International Journal of Tropical Insect Science (2020) 40:199–208

https://doi.org/10.1007/s42690-019-00070-1

ORIGINAL RESEARCH ARTICLE

Influence of biotic and abiotic factors on the population fluctuation

of Tuta absoluta (Lepidoptera: Gelechiidae) in an organic tomato
farming
Flavia da Silva Krechemer 1 & Luís Amilton Foerster 2

Received: 14 May 2019 / Accepted: 29 October 2019 / Published online: 13 December 2019
# African Association of Insect Scientists 2019

Abstract
The tomato leafminer, Tuta absoluta (Meyrick, 1917), is an important pest of tomato in South America, and has been reported in
many countries in Europe and the Middle East. The population fluctuation of this species was examined during three consecutive
crop years, in a commercial organic greenhouse in southeastern Paraná, subtropical region of Brazil. The T. absoluta abundance
was evaluated in the tomato Cordilheira variety during the three crop years, along with TO60 cultivar in the first and Pizzadoro in
the last two periods evaluated. Larvae and pupae of T. absoluta were collected; pest threshold levels were not reached in any of
the crop years examined. A stepwise multiple regression revealed that minimum and mean temperature were factors that
significantly affected the abundance of the tomato leafminer. The peaks of abundance coincided with high previous temperatures.
Larval T. absoluta density was highest during the fruiting stage and the abundance was highest on the Cordilheira variety in all
seasons and during the three crop years. Four species of parasitoids distributed in three families of the order Hymenoptera were
found: Conura sp. Spinola, 1837 (Chalcididae), Earinus sp. Wesmael, 1837 (Braconidae), Myosoma sp. Robertson, 1900
(Braconidae), and Casinaria sp. Holmgren, 1859 (Ichneumonidae). The latter two are cited for the first time parasitizing
T. absoluta. Based on the low level of infestation of the species, our findings demonstrate that the lower temperatures prevent
T. absoluta from becoming a major pest in the evaluated region, characterized by subtropical climate.

Keywords Tomato leafminer . Phenology . Multiple regression . Organic crop . Tomato pest

Introduction 2011; Abbes et al. 2012; Baniameri and Cheraghian 2012;

