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A physiologically based approach for degree-day calculation in pest

phenology models: The case of the European Corn Borer (Ostrinia nubilalis
Hbn.) in Northern Italy

Article  in  International Journal of Biometeorology · July 2011

DOI: 10.1007/s00484-011-0464-z · Source: PubMed

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Int J Biometeorol (2012) 56:653–659
DOI 10.1007/s00484-011-0464-z
ORIGINAL PAPER
A physiologically based approach for degree-day calculation
in pest phenology models: the case of the European Corn
Borer (Ostrinia nubilalis Hbn.) in Northern Italy
Andrea Maiorano
Received: 31 March 2011 / Revised: 10 June 2011 / Accepted: 12 June 2011 / Published online: 2 July 2011
# ISB 2011
Abstract Phenological models based on degree-day
accumulation have been developed to support the
integrated pest management of many insects. Most of
these models are based on linear relationships between
temperature and development, and on daily time step
simulations using daily minimum and maximum temperatures.
This approach represents an approximation that does not take
into account the insect physiological response to temperature,
and daily temperature fluctuations. The objective of this work
has been to develop a phenological model for the European
corn borer (ECB) based on the insect physiological response to
temperature and running at an hourly time step. Two modeling
solutions based on the same generic compartmental system
have been compared: the first based on a physiologically based
relationship between temperature and development, and using
hourly derived temperatures as input (HNL modeling
solution); and the second based on a linear relationship
between temperature and degree-day accumulation and
using daily temperature (DL modeling solution). The two
approaches have been compared using ECB moth capture
data from the Piemonte region in Northern Italy. The
HNL modeling solution showed the best results for all
the accuracy indicators. The DL modeling solution
showed a tendency to anticipate ECB phenological
development too early. This tendency is attributable to
the linear relationship between temperature and development,
which does not take into account (1) the decline of this
relationship at high temperatures, and (2) the daily fluctuation
A. Maiorano (*)
Institute for Environment and Sustainability, Monitoring
Agricultural Resources Unit (MARS), AGRI4CAST Action,
European Commission DG Joint Research Centre,
via Fermi 2749-T.P. 483,
Ispra, VA, Italy
e-mail: andrea.maiorano@jrc.ec.europa.eu
of temperature. As a consequence, degree-days accumulation
is accelerated in the DL modeling solution and the phenological
development anticipated.
Keywords Degree-day . Physiologically based approach .
Pest phenology . European corn borer
Introduction
The European corn borer (ECB, Ostrinia nubilalis Hb.) is
a species of great concern for all maize growers in
Europe and North America. Damage and yield losses
result mainly from leaf feeding, stalk tunneling and ear
damage (Lynch et al. 1980).
The main strategy adopted to manage ECB damage is
chemical treatment by means of self-powered spraying
machines applying organophosphates, pyrethroids and other
insecticides aimed at reducing the population of young
second generation larvae. This has been demonstrated to be
an effective practice to reduce ECB impact on maize
production (Mazurek et al. 2005; Bažok et al. 2009).
Timing of the chemical treatment is critical to the integrated
pest management of ECB. In fact, the treatment must be
applied before the larvae (second generation) start boring
into the plant. Therefore, the best period for a single
application is when most of the ECB population is in the
phase of egg hatching, which should be from 10 to 14 days
after initiation of egg lying, which would be 0–4 days after
the adult flight peak (Mason et al. 1996).
Simulation models can be of great help in identifying the
right ‘application window’ for chemical treatments. The
poikilothermic characteristic (internal temperature varies
along with that of the ambient environmental temperature)
of insects like the ECB has been used to develop
654 Int J Biometeorol (2012) 56:653–659

