Biological Control 179 (2023) 105179

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Biological Control
journal homepage: www.elsevier.com/locate/ybcon

Performance of two dominant trichogrammatid species of fall armyworm

from China and Africa under contrasted temperature and humidity regimes
Liang-De Tang a, Jia-Wei Sun b, Peng Dai b, Ming-Yue Mu c, Phillip O.Y. Nkunika d,
Nicolas Desneux e, Lian-Sheng Zang a, *
a
National Key Laboratory of Green Pesticide, Key Laboratory of Green Pesticide and Agricultural Bioengineering, Ministry of Education, Guizhou University, Guiyang
550025, China
b
Institute of Biological Control, Jilin Agricultural University, Changchun 130118, China
c
Kweichow Moutai Group, Zunyi 564501, China
d
Department of Biological Sciences, School of Natural Sciences, University of Zambia, 10101 Lusaka, Zambia
e
Université Côte d’Azur, INRAE, CNRS, UMR ISA, 06000 Nice, France

H I G H L I G H T S

• Trichogramma dendrolimi and Trichogrammatoidea lutea are two dominant egg parasitoids of FAW from China and Africa, respectively.
• Performance of both trichogrammatid species on FAW eggs were evaluated under different temperature and humidity conditions.
• T. dendrolimi had a better temperature and humidity adaptation than that of T. lutea.
• T. dendrolimi appears to be a promising candidate for the control FAW under varying environmental conditions.

A R T I C L E I N F O A B S T R A C T

Keywords: The fall armyworm (FAW), Spodoptera frugiperda (J.E. Smith), has become an international pest with its ability to
Spodoptera frugiperda spread rapidly. The FAW has successfully invaded Africa, Asia, and Australia, and recently China. It has become a
Trichogramma serious threat to food security as a major pest of cereals and other crops. Trichogrammatid parasitoids are the
Trichogrammatoidea
dominant biological control agents that have been applied to control lepidopteran pests of crops, vegetables and
Biological control
forests worldwide. The aim of this study was to evaluate parasitism, development, and emergence of two tri­
chogrammatid species, Trichogramma dendrolimi and Trichogrammatoidea lutea, from China and Africa on FAW at
four temperatures (21, 25, 29, 33 ◦ C) and three relative humidity (RH) (30, 60, 90 %) conditions. The tem­
perature and humidity significantly affected the performance of the two trichogrammatid species on their host,
including parasitic ability and development. The parasitism of T. dendrolimi was significantly higher than that of
T. lutea (except for the treatment of 33 ◦ C × RH 60 %) under various temperature and humidity conditions,
however, T. lutea could not parasitize host eggs at 33 ◦ C × RH 90 %. The higher parasitism was observed at 25 ◦ C
and 29 ◦ C, while the lower at 21 ◦ C and 33 ◦ C for both two trichogrammatid species. The developmental time of
T. dendrolimi and T. lutea significantly decreased with the increase of temperature under all three humidity
treatments. The developmental time of T. dendrolimi under different temperature and humidity conditions
(except for the treatment of 33 ◦ C × RH 30 %), was significantly shorter than that of T. lutea. Temperature and
humidity significantly influenced the sexual ratio of T. dendrolimi, the highest female ratio (94.6 %) was recorded
at 33 ◦ C × RH 60 %, while the lowest (79.5 %) was recorded at 25 ◦ C × RH 60 %, but had no effect on T. lutea.
The emergence rate of T. dendrolimi and T. lutea under different temperature and humidity conditions was only
significantly different at 25 ◦ C. Generally, T. dendrolimi had a better temperature and humidity adaptation than
that of T. lutea, thus, T. dendrolimi appears to be a potential candidate for the control FAW under varying
environmental conditions.

