PHYSIOLOGICAL ECOLOGY

Modeling Embryo Development of Sitona discoideus Gyllenhal

(Coleoptera: Curculionidae) Under Constant Temperature
ABBAS ARBAB,1 DIMITRIS C. KONTODIMAS,2 AND MARK R. MCNEILL3

Environ. Entomol. 37(6): 1381Ð1388 (2008)

ABSTRACT The alfalfa root weevil, Sitona discoideus (Coleoptera: Curculionidae), is an important
pest of alfalfa. The developmental rates of the embryo development were recorded at eight constant
temperatures ranging from 8.5 to 30⬚C. Using 10 models (1 linear and 9 nonlinear), we evaluated the
relationship between constant temperature and developmental rate. Embryo development was short-
est (8.5 d) and longest (69 d), at 28 and 8.5⬚C, respectively. The threshold temperature (T0) and the
thermal constant (K) were estimated using linear regression to be 4.7⬚C and 207.7 DD, respectively.
The two most efÞcient nonlinear models, the Lactin and the Sharp and DeMichele, gave estimates of
Tmin and Tmax of 4.4 and 3.9 and 30.0 and 30.9⬚C, respectively. This information has potential
application in predicting the suitability and optimal time of release of an egg parasitoid of S. discoideus.

KEY WORDS Sitona discoideus, temperature, embryo development, developmental rate, modeling

Alfalfa (Medicago sativa L.) is the father of herbs and
the queen of forage. It is widely cultivated on ⬎640,000
h in Iran. Of the 14 species of Sitona spp. (Coleoptera:
Curculionidae) that are reported to feed on alfalfa,
only a few such as Sitona discoideus are economically
important (Modarres Awal 1994, Arbab and Boru-
mand 2002). The alfalfa root weevil, Sitona discoideus
Gyllenhal (Coleoptera: Curculionidae), is a native
pest of alfalfa in Iran that is distributed throughout the
country where alfalfa is grown (Behdad 1993). Re-
search in New Zealand found that feeding by the
larvae had a major effect on the sustainability of alfalfa,
resulting in an average decline in crop growth of 40%
per year (Goldson and French 1983, Goldson et al.
1985). Adult feeding damage is characterized by
notching of the leaßet edges, which can cause severe
damage to seedlings, especially when plant growth
conditions are unfavorable. Eggs are laid in the mid-
spring on the soil surface near, or less often, attached
to the alfalfa plants. First-instar larvae emerge and
borrow into the soil to locate the root nodules on
which they feed, destroying the N2-Þxing Rhizobium
bacteria. As the larvae mature and nodules are con-
sumed, the plant rootlets and root hairs are subse-
quently attacked (Aeschlimann 1986). There are Þve
larval instars (Frampton 1986). This insect is univol-
tine and aestivates seasonally in Iran (Behdad 1993),
with adult densities reaching 50 Ð70 weevils/m2 during
pest outbreak years. Elimination of root tubercles by
1 Entomology Research Laboratory, Islamic Azad University, Take-
stan Branch, Takestan, Iran.
2 Corresponding author: Department of Entomology and Agricul-
tural Zoology, Benaki Phytopathological Insitute, 8 St. Delta Street,
145 61 KiÞssia, Greece (e-mail: dckontodimas@hotmail.com).
3 AgResearch Lincoln, Private Bag 4749, Christchurch 8140, New
Zealand.
larvae decreases the ability of the plant to Þx nitrogen,
therefore reducing the accumulation of nitrogen in
plants and soil (Petrukha 1969). Larval damage is more
commonly apparent in older alfalfa stands.
The period between egg hatch and occupation of
root nodules by Þrst-instar larvae is probably the most
vulnerable part in the life cycle: larvae that do not
locate root nodules quickly die of starvation (Johnson
et al. 2007). Understanding the inßuence of temper-
ature on development rate of poikilotherms allows for
the prediction of incubation time of the egg stage
(Hamel et al. 1997). This relationship between insect
development and temperature represents an impor-
tant ecological variable for modeling population dy-
namics of insects (Jarosik et al. 2002). Understanding
temperature-dependent development can be used for
accurate forecasting and phenological prediction and
is paramount to many successful pest management
programs (Tobin et al. 2001). For example, Anaphes
diana (Girault) (Hymenoptera; Mymaridae) is a po-
tential biological control agent against S. discoideus in
Iran. A. diana is an egg parasitoid abundant in the
Mediterranean region (Aeschlimann 1986) and, al-
though introduced into Australia, establishment was
never conÞrmed (Aeschlimann et al. 1989). The suit-
ability of A. diana as a biological control agent is
dependent on temperature and other ecoclimatic con-
ditions (Worner et al. 1989) and therefore a key step
contributing to the success of a biological control
introduction would be to determine the degree of
synchrony between A. diana developmental times
with that of S. discoideus eggs.
Many models are available to describe mean devel-
opmental times or rates of development as a function
of temperature: from the earliest and most common
used linear or day-degree model, a concept that dates

