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Acta Scientiarum 

 

http://www.uem.br/acta 
ISSN printed: 1679-9283 
ISSN on-line: 1807-863X 
Doi: 10.4025/actascibiolsci.v39i3.33426 

 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

Biological parameters of three Trichogramma pretiosum strains 

(Riley, 1879) (Hymenoptera: Trichogrammatidae) on eggs Helicoverpa 
armigera
 (Hübner, 1805) (Lepidoptera: Noctuidae)  

Gabriel dos Santos Carvalho

*

, Luciana Barboza Silva, Maisa Sousa Veras, Eliane Carneiro 

Bueno dos Santos, Mayra Layra dos Santos Almeida and Soislan Sousa Reis 

Programa de Pós-graduação em Agronomia Fitotecnia, Universidade Federal do Piauí, Campus: Professora Cinobelina Elvas, BR-135, km 3, 
Bairro Planalto Horizonte, 64900-000, Bom Jesus, Piauí, Brazil. *Author for correspondence. E-mail: gabrieldossc@hotmail.com 

ABSTRACT. This project has an objective to study the biological parameters of Trichogramma pretiosum on 

eggs of H. armigera. The three strains of T. pretiosum were evaluated: TM, TMC and TLEM, from different 
places. The experimental establishing was completely randomizing with twenty repeats per treatment, 
being used by a female parasitoid by repetition and later on they were offered 20 H. armigera eggs. The 
experiment was kept on BOD cameras to 25 ± 2° C, UR 60 ± 10% and photo phase of 14 hours. 
Evaluating the following biological parameters: parasitism percentage, emergency percentage, number of 
adults emerged per egg, sex ratio, viability, and longevity and cycle duration. The parasitism percentage, 
viability and number of individuals per egg were higher for TM and TMC. The TMC strain presented a 
larger sex ratio proportion, not being different statistically from the TM stream. The longevity of the strain 
TM was different regarding the others. There was no variation regarding the cycle duration. Therefore, 
according with the evaluated biologic parameters, it is concluded that Trichogramma pretiosum strain TM 
obtained a better egg development of H. armigera on laboratory conditions. 

Palavras-chave: Controle biológico, lagarta da soja, parasitoide de ovos. 

Parâmetros biológicos de três linhagens de Trichogramma pretiosum (Riley, 1879) 
(Hymenoptera: Trichogrammatidae) sobre ovos de Helicoverpa armigera (Hübner, 1805) 

(Lepidoptera: Noctuidae) 

RESUMO. Este trabalho teve como objetivo estudar os parâmetros biológicos de Trichogramma pretiosum 
em ovos de H. armigera. As três linhagens de T. pretiosum avaliadas foram: TM, TMC e TLEM, oriundas de 
diferentes localidades. O delineamento experimental foi inteiramente casualizado com vinte repetições por 
tratamento, sendo utilizada uma fêmea do parasitoide por repetição e posteriormente foram oferecidos 20 
ovos de H. armigera. O experimento foi mantido em câmaras BOD a 25 ± 2° C, UR 60 ± 10% e fotofase de 
14 horas.  Avaliou-se os seguintes parâmetros biológicos: porcentagem de parasitismo, porcentagem de 
emergência, número de adultos emergidos por ovo, razão sexual, viabilidade, longevidade e duração do 
ciclo. A porcentagem de parasitismo e viabilidade e número de indivíduos por ovo foram superiores para as 
linhagens TM e TMC. A linhagem TMC apresentou a maior proporção para razão sexual, não diferindo 
estatisticamente da linhagem TM. A longevidade da linhagem TM se destacou em relação às demais. Não 
houve variação com relação a duração do ciclo. Assim de acordo com os parâmetros biológicos avaliados, 
conclui-se que Trichogramma pretiosum linhagem TM obteve o melhor desenvolvimento nos ovos de H. 
armigera
 em condições de laboratório.

 

Keywords: Biological control, soy caterpillar, parasitoid eggs. 