* Correspondence author.
E-mail address: lsz0415@163.com (L.-S. Zang).

https://doi.org/10.1016/j.biocontrol.2023.105179
Received 22 September 2022; Received in revised form 27 January 2023; Accepted 30 January 2023
Available online 3 February 2023
1049-9644/© 2023 Elsevier Inc. All rights reserved.
L.-D. Tang et al.
1. Introduction
The fall armyworm (FAW), Spodoptera frugiperda, is a serious crop
pest native to tropical and subtropical regions of the Americas. It has
successfully invaded Africa, Asia, Australia, as well as in Canary Islands
(Kenis et al., 2023). It is a destructive pest of agricultural crops, espe­
cially gramineous crops such as corn, rice, sorghum, wheat etc. (Mon­
tezano et al., 2018; Malo and Hore, 2020; Wang et al., 2022Kenis et al.,
2023). The FAW has a wide host range, wide adaptability, strong
migratory ability, voracious feeding behaviour, high fecundity, and
rapid development of resistance to insecticides (Montezano et al., 2018;
Sisay et al., 2019; Wu et al. 2021Kenis et al., 2023). It can cause corn
yield losses of 8.3 to 20.6 m tonnes per year in 12 major African
corn-producing countries, which represent a range of 21–53 % of the
annual production of corn in the countries involved (Day et al.,
2017Kenis et al., 2023). In Africa, the crop losses caused by FAW were
between US$ 2.5 billion to US$ 6.3 billion in 2017 (Day et al., 2017).
FAW is estimated to cause up to US$13 billion per annum in maize, rice,
sorghum, and sugarcane losses across sub-Saharan Africa (Abrahams
et al., 2017). In America, FAW causes an average of 45 % of crop eco­
nomic loss (Bhandari, 2021), the annual value of yield lost to FAW being
around US$300 million, rising to US$500 million or more in major
outbreak years (Mitchell, 1979). In Brazil, an estimated US$600 million
was spent in 2009 controlling FAW, equivalent to approximately US
$40/ha (Ferreira Filho et al., 2010).
The current management measures used to control FAW have
depended primarily on intensive use of chemical insecticides, even
though the adverse effect of insecticides is well known, such as pesticide
residues in crops, pesticide resistance, negative impacts on non-targeted
organisms and environmental pollution (Desneux et al., 2007;
Richardson et al., 2020; Palma-Onetto et al., 2021). Augmentative bio­
logical control of insects is a tool of integrated pest management (IPM)
programmes due to its effective, sustainable and environmentally
friendly nature (Díaz et al., 2012). The use of parasitoids as biological
control agents is largely used in many agroecosystems. It is reported that
there are more than 121 species of parasitic wasps distributed in 10
families that can be used against FAW (Sun et al., 2021), and ~ 150
different parasitoid species were found to attack FAW in the Americas
(Molina-Ochoa et al., 2004; Salazar-Mendoza et al., 2020; Kenis et al.,
2023). Amongst these parasitoid wasps, Trichogramma species are
important natural enemies, including T. pretiosum, T. chilonis,
T. ostriniae, T. atopovirilia, T. rojasi and T. fasciatum (Sousa et al., 2021;
Jin et al., 2021; Young and Hamm, 1967; DaSilva et al., 2016; Camera
et al., 2010). Being egg parasitoids, they have great advantages for
controlling agricultural pests. They prevent damage to the crops, attacks
the offspring before they hatch, and are relatively easy to mass-produce
(Yang et al., 2016; Dong et al., 2021).
Trichogramma dendrolimi is a generalist parasitoid species, has been
considered as an important biological control agent due to its wide range
of host and because it can be mass-produced on the alternative host eggs
of Antheraea pernyi Guerin-Meneville (Lepidoptera: Saturniidae) (Zhang
et al., 2018; Wang et al., 2020; Zhang et al., 2021b). Trichogramma
parasitoids have been widely used in field conditions in China over the
years (Huang et al., 2020; Zang et al., 2021), and T. dendrolimi was
successfully used to control several agricultural and forest pests (Dong
et al., 2021), such as Ostrinia furnacalis (Zhang et al., 2018; Zang et al.,
2021), Grapholita molesta (Li et al., 2016; Zhang et al., 2021a),
G. funebrana (Qu et al., 2020) and Chilo suppressalis (Yuan et al., 2012;
Zhang et al., 2014; Zang et al., 2021). It is reported that T. dendrolimi
also can effectively parasitize eggs of FAW (Sun et al., 2020), however,
the parasitism rate is significantly affected by host scale thickness (Hou