The tomato leafminer, Tuta absoluta (Meyrick, 1917)
(Lepidoptera: Gelechiidae), has been a limiting factor in to-
mato production in South America since the 1950s (Desneux
et al. 2010). Tuta absoluta is a highly invasive pest and since
2006 has been reported in several countries in Europe, Middle
East, Africa and parts of Asia (Germain et al. 2009; Viggiani
et al. 2009; Kiliç 2010; Roditakis et al. 2010; Desneux et al.
* Flavia da Silva Krechemer
flakrechemer@gmail.com
1 stages of tomato cultivation in Brazil (Guedes and Siqueira
Centro de Ciências Rurais, Universidade Federal de Santa Catarina,
Campus de Curitibanos, Rodovia Ulysses Gaboardi, Km 03,
P.O. Box 103, Curitibanos, SC Zip Code 89520-000, Brazil
2
Departamento de Zoologia, Universidade Federal do Paraná,
P.O. Box 19.020, Curitiba, PR Zip Code 81531-990, Brazil
Campos et al. 2017).
Tuta absoluta is a multivoltine species that mines tomato
leaves, flowers, stems, and fruits (Pereyra and Sánchez 2006).
Damage occurs when larvae bore tunnels in leaves and feed
on the leaf mesophyll (Coelho and França 1987; Fernandez
and Montagne 1990; Uchôa-Fernandes et al. 1995), affecting
the photosynthetic capacity of the plant (Pereyra and Sánchez
2006). The damage caused by this pest can generate losses of
up to 100% of the production, depending of the intensity of
the attack and time of the year (Desneux et al. 2011; Guedes
and Picanço 2012).
Currently, the control of T. absoluta is mainly based on
broad-spectrum insecticides (Guedes and Siqueira 2012;
Campos et al. 2015) and excessive applications occur at all
2012). However, many studies have demonstrated the poten-
tial of this pest to develop resistance to insecticides, including
biopesticides, widely used in organic and traditional agricul-
ture. (Siqueira et al. 2000; Siqueira et al. 2001; Silva et al.
200
2011; Haddi et al. 2012; Silva et al. 2016). In addition, insec-
ticides can act on natural enemies, compromising the imple-
mentation of alternative control methods such as biological
control (van der Blom et al. 2009; Urbaneja et al. 2012;
Campos et al. 2015). Therefore knowledge of the natural en-
emies present in the crop, as well as the factors that affect the
abundance of T. absoluta are important for the development of
Integrated Pest Management programs (IPM).
The interaction of the insect with its host is an important
factor in the population dynamics (Krechemer and Foerster
2017). The development and reproduction of insects, as well
as population growth, depend on the quality of the host plant
(Awmack and Leather 2002). On the other hand, the suscep-
tibility of the plant to insect attack depends on its chemical and
morphological characteristics (Han et al. 2014, 2015; Larbat
et al. 2016). Therefore, the choice of the tomato variety to be
cultivated is an important step in the management of
T. absoluta, since the association of biotic and abiotic factors
will be determinant in the level of infestation of the species.
Other admittedly important factors in insect abundance and
distribution are climate variables (Estay et al. 2009). Drastic
changes in temperature, as well as extreme temperatures, are
important factors that can also prevent insect population
growth (Cornell and Hawkins 1995; Cui et al. 2008; Nigro
et al. 2007). The influence of temperature on a widely distrib-
uted species, such as T. absoluta, may vary according to pop-
ulation origin. In a study conducted by Martins et al. (2016),
with T. absoluta individuals from a tropical climate region, the
authors estimated, based on life table data, the lowest temper-
ature threshold to be 14 °C. On the other hand, Krechemer and
Foerster (2015) in a study conducted with a population from a
subtropical region and with rate of development data, estimat-
ed the same parameter to be 8 °C. Therefore, the temperature
may be a determining factor in the abundance of this species
as a pest in some tomato growing regions.
In tropical regions, where tomato crops are grown year-
round, T. absoluta occurs throughout the year, with peak oc-
currence during the driest months and then a decreased occur-
rence in the wettest periods. This occurs because rain is a
limiting factor for the occurrence and population increase of
the species (Haji et al. 1988; Castelo Branco 1992; Bacci et al.
2019). Tomato is also cultivated in subtropical regions during
the warmest months of the year, and no information is avail-
able from these tomato growing areas where climatic condi-
tions may halt the occurrence of the species during winter.
And if so, can infestation levels reach economic thresholds?
In these regions, information on the population fluctuation of
T. absoluta is especially important, because usually the culti-
vation takes place in greenhouse, protected from the action of
rains. In addition, in the subtropical region of Brazil some
areas have an annual average temperature between 17 and
22 °C, and extremely low temperatures can occur in late fall,
winter and early spring (Alvares et al. 2014). Given this
Int J Trop Insect Sci (2020) 40:199–208
information and the invasive potential of T. absoluta, it is of
great relevance to evaluate pest population fluctuation in sub-
tropical regions where the availability of host plants is
interrupted for some months of the year.
Many factors can affect the seasonality of insect pests, in-
cluding climate, host plant traits and natural enemies occur-
rence (Wallner 1987). Therefore, the objective of this study
was to evaluate the influence of biotic (phenological stages
