American Journal of Plant Sciences, 2011, 2, 449-456
doi:10.4236/ajps.2011.23052 Published Online September 2011 (http://www.SciRP.org/journal/ajps)
Copyright © 2011 SciRes. AJPS
449
Rearing the Predator Brontocoris tabidus
(Heteroptera: Pentatomidae) with Tenebrio
molitor (Coleoptera: Tenebrionidae) Pupa
on Eucalyptus grandis in the Field
José C. Zanuncio1*, Ana M. R. M. Ferreira2, Wagner S. Tavares3, Jorge B. Torres4, José E. Serrão5,
Teresinha V. Zanuncio1
1Departamento de Biologia Animal, Universidade Federal de Viçosa, Viçosa, Brazil; 2Campus Universitário de Curitibanos, Univer-
sidade Federal de Santa Catarina, Curitibanos, Brazil; 3Departamento de Fitotecnia, Universidade Federal de Viçosa, Viçosa, Brazil;
4Departamento de Agronomia-Entomologia, Universidade Federal Rural de Pernambuco, Recife, Brazil; 5Departamento de Biologia
Geral, Universidade Federal de Viçosa, Viçosa, Brazil.
Email: {*zanuncio, wagner.tavares, jeserrao}@ufv.br, ana.margarete@cbs.ufsc.br, jtorres@depa.ufrpe.br
Received February 24th, 2011; revised April 6th, 2011; accepted April 19th, 2011.
ABSTRACT
The use of natural enemies represents an important strategy in programs of Integrated Pest Management (IPM).
Asopinae predators are reared with alternative prey, but supplementary plan t may enhance the fecundity and long evity
of their females. The objective of this research was to evaluate the development and reproduction of the predator Bron-
tocoris tabidus Signoret, 1852 (Heteroptera: Pentatomidae) fed with Tenebrio molitor L., 1785 (Coleoptera: Tenebri-
onidae) pupae in a Eucalyptus grandis Hill ex Maiden (Myrtaceae) plant in the field. The duration and survival of the
nymphal stage of B. tabidus were 32.07 ± 8.95 days and 77.00% ± 0.42%, respectively with 15.55 ± 8.19 egg masses,
603.00 ± 379 .20 eggs and 387.4 5 ± 291.40 nymphs per fema le of this predator while longevity of its males and females
was 119.80 ± 32.80 and 160.20 ± 42.13 days, respectively. Better resu lts with E. grandis pla nt in the f ield and the fact
that B. tabidus will be adapted at release time show that this predator should be rear ed in these conditions.
Keywords: Asopinae, Insect-Plant Interactions, Integrated Pest Management, Rearing Predators, Supplementary Food
1. Introduction
The adoption of Integrated Pest Management (IPM)
reduces problems such as pest resistance and the impact
of pesticides on natural enemies [1-3]. Biological control
is an important tactic in IPM programs for handling
pathogens and arthropods, including the Pentatomidae, a
predatory bug species in reforested areas [4] where the
defenses in plants can be beneficial [5], harmful or have
no impact [6] on natural enemies.
Predators have a higher reproductive rate when they
get plenty of food and this rate tends to decrease with
less availability of food to benefit the survivors. When
predatory bugs are fed more food to gain weight, there is
an increase in the frequency of attacks on prey, and pos-
ture and development are faster [7].
Supputius cincticeps Stal, 1860 (Heteroptera: Pentato-
midae) nymphal stage was shorter and its females heavier
when fed with pupae of Tenebrio molitor L., 1785 (Cole-
optera: Tenebrionidae) and on seedlings of Eucalyptus
urophylla ST Blake (Myrtaceae) [8]. Podisus nigrispinus
Dallas, 1851 (Heteroptera: Pentatomidae) had shorter du-
ration of nymph al stage with Bombyx mori L., 1758 (Le-
pidoptera: Bombycidae) caterpillars, except in the fourth
instar, when fed on cotton and tomato plants and prey than
when they were fed only with prey [9]. Moreover, the
availability of cotton or weeds reduced the impact of the
shortage of prey in the partial duration, viability and ny-
mphal stages of this predator, but it has not reached sex-
ual maturation and not oviposited without prey [10,11].