Introduction 

Among the insect pests that are able to limit the 

production of soybean, we emphasize the 

(Hemiptera: Pentatomidae) bugs and the complex of 

defoliating caterpillars. Recently this situation has 

worsened with the recording of the occurrence of 

Helicoverpa armigera (Hübner, 1805) (Lepidoptera: 

Noctuidae)  in   Brazil   (Czepak,   Albernaz,   Vivan, 

Guimarães, & Carvalhais, 2013; Tay et al., 2013; 
Gómez et al., 2016), where it was classified as an A1 
quarantine pest and it is currently found in the states 
of Goiás, Bahia, Mato Grosso and Piauí mainly 
associated to soybean, cotton and tomato crops 
(Czepak et al., 2013; Gómez et al., 2016).  

This fact has led to high adoption of chemical 

controls, to contain this pest, causing serious 

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350 

Carvalho et al. 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

consequences that entail disadvantages due to high 
use of toxic substances, being unselective and with 

slow environmental degradation, which leads to 

imbalance in the agricultural ecosystems and damage 

to farmers (Saber, 2011; Wang, Chen, Ma, Zhu, & 

Lei, 2015; Amichot, Curty, Benguettat-Magliano, 

Galleti, & Wajnberg, 2016).  

Thus, alternative measures must be adopted and 

biological control using parasitoids of Trichogramma 

eggs, is an important measure because they are key 

species in the regulation of the populations of 

several species of Lepidoptera pests, however, there 

are still insufficient studies involving the use of 

Trichogramma spp., on H. armigera (Bueno, Parra, 

Bueno, & Haddad, 2009; Molnár, López, Gámez, & 

Garay, 2016).  

However, the successful use of Trichogramma in 

biological control, depends on the knowledge of 
bio-ecological characteristics of the parasitoid and 
the interaction with the target host (Bourchie & 
Smith, 1996). Thus, it is necessary to understand the 
bio-ecology of the parasitoid in the target pest, 
because the efficiency has shown to differ between 
species and/or strains of Trichogramma, making it 
necessary to study the performance of different 
strains of Trichogramma, collected in different 
ecosystems on the target pest (Hassan, Kolher, & 
Rost, 1998; Bueno et al., 2009). Such knowledge 
enables selecting strains that are well adapted to the 
pest to be controlled (Bezerra & Parra, 2004).  

Thus, this study aimed to evaluate the biological 

parameters of three strains of Trichogramma pretiosum 
(Riley, 1879) (Hymenoptera: Trichogrammatidae) 
and indicate the most efficient for Helicoverpa 
armigera
 control in laboratory conditions. 

Material and methods 

Location of the experiment 

The experiment was conducted in the Plant 

Science Laboratory of the Universidade Federal do 

Piauí, kept in BOD with constant temperature of 25 

± 2° C, relative humidity 60 ± 1% of the Campus: 

Professor Cinobelina Elvas - CPCE. 

Raising of Helicoverpa armigera 

The used population of H. armigera originated 

from the insect breeding laboratory, where they 

were kept in an artificial diet adapted from Kasten 

Jr., Precetti, and Parra (1978). Neonate larvae (< 24 

hours old) were individualized and transferred to 

plastic containers with a lid, containing 100 ml of 

artificial diet until they reached the pupal stage. 

When they became adults, they were transferred to 

PVC cages (40 cm H x 30 cm Ø), internally coated 

with bond paper sheets for oviposition. The moths 
were fed with a honey-based solution (10%) and 

kept under controlled conditions (25 ± 5° C, 60 ± 

10% RH, 12:12). The eggs were collected and stored 

in pots and kept in laboratory conditions until the 

hatching of the caterpillars, where one half was 

intended for experiments and the other for 

maintenance of the creation in the laboratory. 

Strains of Trichogramma pretiosum for Helicoverpa armigera 

control 

The selection was made from strains of 

Trichogramma pretiosum. The LEM strain was 

obtained from the Insect Biology Laboratory, 

Department of Entomology and Acarology, "Luiz de 

Queiroz" Agricultural College (ESALQ/USP); and 

the TMC and TM strains were collected in traps, 

with eggs of the alternative host A. kuehniella and H. 

armigera eggs, respectively. Samples were collected in 

soybean commercial plantations at Cerrado 

(Brazilian savannah), of the municipality of Baixa 

Grande do Ribeiro-Piauí, Brazil. This municipality 

has sub-humid tropical climate, with temperatures 

between 26 to 36°C and average rainfall of 700mm 

to 1200mm between the months of December to 

May (Companhia de Pesquisa de Recursos Minerais 

[CPRM], 2004). Three strains of T. pretiosum were 

established (Table 1). 

