Karaca et al.

Egyptian Journal of
Egyptian Journal of Biological Pest Control (2022) 32:84
https://doi.org/10.1186/s41938-022-00577-9 Biological Pest Control

RESEARCH Open Access

Efficacy of some entomopathogenic

fungi against tomato leafminer, Tuta absoluta
(Meyrick) (Lepidoptera: Gelechiidae)
Gürsel Karaca1, Alime Bayındır Erol2* , Burcu Açıloğlu Çığgın1, Hatice Acarbulut1 and İsmail Karaca1

Abstract
Background: Effects of entomopathogenic fungi (EPF); Beauveria bassiana, Isaria fumosorosea and Pupureocillium
lilacinum against tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae), which is one of the most eco-
nomic pests of tomato, were investigated in Petri dish, pot and greenhouse experiments. Commercial bioinsecticide
Met 52 was also used in the experiments. In the Petri dish trials, I. fumosorosea applied to the third instar larvae by dip-
ping method was recorded as the most effective entomopathogen, while the efficacy of B. bassiana was high in the
spray and residue methods. In the pot experiments, entomopathogenic fungi were applied to tomato plants before
and after infestation with T. absoluta.
Results: As a result of the applications, it was found that the EPF significantly reduced the formation of galleries on
tomato leaves when applied before or at the beginning of tomato leafminer infestation. In the greenhouse experi-
ments a registered insecticide Voliam Targo was also applied. All applications significantly reduced the numbers of
galleries on tomato leaves than in the control plants, in both greenhouse trials, made in Antalya and Isparta Provinces.
I. fumosorosea was the most effective one among the tested 3 EPF.
Conclusions: In this study, it was determined that the EPF B. bassiana and P. lilacinum can reduce tomato leafminer
damage, while the efficacy of I. fumosorosea was the highest, and especially after two applications it was nearly effec-
tive as the registered insecticide.
Keywords: Tuta absoluta, Entomopathogenic fungi, Biological control, Efficacy

Background control measure is applied (Durmuşoğlu et al. 2011).

Tomatoes are one of the most common and important The pest can complete its life cycle in 28–29 days and
vegetable crops in terms of production and consumption has 10–12 generations per year (EPPO 2005). Differ-
all over the world. The tomato leafminer, Tuta absoluta ent control methods have been used against T. absoluta.
(Meyrick), has become the most destructive pest that Pheromone traps have been used to catch the adults and
causes significant losses, since tomato growers had no decrease the population (Ünlü 2011). Chemical control
experience on this pest. The pest was recorded in Tur- has inevitably been used against the pest, because other
key in 2009 (Keçeci 2010). The pest can cause 80–100% control methods do not totally prevent its damage. Reg-
yield loss in greenhouses or field grown tomatoes, if no istered insecticides, mainly Azadirachtin, Metaflumi-
zone and Spinosad have been used if leaves, twigs, stem
or fruits are infested (Kılıç 2011). Although insecticides
*Correspondence: [email protected] are considerably effective to reduce the pest popula-
2
Organic Farming Business Management Department, Faculty of Applied
tion, they can also kill natural enemies and have negative
Sciences, Pamukkale University, 20680 Çivril, Denizli, Turkey effects on human health and environment (Topuz 2013).
Full list of author information is available at the end of the article In addition, there are some reports on unsuccessful

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Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 2 of 7