et al., 2022). Trichogrammatoidea lutea is also a polyphagous egg para­
sitoid of Lepidopteran species (Kfir, 1982), and is indigenous to Africa
(Parsons and Ullyett, 1936). Its hosts include the African bollworm
Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), the spotted
stemborer C. partellus, the spiny bollworm Earias biplaga, and the codling
2
Biological Control 179 (2023) 105179
moth Cydia pomonella (Mawela et al., 2013). Recently, it was found to
parasitize FAW and exhibit better parasitism than other three local
Trichogramma species in China (Sun et al., 2020; Hou et al., 2022). It is
evident that both T. dendrolimi and T. lutea are potential biological
control agents for the control of FAW in China and elsewhere in Africa,
as indigenous parasitoids.
Biotic and abiotic factors significantly affect the performance of
parasitoids (Nechols et al., 1989; Thierry et al., 2022). Among abiotic
factors, temperature and humidity, in particular, influence their per­
formance (Kalyebi et al., 2005a; Emana, 2007). The African continent is
a typical tropical climate with characteristics of high temperature and
low humidity (Alahacoon et al., 2021), while the climate in mainland
China is more complex and diverse (Lei and Gao, 2013). Most regions,
especially the area invaded by FAW in China, are affected by temperate
monsoon and subtropical monsoon climates, showing high humidity
environment (Wu et al., 2022). The aim of this study was to evaluate the
effect of temperature and relative humidity (RH) on parasitism and
developmental fitness of two dominant trichogrammatid species
(T. dendrolimi and T. lutea) of FAW from China and Africa.
2. Material and methods
2.1. Insects
Trichogrammatoidea lutea original population were collected from
FAW on corn fields in Lusaka, Zambia (15◦ 21′ S, 28◦ 27′ E), and intro­
duced from China-aid Zambia Agricultural Technology Demonstration
Centre, in September 2019 (Sun et al., 2021). The local Chinese Trich­
ogramma species T. dendrolimi original population was collected from
parasitized eggs of Chilo suppressalis (Walker) (Lepidoptera: Crambidae)
from rice field at Jilin Agriculture University (Changchun, Jilin Prov­
ince, China) in 2009. In order to coordinate, both of these two pop­
ulations were reared on rice moth Corcyra cephalonica eggs, whose
embryos were killed by ultraviolet (UV), and maintained under labo­
ratory conditions at 25 ± 1 ◦ C, RH 70 ± 5 % and a photoperiod of 14:10
(L:D) h.
The FAW egg mass were originally collected from corn fields located
in Anlong County (25◦ 05′ N, 105◦ 41′ E), Guizhou Province, China in
2019, and the hatching larvae reared in laboratory conditions at 26 ± 1
◦
C, RH 50 ± 5 % and a photoperiod of 14:10 (L:D) h using a basic
artificial diet formula (Bowling, 1967), and modified with adding maize
leaf powder and multivitamins. For the collection of fresh egg masses,
the pupae were collected, and put into a cage (100 mesh, 55 × 55 × 55
cm) under similar conditions as same described above, while waiting for
emergence. Newly emerged adults were fed with 20 % honey water and
allowed to freely oviposit on plastic film, which were stuck on the wall
cage. The egg masses deposited on the plastic films which were of the
scale layer thickness at level I (<80 μm) (Grade standard refer to Hou
et al., 2022) were collected daily between 8:00 and 9:00 h and used for
the experiments.
2.2. Experimental design
One newly emerged (<6h old), mated female parasitoid was intro­
duced into a glass tube (Diameter = 1 cm, Length = 5 cm) with one fresh
egg mass (<8h) containing ~ 100 eggs. The glass tubes were set at four
different temperatures (21, 25, 29, 33 ◦ C) with three relative humidities
(30, 60, 90 %), respectively. A total of 12 treatment combinations for
each parasitoid species were done. Each female adult was allowed to
oviposit for 24 h. There were 15 replicates for each species tested. Tests
involving individuals that died or were subsequently lost during the
experimental period were considered invalid. To avoid the larvae
hatched from unparasitized host eggs to feed parasitized eggs, the larvae
were removed by brush as soon as they hatched. The number of para­
sitized eggs was recorded under a stereoscopic microscope, eight days
after the parasitoids were removed based on preliminary test. The eggs
L.-D. Tang et al. Biological Control 179 (2023) 105179