and varieties of the tomato plant, and natural enemies) and
abiotic factors (minimum, maximum and mean temperatures
and relative humidity) on the population fluctuation of
T. absoluta in an organic tomato crop for three consecutive
seasons in a region with a subtropical climate and interrupted
availability of the host plant.
Material and methods
Study area
The study was carried out in a commercial organic farm in
the municipality of São José dos Pinhais, southeastern
Paraná, Brazil (25° 69′ 63” S, 49° 21′ 74” W). The area
is characterized by fragments of native forest in the sur-
roundings, able to provide shelter and alternative hosts to
natural enemies when the pest is not available in the field
(Thomson and Hoffmann 2009). According to Köppen
classification, the climate of the region is cfb (mesothermal
subtropical humid), characterized by mild summers, fre-
quent frosts and undefined dry season, thus preventing to-
mato cultivation all year round.
Surveys were carried out in four greenhouses, two per sea-
son, with rotation of varieties. The greenhouses were covered
with transparent plastic material, but without side cover. Each
greenhouse was 45 m long, 7 m wide and 2.5 and 3.8 m of
lateral and central height, respectively. The cultivars
Cordilheira, TO60 e Pizzadoro were selected by the producer,
according to commercialization characteristics. Cordilheira
and TO60 are grafted cultivars with rootstock resistant to the
pathogen Ralstonia solanacearum, as the area has a history of
incidence of bacterial wilt disease. However, the latter un-
dergoes early softening during transport, causing losses to
the producer, and for this reason, was replaced by the hybrid
cultivar Pizzadoro, resistant to fungi, bacteria and nematodes.
Six hundred tomato seedlings were planted in each green-
house. The distance between plants was 50 cm, with 110 cm
between lines and a drip irrigation system was used.
The fertilization and soil management followed the proto-
cols recommended for organic agriculture, with application of
cattle manure, magnesium thermophosphate based fertilizer
and granular boric acid. Bordeaux mixture was applied twice
a week as fungicide and no insecticide was used during the
study period.
Int J Trop Insect Sci (2020) 40:199–208
Population fluctuation of T. absoluta in a protected
crop of organic tomato
Weekly surveys were carried out during three crop years be-
tween 2010 and 2013. Sampling was conducted immediately
after seedlings were transplanted and extended to up to two
weeks after harvest. In the three evaluation years seedling
transplantation occurred in the first week of September. In
the 2010/2011 cropping season, sampling of T. absoluta was
done on the Cordilheira and TO60 varieties, with surveys until
the end of April 2011. In the 2011/2012 and 2012/2013 sam-
pling of T. absoluta was done on the Cordilheira and
Pizzadoro varieties, with surveys conducted until May 2012
and March 2013, respectively. The varieties were planted in
separate greenhouses.
Each plant was considered a sampling unit, and in each
survey, 30 plants of each cultivar, excluding border lines, were
randomly selected for counting and collecting all immature
individuals (caterpillars and pupae) of T. absoluta found in
the analyzed part of the plant. Initially whole plants were
examined; after reaching 1 m tall, only the apical half was
inspected; and after plants reached 1.5 m tall, only the apical
third was examined. This methodology was chosen due to the
preference of T. absoluta for ovipositing in the apical third of
the tomato plant (Haji et al. 1988; França and Castelo Branco
1992). Daily data of minimum and maximum temperature, as
well as relative humidity, recorded every 15 min, were obtain-
ed from the meteorological station of the Technological
Institute of Paraná (SIMEPAR) away ca. 20 km from the study
area. The weekly mean of these data (the day following the
date of collection until the next collection), were used in the
statistical analysis.
The collected insects were fed tomato leaves washed with
1% sodium hypochlorite solution to prevent contamination by
pathogens. The individuals were maintained in a climate
chamber at 20 ± 2 °C, 12 h photophase and 70 ± 10% relative
humidity until the emergence of adults of T. absoluta, or larval
parasitoids. Specimens of larval parasitoids were then fixed in
70% alcohol for morphological identification.
Statistical analysis
The influence of abiotic factors on the population fluctuation
of T. absoluta was analyzed with a stepwise multiple regres-
sion (Draper and Smith 1981). The contribution of each var-
iable was determined by the coefficient of determination (r2)
and the p value. Tuta absoluta abundance (weekly average of
caterpillars per plant) was considered the dependent variable
and abiotic factors that could influence the occurrence of the
pest were: minimum, maximum and mean temperatures (°C),
and relative humidity (%). An F value higher than 1.0 were
used as a criterion for a variable to enter in the final model. For
201
this analysis the abundance data were transformed using the
Box-Cox method.
The t-test was used to compare T. absoluta abundance be-
tween varieties in the different seasons in each crop year sep-
arately. The analysis of variance (ANOVA) was used to com-
pare T. absoluta abundance among the seasons, within each
variety, in each crop year. The same test was used to compare
the abundance of this species among phenological stages
(vegetative, flowering, fruiting and senescence) of the plant