phenological models based on degree-day accumulation out simulations for a specific goal. This work compares the
(Brown 1982; Got and Rodolphe 1989; Mason et al. 1996; performances of two modeling solutions simulating the
Trnka et al. 2007). Most of these models are based on the phenological development of the ECB. Each modeling
standard averaging method of Arnold (1960), which solution is composed of a developmental model and a
calculates degree-day using the mean temperature of the degree-day model. The developmental model, which is the
day (calculated from the maximum and the minimum same for the two modeling solutions, is the generic degree-
temperature of the day), then subtracts from that figure day compartmental system model proposed by Brown (1982).
the lower developmental temperature for the specific pest. The degree-day model of the first modeling solution is based
This is a linear method because the rate of development is on a linear approach to calculate degree-days and on daily
presumed to be a straight line related directly to temperature time step calculation (DL modeling solution). The second
(Wilson and Barnett 1983; Trudgill et al. 2005). The modeling solution is based on a non-linear physiologically
assumption of linearity has been made mainly because it based approach to calculate degree-day and on hourly time
is considered that insects are well adapted to local climatic step calculation (HNL modeling solution).
conditions, and exposure to extreme temperatures is rare in
the field (Campbell et al. 1974). Other reasons for the Insect development model
success of this kind of approach are its computation and
implementation simplicity in model systems, and low In the compartmental system approach proposed by Brown
requirement for data (minimum and maximum daily (1982), the number of individuals in each life stage at a
temperature) and parameters (base temperature). Neverthe- given time is given by:
less, this approach represents an approximation that is
adequate only if air temperatures fall within the linear
dNi
dt ¼ X  Ni1  Y  Ni
region of the organism’s thermal response: when temper- where ð1Þ
atures are outside of this region, simulations might not be
X ¼ tBi
Ei1 Bi ; if Bi  t  Ei1
adequate as all biological processes respond to temperature
in terms of three cardinal temperatures, namely the minimum,
X ¼ 0; if t < Bi or t > Ei1
the optimum, and the maximum temperatures (Régnière and
Logan 2003). Another approximation of this method is and
represented by the simulation at daily time step, instead of t  Biþ1
Y¼ ; if Biþ1  t  Ei
hourly time step: simulations at daily time step do not take Ei  Biþ1
into consideration the daily temperature fluctuations that
influence the performance of phenological models (Worner Y ¼ 0; if t < Biþ1 or t > Ei
1992). Even though hourly weather data is not always
where N is the number of individuals in life stage i at time t
available for every location, models that estimate these
(in degree days), B is the degree day accumulation at which
values by approximating diurnal temperature trends have
that stage begins to appear and E is the degree day
been developed (Campbell 1985; Goudriaan and Van Laar
accumulation for terminating that life stage. In the case of
1994; Ephrath et al. 1996; Cesaraccio et al. 2001; Stockle
the first life stage N0 (which is ‘overwintering larvae’ in the
2002) and have been shown to have a positive impact on
case of the ECB), the equation is:
degree-day model performance (Cesaraccio et al. 2001).
The objective of this work was to propose a non-linear dN0 ðt  Bi Þ
physiologically based approach for the calculation of ¼ ; t  Bi ð2Þ
dt E0  Bi
degree-days running at hourly time step, as an alternative
to the more commonly used approach based on the standard This approach allows the total number of individuals
averaging method running at daily time step. The two flowing from one life phase to another to remain constant.
approaches were compared to test their performances in According to Brown (1982), the initial number of overwinter-
predicting the adult flight peak of the ECB in the Piemonte ing larvae, N0, is an arbitrary value for phenological forecasting
region in Northern Italy. since the model is not intended for use as a density forecasting
tool. For predictive purposes, stage-specific output is converted
into percentage of peak occurrence (Brown 1982).
Materials and methods
Degree-day models
According to the definition given by Confalonieri (2009), a
modeling solution is a discrete simulation engine where The degree-day model to determine the initiation (Bi) and
different models are selected and integrated in order to carry termination (Ei) of each ECB life phase in the DL modeling
Int J Biometeorol (2012) 56:653–659
solution is based on the standard and widely used
averaging method (Arnold 1960) with a lower tempera-
ture threshold (namely base temperature, Tbase):
Tmax ðdÞþTmin ðdÞ
D ðdÞ ¼ 2  Tbase
where
Tmin ðdÞ ¼ Tbase ; if Tmin ðdÞ < Tbase
Tmax ðdÞ ¼ Tbase ; if Tmax ðdÞ < Tbase
where D°(d) is the degree-day accumulated during the day
d, Tmin(d) is the minimum temperature of the day, and
Tmax(d) is the maximum temperature of the day. This is a
linear method as the rate of development is presumed to be
a straight line directly related to temperature (Wilson and
Barnett 1983). This model, used with a Tbase of 10°C, is
the most commonly used to estimate ECB development
times (Matteson and Decker 1965; Got and Rodolphe
1989; Mason et al. 1996; Trnka et al. 2007).
The physiologically based degree-day modeling solution
(HNL) is based on the beta-function developed by Yin et al.
(1995), in the form proposed by Yan and Hunt (1999), and
adapted in this work to degree-day calculation:
0 


