Development of the predatory pentatomid Picromerus bidens (L.) at various constant temperatures

Abstract

Development of the palearctic predatory heteropteran Picromerus bidens was assessed at constant temperatures (15, 18, 20, 23, 27, 32 and 35±1°C) using larvae of the cotton leafworm Spodoptera littoralis as prey. All experiments were done at a 12:12 (L:D) h photoperiod and 65±5% relative humidity. The predator developed to maturity between 18 and 32°C, but eggs failed to hatch at 15 and 35°C. Duration of development of the different immature stages of P. bidens decreased with increasing tempera-ture from 18 to 32°C. The total development time for P. bidens ranged from 24.8 days at 32°C to 85 days at 18°C. The estimated lower thresholds for development varied between life stages and ranged from 8 to 16°C. The thermal requirements for development of the egg stage, completion of the nymphal period and total development of P. bidens were estimated to be 208, 270 and 500 degree-days with lower thresholds of 10.5, 13.8 and 12.2°C, respectively. Upper threshold temperature for development of eggs and nymphal stages was estimated to be between 32 and 35°C. Egg hatch percentage, nymphal survival and sex ratio were deter-mined at each temperature. The data reported here should be helpful in predicting development of P. bidens populations in the field and offer valuable basic information for the use of this native predator in biological control programs.

Full text

Belg. J. Zool., 138 (2) : 135-139 July 2008
Development of the predatory pentatomid Picromerus bidens (L.)
at various constant temperatures
Kamran Mahdian1,2, Luc Tirry1 & Patrick De Clercq1*
1Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure
Links 653, B-9000 Ghent, Belgium
2Department of Crop Protection, Faculty of Agriculture, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran
Corresponding author : * Patrick De Clercq, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University,
Coupure Links 653, B-9000 Ghent, Belgium. E-mail: patrick.declercq@ugent.be
ABSTRACT. Development of the palearctic predatory heteropteran Picromerus bidens was assessed at constant temperatures (15,
18, 20, 23, 27, 32 and 35±1°C) using larvae of the cotton leafworm Spodoptera littoralis as prey. All experiments were done at a
12:12 (L:D) h photoperiod and 65±5% relative humidity. The predator developed to maturity between 18 and 32°C, but eggs failed
to hatch at 15 and 35°C. Duration of development of the different immature stages of P. bidens decreased with increasing tempera-
ture from 18 to 32°C. The total development time for P. bidens ranged from 24.8 days at 32°C to 85 days at 18°C. The estimated
lower thresholds for development varied between life stages and ranged from 8 to 16°C. The thermal requirements for development
of the egg stage, completion of the nymphal period and total development of P. bidens were estimated to be 208, 270 and 500
degree-days with lower thresholds of 10.5, 13.8 and 12.2°C, respectively. Upper threshold temperature for development of eggs
and nymphal stages was estimated to be between 32 and 35°C. Egg hatch percentage, nymphal survival and sex ratio were deter-
mined at each temperature. The data reported here should be helpful in predicting development of P. bidens populations in the field
and offer valuable basic information for the use of this native predator in biological control programs.
KEY WORDS : Picromerus bidens, Pentatomidae, predator, temperature thresholds, thermal requirements
INTRODUCTION
Picromerus bidens (Linnaeus) is a predatory pentato-
mid, which is widely distributed in the western Palearctic
region. In the Nearctic region this species has been
recorded from more than 180 locations in North America
since its introduction some time before 1932 (LARIVIÈRE
& LAROCHELLE, 1989). This pentatomid is associated with
a wide range of habitats including wet and dry areas such
as bushes, fields and forests, where it prefers shrubby
areas rich in woody plants (trees or bushes), but it is also
found on herbaceous plants (SCHUMACHER, 1911; MAYNÉ
& BRENY, 1948; SOUTHWOOD & LESTON, 1959). P. bidens
is a polyphagous predator that preys on larvae of many
Lepidoptera, Coleoptera and leaf-eating Hymenoptera,
and more rarely on pupae and adults of soft-bodied
insects (JAVAHERY, 1986; LARIVIÈRE & LAROCHELLE,
1989). Several authors have emphasized the potential of
P. bidens for reducing populations of insect pests in a
variety of ecosystems (see DE CLERCQ, 2000).
P. bidens may be a possible alternative for the exotic
species Podisus maculiventris, (Say) which is indigenous
throughout North America. There have been multiple
introductions of this species in Europe since the 1930s for
classical biological control of the Colorado potato beetle,
Leptinotarsa decemlineata (Say) but the predator has
never succeeded in establishing. From the late 1990s up
to recently, P. maculiventris was commercially available
in Europe for augmentative biological control of caterpil-
lar pests in greenhouse crops. However, commercializa-
tion of this exotic polyphagous predator was discontinued
as a result of growing environmental concerns (VAN LEN-
TEREN et al., 2003). Considerable knowledge exists on the
seasonal cycle of Picromerus bidens (MAYNÉ & BRENY,
1948; JAVAHERY, 1986; MUSOLIN, 1996 ; MUSOLIN &
SAULICH, 2000) but information regarding the effect of
climate on the bio-ecology of this species is still scarce.
Understanding the relationship between temperature and
development of arthropod predators is essential for accu-
rately predicting natural enemy interactions with pests
(ROSEN & HUFFAKER, 1983; OBRYCKI & KRING, 1998;
NECHOLS et al., 1999). Although temperature is only one
of the ecological factors in predator-prey dynamics, it is a
primary factor affecting the ability of a predator to regu-
late pest populations. The objective of the current study
was to determine the temperature-dependent development
of the different immature stages of P. bidens at constant
temperatures.
MATERIALS AND METHODS
A culture of P. bidens was started with eggs originating
from a laboratory colony at the Department of Entomol-
ogy and Biological Control, All-Russian Research Insti-
tute for Plant Quarantine, Moscow, Russia. The colony of
P. bidens used in this study was maintained at 23±1°C,
65±5% relative humidity (RH), and a 12:12 (L:D)h pho-
toperiod. The food of the stock colony of the predator
consisted mainly of larvae of the cotton leafworm Spo-
doptera littoralis (Boisduval) reared on an artificial diet
modified from POITOUT & BUES (1970).
Eggs of P. bidens undergo obligatory diapause and
need to be stored at low temperatures (2-3°C) for at least
one month to initiate embryonic development. Egg
masses that underwent such cold treatment were used in