in each crop year. In this case, varieties were not discriminated
and the total number of individuals per sampling was used as a
replicate. When differences were found, the Tukey test
(p < 0.05) was used to compare means. Normality and vari-
ance homogeneity were evaluated with the Shapiro-Wilks and
Levene tests, respectively. The datasets that did not meet
ANOVA assumptions of normality and homoscedasticity
were transformed using log (x + 1), for abundance data com-
parison between seasons, and (x + 0.5)1/2, for abundance data
comparison between cultivars. All analyses were performed
with the software Statistica 7.0 (Statsoft 2007).
For all the analysis, the periods with presence of the host
were considered. Parasitism was not considered in the analysis
due to the low number of parasitoids collected.
Results
Population fluctuation of T. absoluta
Despite the availability of food starting in September in the
periods examined, only in 2012/2013 were larvae present in
the field since the beginning of the cropping season. The re-
cords of highest abundance of this species occurred between
December and April, with variations among the periods eval-
uated (Fig. 1), it was preceded by periods of higher
temperature.
The mean number of larvae and pupae collected during
2010/2011 and 2011/2012 was 0.3 and 0.4 insects/plant, sig-
nificantly higher than in 2012/2013, when only 0.08 larvae/
pupae were recorded in each plant (F(2,94) = 4.28; p = 0.01).
No differences were found between the first and second crop
years.
In the 2010/2011 cropping season, T. absoluta immature
specimens were more abundant in Cordilheira cultivar than in
TO60 during the period evaluated (F(1,66) = 3.37; p = 0.03).
Regarding abundance among seasons of the year, no differ-
ences were found for the Cordilheira variety (Table 1). The
same was observed for TO60, as T. absoluta abundance in the
summer did not differ from the spring population. These were
the only seasons when the pest was found in this variety in the
field (Table 1).
In the 2011/2012 cropping season, T. absoluta was record-
ed only in summer and fall, and there was no statistical
202
Fig. 1 Population fluctuation of Tuta absoluta in organic tomato crop in a
subtropical region of Brazil in the crop years 2010/2011, 2011/2012,
2012/2013
difference in the density of T. absoluta between cultivars
Cordilheira and Pizzadoro (F(1,70) = 0.92; p = 0.34). For
Cordilheira, T. absoluta population peaked in the fall, with a
mean of 0.5 individuals per plant and reaching 1.4 in March, if
considered by month (Table 1, Fig. 1). This was the highest
density observed among all crop years evaluated. Densities of
T. absoluta was lower in spring than in fall and summer for
Cordilheira, as well as for Pizzadoro (Table 1).
Int J Trop Insect Sci (2020) 40:199–208
In the 2012/2013 cropping season, T. absoluta was present
in Cordilheira plants since transplanting. Nevertheless, during
the period evaluated, T. absoluta abundance in Cordilheira
plants was not higher than in Pizzadoro (F(1,52) = 2.24; p =
0.14). In the latter, T. absoluta was recorded only in summer.
No differences were found among seasons of the year for
Cordilheira during the last crop examined, but in Pizzadoro
the abundance was significantly higher in summer (Table 1).
Influence of biotic and abiotic factors on T. absoluta
abundance
The stepwise multiple regression analysis revealed that mini-
mum and mean temperature significantly affected T. absoluta
abundance. These factors combined explained 40% of the
variation in the abundance of this pest (Table 2).
The most important factor in the abundance of the species
was the minimum temperature (partial r2 = 0.38) (Table 2),
with the positive coefficient indicating that the increase in
minimum temperature allows the increase of T. absoluta pop-
ulation. The results on abundance related to abiotic factors are
presented in Fig. 2.
The phenological stage significantly affected T. absoluta
abundance. In the 2010/2011 crop, immature specimens were
more abundant during the fruiting stage than in the vegetative
stage, but did not differ from the flowering and senescence
stages (Table 3). In the 2011/2012 crop, T. absoluta was ob-
served only in the fruiting stage, and the mean recorded for
this period was significantly higher than those of other stages.
In the last crop year, no differences in T. absoluta abundance
were found among phenological stages regarding T. absoluta
abundance. However, a continuous increase in population was
observed with a peak in the fruiting stage (Table 3).
Hymenopteran larval parasitoids of T. absoluta from the
families Braconidae, Chalcididae, and Ichneumonidae were
found only in the first two crop seasons. In the 2010/11 crop
one specimen of Conura Spinola, 1837 (Hymenoptera:
Chalcididae), five specimens of Earinus Wesmael, 1837
(Hymenoptera: Braconidae) and four specimens of
Myosoma Robertson, 1900 (Hymenoptera: Braconidae) were
collected. In the 2011/12 crop, only one larval parasitoid of T.
absoluta of the genus Casinaria Holmgren, 1859
(Hymenoptera: Ichneumonidae) was collected. The speci-
mens were deposited in the entomological collection of the
Laboratory of Integrated Insect Control, located in the
Department of Zoology at the Federal University of Paraná,
and assigned the catalog numbers 771, 772, 773 and 774.
Discussion
The seasonal cycle of phytophagous insects varies according
to factors such as climatic changes, food availability, and host
Int J Trop Insect Sci (2020) 40:199–208 203