applications depending on the decreasing susceptibility 29°20’–32°35’East and latitudes 36°07’–37°29’North) and
of tomato leafminer against some synthetic insecticides transferred to healthy tomato seedlings in the climatic
(Desneux et al. 2010). Excessive use of insecticides causes rooms. Healthy plants were regularly transferred to the
an increase in production costs and harm on environ- climatic room and changed with the severely damaged
ment. Pesticide residue is another problem for tomato plants.
export (Durmuşoğlu et al. 2011). Because of the men-
tioned disadvantages of synthetic pesticides, biological Entomopathogenic fungi (EPF)
control gained importance (Topuz 2013). Besides natu- Fungal material used in the study were Beauveria bassi-
ral enemies, EPF are among the biological agents that ana, Isaria fumosorosea and Purpureocillium lilaci-
were used against T. absoluta. Isaria fumosorosea (Wize) num isolates obtained from the culture collection of the
Brown and Smith, Beauveria bassiana (Balsamo) Vuil- Mycology Laboratory of Plant Protection Department,
lemin and Metarhizium anisopliae (Metsch.) Sorokin Faculty of Agriculture, Isparta University of Applied Sci-
are the most common ones (Faria and Wraight 2007). I. ences. EPF were previously isolated from Hyphantria
fumosorosea, which has a wide host range, has been tried cunea Drury pupae and tested against this pest (Sullivan
against different agricultural and forest insect pests as a 2011). Fungal isolates were activated and reproduced
mycoinsecticide (Konopicka et al. 2017). It was also tried on Potato Dextrose Agar (Merck). Spores of the fungi
against tomato leafminer. Blastospores of a strain of this were transferred to a sterile glass bottle after scraping
fungus was applied onto tomato plants with T. absoluta by a sterile scalpel and by washing with sterile distilled
eggs and it was found that the number of pest larvae sig- water containing 0.02% Tween 20, through two layers of
nificantly reduced (Zemek 2013). Similarly, M. anisopliae cheesecloth, in order to separate mycelia. Concentration
var. anisopliae and B. bassiana caused high mortality on of the suspension was adjusted to 2 × ­108 conidia/ml by
the eggs of the pest (Pires et al. 2009). In another study adding some more spores or sterile water.
applied in Turkey, efficiency of B. bassiana on eggs and
first instar larvae of tomato leafminer, seven days after Petri trials
application by dipping method, were 42 and 4%, respec- Third instar larvae of the moth were used in the Petri
tively, whereas M. anisopliae showed 92% efficiency trials. Spore suspensions of the EPF were applied to the
against both stages of the pest (İnanlı et al. 2012). It was larvae, tenderly released from the leaf tissue, by three dif-
also tested against tomato leafminer and found to reduce ferent methods. In the first method, larvae were trans-
the hatching ratio of the pest from 86 to 22% (Yüksel ferred to cheesecloth and dipped into spore suspension
et al. 2017). The aim of this study was to investigate the for 5 s. Then, the larvae were transferred onto tomato
possible use of three EPF against T. absoluta, and to com- leaflets on blotter paper in a sterile Petri dish. In the sec-
pare their effects with Met 52, a mycoinsecticide contain- ond method, larvae were first transferred onto tomato
ing spores (5.5 × ­109 cfu/g) of Metarhizium anisopliae leaflets and then sprayed by the spore suspension. In the
strain F52, and a registered insecticide, Voliam Targo 063 third method; tomato leaves were dipped into spore sus-
SC, under laboratory and greenhouse conditions. pension for 5 s and placed onto blotter paper in a Petri
dish. Then, larvae were transferred onto the leaves. For all
Methods methods, applications made with sterile distilled water,
Plant material instead of spore suspension, were used as controls and
Three weeks old tomato seedlings of H2274 cultivar were the trials were performed by 20 replicate plates (5 larvae
regularly supplied from the commercial growers and in each). Larval mortality rates were determined 3 and
transplanted to 20 cm diameter plastic pots containing 7 days after the applications.
sterilized soil-peat-manure mixture, one seedling per
pot. Seedlings were then grown in a climatic room at the Pot trials
Department of Plant Protection, Faculty of Agriculture, Tomato plants at 8–10 leaf stage grown in plastic pots in a
Isparta University of Applied Sciences, at 25 ± 2 °C tem- clean growth room were used in the pot trials. Efficiency
perature, 60 ± 5% RH and 16:8 h. photoperiod. Tomato of the EPF was determined by three different methods.
plants were transferred to separate growth chambers for In the first method, spore suspension was prepared as
tomato leafminer reproduction and in vivo experiments. in the Petri dish trials and sprayed onto tomato plants.
These plants were then transferred to another climatic
Tuta absoluta room with tomato moth infested plants and kept there
Eggs, larvae and pupae of tomato leafminer, T. abso- for two days in order to ensure infestation. In the second
luta, were collected from the greenhouses in Antalya method, tomato plants with 8–10 leaves were first kept
(situated in south-west Anatolia, between the longitudes for 2–3 days in the moth infested room and then sprayed
Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 3 of 7