0046-225X/08/1381Ð1388$04.00/0 䉷 2008 Entomological Society of America

1382 ENVIRONMENTAL ENTOMOLOGY Vol. 37, no. 6

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

LBT, lower base development threshold. Discussion

Temperature is a major factor determining insect
decreased with increasing temperatures within the egg development (Johnson et al. 2007), although the
range of 8.5Ð28⬚C. At 8.5⬚C, it took 69.01 ⫾ 0.92 (SE) relationship between arthropod developmental rate
d for eggs to hatch and only 8.46 ⫾ 0.14 d at 28⬚C. and temperature has generally been shown to be non-
Above 28⬚C, development slowed so that, at 30⬚C, linear. Typically, the development rate curve shows an
times are equivalent to those obtained at 26⬚C. increase from zero at a low temperature threshold,
Linear Model. As shown by the high coefÞcient of reaches a maximum at an optimal temperature, and
determination (r2 ⫽ 0.9784) obtained for embryo de- decreases rapidly to zero at an upper lethal temper-
velopment of S. discoideus, the linear model adequately ature. Data from our study Þt this relationship. The egg
described the lower temperature threshold tb ⫽ 4.7⬚C development period of S. discoideus was longest at
and degree-days required for development (207.7 DD) 8.5⬚C was fastest at 29⬚C and showed an increase at
(Table 2). The linear regression as applied to the data set 30⬚C. The temperature optimum, where the minimum
recorded in this study is shown in Fig. 1. developmental times were recorded, was within the
Model Evaluation. All Þtted parameters were esti- range of 28.5Ð29.9⬚C (Table 3). These are common
mated by regression analysis, whereas some other temperature conditions that the weevil experienced
measurable parameters were calculated by solving the during late of spring and summer in the Qazvin region.
equations (tmin in Linear and Lactin model) or their In a study on S. crinitus Herbst, El Damir et al.
Þrst derivatives (topt). The values of estimated coef- (2004) found that the embryo development period
Þcients and measurable parameters of the models are was the shortest at 30⬚C (7 d) and longest at 8⬚C (69
presented in Table 3. The inßuence of temperature on d), whereas at 5⬚C, no eggs hatched over the 3-mo
the embryo developmental rate Þtted by each model period of the experiment. Conversely, Melamed
is shown in Fig. 1. With the exception of the Briere (1966) reported a temperature threshold for egg de-
model, the R2 values obtained from the logistic model velopment of 5.8 for S. crinitus. The temperature
was low compared with those of the other nonlinear threshold for egg development of S. lividips, S. hispidu-
models (Table 3) and values of RSS were high, sug- lus, and S. lineatus was reported to be 4.8, 4.6, and
gesting that this model does not describe the observed 6.5⬚C, respectively (Melamed 1966). Grieb (1976)
data well. However, high values of R2 and low values found that eggs of S. lineatus failed to develop when
of RSS for other models (Table 3) indicate a better Þt incubated at 27⬚C if they were held for 70 d at 4⬚C,
to the observed development data set. although 90% hatched if they were held only 56 d at
The lower temperature threshold calculated by this low temperature. This indicated that 4⬚C must be
each model generally ranged between 3.9 and 4.7⬚C. close to a lower lethal threshold. Similar research on
The exceptions were the Hilbert and Logan model, S. lineatus L. by Lerin (2004) examining egg devel-

Logistic Analytis Linear Sharpe and DeMichele Stinner

0,15 0,15 0,15
0,15 0,15

0,10 0,10 0,10

0,10 0,10

0,05 0,05 0,05

0,05 0,05

0,00 0,00 0,00 0,00

0,00
0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35
0 5 10 15 20 25 30 35

Lamb Logan-6 Hilbert and Logan Lactin Briere

0,15 0,15
0,15
0,15
0,15

0,10 0,10
0,10 0,10
0,10

0,05 0,05 0,05 0,05

0,05

0,00 0,00 0,00 0,00 0,00

0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 0 5 10 15 20 25 30 0 5 10 15 20 25 30 35 0 5 10 15 20 25 30 35