Kamran Mahdian, Luc Tirry & Patrick De Clercq
136
the experiments on development. Development of P.
bidens was monitored under the following constant tem-
peratures: 15, 18, 20, 23, 27, 32 and 35±1°C. All experi-
ments were done at a 12:12 (L:D) h photoperiod and
65±5% RH. At each temperature, development of the egg
stage was monitored using 100 eggs and development of
nymphs was followed starting with 40 first instars. Egg
batches were taken from cold storage, transferred to plas-
tic Petri dishes (9cm diameter) and placed in incubators at
each of the test temperatures. Development of incubated
eggs was monitored daily and hatching recorded. Newly
emerged nymphs (less than 12h old) of P. bidens were
transferred to individual Petri dishes (9cm diameter) lined
with absorbent paper. A moist paper plug fitted into a
small plastic cup provided water. Nymphs were offered
prey from the second instar onwards because, as in other
asopines, first instars of P. bidens do not feed and only
take up water (DE CLERCQ, 2000). Upon reaching the sec-
ond instar, the predator was fed daily with an excess of
fifth instars of the cotton leafworm S. littoralis. Nymph
development and survival of P. bidens were monitored on
a daily basis. Sex was determined when the individuals
reached the adult stage.
Development rate of each immature stage of P. bidens
was calculated using the reciprocal of the average devel-
opment duration (i.e., 1/d). The relationship between
development rate and temperature was described by a lin-
ear regression model (ARNOLD, 1959) fit to the linear sec-
tion of the data points. Temperature points above and
below the linear portion of the development rate curve
were not used to estimate thermal requirements (in
degree-days or DD) or lower threshold temperatures. The
lower temperature thresholds for each of the immature
stages of P. bidens were determined as the x-intercept (t=-
a/b) (ARNOLD, 1959) and the degree-day requirements (K)
were determined as the inverse of the slope (k=1/b) of the
regression lines (CAMPBELL et al., 1974).
TAB L E 1
Duration (days) of the immature stages of P. bidens at five constant temperatures
Stag e Tem p e r a t ure
18°C 20°C 23°C 27°C 32°C
Egg 32.62±0.48 22.70±0.30 14.44±0.34 12.78±0.15 10.14±0.10
First instar 8.35±0.20 5.56±0.07 4.61±0.08 3.43±0.09 2.00±0.00
Second instar 9.15±0.22 7.54±0.12 6.07±0.19 4.56±0.16 3.20±0.07
Third instar 8.52±0.27 7.50±0.23 6.02±0.28 4.56±0.16 2.82±0.09
Fourth instar 9.46±0.29 8.23±0.25 6.45±0.16 3.79±0.10 2.82±0.10
Fifth instar 13.13±0.24 11.23±0.12 9.84±0.14 6.30±0.28 4.18±0.08
Total nymph period 47.60±1.08 39.80±0.46 32.40±0.42 19.26±0.34 14.80±0.21
Total development 85.00±1.39 62.43±0.59 47.32±0.50 35.77±0.46 24.75±0.27
0
0.01
0.02
0.03
0.04
0.05
0 10203040
Temperature (°C)
Developmental rate
Fig. 1. – The relationship between temperature and development rate for total
development (egg-adult) of P. bidens at constant temperatures. The line repre-
sents the linear regression of the data between 18 and 32°C.