Before the installation of the experiments, three 

strains of Trichogramma pretiosum were maintained for 

one generation, in H. armigera eggs in order to 

eliminate a possible pre-imaginal conditioning by 

raising them in an alternate host (A. kuehniella). The 

species was identified by morphological 

characteristics according to (Querino & Zucchi, 
2003). 

Table 1. Strains of Trichogramma pretiosum with their respective 

collection origins used in the screening test for the control of 
Helicoverpa armigera

Treatments Species/Strains

Origin Host 

T1-TLEM

T. pretiosum

TLEM 

Luiz Eduardo Magalhães, 

BA/ESALQ 

T2-TMC 

T. pretiosum/ 

TMC 

(Area1) 

(S08°40’58.7’’) (W045°05’39.2’’) 

Baixa grande do Ribeiro, PI 

H. armigera

T3-TM 

T. pretiosum/ TM

(Area2) 

(S08°40’56.4’’) (W045°05’39.2’’) 

Baixa grande do Ribeiro, PI 

H. armigera

Raising and maintenance of Trichogramma pretiosum 
strains 

The raising of Trichogramma was performed 

according to the methodology of (Stein & Parra, 

1987), eggs of the alternative host Anagasta kuehniella 

(Zeller, 1879) (Lepidoptera: Pyralidae). The diet of 
the alternative host was placed in plastic trays 

containing corrugated cardboard strips, pre-cut that 

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Biology of parasitoids in Helicoverpa armigera 

351 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

aim to provide support and also serve as a place for 
pupation. 

In each tray, 0.35 g of A. kuehniella eggs was 

placed and each tray was covered with a plastic bag 

with an opening covered with "voile" type tissue 

allowing internal ventilation. This procedure was 

performed to prevent an attack of the parasitoid 

Bracon hebetor (Say, 1857) (Hymenoptera: 

Braconidae) that parasites A. kuehniella caterpillars in 

the final instar of the host. Then the trays were 

placed in a larval development room, where they 

remained until the beginning of adult emergence. 

After the emergence of the first adults, their diet, 

hardened due to the formation of webs by the 

caterpillars, was moved and fixed inside the adult 

collection boxes. 

For the collection of the adult A. kuehniella that 

had emerged, a vacuum cleaner that was adapted to 

suck the insects inside the creation of boxes was 

utilized and later the adults were transferred to 

plastic containers (2.5 L). At the end of the process, 

the eggs were collected from the plastic containers 

through a fine mesh screen that stays in the bottom 

where the eggs fall. 

Once collected, the eggs of the factitious host 

were fixed in blue cardboard pieces (8.0 x 2.0 cm) 

with diluted gum arabic in water (50%), and then 

were subjected to the unviability process through 

exposure of the eggs to ultraviolet germicidal light 

for a period of 50 minutes and at a distance of 15 cm 

from the light source. At the extremities of the 
cartouches were recorded the date of parasitism and 

the strain identification code, allowing control of 

Trichogramma pretiosum strains. 

Experiment execution 

The experiment was carried out in climatic 

chambers regulated at 25 ± 2° C, RH 70±10% and 

photoperiod of 14 hours in a completely 

randomized design with the treatments consisting of 

the three strains, using twenty repetitions with a 

female parasitoid by repetition. 

Females of each strain were individualized, with 

24 hours of age in glass tubes (12 mm diameter and 

75 mm height) capped with PVC plastic film 

(Magipack™) being fed with a droplet of pure 

honey. Female parasitoids were identified through 

sexual dimorphism displayed by the antennas 

(Bowen & Stern, 1966), with the help of a 

stereoscopic microscope. 

For each strain, 20 cartouches containing 20 eggs 

of H. armigera with 24 hours of age were used. After 

24 hours, the females were removed from the glass 

tubing with each strain (treatment) containing 20 
replicates. 