with the spore suspensions and transferred to plexiglass 1925). In addition, data on the numbers of death larvae
cages in another room. In the third method, tomato and galleries were subjected to analysis of Variance and
plants were kept in the room with the infested plants for were statistically compared with Tukey test by using SPSS
6–7 days and waited for the pest larvae to form galler- program (SPSS16_Mac_OSX_L).
ies on the leaves, then spore suspensions were applied
and plants were transferred to plexiglass cages in a clean Results
room. Plants sprayed with distilled water were used as In vitro efficiency of EPF
control and the trials were performed with 12 replicate When the effects of EPF in Petri dish trials were evalu-
pots. In order to observe the development of the pest on ated by Abbott formula, it was determined that the
the plants subjected to different applications, 2 leaflets efficacy started 72 h after the application and all fungi
from each plant in 6 replicate pots for each treatment caused death of almost all of the larvae 7 days after the
were harvested every week for 4 weeks. Eggs, larvae, applications. In the first application method (dipping),
pupae and alive individuals of the pest and also the num- in which larvae were dipped into the spore suspensions
ber of the galleries formed by the larvae were counted of the EPF and transferred to clean tomato leaflets in a
under a stereomicroscope. All leaves of the plants in sterile petri dish, B. bassiana caused 87.65% mortality
other three pots were harvested after 15 days, and those 72 h after the application, while I. fumosorosea showed
of remaining three plants were harvested 30 days after the highest effect and killed all larvae after 7 days, as the
the applications, and galleries formed by tomato moth bioinsecticide Met 52 (Table 1). In the second method
and alive individuals were counted. Thus, damage caused (spraying), where spore suspensions were sprayed onto
by T. absoluta was evaluated both by weekly and two or larvae transferred on tomato leaflets in the Petri dishes,
four weeks after the applications. the highest mortality was obtained by Met 52 and fol-
lowed by I. fumosorosea on the third day, but all agents
Greenhouse trials except P. lilacinum killed all larvae after 7 days. In the
Trials were performed in two greenhouses, one of which third application method (residue), where larvae were
was a grower’s greenhouse about one decare in Kumluca transferred onto and fed with tomato leaflets sprayed
District of Antalya Province, and the other with the same with spore suspensions, B. bassiana showed the high-
size, in the campus area of Isparta University of Applied est mortality on the third day and on the seventh day its
Sciences, Isparta Province. Tomato seedlings were trans- effect was similar with Met 52 causing 100% mortality.
ferred to the greenhouses and regular agricultural prac- When the results of Petri dish trials were statisti-
tices were performed. Necessary measures were applied cally evaluated, there was significant difference among
in order to prevent the possible pest and disease damage, the mean numbers of alive larvae, 3 days after applica-
but chemical control was not applied in the greenhouses. tion with EPF, by dipping and spraying methods, while
Before the applications, tomato plants in the greenhouses in the residue method they arranged in the same group
were protected in order to determine the natural infesta- (Table 2). There was no significant difference among the
tion rates of the pest. In the greenhouse in Antalya Prov- mean numbers of alive larvae 7 days after application
ince, infestation rate of the pest was severe enough, while
that in the greenhouse in Isparta was rather low and
infested plants in the growth cages were transferred to Table 1 Efficacy of entomopathogenic fungi against third instar
the greenhouse and two pots per row were placed among Tuta absoluta larvae, 3 and 7 days after applications by three
the plants in order to increase the infestation rate. In the methods in petri dish trials
greenhouses, parcels with 60 plants for each treatment Time after Applications Mortality (%)
were formed for 6 treatments; 3 fungal isolates, bioinsec- applications
(Days) Dipping Spraying Residue
ticide Met 52, a registered insecticide Voliam Targo 063
SC (Chlorantraniliprole 45 g/l + Abamectin 18 g/l, Syn- 3 Beauveria bassiana 87.65 34.07 60.00
genta Company) and control. Label rates of the insecti- Isaria fumosorosea 86.42 64.84 46.67
cides and 2 × ­108 spores/ml concentration of the fungal Purpureocillium 27.58 50.55 48.00
isolates were used in the trial. Applications in the green- lilacinum
houses were made by spraying tomato plants with 8–10 Met 52 67.44 69.77 52.33
leaves. One week after the first application, 30 plants 7 B. bassiana 98.68 100.00 100.00
in each parcel were sprayed again and then plants were Isaria fumosorosea 100.00 100.00 98.57
controlled weekly for four weeks and larvae and galler- Purpureocillium 97.37 98.90 94.29
lilacinum
ies on the leaves were counted. Abbott formula was used
Met 52 100.00 100.00 100.00
to determine the efficiency of the applications (Abbott
Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 4 of 7