 TTmaxTTopt
B T ðhÞ  Tmin Tmax  T ðhÞ opt
D ðhÞ ¼ Dmax @
Topt  Tmin Tmax  Topt
where, D°(h) is the degree-days accumulated during the
hour h, Tmin is the minimum extreme temperature for insect
development, Tmax is the maximum extreme temperature
for insect development, Topt is the optimum temperature for
insect development, T(h) is the hourly air temperature, D
°max is the maximum degree-days that can be accumulated
at the optimum temperature Topt, and c is the shape
parameter. In comparison to other beta-functions (Logan
et al. 1976), this equation has the advantage that all
parameters except c are biologically meaningful. In order
to be used at an hourly time step, at each time step the
hourly degree-days are multiplied for 1/24 and then
accumulated.
Parameters and biofix
In order to compare the performances of the DL modeling
solution (parameterized with Tbase =10°C) to the HNL
modeling solution under the same conditions, the HNL
modeling solution should be parameterized by fitting to the
same laboratory data that were used to parameterize the DL.
Since the original data are unknown, parameters of the
HNL model were determined through optimization (GRG
655
solver method, Excel 2010® Solver, Microsoft®) by
minimizing the root mean square errors (RMSE) over the
points of the line describing the relationship temperature–
degree-days of the DL modeling solution in the range 10–
30°C, which is the ECB range of linear response to
temperature (Got et al. 1994). Parameters were made
varying subject to the following constraints, set according
ð3Þ
to the information found in literature: Tmin: 5–11°C (Onstad
1988; Capinera 2000); Topt: 28–35°C (Caffrey and Worthley
1927 in Got et al. 1996; Matteson and Decker 1965;
Anderson et al. 1982; Calvin et al. 1991); D°max and c no
constraints. Since no information was found available in the
literature about ECB development at temperatures over
32°C, parameter Tmax has been fixed arbitrarily as being
equal to 41 (according to Got et al. 1996).
The parameters Bi and Ei for each ECB life phenological
stage were taken from Bessin (2003) and are shown in
Table 1. Although these parameters refer to ECB popula-
tions from the central and northern United States, they had
to be used as no specific data from Italian or European
populations were found in the literature.
The date to begin accumulating degree-days (biofix) was
fixed according to the information found in the literature on
ECB diapause termination. According to the studies of
 1c Skopik and Bowen (1976), diapause termination starts after
4 days with scotophase<10 h. In the Piemonte region,
min C
A scotophase is <10 h at 8 April. Furthermore, according to
Trnka et al. (2007), if, during the period up to the stage of
the first flight initiation (flight of the overwintering
ð4Þ
generation), the temperature drops below a certain threshold
for 3 consecutive days, the thermal time calculation is
resumed from the beginning of the cycle. Trnka et al. fixed
this limit to 0.2°C. In the present work, a more generic limit
of 0°C has been preferred.
Data source and model testing
The data source used to test the models and compare their
performance consisted of dates and the numbers of moths
caught in pheromone cone traps (Coretrap®, Riff98,
Bologna, Italy) baited with sex pheromones (E and Z lures,
E:Z=97:3) and phenylacetaldehyde. Traps were placed in
collaborating maize farms fields located in the Piemonte
region in Northern Italy from 2004 to 2009 (Fig. 1). Traps
were used by the collaborating farmers to identify the best
period for the chemical treatment against the ECB through
the monitoring of the first generation adult flight (Mason et
al. 1996). Since the first generation adult flight in the
Piemonte region is usually observed around mid- to late-
July, the traps were placed at the end of June and checked
every day from 1 July to 31 August of each year. The
number of collaborating farms varied each year, for a total
figure of 16 monitored traps (Table 2). Daily temperature
656 Int J Biometeorol (2012) 56:653–659