We evaluated the following biological parameters 

of T. pretiosum

parasitism percentage by counting 

the darkened eggs; 

emergence percentage

emergence percentage by counting of adults; 
viability percentage acquired by counting the host 
eggs that had outlet orifice of the adults viewed 
under a stereoscopic microscope; 

number of 

adults emerged per egg calculated using the 
formula: 

Adults emerged per egg =

N

o

 of females + N

o

 of males 

N

o

 of parasitized eggs 

For 

sex ratio based on the methodology 

proposed by (Bowen & Stern, 1966), calculated 

using the formula: 

sr =

N

o

 of females 

N

o

 of females + N

o

 of males 

 

Longevity, accomplished through daily 

observations, always at the same time, with 24 hours 
intervals for mortality accounting; 

cycle duration 

(egg-adult), conducted through daily observations, 
always at the same time, with 24 hours intervals. 
The determination of the number of individuals per 
egg was calculated by dividing the total number of 
adults by the total number of holes observed in 20 
H. armigera eggs in each tube. The results were 
submitted to analysis of variance and averages were 
compared by the Tukey test (P ≤ 0.05). The data 
was analyzed using the statistical program R version 
3.0.3. 

Results 

When analyzing the performance of the three 

strains of Trichogramma pretiosum, there were 
differences in the evaluated parameters. For 
parasitism, we observed differences in the 
aggressiveness of the strains evaluated on the H. 
armigera  
eggs being TM and TMC the superior 
strains in relation to TLEM, respectively (Figure 
1A). 

The emergence percentage of the studied T. 

pretiosum strains differ significantly where the TM 
and TMC strains showed the highest percentages of 
84.4 and 73.9%, respectively (Figure 1B). 

For the viability percentage, the TMC and TM 

strains showed significantly higher values than the 
TLEM strain (Figure 1C). 

The number of adults emerged per egg was 

greater for the TM strain when compared to TMC 
and TLEM with 1.19, 0.98, and 0.94 individuals per 
egg, respectively (Figure 1D).  

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352 

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Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

 

 

Figure 1. (A) Parasitism percentage, (B) Emergence percentage (C) Viability percentage, (D) Individuals per egg (E) Sex ratio (F) Adult 
longevity, (G) Cycle duration of the three strains of Trichogramma pretiosum: TM, TMC and TLEM created in Helicoverpa armigera eggs. 
Temperature of 25±1ºC, RH 70±10% and photoperiod of 14 hours. Averages of the bars followed by the same letter do not differ by 
Tukey’s test at 5% probability.  

 

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Biology of parasitoids in Helicoverpa armigera 

353 

Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

 

By analyzing the sex ratio, there was no 

significant difference between the TMC and TM 
strains, having the highest proportions of females 
compared to the TLEM strain with the lowest 
proportion (Figure 1E). 

The longevity of the descendants of the T. 

pretiosum TM strain when developed in H. armigera 
eggs was greater with 12.35 days of adult survival in 
comparison to TMC and TLEM whose strains 
lasted 9.05 and 9.10 days, thus, the TM strain 
according to the results, produces females have a 
greater survival time (Figure 1F). 

The duration of the cycle, did not vary between 

the strains evaluated, with an average of 10 days 
when subjected to the host in the study (Figure 1G). 

Discussion 

The parasitism percentage of H. armigera eggs by 

the strains TM (31.5%) and TMC (25.9%) was 
higher compared to the TLEM strain. The 
parasitism efficiency reveals a variation in the 
characteristics of each strain of T. pretiosum studied. 
This factor may be associated with acceptance of the 
parasitoid by the host strains studied, as a result of a 
physicochemical characteristic used to recognize H. 
armigera
 eggs. Similar percentages of parasitism, 
between 81 and 56% were obtained by (Bueno, 
Parra, & Bueno, 2012), By evaluating 13 
Trichogramma strains in Chrysodeixis includens (Walker, 
1958) eggs (Lepidoptera: Noctuidae). Ko et al. 
(2014) had results that were similar to the present 
study, when evaluating a strain of T. pretiosum on 
eggs of Plutella xylostella (Linnaeus, 1758) 
(Lepidoptera: Plutellidae). Öztemiz (2008) observed 
an efficiency between 66 and 90% in the parasitism 
of  H. armigera using  T. euproctidis (Giralt, 1911) 
(Hymenoptera: Trichogramatidae) with cotton 
cultures in field conditions. 