Females of Podisus connexivus Bergroth, 1891 (= P.
nigrispinus) (Heteroptera: Pentatomidae) had greater wei-
ght gain with E. urophylla and prey. Podisus maculiven-
tris Say, 1832 (Heteroptera: Pentatomidae) showed higher
survival rates and shorter pre-oviposition and nymphal
periods when fed on prey and potato leaves [5].
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor
450 (Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
The longevity of P. nigrispinus was similar for both
sexes, but males showed greater longevity when fed on
prey and cotton plants [9]. Females of P. maculiventris
showed a higher survival rate when they were given po-
tato or tomato than when they were only given water
until the 35th day of life, with values of 31.9, 28.8 and
27.1 days for the potato, tomato or water diets, respe-
ctively [12]. The availability of prey with cotton plants
increased longevity of P. nigrispinus with 30.3 ± 10.53
days for females and 43.8 ± 17.70 for males, versus 16.0 ±
11.4 and 19.93 ± 4.56 days for males and females of this
predator, respectively, only, with prey [9]. The ability of
predators to obtain moisture and plant nutrients can be
considered an adaptation to improve survival rate at these
times of scarcity of prey [13,14].
The aim of this research was to investigate the rearing
of Brontocoris tab idus Signoret, 1852 (Heteroptera: Pen-
tatomidae) fed with T. molitor pupae associated to Euca-
lyptus grandis Hill ex Maiden (Myrtaceae) plant in field
conditions.
2. Materials and Methods
This study was conducted in an area (field) of the “De-
partamento de Biologia Animal (DBA)” of “Universidade
Federal de Viçosa (UFV)” in the city of Viçosa, Minas
Gerais State, Brazil. The mean temperature during the
nymphal and adult stages of B. tabidus was 19.55˚C,
with the minimum temperature of 11.70˚C recorded in
July and the maximum temperature of 30˚C recorded in
March. The relative humidity was 77.58% (Table 1).
Nymphs of B. tabidus were obtained at the “Labo-
ratório de Controle Biológico de Insetos (LCBI)” of the
“Instituto de Biotecnologia Aplicada à Agropecuária
(BIOAGRO)” of UFV, where the referred species is
reared at 25˚C 2˚C, 70% 5% of relative humidity and
photoperiod of 12 hours. Egg masses and first instar ny-
mphs of B. tabidus were maintained in Petri dishes (9.0 ×
1.2 cm) with a cotton pad soaked in distilled water. One
hundred second instar nymphs of B. tabidus were placed
in a white organza bag (20 × 30 cm) involving the ex-
tremity of a branch of an approximately 2-year-old E.
grandis plant. Nymphs were fed with T. molitor pupae
from a mass rearing facility of the UFV. Water was sup-
plied to this predator in 2.5 mL tubes (similar to those
used in dental anesthesia) fastened to E. grandis branches
with adhesive ribbon (Figure 1).
Mortality of nymphs, change of instars an d emergence
of B. tabidus adults were daily observed [15]. Adults of
this predator were weighed using a scale with 0.1 mg pre-
cision, approximately 24 hours after their emergence
when they were sexed and individually placed in Petri
dishes [16,17].
Table 1. Monthly mean, maximum (Max.), minimum (Min.) and mean per period of temperature (temp), relative humidity
(%); mean daily rainfall (mm) and photoperiod (hours per day). Municipality of Viçosa, Minas Gerais State, Brazil. March
to November 2010.
Months Temp. Mean (˚C) Temp. Max. (˚C) Min. Temp. (˚C)Rel. Hum. (%) Rainfall (mm) Photoperiod (hours)
March 23.00 30.00 19.06 80.79 1.06 11.88
April 21.86 29.86 16.95 77.65 1.12 11.52
May 19.12 26.31 14.69 78.96 1.91 11.02
June 17.92 25.61 13.30 80.71 0.01 10.76
July 16.84 25.00 11.70 77.91 0.06 10.87
August 18.33 26.53 12.41 74.81 0.21 11.03
September 19.07 25.87 14.28 74.05 2.67 11.89
October 20.49 26.72 16.19 74.29 4.91 12.49
November 22.18 27.70 18.68 81.73 7.71 13.00
Temp 19.55 26.77 14.86 77.58 2.29 11.61
Copyright © 2011 SciRes. AJPS
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor 451
(Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
Figure 1. Organza bag used to rear Brontocoris tabidus on Eucalyptus grandis plant in the field. A—anesthesic odonthological
tube; B—organza cloth. C—Eucalyptus grandis branch.