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

Model Parameters Value ⫾ SE R2/RSS

Logistic k 0.116373 ⫾ 0.017540 0.9153
a 3.067982 ⫾ 0.746798 0.000408
b 0.183446 ⫾ 0.062131
Stinner c 0.166652 ⫾ 0.076373 0.9684
a 2.884306 ⫾ 0.346334 0.000265
b ⫺0.129397 ⫾ 0.050389
topt 29.037736 ⫾ 0.830781
a1 18.718668 ⫾ 0.000000
b1 ⫺0.679245 ⫾ 0.000000
Logan-6 ⌿ 0.014279 ⫾ 0.005030 0.9547
␳ 0.077415 ⫾ 0.018301 0.000380
TL (⫽tmax) 31.704057 ⫾ 1.940790
⌬T 1.355864 ⫾ 1.714231
topt 28.5
Analytis a 0.013721 ⫾ 0.000556 0.9684
tmin 8.229450 ⫾ 0.599315 0.000319
tmax 30.000090 ⫾ 0.000005
n 0.680310 ⫾ 0.013526
m 0.011551 ⫾ 0.004199
topt 29.8
Sharpe and DeMichele a 246.153198 ⫾ 0.112017 0.9789
(tmin and tmax are b 1014.969063 ⫾ 2.448041 0.000177
calculated c 689.878680 ⫾ 0.000000
graphically) d 14203.310779 ⫾ 11.180908
f 1008.233423 ⫾ 0.000000
g 251.432022 ⫾ 0.000000
topt 29.7
tmin ⬇3.9
tmax ⬇30.9
Lamb Rm 0.106783 ⫾ 0.005646 0.9567
Tm(⫽topt) 29.22262 ⫾ 0.000000 0.000361
T␴H 11.272893 ⫾ 0.839254
T␴L 1.853074 ⫾ 1.003527
Hilbert and Logan ⌿ 0.326601 ⫾ 0.031361 0.9757
d 42.145626 ⫾ 7.694335 0.000203
TL (⫽tmax) 32.565342 ⫾ 5.773034
⌬T 0.023153 ⫾ 0.000000
T0 (⫽tmin) ⫺2.504914 ⫾ 0.757767
topt 29.9
Lactin ␳ 0.004429 ⫾ 0.000291 0.9802
TL (⫽tmax) 30.075077 ⫾ 0.014323 0.000166
⌬T 0.019551 ⫾ 0.000000
␭ ⫺1.019721 ⫾ 0.006482
tmin 4.4
topt 29.9
Briere a 0.000074 ⫾ 0.000011
To (⫽tmin) 4.434771 ⫾ 2.603392 0.9152
TL (⫽tmax) 32.377358 ⫾ 0.000000 0.000758
topt 26.5

opment times over a range of temperatures, and
using the Sharpe and DeMichele model, calculated
an optimum temperature for egg hatch and devel-
opment of 29⬚C.
Research elsewhere has highlighted the effect of
temperature on embryo development rates for Sitona
species (Andersen 1931, Melamed 1966). Melamed
(1966) reported that the percentage of egg hatching
for four species of Sitona (S. hispidulus, S. lividips, S.
lineatus, and S. crinitus) fed on pea leaßets was re-
duced when temperature exceeded 25⬚C. In Finland,
the embryo development period of 11 species of Sitona
including S. crinitus was 29 Ð32 d at a mean tempera-
ture of 11.5Ð12⬚C (Markkula 1959). The incubation
period of S. hispidulus was 21 d in summer and 150 Ð200
d in winter (Underhill et al. 1955).
The curvilinear developmental rateÐtemperature
relationship for this species is typical of many other
insects and mites (Briere and Pracros 1998). Nonlin-
earity of the relationship between developmental rate
and temperature conÞrms the hypothesis that the rate
processes that control development in S. discoideus is
nonlinear (Lamb 1992).
Among the models that estimated lower tempera-
ture threshold, all models except for Analytis and
Hilbert and Logan calculated tmin values of between
3.9 and 4.7⬚C that are close to the observed values. The
optimum temperature and upper temperature thresh-
olds estimated by the majority of the models were
28.5Ð29.9 and 30 Ð32.6⬚C, respectively.
Our results suggest that, among the Þve models
(Analytis, Sharpe and DeMichele, Hilbert and Logan,
Lactin, and Briere) that estimated all three parameters
(tmin, topt, tmax), the Sharpe and DeMichele and Lactin
models more accurately described the relationships
between egg developmental rate and temperature.
December 2008 ARBAB ET AL.: EMBRYO DEVELOPMENT OF S. discoideus
The biophysical model of Sharpe and DeMichele
(1977) describes a nonlinear response between de-
velopmental rates at low and high temperatures, as
well as a linear response at intermediate temperatures
(Medeiros et al. 2004). For this reason, Wagner et al.
(1984) and Fan et al. (1992) considered that this
nonlinear model better describes the effect of con-
stant temperatures on insects development. This
model was applied and evaluated by Gould and El-
kinton (1990), Orr and Obrycki (1990), Fan et al.
(1992), Morales-Ramos and Cate (1993), Judd and
McBrien (1994), Harari et al. (1998), Medeiros et al.
(2003, 2004), and Lerin (2004) and was considered
appropriate for determination of developmental rates
studied. However, the disadvantage of the biophysical
model is the relatively high number of the parameters
(six) required to generate a valid output.
Lactin et al. (1995) stated that LactinÕs model is
preferable when temperatures are frequently near the
lower development threshold, which is the case in
early spring in Qazvin province. The Lactin model was
also found to be highly efÞcient in modeling devel-
opmental rate of some insects such as the rice root
aphid, Rhopalosiphum rufiabdominalis (Tsai and Liu
1998), Lobesia botrana (Briere and Pracros 1998),
Stethorus punctillium and its prey Tetranychus mc-
danielli (Roy et al. 2002), Alabama argillacea (Medei-
ros et al. 2003), soybean aphid, Aphis glycines (Mc-
Cormack et al., 2004), Sitona lineatus (Lerin 2004),
Nephus includes and N. bisignatus (Kontodimas et al.
2004), striped cucumber beetle, Acalymma vittatum
(Ellers-Kirki and Fleischer 2006), and Aphis pomi
(Arbab et al. 2006).
This work describes the identiÞcation of appropri-
ate models to describe the development and eclosion
of Qazvin populations of S. discoideus larvae over a
range of temperatures generally prevailing in this re-
gion, and from which the key bioclimatic parameters
for the egg stage of this pest could be estimated.
Nevertheless, more knowledge of development at
temperatures close to the lower development thresh-
old during periods of cold temperatures is required to
validate the results reported here (Liu and Meng
1999).
The relationship between temperature and devel-
opmental parameters detailed in our study should
prove useful for predicting S. discoideus infestations,
although further research is required to validate the
Lacitn and the Sharp and DeMichele models against
Þeld observations. Moreover, both models provide a
useful tool for incorporation into a putative biological
control program targeting the egg stage of S. discoi-
deus, with the parasitoid A. diana. Parasitoid develop-
ment that is synchronized with its host offers an im-
proved opportunity for success compared with one
where there is a divergence between host and para-
sitoid both in development rates and temperature
thresholds (Hemachandra et al. 2007, Krugner et al.
2007). Development rate information can also be in-
corporated into a model to determine the optimal time
of release of A. diana.
1385
Acknowledgments
The authors thank three anonymous reviewers for edito-
rial comment on an earlier draft of this manuscript.
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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