Table 1 Mean (±SE) of immature specimens of Tuta absoluta recorded per survey in each season during three consecutive crop years

Crop Variety Season

Winter Spring Summer Fall

2010/11 Cordilheira 0.0 ± 0.0 aB 5.6 ± 3.3 aA 7.5 ± 2.0 aA 9.33 ± 4.3 aA F(3,30) = 1,19; p = 0.05
TO60 0.0 ± 0.0 aB 2.8 ± 0.9 bAB 4.0 ± 1.0 bA 0.0 ± 0.0 bB F(1,24) = 0.96; p = 0.34
t – −415.17 −460.99 −249.03
p – 0.00 0.00 0.00
2011/12 Cordilheira – 0.0 ± 0.0 aB 9.7 ± 2.9 aA 15.8 ± 13.4 aA F(2,33) = 16.08; p = 0.00
Pizzadoro – 0.0 ± 0.0 aB 6.9 ± 2.5 bA 5.1 ± 3.5 bAB F(2,33) = 8.59; p = 0.00
t – – −443.84 −245.74
p – – 0.00 0.00
2012/13 Cordilheira 1.3 ± 1.3 aA 0.4 ± 0.4 aA 3.6 ± 1.4 aA – F(2,24) = 3.38; p = 0.05
Pizzadoro 0.0 ± 0.0 bB 0.0 ± 0.0 bB 1.5 ± 0.7 bA – F(2,24) = 5.00; p = 0.01
t −143.40 −467.39 −432.57 –
p 0.03 0.00 0.00 –

Means followed by the same lower case letters in columns (t test) and by the same uppercase letters in rows (Tukey), were not significantly different
(p < 0.05). Hyphens indicate absence of the host and/or pest in the field