Twenty B. tabidus females weighing more than 120
mg were selected to reduce the influence of this trait on
female productivity and mated four days after their
emergence [18]. Pairs of this predator were involved in
organza bags similar to those used for their nymphs and
maintained on E. grandis plan t in the field until the death
of males and females. The males that died before their
respective females were replaced by other ones reared
under similar conditions. Pairs of B. tabidus were given
water daily and fed on T. molitor pupae, when the dura-
tion of pre-oviposition, oviposition and post-oviposition
periods, as well as the number of egg masses, eggs and
nymphs per female, egg viability and longevity of fe-
males of this predator were evaluated. Egg masses of B.
tabidus were daily collected and placed in Petri dishes
(9.0 × 1.2 cm) with a cotton pad soaked in distilled water
and its nymphs were counted 24 hour s po st-eclosion.
3. Results
Brontocoris tabidus did not prey during the first instar
that lasted 3.52 0.50 days, whereas the second, third,
fourth and fifth instars lasted 5.80 1.38, 4.93 1.50,
6.10 3.04 and 11.72 2.68 days (Figure 2(a)). The d u-
ration of the nymphal stage of this predator was 32.07
8.95 days on E. grandis plant (Figure 2(a)).
The survival rate of B. tabidus was 91.00% 0.28%,
92.30% 0.26%, 94.04% 0.23% and 97.46% 0.15%
during the second, third, fourth and fifth instars, whereas
adult emergence of this predator reached 77.00% 0.42%
on the E. grandis plant with T. molitor pupae (Figure 2(b)).
A
Duration (Days)
0
10
20
30
40
I
II III
IV
V Nymph stage
Instars
(a)
IIIIII IV VNymph stage
B
Survival (%)
0
20
40
60
80
100
Instars
(b)
Figure 2. Duration (a) and survival (b) (mean standard
deviation) during each instar and of the nymphal stage of
Brontocoris tabidus fed with Tenebrio molitor pupae on a
Eucalyptus grandis plant in the field. Municipality of Viçosa,
Minas Gerais State, Brazil.
Copyright © 2011 SciRes. AJPS
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor
452 (Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
The pre-oviposition, oviposition and post-oviposition
periods of B. tabidus females were 50.16 35.12, 108.79
38.76 and 7.84 6.85 days, respectively with 603.00
311.20 eggs and 15.55 8.19 egg masses per female
(Table 2). The nymphal stage of this predator was as
follows: 387.45 291.4 0 nymphs p er female and 58.83%
24.23% nymph hatching (Table 2).
The survival rate of B. tabidus females was over 50%
until they were 170 days old and egg production was
greater between days 60 and 160 of their life (Figure 3).
This predator had 0.0 to 5.49 eggs and 0.0 to 4.72 nymphs
per day per fertile female (Figure 4).
Table 2. Re pro ductive c haracteri stic s, longe vity and weight (mean standard deviation) of males and females Brontocoris tabidu s
fed with Tenebrio molitor pupae on a Eucalyptus grandis plant in the field. Municipality of Viçosa, Minas Gerais State, Braz il.
Characteristics evaluated Results
Incubation period (days) 5.16 0.50
Pre-oviposition period (days) 50.16 35.12
Oviposition period (days) 108.79 38.76
Post-oviposition period (days) 7.84 6.85
Number of eggs/female 603.00 311.20
Number of egg masses/female 15.55 8.19
Number of eggs p e r egg mass 37.01 7.44
Number of eggs p e r day 3.5 1.60
Percentage of nymph hatching (%) 58.83 24.23
Number of nymphs per female 387.45 291.40
Number of nymphs per egg mass 21.52 8.02
Longevity of males (days) 119.80 32.50
Longevity of females (days) 160.20 42.13
Weight of males (mg) 102.70 5.91
Weight of females (mg) 138.80 11.24
Days
020406080100 120 140 160 180 200 220
Porcentage
0
25
50
75
100
Number
0
20
40
60
80
Accumulated percentage of eggsSurvival
Number of eggs
Figure 3. Number of eggs per period of 10 days, accumulated percentage of eggs produced and survival of Brontocoris tabidus fe-
males fed with Tenebrio molitor pupae on a Eucalyptus grandis plant in the field. Municipality of Viçosa, Minas Gerais State, Brazil.