Model Equation Commentary Reference

Logistic r共T兲 ⫽ k/共1 ⫹ e共a ⫺ b 䡠 T兲 兲 Where a, value which deÞnes the Davidson (1942, 1944),
place of the regression line in Analytis (1977)
relation to the x-axis; b, slope of the
curve line; k, constant deÞning the
upper limit of the sigmoid line; T,
temp
Linear r共T兲 ⫽ a ⫹ b 䡠 T a is developmental rate at T ⫽ 0⬚C and Campbell et al. (1974),
b is the slope of the regression line. Lamb (1992), Roy et
The low development threshold, ␪ al. (2002)
(⬚C) is calculated as ␪(⬚C) ⫽ ⫺a/b,
and the thermal constant, K (day-
degrees), from birth to adult as K ⫽
1/b
Stinner et al. C Where C, a, b, a1, and b1, empirical Kontodimas et al.
r共T兲 ⫽ if T ⱕ topt constants (2004)
1 ⫹ e共a ⫹ b 䡠 T兲
C
r共T兲 ⫽ if T ⬎ topt
1 ⫹ e关a 1 ⫹ b 1 䡠 共2 䡠 t opt ⫺ T兲兴 T L ⫺ T
Logan et al.
r共T兲 ⫽ ␺ 䡠 关e␳ 䡠 T ⫺ e ␳ 䡠 T L ⫺ ⌬T 兴冉 冊 Where ␺ is the max developmental Logan (1976), Roy et
rate, ␳ is a constant deÞning the rate al. (2002),
at optimal temp TL is the ethal max Kontodimas et al.
temp, and ⌬T is the temp range over (2004)
which physiological breakdown
becomes the overriding inßuence
Analytis r共T兲 ⫽ a 䡠 共T ⫺ Tmin 兲n 䡠 共Tmax ⫺ T兲m Where a, n, and m are constants, and Analytis (1977),
Tmin and Tmax are the lower and Kontodimas et al.
upper temp thresholds (2004)
Sharpe and
De-Michele
r共T兲 ⫽
RHO25 冉 冊 T
298.15
䡠 e 冋 冉HA
R
䡠
1
298.15
⫺
1
T
冊册 Where R, universal gas constant (1.987
cal degree⫺1mole⫺1); RHO25,
Sharpe and DeMichele
(1977), SchoolÞeld

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. T␴L 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, T␴H 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).