phenological stage (Wolda 1988; Spiegel and Price 1996;
Waltz and Whitham 1997). Although tomato crops are culti-
vated throughout the year in some regions of Brazil, in others
it is available for short and irregular periods of time (Bacci
2006), especially when it is part of a crop rotation system. In
subtropical regions of Brazil, tomato is grown between
September and April, which corresponds to spring, summer
and early fall, and it is unfeasible during winter. Species that
exploit resources with an irregular distribution, such as tomato
crops in southern Brazil, tend to have good dispersion ability
(Harrison 1980; Novotný 1994).
Two hypotheses may explain the colonization of tomato
fields by T. absoluta in southeastern Paraná. The first one is
that between harvests, individuals disperse to neighboring
crops in search of alternative hosts, such as the American
black nightshade (Solanum americanum Mill.) and the love
apple (Solanum aculeatissimum Jacq.) (França and Castelo
Branco 1992) and return to tomato plants when available
(Cocco et al. 2015). Love apple is an abundant plant species
in many regions and where the study was conducted.
According to França and Castelo Branco (1992), the architec-
ture of this plant as well as its biochemical and morphological
characteristics are adequate for the development of the tomato
leafminer and can therefore support a population of
T. absoluta between crops. The second hypothesis is that a
fraction of the population can be maintained in the remains
of tomato plants that were not removed or in new tomato
plants that germinate from fallen fruits. The latter is the hy-
pothesis that better explains the presence of T. absoluta soon
after planting in the third cropping year (2012/2013), since the
previous period was extended until mid-May. In addition,
contrary to the recommendation to destroy plants after harvest,
the farmer responsible for the area did not dispose of plant
debris, keeping them until the beginning of the next planting
season. This might have allowed the survival of the population
of T. absoluta in the area during winter (Cocco et al. 2015).
Minimum temperature was the factor that most affected
T. absoluta abundance. In the present study, abiotic data were
obtained from a meteorological station. Nevertheless, the
greenhouse had only top cover (free sides), allowing efficient
exchange of temperature and humidity with the external
environment. Therefore, it is safe to say that the positive
coefficient obtained with the linear regression indicated that
the higher the minimum temperature recorded, the higher the

Table 2 Stepwise multiple regression analysis with abundance of Tuta absoluta as dependent variable and abiotic factors as independent variables and
mean (standard deviation) of the minimum, mean and maximum temperatures (°C), and relative humidity (%) for the evaluated periods

Variable Coefficient SE t value p Cumulative r2 2010/2011 2011/2012 2012/2013

Minimum temperature 0.04 0.33 0.11 0.00 0.38 15.05 (2.44) 14.11 (2.58) 15.48 (2.60)
Mean temperature 0.47 0.37 1.28 0.00 0.40 19.10 (2.26) 18.47 (2.77) 19.85 (2.75)
Relative Humidity 0.10 0.15 0.67 0.30 0.40 82.87 (4.88) 79.58 (7.29) 80.15 (4.11)
Maximum temperature - 0.12 0.26 - 0.46 0.11 0.41 25.41 (2.63) 25.00 (3.59) 25.93 (0.36)
204 Int J Trop Insect Sci (2020) 40:199–208

Fig. 2 Abundance (total number)

of Tuta absoluta (columns) and
abiotic parameters (lines) in or-
ganic tomato crop in a subtropical
region of Brazil in the crop years
2010/2011, 2011/2012,
2012/2013