Table 2 Mean numbers of alive third instar Tuta absoluta larvae, 3 and 7 days after the applications of entomopathogenic fungi by
three methods in petri dish trials
Applications Number of alive larvae

Dipping Spraying Residue

3 days 7 days 3 days 7 days 3 days 7 days

Beauveria bassiana 0.50d* 0.05b 3.00b 0.00b 1.50b 0.00b

d b d b b
Isaria fumosorosea 0.55 0.00 1.60 0.00 2.00 0.05b
b b c b b
Purpureocillium lilacinum 2.85 0.10 2.25 0.05 1.95 0.20b
c b d b b
Met 52 1.40 0.00 1.30 0.00 2.05 0.00b
a a a a a
Control 4.05 3.80 4.55 4.55 3.75 3.50a
*
Means in the same column followed by the same letters were not significantly different from each other according to Tukey test (P ≤ 0.05)

with EPF and all isolates were found to be effective as the with B. bassiana and P. lilacinum were statistically
bioinsecticide Met 52. arranged in the same group with the control plants,
As a result of gallery counts in the pot trials, 15 and while I. fumosorosea significantly reduced the number
30 days after the application of EPF, all fungi were found of galleries, but not as Met 52 and insecticide Voliam
to be significantly decreased the numbers of galleries Targo (Table 4). However, 7 days after the second appli-
on tomato leaves, compared to controls, when applied cation, all treatments significantly decreased the num-
before or after infestation. However, efficiency of the EPF ber of galleries on the leaves caused by T. absoluta
decreased if the applications were made after infestation compared to control, and I. fumosorosea arranged in
and in the third method, when applications were applied the same group with the insecticide.
after gallery formation, where gallery numbers were As a result of the greenhouse trial carried out in
higher than other methods (Table 3). Galleries could not Isparta Province, the number of galleries on the tomato
be counted 30 days after applications on some plants, plants treated with EPF were significantly less than that
because of the severe damage on the leaves. Efficacy of of control plants. Especially after the second applica-
the EPF as counted by Abbott formula was given in Fig. 1. tion, all treatments decreased the number of galleries
As in the Petri dish experiments, there was no significant and, I. fumosorosea and P. lilacinum were as effective
difference among the efficacy of the EPF against tomato as the insecticides. In the greenhouse trial in Antalya
leafminer damage. According to the pot experiments, it Province, the number of galleries on the tomato
can be mentioned that the EPF should better be applied plants were rather high and very few fruits formed on
before or at the beginning of infestation and applications the plants, while in Isparta Province, less humid than
should be replicated not later than 15 days. Antalya, the number of galleries were less and enough
In the greenhouse trials performed in Antalya-Kum- fruits were produced to evaluate the effects of treat-
luca, according to the counts made one week after the ments on fruit damage. Infested and healthy fruit num-
applications, number of galleries on the leaves sprayed bers showed that all treatments significantly decreased

Table 3 Mean numbers of galleries caused by Tuta absoluta on tomato plants, 15 and 30 days after the application of
entomopathogenic fungi at three methods in the pot dish trials
Applications Mean numbers of galleries / leaf

Dipping Spraying Residue

15 days 30 days 15 days 30 days 15 days 30 days

Beauveria bassiana 12.00b* 33.66b 16.00b 40.66b 36,33b 60.66

b b b b
Isaria fumosorosea 10.33 30.00 13.33 46.33 34,00b, c 55,33
Purpureocillium lilacinum 11.67b 25.00b 15.67b 45.33b 25,33c **
Met 52 9.00b 33.33b 14.00b 39.33b 33.67b, c 59.67
Control 51.33a 64.66a 54.33a 66.66a 56,33a **
*
Means in the same column followed by the same letters were not significantly different from each other according to Tukey test (P ≤ 0.05)
**
Galleries could not be counted because of the severe damage on the leaves
Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 5 of 7