Effect of temperature on development of P. bidens 137
RESULTS
Picromerus bidens developed to adulthood between 18
and 32°C, but eggs failed to hatch at 15 and 35°C, dying
without any observed evidence of embryonic develop-
ment. Therefore, the temperatures tested encompassed the
range of constant temperatures allowing complete devel-
opment of the predator. The total time for development of
P. bidens ranged from 24.8 days at 32°C to 85 days at
18°C. Linear regression equations of development rate of
each life stage versus temperature are given in Table 1.
Fig. 1 shows the relationship between temperature and
development rate for the total development (egg-adult) of
P. bidens. High coefficients of determination (r²>0.97,
P<0.001) indicated a good linear model fit in all cases.
The lower development threshold values and degree-day
requirements for each life stage of P. bidens are presented
in Table 2. The estimated lower thresholds for develop-
ment varied between life stages and ranged from 8 to
16°C. The thermal requirement for development of the
egg stage after cold storage was 208DD with a lower
threshold of 10.5°C. The thermal requirement for comple-
tion of the nymphal period was 270DD with a lower
threshold of 13.8°C. Total development of P. bidens
required 500DD with a lower threshold of 12.2°C. Rapid
decline of development rate between 32 and 35°C sug-
gests that the upper threshold temperature for develop-
ment (i.e. the temperature above which the rate of devel-
opment starts decreasing) of eggs and nymphal stages
was within this temperature range.
Egg hatch ranged from 65 to 86% at temperatures
between 18 and 23°C and averaged 84 and 69% at 27 and
32°C, respectively (Table 3). Survival of nymphs
increased from 28 to 69% with increasing temperature
from 18 to 23°C, and subsequently decreased to 59% as
temperature further increased up to 32°C (Table 3). Sex
ratios of P. bidens adults ranged from 1 male: 0.6 female
to 1 male: 1.7 female at the tested temperatures.
DISCUSSION
MAYNÉ & BRENY (1948) reported that the second, third
and fourth nymphal stadia of P. bidens are of equal
length, about 12 to 14 days each, whereas the fifth sta-
dium takes somewhat longer and total nymph time is
about two months under summer field conditions in Bel-
gium. These authors also noted that 30 to 35 days are
required for development of P. bidens on larvae of Ephes-
tia kuehniella Zeller, 1879, at a constant temperature of
25-26°C. JAVAHERY (1986) reported that development
duration of the nymphal stage of the insect in Québec was
44 days in field cages, and development of the first, sec-
ond, third, fourth and fifth instars took on average 8, 8, 9,
9 and 10 days, respectively. MUSOLIN & SAULICH (2000)
noted that different photoperiods had no effect on nymph
development of P. bidens at 24.5°C. Nymph development
took 25 to 26 days at different photoperiods except for
nymphs reared at a 20:4 (L:D) h photoperiod, which took
28 days to develop (MUSOLIN & SAULICH, 2000). These
authors showed that nymph duration of this predator aver-
aged 36 days under field conditions in the Belgorod
region of Russia. The development durations found in the
current study are comparable with those previously
reported by above-mentioned authors.
We know of no other studies in which temperature
thresholds and thermal requirements for development of
P. bidens have been estimated. MAHDIAN et al. (2006)
indicated that predation behaviour of P. bidens was
affected by temperature; all nymphal stadia of P. bidens
TAB L E 2
Lower development thresholds (t), degree-day requirements (K) and linear regression equations and
coefficients of determination for development of the immature stages of P. bidens at different constant
temperatures
Stag e t (°C) K (DD) Regression equation r² P
Egg 10.48 208.33 Y=-0.0503+0.0048X0.97 <0.001
First instar 10.94 54.94 Y=-0.1991+0.0182X0.98 <0.001
Second instar 9.12 81.96 Y=-0.1113+0.0122X0.99 <0.001
Third instar 8.21 86.95 Y=-0.0945+0.0115X0.99 <0.001
Fourth instar 14.48 49.26 Y=-0.2941+0.0203X0.98 <0.001
Fifth instar 16.50 64.93 Y=-0.2541+0.0154X0.99 <0.001
Total nymph period 13.76 270.27 Y=-0.0509+0.0037X0.98 <0.001
Total development 12.25 500.00 Y=-0.0245+0.002X0.99 <0.001
TAB L E 3
Egg hatch, nymph survival, and sex ratio of adults of P. bidens at five constant temperatures
Temperature (°C) Egg hatch (%) Nymph survival ( %) Sex ratio (male: female)
18 65 28 1:0.6
20 71 48 1:0.9
23 86 69 1:1.7
27 84 60 1:1.0
32 69 59 1:0.9

