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KEY WORDS Sitona discoideus, temperature, embryo development, developmental rate, modeling
Alfalfa (Medicago sativa L.) is the father of herbs and larvae decreases the ability of the plant to Þx nitrogen,
the queen of forage. It is widely cultivated on ⬎640,000 therefore reducing the accumulation of nitrogen in
h in Iran. Of the 14 species of Sitona spp. (Coleoptera: plants and soil (Petrukha 1969). Larval damage is more
Curculionidae) that are reported to feed on alfalfa, commonly apparent in older alfalfa stands.
only a few such as Sitona discoideus are economically The period between egg hatch and occupation of
important (Modarres Awal 1994, Arbab and Boru- root nodules by Þrst-instar larvae is probably the most
mand 2002). The alfalfa root weevil, Sitona discoideus vulnerable part in the life cycle: larvae that do not
Gyllenhal (Coleoptera: Curculionidae), is a native locate root nodules quickly die of starvation (Johnson
pest of alfalfa in Iran that is distributed throughout the et al. 2007). Understanding the inßuence of temper-
country where alfalfa is grown (Behdad 1993). Re- ature on development rate of poikilotherms allows for
search in New Zealand found that feeding by the the prediction of incubation time of the egg stage
larvae had a major effect on the sustainability of alfalfa, (Hamel et al. 1997). This relationship between insect
resulting in an average decline in crop growth of 40% development and temperature represents an impor-
per year (Goldson and French 1983, Goldson et al. tant ecological variable for modeling population dy-
1985). Adult feeding damage is characterized by namics of insects (Jarosik et al. 2002). Understanding
notching of the leaßet edges, which can cause severe temperature-dependent development can be used for
damage to seedlings, especially when plant growth accurate forecasting and phenological prediction and
conditions are unfavorable. Eggs are laid in the mid- is paramount to many successful pest management
spring on the soil surface near, or less often, attached programs (Tobin et al. 2001). For example, Anaphes
to the alfalfa plants. First-instar larvae emerge and diana (Girault) (Hymenoptera; Mymaridae) is a po-
borrow into the soil to locate the root nodules on tential biological control agent against S. discoideus in
which they feed, destroying the N2-Þxing Rhizobium Iran. A. diana is an egg parasitoid abundant in the
bacteria. As the larvae mature and nodules are con- Mediterranean region (Aeschlimann 1986) and, al-
sumed, the plant rootlets and root hairs are subse- though introduced into Australia, establishment was
quently attacked (Aeschlimann 1986). There are Þve never conÞrmed (Aeschlimann et al. 1989). The suit-
larval instars (Frampton 1986). This insect is univol- ability of A. diana as a biological control agent is
tine and aestivates seasonally in Iran (Behdad 1993), dependent on temperature and other ecoclimatic con-
with adult densities reaching 50 Ð70 weevils/m2 during ditions (Worner et al. 1989) and therefore a key step
pest outbreak years. Elimination of root tubercles by contributing to the success of a biological control
introduction would be to determine the degree of
1 Entomology Research Laboratory, Islamic Azad University, Take- synchrony between A. diana developmental times
stan Branch, Takestan, Iran. with that of S. discoideus eggs.
2 Corresponding author: Department of Entomology and Agricul-
Many models are available to describe mean devel-
tural Zoology, Benaki Phytopathological Insitute, 8 St. Delta Street,
145 61 KiÞssia, Greece (e-mail: dckontodimas@hotmail.com).