Fig. 1 Efficacy rates of the entomopathogenic fungi on the gallery formation on tomato leaves 15 and 30 days after the applications by three
methods

Table 4 Mean numbers of galleries on the tomato plants in the greenhouses in Antalya and Isparta, 1,2 weeks after applications of
entomopathogens (gallery/plant) and mean rates of infested fruits
Applications Antalya Isparta

gallery/plant gallery/plant Infested fruit (%)

First week Second week First week Second week

Beauveria bassiana 39.10a* 38.25b 11.4b 14.1b 8.0b

b c b b, c
Isaria fumosorosea 23.53 24.37 11.4 9.9 7.3b
a b c b, c
Purpureocillium lilacinum 38.00 37.73 8.0 12.5 6.5b
c d b, c c
Met 52 10.50 9.70 8.9 9.3 6.5b
c c, d c c
Insecticide 13.00 15.03 6.1 8.6 7.0b
a a a a
Control 37.73 52.31 15.0 21.9 12.7a
*
Means in the same column followed by the same letters were not significantly different from each other according to Tukey test (P ≤ 0.05)

the fruit damage and effects of EPF were similar with et al. 2014). As a result of this research performed by
insecticides. Petri dish, pot and greenhouse experiments, it was found
that the EPF; B. bassiana, I. fumosorosea and P. lilaci-
Discussion num significantly reduced the damage caused by the
Tuta absoluta is one of the most economic pest species tomato leafminer. The numbers of galleries on tomato
causing significant damage on tomato plants. Chemical leaves formed by the pest were reduced, especially with
control is mainly used against tomato leafminer, however the applications of the EPF before or at the beginning of
the commonly used insecticides have gradually lost effec- pest infestation. Pot and greenhouse experiments showed
tiveness because the pest developed resistance. Thus, bio- that all the EPF may reduce the damage caused by the
logical control gained importance (Gomez-Valderrama tomato leafminer, however the highest effect similar to
Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 6 of 7