Table 1 Accumulated degree-days (°C day−1)a necessary to reach the beginning (Bi) and end (Ei) of different European corn borer (ECB)
phenological stages (Bessin 2003)

Insect stage

Egg Larval stage Pupa Adult Flight

1 2 3 4 5

Winter generation
Bi Diapause 139 233 306
Ei 250b 311 422 500
First generation
Bi 339 417 539 633 717 789 800 900 922
Ei 550 606 672 750 828 900 961 1,078 1,217
Second generation
Bi 967 1,033 1,094 1,189 1,250 1,317
Ei 1,311 1,383 1,439 1,511 1,578 1,944
a
Values from Bessin are given in Fahrenheit degree-days. Data were converted to Celsius degree-days by multiplying the °F value by 5/9
b
Since the value Ei for the diapausing larvae (5th larval stage) is not given by Bessin, it was fixed arbitrarily according to the following rationale:
Ei for Pupae (wintering generation) minus the difference between Ei of pupae stage (first generation) and 5th instar larve (first generation)

data (maximum and minimum temperature) from 1 January less diurnal temperature function Γ(hr), is obtained based
of each year were taken from weather stations placed close on a two-term Fourier series:
to the traps. Hourly temperature data were derived using the


p »hr 2»p »hr
model by Stockle included in the AirTemperature software Γ ðhrÞ ¼ a þ b» sin þ c þ d » sin þe
component (Donatelli et al. 2010) (http://agsys.cra-cin.it/ 12 12
tools/airtemperature/help/). The model by Stockle (2002)
allows the derivation using just the daily minimum and the where hr is the time of day in hours. Reference values for
maximum temperatures. In Stockle’s model, a dimension- the coefficients are a=0.44, b=−0.46, c=0.9, d=0.11, e=

Fig. 1 Locations of European corn borer (ECB) pheromone traps in the Piemonte region in Northern Italy during the period 2004–2009
Int J Biometeorol (2012) 56:653–659 657

Table 2 Locations and years of traps and weather stations

Location Elevation (m) Monitored years

Cardè 263 2005, 2008

Carmagnola 232 2008, 2009
Ceresole d’Alba 305 2005
Chieri 300 2005, 2006
Genola 347 2005
Novara 160 2006
Racconigi 280 2005, 2006
Vigone 295 From 2004 to 2008