were checked daily to determine the emergence of parasitoids until no Table 1

further wasps emerged. For each treatment, the number of parasitized Effects of temperature, relative humidity (RH) and parasitoid species (PS) on
eggs (black), the developmental time (d), percent emergence, and sexual biological parameters of Trichogramma dendrolimi and Trichogrammatoidea lutea.
ratio were recorded. The parasitoid sex was identified by the charac­ Biological parameter Variance Source df F P
teristics of the antenna as descripted by Cônsoli et al. (2010). Number of eggs PS 1 248.849 <
parasitized 0.0001
2.3. Data analysis Temperature 3 35.267 <
0.0001
RH 2 0.607 0.5462
The number of eggs parasitized, percent emergence, developmental
PS × Temperature 3 12.930 <
time, and sexual ratio obtained from bioassay experiments were 0.0001
analyzed through three-way ANOVA and means were separated by PS × RH 2 3.985 0.0193
Tukey’s honest significant difference (HSD) test (P < 0.05). Log trans­ Temperature × RH 6 1.450 0.1951
formation of number of eggs parasitized was applied, percent emergence PS × Temperature × 6 1.596 0.1472
RH
and percent female progeny were arcsine square-root transformed to Error 344 – –
homogenize variances and were subjected to the Shapiro–Wilk test fol­ Percent emergence PS 1 4.019 0.0458
lowed by ANOVA. All statistical analyses were performed using the SPSS Temperature 3 23.798 <
version 20 software package (SPSS Inc., Chicago, IL, USA). 0.0001
RH 2 8.555 0.0002
The percent emergence and percent female progeny were calculated
PS × Temperature 2 8.555 0.0002
by following Abbott’s equation (Abbott, 1925). PS × RH 2 7.818 0.0005
Temperature × RH 6 8.078 <
The number of parasitized eggs with emergence holes
Percent emergence = 0.0001
Total number of parsitized eggs PS × Temperature × 5 12.227 <
× 100 RH 0.0001
Error 329 – –
Developmental time PS 1 94.939 <
The number of emerged females 0.0001
Percent female Progeny = × 100 Temperature 3 4445.990 <
Total number of emerged females and males
0.0001
RH 2 4.164 0.0164
3. Results PS × Temperature 3 25.489 <
0.0001
PS × RH 2 3.738 0.0248
3.1. Parasitism of both trichogrammatid species on FAW under different Temperature × RH 6 7.617 <
temperatures and humidities 0.0001
PS × Temperature × 5 4.178 0.0011
Temperature significantly affected the parasitism of the two para­ RH
Error 329
sitoid species, while relative humidity did not. The interaction between
– –
Sexual ratio PS 1 0.761 0.3837
parasitoid species and temperature or humidity also significantly Temperature 3 3.233 0.0226
affected parasitism of the two parasitoid species (Table 1). The effect of RH 2 1.624 0.1988
temperature and relative humidity on parasitism of T. dendrolimi and PS × Temperature 3 3.592 0.0140
PS × RH 2 3.184 0.0427
T. lutea on FAW are showed in Fig. 1. The parasitism of both trichog­
Temperature × RH 6 2.414 0.0269
rammatid species increased first and then decreased with the tempera­ PS × Temperature × 5 3.441 0.0048
ture increase under all three relative humidity levels. The higher RH
parasitism were found on middle temperatures (25 and 29 ◦ C), while the Error 329 – –
lower parasitism were found at 21 and 33 ◦ C in all tested relative hu­
midity levels (Fig. 1).
3.2. Development of both trichogrammatid species on FAW under
We also found that the interaction between temperature and relative