opmental times or rates of development as a function
3 AgResearch Lincoln, Private Bag 4749, Christchurch 8140, New of temperature: from the earliest and most common
Zealand. used linear or day-degree model, a concept that dates
to the 1700s (Wang 1960), to the nonlinear models of Table 1. Development time and developmental rate of the
Stinner et al. (1974), Logan et al. (1976), Sharpe and embryo of S. discoideus at eight constant temperatures (mean ⴞ SE)
DeMichele (1977), and Lactin et al. (1995). However,
Temperature Development Developmental
it is not always obvious, a priori, which model is the (⬚C) time (d) rate (d⫺1)
most suitable for practical integrated pest manage-
8.5 69.01 ⫾ 0.92 0.0145
ment (IPM) implementation. The purpose of this n ⫽ 73
study was to determine which of the several models 12.5 24.6 ⫾ 0.16 0.0407
tested better described embryo development of S. n ⫽ 75
discoideus. 14.5 19 ⫾ 0.24 0.0526
n ⫽ 69
20 14.51 ⫾ 0.23 0.0689
Materials and Methods n ⫽ 74
23 11.21 ⫾ 0.18 0.0892
Temperature-dependent Development. Sexually n ⫽ 70
26 10.47 ⫾ 0.13 0.0955
mature adults were collected by sweep net in mid- n ⫽ 75
April 2002 from several commercial alfalfa Þelds in 28 8.46 ⫾ 0.14 0.1182
Qazvin province, Iran (36⬚17⬘ N, 49⬚24⬘ E and 1,450 m n ⫽ 68
above sea level). To obtain an egg cohort, 100 adults 30 10.22 ⫾ 0.052 0.09782
n ⫽ 72
were placed in rearing cages (15 by 11 by 11 cm) and
held under laboratory conditions (24 ⫾ 2⬚C, 60 ⫾ 5%
RH, 14:10 L:D) and provided with alfalfa stems con-
sisting of between four to eight leaves. The cages were developmental rate function along time (as in the
checked every 12 h, and the eggs (⬍12 h old) were models of Davidson 1942, 1944, Stinner et al. 1974,
collected. Newly laid S. discoideus eggs are white but Sharpe and DeMichele 1977, Lactin et al. 1995) can be
turn gray and then black in a few hours or a few days used to simulate the development of an organism ex-
depending on temperature. Grieb (1976) indicated posed to different temperatures.
that egg melanization took 5 d at 4⬚C and 2 d at 12⬚C, Linear Modeling. The relationship between tem-
whereas Schotzko and OÕKeeffe (1986) showed that, perature (T) and developmental rates (r ⫽ 1/d) for
at 21⬚C, the melanization was completed after ⬃17 h. the egg stage was modeled using linear regression,
Random samples of 25 white eggs were arranged with where r(T) ⫽ a ⫹ bT, within the temperature range
a brush on wet Þlter paper in petri dishes and trans- in which the relationship is linear (8.5Ð28⬚C). The
ferred to controlled environment chambers (model model was Þtted using the statistical program JMP (v.
GL-700W; Dena, Takestan, Iran). The chambers were 4.02; SAS Institute 1989, 2000). The lower develop-
set at one of eight constant temperatures (8.5, 12.5, mental threshold temperature was estimated by ex-
14.5, 20, 23, 26, 28, and 30⬚C). Each chamber was trapolating the regression line to the temperature axis,
divided into three sections, and one petri dish with 25 tb ⫽ ⫺a/b. In addition, degree-day estimations for
eggs was placed in each section. The photoperiod development were calculated using the formula K ⫽
setting for all experiments was 0:24 L:D, with the (T ⫺ tb)Dev, where K is degree-days, Dev is the mean
absence of light shown to have no inßuence on the rate number of days to complete development at a constant
of development (Grieb 1976). Egg viability of S. dis- temperature (T), and tb is the lower threshold tem-
coideus is between 95 and 99% (Aeschlimann 1975, perature (Gordon 1984).
Frampton 1984), and to maximize egg hatching, hu- Nonlinear Modeling. Temperature-dependent mean
midity around the eggs was maintained by adding a rates of egg development, r(T), were modeled using nine
few drops of distilled water to the petri dishes every descriptive nonlinear models (Appendix 1).
morning. Larval eclosion was determined by examin- The parameters of the nonlinear models were esti-
ing individual petri dishes under a binocular micro- mated with the nonlinear regression model of Mar-
scope (⫻40) twice daily until all eggs hatched. Un- quardt (1963) using the JMP and SPSS (version 9.0;
fertilized eggs remained white and were removed at SPSS 1999) statistical programs. Lower and upper de-
the end of the experiment. velopmental thresholds were estimated from the
Mean developmental rate of embryos at various tem- equations.
