits the amount of water that twospotted spider mite
excretes, allowing the mite to spend more energy on
reproduction (Boudreaux 1958).
In the field experiment, low soil moisture promoted
twospotted spider mite reproduction. Temperatures
during early season averaged 27C with low levels of
rainfall. These conditions were similar to those cre-
ated in the laboratory where low soil moisture also
increased twospotted spider mite reproduction. After
8 December, temperatures in north central Florida fell
below 18C, and mite populations fell significantly.
Observations during the laboratory experiments indi-
cated that a temperature of s18'C caused a cessation
in twospotted spider mite reproduction. The period
between 8 December and 15 February was charac-
terized by low numbers of twospotted spider mite in
the field. After 15 February, temperatures exceeded
February 2005
JOURNAL OF ECONOMIC ENTOMOLOGY
18C, increasing reproduction and development of
twospotted spider mite populations.
Unseasonably high levels of precipitation occurred
from 15 February to 1 March, which interfered with
our soil moisture treatments during mid-season and
may have accounted for some of the insignificant dif-
ferences recorded during that period. Strawberry
plants exposed to drip/ overhead irrigation had a much
higher incidence of angular leaf spot than plants under
dripirrigation only. .I : Il. .) :1, severity of this
disease was magnified in all treatments because of the
mid-season rains coupled with nighttime irrigation to
prevent frost injury.
Higher populations of twospotted spider mite also
were recorded in our drip/overhead irrigation com-
pared with drip (across treatments) at the beginning
and the end of the season. The reason for the higher
numbers of twospotted spider mite under drip/over-
head irrigation is unknown and needs further inves-
tigation. As in our soil moisture field experiment, we
suggest that the reason why treatment differences
were not significant during mid-season in our irriga-
tion studies was due to the excessive amount of rain
during that time.
Our work indicates that soil moisture management
is critical when addressing arthropod (twospotted spi-
der mite) and disease problems in strawberries. Ear-
lier work showed that soil moisture is also important
in increasing berry size and overall marketable yields
(Blatt 1984, Dwyer et al. 1987). Strawberry growers
involved in IPM programs should take precautions to
ensure plants do not become water stressed or are not
overwatered because these practices increase the po-
tential for mite and disease problems, which ulti-
mately affects .1 marketable yields. The use of
drip irrigation during the production season seems to
be an important tool in managing soil moisture levels.
The amount of water and frequency of irrigation a
strawberry crop should receive depends on the grow-
er's locality, soil type, and crop stage of development.
Acknowledgments
We thank Scott Taylor and the staff at the University of
Florida, Plant Science Research and Education Unit in Citra
for help in maintaining the strawberry field experiment. We
also thank the entire Fruit and Vegetable IPM staff for as-
sistance II ... leaf samples and counting mites. Drs.
James Cuda and J. Howard Frank edited the first draft of this
manuscript. This work was partially funded by EPA Straw-
berry grant #00043127. This is Florida Experiment station
publication article no. R-10152.
References Cited
Blatt, C. 1984. Irrigation, mulch, and double row planting
related to fruit size and yield of 'bounty' strawberry.
Hortic. Sci. 19: 826 827.
Boudreaux, H. B. 1958. The effect of relative humidity on
egg-laying, hatching, and survival in various spider mites.
J. Insect Physiol. 2: 65 72.
Decou, 199. Biological control of the twospotted spi-
der mite (Acarina: Tetranychidae) on commercial straw-
berries in Florida with Phytoseiuus persimilis (Acarina:
Phytoseiidae). Fla. Entomol. 77: 33 41.
Dwyer, L. M., D. W. Stewart, L. Houwing, and D. Balchin.
1987. Response of strawberries to irrigation scheduling.
Hortic. Sci. 22: 4244.
English-Loeb, G. M. 1989. Nonlinear responses of spider
mites to drought-stressed host plants. Ecol. Entomol. 14:
41555.
Ferro, D. N., and R. B. C( .... 1979. Effects of different
constant humidities and temperatures on twospotted spi-
der mite egg hatch. Environ. Entomol. 8: 701 705.
Ho, C.-C. and K.-C. Lo. 1979. Influence of temperature on
life history and population parameters of Tetranychus
urticae. J. Agric. Res. China 28: 261 271.
Hochmuth, G. J. 1988. Strawberry production guide for
Florida. Fla. Coop. Ext. Serv. Circ. 142C.
Hoy, M. A. 1985. Almonds (California), pp. 299-310. Ia W.
Ilelle and M. W. Sabelis [eds.], Spider mites. Their bi-
ology, natural enemies and control, vol. lB. Elsevier, New
York.
Jepson, L. R., H. H. Keifer, and E. W. Baker. 1975. Mites
injurious to economic plants. University of California
Press, Berkeley, CA.
Liburd, 0. E., G. G. Seferina, and D. A. Dinkins. 2003.
Suppression of twospotted spider mites. University of
Florida, Institute of Food and Agricultural Sciences Ext.
Newsl. Berry/ : -. i Times 3: 3 4.
[NASS] National Agricultural Statistics. 2004. Noncitrus
fruits and nuts 2003; :;. i...... summary. U.S. Dep.
Agric., Washington, DC.
SAS Institute. 2002. The SAS system 9 for Windows. SAS
Institute, Cary, NC.
Trumble, J. T., and J. P. Morse. 1993. Economics of inte-
grating the predaceous mite : .'. pcrsimilis
(Acari: Phytoseiidae) with pesticides in strawberries. J.
Econ. Entomol. 86: 879-885
White, T.C.R. 1984. The abundance of invertebrate herbi-
vores in relation to i .. .. 1 .1, of nitrogen in stressed
food plants. Oecologia (Berl.). 63: 90 105.
Received 9 April 2004; accepted 11 October 2004.
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