different temperatures and humidities
humidity significantly affected the parasitism of T. dendrolimi. The
parasitism of T. dendrolimi under the combinations of 21 ◦ C × RH 60 %
The parasitoid species, temperature, relative humidity and their in­
(F2,55 = 3.997, P = 0.024) and 33 ◦ C × RH 60 % (F3,63 = 6.772, P =
teractions significantly affected the developmental time of both tri­
0.003) were significantly lower than other accordingly temperature
chogrammatid species (Table 1). The developmental time of
with different relative humidity. There were no significant differences
T. dendrolimi on FAW, in general, significantly decreased with increasing
under 25 ◦ C (F2,57 = 1.483, P = 0.2356) and 29 ◦ C (F3,63 = 0.831, P =
temperature, regardless of relative humidity (30 %: F3,77 = 2613.805, P
0.4413) among different relative humidity conditions. Compared to
< 0.0001; 60 %: F3,63 = 178.325, P < 0.0001; 90 %: F3,65 = 1913.729, P
T. dendrolimi, the parasitism of T. lutea was completely different. The
< 0.0001). Similar results were also found on T. lutea (30 %: F3,70 =
highest parasitism was found on the combination of 25 ◦ C × RH 60 %,
1003.774, P < 0.0001; 60 %: F3,37 = 380.995, P < 0.0001; 90 %: F2,20 =
which was significantly higher than under the same temperature (25 ◦ C)
95.173, P < 0.0001) (Fig. 2). Moreover, the developmental time of both
with different relative humidity conditions (30 % and 90 %) (F2,33 =
trichogrammatid species on FAW was also significantly influenced by
4.731, P = 0.016). For other three temperatures, no significant differ­
relative humidity. The developmental time of T. dendrolimi was signifi­
ences were found on parasitism of T. lutea among different relative hu­
cantly shorter under high relative humidity than that under low relative
midity conditions (21 ◦ C: F2,34 = 2.467, P = 0.100; 29 ◦ C: F2,33 = 0.072,
humidity when at 21 ◦ C (F2,55 = 5.219, P = 0.0084) and 29 ◦ C (F2,53 =
P = 0.931); although T. lutea did not parasitize under the combination of
4.920, P = 0.0109). While it was opposite at 25 ◦ C, shorter develop­
33 ◦ C × RH 90 % (F2,33 = 0.072, P = 0.931). In all tested conditions, the
mental time was found on lower relative humidity (30 %) (F2,57 =
parasitism of T. dendrolimi was significantly higher than that of T. lutea,
12.976, P < 0.0001). For T. lutea, a shorter developmental time was also
except for the combination of 33 ◦ C × RH 60 % (Fig. 1).
found on high relative humidity (90 %) at 29 ◦ C (F2,33 = 3.705, P =
0.0353), but a longer developmental time was found on higher relative
humidity (60 % and 90 %) when at 25 ◦ C (F2,33 = 5.344, P = 0.0098).
However, T. lutea did not develop under the combination of 33 ◦ C × RH

3
L.-D. Tang et al. Biological Control 179 (2023) 105179

Fig. 1. The egg number of Fall Armyworm (means ± SE) parasitized in 24 h by two trichogrammatid species under different temperature and humidity conditions.
Different lower-case letters above the histograms indicate significant difference in number of host parasitized among different relative humidity, per parasitoid
species (at the same temperature). Different upper-case letters above the histograms indicate significant difference in number of host parasitized among different
temperature, per parasitoid species (at the same relative humidity). * indicates significant difference between two parasitoid species (Tukey’s test at P < 0.05).