Copyright © 2011 SciRes. AJPS
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor 453
(Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
Females
01234567891011121314151617181920
Number
0
10
20
30
40
50
60
Weight
0
20
40
60
80
100
120
140
160
180
Eggs
N
ymphs Weight
Figure 4. Number of eggs and nymphs per day per Brontocoris tabidus female (related to its weight) fed with Tenebrio molitor
pupae on a Eucalyptus grandis plant in the field. Municipality of Viçosa, Minas Gerais State, Brazil.
Some B. tabidus findings regarding oviposition are:
15.67 to 51.21 eggs and 5.00 to 37.50 nymphs per egg
mass (Figure 5), whereas the mean number of eggs and
nymphs for all egg masses of each female ranged from
0.00 to 52.11 and 0.00 to 40.78, respectively (Figure 6).
The mean longevity and weight of B. tabidus males
were 119.80 32.50 days and 102.70 5.91 mg, respect-
tively, whereas these values were 160.20 42.13 days
and 138.40 11.24 mg for females of this predator with
T. molitor on the E. grandis plant in the field ( Table 2).
4. Discussion
The B. tabidus had five instars on E. grandis plant, with
similar results for this predator fed with an artificial diet
based on beef meat and liver and/or T. molitor pupae [19].
This suggests that the number of instars of B. tabidus is
similar for this predator fed with prey and/or on a diet
with or without plants.
The fourth instar of B. tabidus had a similar duration
on the E. grandis plant with T. molitor pupae compared
to this predator fed only with T. molitor pupae [19]. How-
ever, the duration of the fifth instar of B. tabidus with T.
molitor on E. grandis was longer than that observed for
this predator with pupae of T. molitor [19]. This is con-
sistent with the long er duration of the fourth and fifth in-
stars of P. maculiventris with prey [third instar of Lepti-
notarsa decemlineata Say, 1824 (Coleoptera: Chrysomeli-
dae)] and plants [Solanum tuberosum L. and Lycopersi-
con esculentum Mill. (Solanaceae)] compared to that of B.
tabidus fed only on prey [12].
The nymphal stage of B. tabidus was longer on eucaly-
ptus plant in the field than this predator in the same stage
fed only with T. molitor pupae [19]. The longer duration
of the nymphal stage of B. tabidus fed with plant is si mi-
lar to that found for S. cincticeps fed with T. molitor and
Myrtaceae plants [20]. Although this may delay the
emergence of B. tabidus adults, the predation rate is in-
creased, since the Podisus rostralis Stal, 1860 (Heterop-
tera: Pentatomidae) killed a greater number of B. mori
caterpillars when these had a longer nymphal period [17].
The survival rate during the nymphal stage of B. tabidus
was longer than during the stage where the predator was
fed with pupae of T. molitor [19]. The higher survival of
B. tabidus in the field can be due to a change in tem-
perature, relative humidity and photoperiod [21]. It may
affect biological traits of insects because their activities
can be regulated by dur ation of the day [22].
The pre-oviposition and oviposition periods of B. tabi-
dus were longer than that with Musca domestica L., 1758
(Diptera: Muscidae) larvae [23], which can be explained
by the low temperature before the reproductive stage of
this predator and to the decreasing phot operi o d i n t he fi el d.
The longer interval between egg mass laying and preovi-
position and oviposition periods, and the longevity of P.
nigrispinus and S. cincticeps, were also reported as pos-
sibly due to the reduction on their metabolic activities at
Copyright © 2011 SciRes. AJPS
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor
454 (Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
Egg masses
0510 15 20 25 30 35
Number
0
20
40
60
80
Percentage
0
20
40
60
80
100
Eggs Nymphs Eggs viability
Figure 5. Number of eggs and nymphs per egg mass of Brontocoris tabidus fed with Tenebrio molitor pupae on a Eucalyptus
grandis plant in the field. Municipality of Viçosa, Minas Gerais State, Brazil.