abundance of T. absoluta and vice versa. Since minimum
temperature is one of the determinant factors in the
occurrence of this species, the seasons of the year were also
expected to affect the density of T. absoluta, as in fact was
observed. The higher density of this pest with the increase in
temperature has been already reported in many studies. Balzan
and Moonen (2012) reported that during the warmest months
in Italy, the population growth of T. absoluta was exponential
and uncontrolled. Other studies in the Mediterranean region
also recorded an increase in the population of T. absoluta co-
inciding with an increase in temperature. (Allache et al. 2012;
Harbi et al. 2012; Cocco et al. 2013, 2015). On the other hand,
in some tropical regions where tomato is cultivated the whole
year, the population peak of the pest occurs in winter (Haji
et al. 1988; Mahmoud et al. 2015; Bacci et al. 2019), which is
attributed to the action of natural enemies and abiotic effects,
such as rain, recognized as a limiting factor for the increase in
population of the species (Castelo Branco 1992). However, in
Int J Trop Insect Sci (2020) 40:199–208
Table 3 Mean (± SE) of immature specimens of Tuta absoluta recorded
in each week during phenological stage of tomato plants during three crop
years in a region with subtropical climate
Phenological stage Number of immature
2010/11 2011/12 2012/13
Vegetative 0.0 ± 0.0 b 0.0 ± 0.0 b 0.6 ± 0.6 a
Flowering 5.3 ± 2.9 ab 0.0 ± 0.0 b 1.7 ± 1.7 a
Fruiting 11.9 ± 6.7 a 14.7 ± 5.4 a 4.4 ± 1.4 a
Senescence 6.0 ± 3.5 ab 0.0 ± 0.0 b 0.0 ± 0.0 a
F(3,30) = 3.50 F(3,32) = 3.42 F(3,23) = 2.14
p = 0.03 p = 0.03 p = 0.12
Means followed by the same letters in columns were not statistically
different by the Tukey test (p < 0.05)
the present study, the population fluctuation of the tomato
leafminer was evaluated in greenhouses and thus, precipita-
tion did not affect population fluctuation of the species.
In areas where tomato is grown year-round, with higher
mean monthly temperatures than in subtropical regions,
T. absoluta is found in all stages of tomato development
(Haji et al. 1988; Castelo Branco 1992; Bacci 2006). In addi-
tion to temperature, uninterrupted food availability may also
promote the continuous growth of this pest. Thus, a favorable
climate, combined with constant host availability, makes this
species the main pest of tomato plants in the tropical areas of
the world. On the other hand, the conditions of the study area
were favorable to the population increase of T. absoluta, be-
cause insects were not subject to rainfall. In addition, the
greenhouses had no lateral cover, which would facilitate the
entry and dispersal of adult insects, besides the absence of
insecticides. Even though all these factors, and although our
study evaluated the number of caterpillars, the levels of
occurrence of the species was always far below the level of
economic damage, established by Martins et al. (2018) of
three eggs per unit sampling (two leaves of the site where
the highest number of eggs can be found according to the
plant’s phenological stage) in any of the three crop years
examined.
In a study conducted with a population from the same re-
gion as the present study, the lowest developmental threshold
estimated for the egg-adult life cycle of T. absoluta was 8.0 °C
(Krechemer and Foerster 2015). Despite the significant influ-
ence of the minimum temperature on the population fluctua-
tion of this species, during field surveys the temperature rarely
reached this lower threshold. Furthermore, Van Damme et al.
(2015) stated that a constant temperature of 5 °C for more than
a month would be necessary to kill 90% of pupae and adults of
T. absoluta, and this temperature condition was not observed
in this study area. The net reproduction rate (R0) and intrinsic
rate of increase (Rm) are usually employed to evaluate the
effects of temperature on insect population growth (Martins
205
et al. 2016). For T. absoluta, the highest Rm was estimated at
30 °C in populations from the tropical region of Brazil. This
same population stops growing when exposed at a constant
temperature of 14 °C. Our results are intriguing if analyzed
exclusively from the point of view of temperature variation,
considering that the average temperature remained above
18 °C in the three seasons evaluated in this study, and that
the studied population is from the subtropical region, and thus
supposedly more adapted to colder climate. In this context, it
was expected a higher population growth in the study area and
that the population reached the control level.
This result strengthens the hypothesis that other factors
limit the population increase of the species in the studied re-
gion. In addition, climatic conditions prevailing in winter do
not allow the growth of tomatoes all year round in this region
and thus the continuous food supply to the insect. The survival
of T. absoluta in alternative hosts during winter has already
been reported (Delrio et al. 2012; Cocco et al. 2015).
However, the subtropical region has long periods of low tem-
peratures and frequent frosts. The susceptibility of the tomato
leafminer to low temperatures has been reported in other stud-
ies (Mahdi and Doumandji 2013; Krechemer and Foerster
2015; Marchioro et al. 2017). Therefore, the climate of the
Brazilian subtropical region, as in the present study, may limit