Fig. 2. The developmental time of two trichogrammatid species on Fall Armyworm (means ± SE) under different temperature and relative humidity conditions.
Different lower-case letters above the histograms indicate significant difference in developmental time among different relative humidity, per parasitoid species (at
the same temperature). Different upper-case letters above the histograms indicate significant difference in developmental time among different temperature, per
parasitoid species (at the same relative humidity). * indicates significant difference between two parasitoid species (Tukey’s test at P < 0.05).

90 %. In addition, T. lutea had longer developmental time than
T. dendrolimi under the same temperature and relative humidity condi­
tions (except for the combination of 33 ◦ C × RH 30 %) (Fig. 2).
3.3. Emergence and sexual ratio of both trichogrammatid species on FAW
under different temperatures and humidities
The emergence of parasitoids was significantly affected by parasitoid
species, temperature, relative humidity and the interactions among
them (Table 1). Significant differences were found in the percent
emergence of T. dendrolimi (F3,77 = 11.249, P < 0.0001) and T. lutea
(F3,75 = 6.772, P = 0.0029) on RH 30 % and RH 60 % among different
temperatures, and both lower percent emergences were showed at 25 ◦ C
with a value of 96.0 % and 81.5 %, respectively. Except for the signifi­
cant difference in the percent emergence of T. dendrolimi (F2,57 = 5.500,
P = 0.0065) and T. lutea (F2,33 = 8.271, P = 0.0012) among the com­
binations of 25 ◦ C with different humidity, there was no difference in the
percent emergence among the combinations of other temperature and
humidity (Fig. 3). We also found that the percent emergence of
T. dendrolimi was significantly higher than that on T. lutea at 25 ◦ C × RH
60 % (P < 0.05, Fig. 3).
Temperature and its interaction with other factors (parasitoid species

4
L.-D. Tang et al. Biological Control 179 (2023) 105179

Fig. 3. The emergence rate of two trichogrammatid species on Fall Armyworm (means ± SE) under different temperature and relative humidity conditions. Different
lower-case letters above the histograms indicate significant difference in parasitoid emergence rate among different relative humidity, per parasitoid species (at the
same temperature). Different upper-case letters above the histograms indicate significant difference in parasitoid emergence rate among different temperature, per
parasitoid species (at the same relattive humidity). * indicates significant difference between two parasitoid species (Tukey’s test at P < 0.05).

and relative humidity) significantly affected sexual ratio, while hu­
midity and parasitoid species did not (Table 1). There was no signifi­
cantly difference in the female ratio of T. dendrolimi among all tested
temperatures under various relative humidity with an exception of RH
60 % (F3,63 = 4.390, P = 0.0072) (Fig. 4). Trichogramma dendrolimi had
higher female ratio than T. lutea under the combinations of 21 ◦ C × RH
30 % and 21 ◦ C × RH 90 %, respectively (Fig. 4).
4. Discussion
Species with especially close dependence on the environment to
meet physiological requirements, such as insects, are highly susceptible
to environmental changes (Colinet et al., 2015; Sanchez-guillen et al.,
2016; González-Tokman et al., 2020). However, many studies have
suggested that species at higher trophic levels seem to be more sensitive
to changes in environmental conditions, meaning, predators and para­
sitoids may face more severe challenges than their prey or hosts (Voigt
et al., 2003; Furlong and Zalucki, 2017). In all of environmental

Fig. 4. The female offspring of two trichogrammatid species on Fall Armyworm (means ± SE) under different temperature and relative humidity conditions.
Different lower-case letters above the histograms indicate significant difference in percentage of female offspring among different relative humidity, per parasitoid
species (at the same temperature). Different upper-case letters above the histograms indicate significant difference in percentage of female offspring among different
temperature, per parasitoid species (at the same relative humidity). * indicates significant difference between two parasitoid species (Tukey’s test at P < 0.05).