Kamran Mahdian, Luc Tirry & Patrick De Clercq
138
from the second instar onward were able to prey success-
fully upon fourth-instar S. littoralis at temperatures
between 18 and 27°C. Mean daily prey consumption by
male and female adults of P. bidens increased with
increasing temperature. Further, these authors showed
that the type of functional response (i.e. the relationship
between rate of prey consumption and prey density) of P.
bidens switched from type II to type III as temperature
increased from 18 to 27°C.
Several linear and nonlinear models have been pro-
posed to describe the relationship between temperature
and arthropod development (CAMPBELL et al., 1974;
WAGNER et al., 1984; LACTIN et al., 1995; BRIÉRE et al.,
1999). The linear equation has been documented as a suit-
able model for calculation of lower development thresh-
olds and thermal constants in a partial temperature range
(e.g., CAMPBELL et al., 1974; HONĚK, 1999 ; JAROŠIK et al.,
2002; KONTODIMAS et al., 2004). The variability of the
estimated thermal thresholds for the successive develop-
mental stages of P. bidens suggests, however, that the lin-
ear degree-day model may not always yield accurate esti-
mates. For instance, the linear model estimated the lower
thermal threshold for egg development of P. bidens to be
10.5°C, whereas our observations showed that eggs did
not develop successfully at a constant temperature of
15°C. Further, estimates of lower development thresholds
of fourth and fifth instars were considerably higher than
those of the earlier instars. Other models, including non-
linear regression, may enable a more accurate description
of the relationship between development of immature
stages of P. bidens and temperature (for a review, see
KONTODIMAS et al., 2004); however, non-linear models do
not enable the calculation of thermal constants. Also
given its ease of use, the linear degree-day model has
therefore been widely used as a phenological model
(KONTODIMAS et al., 2004).
The results of the current study on P. bidens, together
with reported high predation capacities of this predator
against noctuid caterpillars within a wide range of tem-
peratures, indicate that P. bidens may perform well when
released as a biological control agent of defoliator pests
both in open fields and heated glasshouses. Whereas tem-
perature is one factor that is important for the establish-
ment of the predator's population in the crop and that will
determine its foraging and predation capacity, there are
considerable environmental complexities that may affect
the predator-prey system and will eventually determine
the outcome of a biological control programme. Never-
theless, the current data will be useful in the selection of
the most effective life stage of the predator that is best
adapted to conditions favouring the target pest in a given
crop situation.
ACKNOWLEDGEMENTS
The statistical suggestions of Mohammad Amin Jalali are
gratefully acknowledged. The authors are grateful to the Minis-
try of Science, Research and Technology of Iran for financial
support to K. Mahdian (Ph.D. grant no. 781153)
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