Parasitoids of the Trichogramma genus can be 

easily multiplied in a laboratory with high efficiency 
and low cost (Öztemiz & Kornosor, 2007). 
However, the release in cultures after several 
generations of laboratory breeding can reduce their 
effectiveness due to inbreeding and genetic erosion, 
which reduces the potential foraging and parasitism 
rate (Pratissoli et al., 2005), which may justify the 
performance inferiority of the TLEM strain 
compared to the TM and TMC strains that were 
collected in the field. This shows that H. armigera is 
an excellent host according to the results found, 
especially for the TM and TMC strains, having 
suitable characteristics for the development of the 
parasitoids. 

The high emergence rate of 89.4 and 73.9% 

presented by the TM and TMC strains respectively, 

indicates the nutritional quality of H. armigera eggs. 

These numbers are acceptable in pest control 

programs (Nava, Takahashi, & Parra, 2007, Dias, 

Parra, & Lima, 2008). The concomitant emergence 

rate of parasitism by the TM and TMC strains may 

represent an H. armigera control efficiency, which 

means the mass presence of the parasitoid in the area 

and consequently reduced pest population density. 

As for the number of emerged individuals per 

egg, there was no difference between strains, which 

was not observed in the study by Altoé et al. (2012) 

who studied the T. pretiosum on Trichoplusia ni 

(Hübner, 1803) (Lepidoptera: Noctuidae), which 

observed variation in the number of individuals per 

egg, showing that this parameter is influenced by 

host characteristics. Studies by Bueno et al. (2009) 

reported that egg size can influence the number of 

offspring, a characteristic that was also observed in 

H. armigera eggs, where it presented high quality, for 

the percentages presented in the three strains. 

For sex ratio, all the results were favorable as the 

required standard for the parasitoid. For Navarro 

(1998), the ideal sex ratio should be less than 0.5 for 

use in biological control programs. The TMC strain 

showed a better ratio but did not differ statistically 

from the TM line. These results favor its use in the 

field, by providing a high number of parasitoid 

females, required in Trichogramma quality control. 

The TM strain showed the highest average with 

12.5 days, representing 3.3 and 3.25 days more 

longevity compared to TMC and TLEM. Similar 

results were found by Nava et al. (2007) to evaluate 

the longevity of T. pretiosum L4 strain in Stenoma 

catenifer eggs, 11.5 days. This feature is important in 

biological control programs, for longer-lived 

parasitoids created in H. armigera eggs may have 

greater efficiency in the field and be able to 

parasitize for a longer period of time. 

The biological control, using parasitoids of the 

Trichogramma genus as a tactic of the Integrated Pest 

Management (IPM) has been successfully 

implemented by cotton producers in Asia and North 

Africa who have suffered great losses caused by H. 

armigera. (Heydari & Gharedaghli, 2007). Programs 

like these should be seen as an example for further 

studies for the implementation of this tool in 

integrated pest management for the soybean crop-

producing areas of Brazil. 

Studies have shown variations between species 

and/or strains on the search behavior, host 

preference, response to environmental conditions, 

among other features, emphasizing the importance 

of choosing an appropriate strain for use in 

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Acta Scientiarum. Biological Sciences 

Maringá, v. 39, n. 3, p. 349-355, July-Sept., 2017 

biological control programs, because these variations 
may affect the successful use of Trichogramma spp. 

(Beserra, Dias, & Parra, 2003; Coelho Jr, Rugman-

Jones, Reigada, Stouthamer, & Parra, 2016). 

In the present study the TM strain was the one 

with the greatest potential for use in H. armigera 

control programs, not only having shown high 

parasitism (%) it stood out for having the greatest 

longevity among the evaluated strains, which may 

reflect a greater foraging period in the field and 

greater dispersion. 

Conclusion 

According to the biological parameters evaluated 

in this study, we can say that the T. pretiosum strain 

TM presents the best H. armigera control potential in 

laboratory conditions, standing out due to the high 

percentage of parasitism presented and especially the 

highest longevity among the strains studied, and 

these factors are considered important in biological 

control. It is important to note that more studies are 

needed in field conditions for its implementation 

within the integrated pest management. 

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Received on September 3, 2016. 

Accepted on June 12, 2017. 

 

 

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