0.9, obtained by fitting the average of many days of hourly

air temperature data, normalized so that the minimum was
zero and the maximum was 1. Using this function, the
temperature for any time of the day (Thr, °C) is given by:
Thr ¼ T 0max  Γ ðhrÞ þ Tmin ½1  Γ ðhrÞ; if 0 < hr  5
Thr ¼ Tmax  Γ ðhrÞ þ Tmin ½1  Γ ðhrÞ; if 5 < hr  14
Thr ¼ Tmax  Γ ðhrÞ þ T 00min ½1  Γ ðhrÞ; if 14 < hr  24
where Tmax (°C) is the daily maximum air temperature,
Tmin (°C) is the daily minimum air temperature. The
superscripts ' and " represent the previous day and the next
day, respectively.
The two modeling solutions (DL and HNL) were
compared for their capacity to simulate the peak (the day
with the highest number of moths caught) of first generation
adult flight by evaluating their accuracy using RMSE
(dimensionless, 0 to+∞, optimum=0; Fox 1981), modelling
efficiency (EF, dimensionless, −∞ to 1, optimum =1; where a
negative value indicates that the average of observations is a
better predictor than the model; Nash and Sutcliffe 1970),
and the coefficient of residual mass (CRM, dimensionless,
−∞ to+∞, optimum=0, where a positive value indicates
model underestimation, and negative indicates model
overestimation; Loague and Green 1991).
Results and discussion
Following optimization, the optimal values for the parameters
of the degree-day model of the HNL modeling solution were:
Tmin =8.20°C, Topt =35.00°C, D°max =22.06, and c=1.47.
Figure 2 shows the predictive capability of the two
modeling solutions. Modeling solution HNL shows the best
results for all accuracy indicators. The RMSE is higher in
the case of the DL modeling solution, meaning that the
difference between observed and predicted values is higher
in this model than in the HNL modeling solution. The EF is
negative in the case of the DL modeling solution, meaning
Fig. 2 Observed vs predicted day (days from 1 January) of
occurrence of the first generation adult flight peak for the HNL
(hourly, non-linear) and DL (daily, linear) modelling solutions.
Accuracy indicator values are shown
that the average of adult flight observations is a better
predictor than the model. The CRM indicates a very slight
overestimation tendency for the HNL modeling solution,
while in the case of the DL modeling solution it shows an
evident tendency towards underestimation: this is the main
difference between the two modeling solutions. In fact, Fig. 2
shows that while the data points of the HNL modeling
solution are more homogenously distributed around the 1:1
line, all the data points of the DL model are under the 1:1
line, which means that the model DL tends to underestimate
the peak. The reason for this difference depends on the DL
degree-day calculation, which is based on the linear
relationship between temperature and development which
does not take into consideration (1) the temperature stress
induced by environmental temperatures higher than the
insect optimum developmental temperature, or (2) the daily
temperature fluctuations. As a consequence, in accordance
with the findings of Worner (1992), the adult flight peak is
underestimated because degree-day accumulation in the DL
model is accelerated. Figure 3 gives a practical explanation
of the effects of using hourly temperatures instead of daily
temperatures, and shows a physiologically based relationship
with temperature. In Fig. 3, the hourly temperatures derived
from the daily temperatures registered in Novara on 22 July
2006 are shown with the degree-day calculated for each hour
using the HNL approach. The grey area shows temperatures
over the optimum temperature for development (Topt =35°C).
The hourly degree-day (HNL approach) follows the pattern of
the hourly temperature with the exception of the range of
temperatures exceeding the optimum temperature: in this area,
the more the temperature increases, the more the hourly
degree-day decreases. In this way, in contrast to the DL
658
Fig. 3 Hourly temperatures (derived using Stockle’s model) and
calculated degree-days for each hour for the Novara location, 22 July
2006. Grey area Temperatures over the optimum temperature for ECB
development (Topt = 35°C). Registered minimum and maximum
temperatures are shown. Degree-days accumulated for this day using
the HNL and the DL modeling solutions are shown
approach, the HNL approach takes into account (1) temperature
fluctuations, and (2) stressful conditions determined by high
temperatures. As a result, the degree-days calculated for this
day in Novara using the DL model are 19.84°C day−1, while
using the HNL model the degree-days are 17.37°C day−1: a
difference of 2.47°C day−1 for just 1 day.
Other methods for estimating degree-day accumulations
are frequently and successfully employed in the field. These
methods include procedures that take into account the daily
temperature fluctuation, assuming that a daily temperature
profile can be represented by a specific geometrical shape.
This can be a daily symmetrical curve (single triangle and