peratures was estimated using the following model: Evaluation of Models. Model evaluation was based
on four factors: (1) Þt to data (residual sum of squares
r共T兲 ⫽ 1/e 关兺 ln共dt兲/n兴 [RSS] and coefÞcient of determination or coefÞcient
where r(T) is the mean developmental rate at tem- of nonlinear regression [r2]), (2) number of measur-
perature T (⬚C); dt is the observed development time able parameters, (3) the biological value of the Þtted
in days; and n is number of observations. This method coefÞcients, and (4) accuracy in the estimation of
is recommended by Logan et al. (1976) to account for thresholds (Kontodimas et al. 2004, Arbab et al. 2006).
linearity in the transformation of development time to
developmental rate.
Results
These rates are used in development models where
data are added daily. Development is completed when Temperature-dependent Development. The num-
the sum of their daily developmental rates reaches 1 ber of days for egg development at each temperature
(Curry et al. 1978). Therefore, the integral of the regimen is listed in Table 1. Developmental times
December 2008 ARBAB ET AL.: EMBRYO DEVELOPMENT OF S. discoideus 1383
Table 2. Linear interpolation of LBT and DD requirement for which calculated a lower temperature threshold of
S. discoideus eggs ⫺2.5⬚C, and the Analytis model, which calculated a
threshold of 8.2⬚C. The optimum temperature for egg
Parameter
Value ⫾ SE development rate was calculated to be between 28.5
estimates
and 29.9⬚C (with an exception of 26.5⬚C obtained from
Intercept ⫺0.022609 ⫾ 0.006429
Slope 0.004814 ⫾ 0.000320
the Briere model). The calculated upper temperature
R2 0.9784 threshold at which egg development rate became sub-
RSS 0.000211 optimal was calculated to be between 30 and 32.6⬚C.
LBT 4.696705
DD 207.7
0,10 0,10
0,10 0,10
0,10
Fig. 1. Fitting linear and nonlinear models to observed values of development rates (d⫺1, ordinate) of embryo versus
temperature (⬚C, abscissa). 䡺, observed data. In the linear model, the development time at 30⬚C was omitted.
1384 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 6
Table 3. Parameter estimation using regression analysis of linear and nonlinear models on temperature-dependent developmental rate
opment times over a range of temperatures, and insects and mites (Briere and Pracros 1998). Nonlin-
using the Sharpe and DeMichele model, calculated earity of the relationship between developmental rate
an optimum temperature for egg hatch and devel- and temperature conÞrms the hypothesis that the rate
opment of 29⬚C. processes that control development in S. discoideus is
Research elsewhere has highlighted the effect of nonlinear (Lamb 1992).
temperature on embryo development rates for Sitona Among the models that estimated lower tempera-
species (Andersen 1931, Melamed 1966). Melamed ture threshold, all models except for Analytis and
(1966) reported that the percentage of egg hatching Hilbert and Logan calculated tmin values of between
for four species of Sitona (S. hispidulus, S. lividips, S. 3.9 and 4.7⬚C that are close to the observed values. The
lineatus, and S. crinitus) fed on pea leaßets was re- optimum temperature and upper temperature thresh-
duced when temperature exceeded 25⬚C. In Finland, olds estimated by the majority of the models were
the embryo development period of 11 species of Sitona 28.5Ð29.9 and 30 Ð32.6⬚C, respectively.
including S. crinitus was 29 Ð32 d at a mean tempera- Our results suggest that, among the Þve models
ture of 11.5Ð12⬚C (Markkula 1959). The incubation (Analytis, Sharpe and DeMichele, Hilbert and Logan,
period of S. hispidulus was 21 d in summer and 150 Ð200 Lactin, and Briere) that estimated all three parameters
d in winter (Underhill et al. 1955). (tmin, topt, tmax), the Sharpe and DeMichele and Lactin
The curvilinear developmental rateÐtemperature models more accurately described the relationships
relationship for this species is typical of many other between egg developmental rate and temperature.
December 2008 ARBAB ET AL.: EMBRYO DEVELOPMENT OF S. discoideus 1385
Frampton, E. R. 1986. Determination of the number of Lactin, D. J., N. J. Holliday, D. L. Johnson, and R. Craigen.
larval instars of Sitona discoideus Gyllenhal (Co- 1995. Improved rate model of temperature-dependent
leoptera: Curculionidae) using probit analysis. N.Z.J. development by arthropods. Environ. Entomol. 24: 68 Ð75.