registered insecticides was obtained in the greenhouse to decrease the damage effectively. Other cultural prac-
trials by the two successive applications of I. fumosoro- tices should also be applied to support the EPF.
sea. Various researchers have studied the effects of EPF
Acknowledgements
against the tomato leafminer. Some of them compared Special thanks to the Ministry of Industry and Technology (Project Number:
the effects of EPF against different stages of the pest. M. 00784.STZ.2011-1), Scientific Research Projects Coordination Unite of Süley-
anisopliae Qu-M558 and B. bassiana Qu-B928 isolates man Demirel University (Project Numbers: 2951-YL-11 and 2942-YL-11) and
Bioglobal Company for their financial support and Gregory Sullivan who
recorded 60–80% effective by spraying on the eggs of T. supplied the Hyphantria cunea pupae, from which entomopathogens were
absoluta (Rodriguez et al. 2006a). In another study by the isolated.
same researcher, 68% mortality rates were recorded as a
Author contributions
result of spraying M. anisopliae var. anisopliae Qu-M558 GK, ABE, BAÇ, HA, and İK collaborated in the creation of the manuscript. GK,
and Beauveria bassiana Qu-B912 isolates on the third ABE, BAÇ and HA carried out the experiments, recorded data, interpreted the
stage larvae of T. absoluta (Rodriguez et al. 2006b). In a results, and wrote the manuscript. All authors read and approved the final
manuscript during present study.
research made in Turkey, efficiency rates of B. bassiana
on the eggs and first instar larvae of tomato leafminer, Funding
9 days after applications, were 67, and 12.5% and those Not applicable.
of M. anisopliae were 100, and 92% (İnanlı et al. 2012). A Availability of data and materials
strain of I. fumosorosea, applied to T. absoluta eggs sig- All data generated or analyzed during this study are included in this
nificantly reduced the number of larvae (Zemek 2013). manuscript.
Abdel-Raheem et al. (2015) reported that the highest
mortality rates against tomato leafminer were obtained Declarations
by the applications of B. bassiana and M. anisopliae Ethical approval and consent to participate
isolates on eggs, second and third instar larvae of T. Not applicable.
absoluta, respectively. It was reported that B. bassiana
Consent for publication
preparation obtained by using liquid-semisolid fermen- Not applicable.
tation technique was 95% effective on T. absoluta larvae
(El Kichaoui et al. 2016). Yüksel et al. (2017) determined Competing interests
The authors declare that they have no competing interests.
that the application of B. bassiana and P. lilacinum
against the eggs of T. absoluta had the potential to con- Author details
1
trol the pest. Similar to the obtained results, B. bassi- Department of Plant Protection, Faculty of Agriculture, Isparta University
of Applied Sciences, 32260 Isparta, Turkey. 2 Organic Farming Business
ana and M. anisopliae applied against T. absoluta larvae Management Department, Faculty of Applied Sciences, Pamukkale University,
under laboratory and field conditions were found to be 20680 Çivril, Denizli, Turkey.
effective (Tadele and Emana 2017). In a study conducted
Received: 28 February 2022 Accepted: 18 June 2022
under field conditions in Ethiopia, it was found that the
application of B. bassiana was 74.14% effective against
tomato leafminer (Shiberu and Getu 2017). It has been
emphasized that M. anisopliae and B. bassiana isolates References
are important within the integrated control program Abbott WS (1925) A method of computing the effectiveness of an insecticide.
against T. absoluta in tomato cultivation in greenhouse J Econ Entomol 18:265–267
Abdel-Raheem MA, Ismail IA, Abdel-Rahman RS, Abdel-Rhman IE, Reyad NF
environment in Romania (Roxana 2018). Abebe (2019) (2015) Efficacy of three entomopathogenic fungi on tomato leafminer,
reported mortality rates of T. absoluta larvae in pot and Tuta absoluta in tomato crop in Egypt. Swift J Agri Resea 1(2):15–21
field experiments by B. bassiana application as 67.79 Abebe N (2019) Review on integrated management of tomato leafminer, Tuta
absoluta (Meyrick) (Lepidoptera: Gelechiidae) on tomato under field and
and 61.84%, and by M. anisopliae as 65.77 and 57.95%, glass house conditions. J Biol AgriHealth 9(17):7–13
respectively. Desneux N, Wajnberg E, Wyckhuys AG, Burgio G, Arpaia S, Narvaez- Vasquez
CA, Gonzalez-Cabrera J, Ruescas DC, Tabone E, Frandon J, Pizzo J, Poncet
C, Cabello T, Urbaneja A (2010) Biological invasion of european tomato
Conclusions crops by Tuta absoluta: ecology, geographic expansion and prospects for
This study showed that EPF; B. bassiana, I. fumosorosea biological control. J Pest Sci 83:197–215
Durmuşoğlu E, Hatipoğlu A, Balcı H (2011) Efficiency of some plant extracts
and P. lilacinum can be used against tomato leafminer. against Tuta absoluta (Meyrick, 1917) (Lepidoptera: Gelechiidae) under
However, in vivo trials showed that the efficacy of laboratory conditions. Turk J Entomol 35(4):651–663
EPF may change, depending on the timing of applica- El Kichaoui A, El-shafai A, Muheisen H, Mosleh F, El-Hindi M (2016) Safe
approach to the biological control of the tomato leafminer Tuta absoluta
tions, and the severity of the damage caused by tomato by entomopathogenic fungi Beauveria bassiana isolates from Gaza Strip.
leafminer related with the climatic conditions of the cul- Int J App Res 2(4):351–355
tivation area. Thus, EPF should better be applied before EPPO (2005) Tuta absoluta. European and Mediterranean plant protection
organization. Bulletin 35:434–435
or at the beginning of the infestation of the pest in order
Karaca et al. Egyptian Journal of Biological Pest Control (2022) 32:84 Page 7 of 7

Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a compre-

hensive list with worldwide coverage and international classification of
formulation types. Biol Control 43:237–256
Gomez-Valderrama J, Herrera L, Uribe-Velez D, Lopez-Ferber M, Villamizar L
(2014) An immunological method for granulovirus detection in larvae of
Tuta absoluta: searching for isolates with prospects for biological control
of this pest in Colombia. Int J Pest Manag 60(2):136–143
İnanlı C, Yoldaş Z, Birgücü AK (2012) Effects of entomopathogenic fungi,
Beauveria bassiana (Bals.) and Metarhizium anisopliae (Metsch.) on larvae
and egg stages of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae). Ege
Uni FaculAgri J 49(3):239–242
Keçeci M (2010) Tomato moth Tuta absoluta (Merick) (Lepidoptera: Gelechii-
dae). Voice Agri J 26:9–12
Kılıç T (2011) The tomato moth (Tuta absoluta (Meyrick) (Lepidoptera:
Gelechiidae) of the measures taken for the distribution and struggle in
Turkey. Turkey IV. In: Plant Protection Congress, 28–30 September 2011,
Kahramanmaras, pp. 225
Konopicka J, Bohata A, Zemek R, Curn V (2017) The effects of natural substrates
and artificial media on the production of conidiospores and blastospores
of the entomopathogenic fungus Isaria fumosorosea, strain CCM 8367
microbial and nematode control of invertebrate pests. IOBC-WPRS Bull.
129:58–64
Pires LM, Marques EJ, Wanderley-Teixeira V, Teixeira AAC, Alves LC, Alves ESB
(2009) Ultrastructure of Tuta absoluta parasitized eggs and the reproduc-
tive potential of females after parasitism by Metarhizium anisopliae.
Micron 40:255–261
Rodriguez MS, Gerding MP, France AI (2006a) Entomopathogenic fungi isolates
selection for egg control of tomato moth Tuta absoluta Meyrick (Lepidop-
tera: Gelechiidae) eggs. Agri Tec 66(2):151–158
Rodriguez MS, Gerding MP, France AI (2006b) Effectivity of entomopathogenic
fungus strains on tomato moth Tuta absoluta Meyrick (Lepidoptera:
Gelechiidae) larvae. Agri Tec 66(2):159–165
Roxana C (2018) Microbial inoculants used to control Tuta absoluta (Meyrick,
1917) (Lepidoptera: Gelechiidae). J Horticul For Biotech 22(3):8–17
Shiberu T, Getu A (2017) Evaluation of bio-pesticides on integrated manage-
ment of tomato leafminer, Tuta absoluta (Meyrick) (Gelechiidae: Lepidop-
tera) on tomato crops in western shewa of central Ethiopia. Shiberu and
Getu, Ento Ornithol Herpetol 6(4):1–8
Sullivan GT (2011) Determination of biological control factors of winter pupa
of Hyphantria cunea and determination of the efficacy of entomopatho-
genic fungi. Süleyman Demirel University, Institute of Science, Master
Thesis, Isparta, 70s
Tadele S, Emana G (2017) Entomopathogenic effect of Beauveria bassiana
(Bals.) and Metarrhizium anisopliae (Metschn.) on Tuta absoluta (Meyrick)
(Lepidoptera: Gelechiidae) larvae under laboratory and glasshouse condi-
tions in Ethiopia. J Plant Pathol Micro 8(5):1–4
Topuz E (2013) Historical background, biology, ecology and fighting methods
of Tuta absoluta, Date of access: 17.04.2013. http://​www.​sariv​elile​rtarim.​
gov.​tr/​upload/​dosya​lar/​Tuta%​20abs​oluta. pdf.
Ünlü L (2011) The presence and population growth of tomato moth, Tuta
absoluta (Meyrick), on greenhouse-grown tomatoes in Konya province.
Selçuk J Agri Food Sci 25(4):27–29
Yüksel E, Açıkgöz Ç, Demirci F, Muştu M (2017) Effects of the entomopatho-
genic fungi, Beauveria bassiana, Isaria farinosa and Purpureocillium
lilacinum, on eggs of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae).
Turk J Biol Cont 8(1):39–48
Zemek R (2013) Evaluation of Isaria fumosorosea CCM 8367 against Tuta abso-
luta. In: Entomological Society of America Annual Meeting 2013, https://​
esa.​confex.​com/​esa/​2013/​webpr​ogram/ Paper78780.html

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