the maintenance of T. absoluta populations during the winter,
even if alternative hosts are available.
Plant phenology significantly influenced the density of
T. absoluta during the period evaluated. In the three crop years
evaluated, fruiting was the phenological stage with the highest
abundance of T. absoluta. When this pest infests tomato fields
in early vegetative and flowering stages, a progressive popu-
lation increase is expected as generations succeed. This would
explain the peak of occurrence observed coinciding with the
fruiting stage, which is the longest period in the tomato crop.
When the infestation begins soon after planting the seedlings,
the peak occurrence may occur during the flowering stage, as
recorded in Egypt (Mahmoud et al. 2015). When senescence
begins, due to nutritional, chemical, and structural changes,
the insect may leave the tomato plant in search of an adequate
host (Leather 1990; Taha et al. 2013).
In all crop years and seasons evaluated, T. absoluta was
more abundant in the Cordilheira variety. Semiochemical and
nutritional components were not quantified in the three varie-
ties, but field results suggest that Cordilheira is more attractive
to T. absoluta, which might be due to nutritional factors or
higher terpene levels responsible for attracting insects.
Climatic conditions and natural enemies are important fac-
tors in the natural mortality of insects and generally have a
great impact on the population fluctuation (Naranjo and
Ellsworth 2005; Bacci et al. 2018, 2019). Biological control
is one of the most promising options in the control of
T. absoluta, since many natural enemies of the species have
already been registered in South America (Desneux et al.
206
2010). Some of these have been successfully used to control
this species (Luna et al. 2007; Sánchez et al. 2009; Luna et al.
2010). The study area is characterized by fragments of native
forest in the surroundings, able to provide shelter and alterna-
tive hosts to natural enemies when the pest is not available in
the field (Thomson and Hoffmann 2009). Therefore, a more
representative number of parasitoids was expected. Thus, the
absence, of natural enemies in the last year may be due to the
low incidence of hosts in the crop.
Larval parasitoids of T. absoluta were found only in 2010/11,
except for one specimen collected in 2011/12. The occurrence of
parasitoids of the genus Conura and Earinus sp. attacking T.
absoluta have already been reported in the literature (Marchiori
et al. 2004). The presence of specimens of these genera suggests
a close interaction with the host in greenhouses (Marchiori et al.
2004). However, this was the first record of the genera Myosoma
and Casinaria parasitizing T. absoluta. The presence of parasit-
oid species shows the importance of Integrated Pest
Management (IPM) strategies, because the use of disease resis-
tant cultivars, and the absence of insecticide application favor the
occurrence of natural enemies (Desneux et al. 2007; Geiger et al.
2010; Holland et al. 2016). Biological control is one of the main
strategies of IPM, therefore, the record of new parasitoids
attacking T. absoluta may represent one more alternative in the
control of this species. Positive results have been achieved with
augmentative and/or conservation biological control through na-
tive parasitoids (Urbaneja et al. 2012). Therefore, the knowledge
and use of new species of parasitoids may be a key alternative in
maintaining the population of T. absoluta below the level of
economic damage and with reduced use of insecticides.
In conclusion, our study demonstrates that the abundance of
T. absoluta was directly correlated with the increase in minimum
temperatures, with the occurrence of the pest mainly between
December and April. The peaks of abundance coincided with
high previous temperatures, during the fruiting stage and greater
abundance in the cultivar Cordilheira. Based on the low level of
infestation of the species, our findings demonstrate that lower
temperature prevents T. absoluta from becoming a major pest in
the study area, a subtropical region of Brazil. The records of two
new genera of parasitoids of T. absoluta in southeastern Paraná
in addition to the lack of information on its natural enemies in
this region provide valuable information for the cultivation of
tomato in subtropical and temperate regions of Brazil.
Acknowledgements The authors thank the Brazilian National Research
Council (CNPq) for scholarship and financial support, Dr. Maria
Christina de Almeida and Dr. Bolívar Rafael Garcete Barrett for the
identification of larval parasitoids, Mr. Massatoshi Shiono and Mrs.
Sumako Shiono by allowing the study to be carried out in their property
and Dr. Carla Pedroso de Moraes for help in the field work.
Author’s contributions FSK and LA conceived and designed the re-
search. FSK obtained the data and conducted data analyses. FSK and
LA wrote the manuscript. All authors read and approved the manuscript.
Int J Trop Insect Sci (2020) 40:199–208
Funding information This study was funded by Brazilian National
Research Council (CNPq) with scholarship (grant number 140548/
2010–6).
Compliance with ethical standards
Conflict of interest The author Flavia da Silva Krechemer has received
scholarship from Brazilian National Research Council (CNPq).
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