Zool. 13: 107Ð111. Lamb, R. J. 1992. Developmental rate of Acyrthosiphon pi-
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lenhal (Coleoptera: Curculionidae), larvae and the asso- viron. Entomol. 21: 10 Ð19.
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Agri. Res. 26: 251Ð255. lineatus (Coleoptera: Curculionidae) in ßuctuating tem-
Goldson, S. L., C. B. Dyson, and J. R. Proffitt. 1985. The peratures. Environ. Entomol. 33: 107Ð112.
effect of Sitona discoideus Gyll. (Col.Curculionidae) on Liu, S. S., and X. D. Meng. 1989. The change pattern of
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Gordon, H. T. 1984. Growth and development of insects, Sci. 9:182Ð190.
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1388 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 6
Appendix 1. Mathematical models that were used to describe the effect of temperature on the embryo development of S. discoideus
冋 冉 冊册 ⫹ e冋 冉 冊册
HL 1 l HH 1 1 developmental rate at 25⬚C et al. (1981), Carrol
䡠 ⫺ 䡠 ⫺
1⫹e R TL T R TH T (298.15⬚K), assuming no enzyme and Hoyt (1986)
inactivation; HA, enthalpy of Roy et al. (2002),
in this study we used the modiÞed formula: activation of the reaction catalyzed Kontodimas et al.
by a rate-controlling enzyme; TL, (2004)
Kelvin temp at which the rate-
controlling enzyme is half active and
half low-temp inactive; HL, change
in the enthalpy associated with low
temp inactivation of the enzyme; TH,
Kelvin temp at which the rate-
controlling enzyme is half active and
half high-temp inactive; and HH,
change in the enthalpy associated
with high-temp inactivation of the
enzyme.
e冉a ⫺ T 冊
b
a, b, c, d, f, g empirical constants
r共T兲 ⫽ T 䡠
1 ⫹ e冉 冊 ⫹ e冉 冊
d g
c⫺ f⫺
T T
Lamb et al.
r共T兲 ⫽ Rm 䡠 e 冋 冉
1
⫺ 䡠
2
T ⫺ Tm
T L 冊册2
if T ⱕ Tm
Where Rm, and Tm are as in TaylorÕs
equation. TL is a shape parameter
Lamb (1992), Roy et
al. (2002),
giving the spread of the curve Kontodimas et al.
(2004)
r共T兲 ⫽ Rm 䡠 e 冋 冉
1
⫺ 䡠
2
T ⫺ Tm
T H 冊册2
if T ⬎ Tm
For T ⬍ Tm, and, TH is a shape
parameter giving the spread of the
curve for T ⬎ Tm
Hilbert and
Logan r共T兲 ⫽ 䡠 冋 共T ⫺ T0 兲2
共T ⫺ T0 兲2 ⫹ d2
⫺ e 冉 ⫺
T L ⫺ 共T ⫺ T 0 兲
⌬T
冊 册 Where , TL, and ⌬T are as in the
Logan-6 model, T0 and d are
empirical parameters
Roy et al. (2002)
Lactin et al.
r共T兲 ⫽ e 䡠 T ⫺ e 冉 䡠 TL ⫺
TL ⫺ T
⌬T
冊 ⫹
Where , TL, and ⌬T are as in the Lactin et al (1995),
Logan-6 model, and forces the Tsai and Liu (1998),
curve to intercept the y-axis at a Roy et al. (2002),
value below zero and thus allows Kontodimas et al.
estimation of a low-temp threshold (2004)
Briere et al. r共T兲 ⫽ a 䡠 T 䡠 共T ⫺ T0 兲 䡠 冑TL ⫺ T Where T is the rearing temp (⬚C), a is Roy et al. (2002),
an empirical constant, T0 is the low Kontodimas et al.
temp development threshold, and TL (2004)
is the lethal temp threshold
In all of the models, r(T) is the mean developmental rate at temperature T (⬚C).