single sine methods) or a double curve based on half-day
curves (double triangle and double sine methods) (University
of California, www.ipm.ucdavis.edu/WEATHER/ddconcepts.
html). In accordance with the findings in the present work,
Roltsch et al. (1999) demonstrated that these methods give
better estimation compared to the averaging method.
In some cases, cut-off method techniques (horizontal,
vertical, intermediate) are taken into account in order to
consider the negative effects of high temperatures. The
cutoff method refers to the manner in which the degree-day
calculation area is modified in relation to the upper
threshold (University of California, www.ipm.ucdavis.edu/
WEATHER/ddconcepts.html). The horizontal cut-off meth-
od assumes that development continues at a constant rate at
temperatures in excess of the upper threshold. This can be
considered an acceptable assumption for temperatures that
are between the cut-off temperature and the physiological
optimum temperature of development, but is incorrect for
temperatures higher than the optimum temperatures. The
vertical cut-off method does not consider development over
the cut-off temperature, thus it does not consider that
development continues increasing until the optimum tem-
Int J Biometeorol (2012) 56:653–659
perature and then slows down until the maximum temper-
ature. The intermediate cut-off method considers that
development slows, but does not stop, at temperatures
above the upper threshold. This approach can be considered
an approximation of the physiological response to temper-
ature, but the underlying assumptions are not coherent with
the insect physiological response to temperature. Firstly, it
assumes that development starts decreasing after the cut-off
temperature, which can be lower by 3–5°C than the
physiological optimum temperature for development
(Gutierrez 1996). Secondly, it assumes that the develop-
mental decrease mirrors developmental increase, without
taking into account that, after the optimum temperature,
development may decrease very rapidly until the physio-
logical maximum temperature (Régnière and Logan 2003).
Roltsch et al. (1999) concluded also that the use of these
methods (triangle and sine methods, and cut-off techniques)
requires specific consideration be given to the time of the year,
geographical location and biology of the organism under study.
The use of a physiological approach like that presented here,
consistent with the biology of the organism taken into
consideration, is expected to reduce these problems, above all
under extreme events. Consequently, the physiological approach
is expected to give better degree-days estimations under very
different conditions. Nevertheless, this should be verified
through the application of this approach with data from
different geographical locations and climate conditions.
Conclusions
The proposed HNL modeling solution to calculate degree-
days based on a physiological approach proved accurate in the
explored conditions, reproducing correctly the appearance of
the adult flight peak. The values obtained for all the accuracy
indicators indicated that the HNL modeling solution was more
accurate than the DL modeling solution. These results have
indicated that the use of a physiologically based response to
temperature and of hourly time step may increase the accuracy
of pest simulation models based on degree-day accumulation.
It is expected that differences between the two approaches
increase during warm years and in studies conducted under
climate change scenarios: the more the occurrence of extreme
temperatures over the organism optimum temperature, the
higher the difference. In fact, in the case of the linear model, the
higher the temperature, the more the degree-days accumulated
daily. On the contrary, in the case of the physiologically based
approach, the more the temperature was above the optimum
temperature, the less the degree-days accumulated.
Further studies using measured hourly temperatures could
be interesting to analyze, indirectly through their effect on
temperature, the effects of daily short rain events or short
cloud coverage on the hourly degree-day calculation.
Int J Biometeorol (2012) 56:653–659
In conclusion, the objective of this paper has been to
suggest the use of a physiologically based approach for the
degree-day calculation as a more adequate approach to
simulate the physiological response of insects to tempera-
ture. The application to the phenological development of
ECB showed very good results that need to be confirmed
by further studies with more data and, above all, under
more environmental and climatic conditions.
Acknowledgments Moths caught for data used for this work were
collected during a research period at the University of Turin,
Department of Agronomy, Forest and Land Management. This
research was supported by a Marie Curie Intra European Fellowship
within the 7th European Community Framework Programme.
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