Females
01234567891011121314151617181920
Number
0
10
20
30
40
50
60
Weight (mm)
110
120
130
140
150
160
170
Eggs Nymphs Weight
Females
Figure 6. Mean number of eggs and nymphs per egg mass of each female of Brontocoris tabidus fed with Tenebrio molitor
pupae on a Eucalyptus grandis plant in the field. Municipality of Viçosa, Minas Gerais State, Brazil.
Copyright © 2011 SciRes. AJPS
Rearing the Predator Brontocoris tabidus (Heteroptera: Pentatomidae) with Tenebrio molitor 455
(Coleoptera: Tenebrionidae) Pupa on Eucalyptus grandis in the Field
temperatures below 25˚C [15,20]. The longer pre-ovi-
position period with Eucalyptus spp. plants may also
result from the higher nitrogen content in their leaves
[14,24]. However, these parameters can be affected by
other factors, because the females of this predator that
weigh 95 to 150 mg and 160 to 220 mg had a greater
pre-oviposition period (16.53 ± 3.33 and 16.09 ± 2.57
days, respectively) [25] than that observed in the present
work. The oviposition period of this predator was 5.7 to
10.4 days when fed with pupae of T. molitor, M. domes-
tica and the combination of both, respectively [23].
Again, the high values for this period demonstrate that
the B. mori has a higher nutritional quality as a prey for
the predator species [1,17].
The number of eggs (603.00 311.20), nymphs (387.45
291.40) and longevity (160.20 42.13 days) of B.
tabidus females showed higher values than that with T.
molitor pupae alone [9]. The females live longer when
predators oviposit more often and stay on the field during
a longer period of time, but may be affected by the type
of food ingested, since females of P. maculiventris and
Podisus sagitta F., 1794 (Heteroptera: Pentatomidae) did
not lay eggs when fed only with green beans and potato
leaves [13]. Other predators such as P. sagitta [13], P.
maculiventris [5] and S. cincticeps [8] have also shown
greater longevity and higher reproduction rates when fed
on plant and prey.
The number of eggs per egg mass was not influenced
by the age of B. tabidus females, which is not consistent
with the findings obtained for P. nigrispinus, since the
older females of this species laid a lower number of eggs
per egg mass [26-28]. Females of B. tabidus had similar
weight, but a variable number of eggs and egg masses,
indicating that these traits may be related to genetic
characteristics of this predator besides its weight [18,25].
The greater longevity and the number of eggs of B.
tabidus fed with T. molitor and seedlings of E. grandis
are important factors for the improvement of the po-
tential of this predator as a biological control. However,
the type of prey alone cannot affect the longevity of
stinkbug predators, because males and females mated S.
cincticeps showed similar longevity, 19.2 ± 3.3 and 21.2 ±
2.7 days and 29.2 ± 6.1 and 30.7 ± 4.1 days when fed
with M. domestica or T. molitor, respectively [8].
5. Conclusion and Future Prospects
The nymphal stage of B. tabidus was longer when the
predator was fed with E. grandis and, thus, this must be
considered in mass rearing and in the implementation of
programs involving this predator. The B. tabidus had
better reproductive parameters such as longer longevity
and shorter period to double its population when fed with
plant and prey. Therefore, this predator should be reared
on eucalyptus plants in the field where its adults would
be better adapted at the moment of their release in bio-
logical control programs.
6. Acknowledgements
To Dr. Patrick De Clercq (Ghent University, Department
of Crop Protection, Belgium) for reviewing this manu-
script. To the Brazilian agencies “Conselho Nacional de
Desenvolvimento Científico e Tecnológico (CNPq)”, “C o-
ordenação de Aperfeiçoamento de Pessoal de Nível Su-
perior (CAPES)” and “Fundação de Amparo à Pesquisa
do Estado de Minas Gerais (FAPEMIG)” for supporting
this study. To Dra. Mônica Ruediger de Britto Velho for
English corrections.
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