5
L.-D. Tang et al.
conditions, however, the most influential factor is the adaptation of a
species or strain to climatic conditions, especially to temperature and
humidity (Yu and Byers, 1994; Smith, 1996). Temperature significantly
influences the performance of Trichogramma species (or strains) on
parasitizing target pests of upland crops (Kalyebi et al., 2005a, b,2006;
Pizzol et al. 2010; Andrade et al., 2011). In contrast, humidity may have
only a limited influence on these parasitoids (Kalyebi et al., 2005b,
2006). When hosts are living on aquatic crops, both temperature and
humidity can significantly affect the performance of Trichogramma
species (Yuan et al., 2012). Temperature and humidity not only affect
the performance of Trichogramma species in aquatic environments, but
also affect their performance in non-aquatic environments. In this study,
besides temperature, humidity also significantly affected the perfor­
mance of T. dendrolimi and T. lutea, including percent emergence,
developmental time and sexual ratio.
Previous researches have showed that T. dendrolimi parasitized the
host eggs over a relative wide temperature range. There were no dif­
ferences in parasitized eggs of T. dendrolimi to C. suppressalis from 18 to
30 ◦ C (Yuan et al., 2012). Our results also indicated that T. dendrolimi
could parasitize FAW eggs at all tested temperatures within the range of
21 to 33 ◦ C. The results of Zhu et al. (2016) indicated that the parasitism
of T. dendrolimi was weakened when exposed to temperatures of over
30 ◦ C, and the most suitable temperatures were 23 ~ 28 ◦ C (Shi and Liu,
1993). Similar results were found in our study, the parasitism of
T. dendrolimi significantly decreased at 33 ◦ C, and performed well at 21
~ 29 ◦ C. Similarly, our results also showed that T. lutea had a relative
wide temperature range, however, it parasitized more eggs at 25 ~ 29 ◦ C
than that at 21 and 33 ◦ C. Generally, the developmental duration
shortened with increasing temperature at the range of 21 to 29 ◦ C, and
then no longer significantly changed at 33 ◦ C for both tested species.
These results were consistent with those of Kalyebi et al. (2005a) who
reported that the development of six trichogrammatid species in Kenya,
with temperature changes. In addition, we found that temperature did
not influence the emergence of both parasitoids in most cases (except
both at 25 ◦ C with RH 30 % for T. dendrolimi, and with RH 60 % for
T. lutea).
There have been a few studies highlighting the effect of humidity on
the parasitic performance of trichogrammatid species in the laboratory,
which showed that most species perform well at 40 ~ 60 % relative
humidity within the temperature range of 20 ~ 29 ◦ C (Smith, 1996). In
this study, the results showed that both T. dendrolimi and T. lutea had a
relative wide humidity range. Within the 30 ~ 90 % relative humidity,
T. dendrolimi can successfully parasitize FAW eggs and complete its life-
cycle at any given temperature, while, T. lutea also can parasitize and
complete its development on host eggs at any given temperature, except
when it is exposed to a high temperature and a high humidity (33 ◦ C ×
RH 90 %). Therefore, high temperature and humidity conditions are not
conducive to T. lutea.
The efficiency of parasitoids in the field is affected by adverse cli­
matic conditions (Kalyebi et al., 2005b); thus, a relatively narrow range
of temperatures and humidity suitable for parasitism would limit the
value of a species for use as a biological control agent in the field (Yuan
et al., 2012). Therefore, in a biological control programme, the micro­
climate condition should be investigated before releasing parasitoids.
Trichogramma dendrolimi is an indigenous parasitoid of China, and it’s
been reported that T. dendrolimi is an effective parasitoid for the bio­
logical control of C. suppressalis due to their wide temperature and hu­
midity adaptation, especially for high humidity (Yuan et al., 2012). And
T. dendrolimi also showed higher parasitism on FAW than other local
Trichogramma species (T. ostriniae, T. leucaniae and T. japonicum) in
northeastern China (Sun et al., 2020), which indicated T. dendrolimi is a
potential biological control agent of FAW. Our findings are highly
consistent with these viewpoints. Trichogramma dendrolimi performed
well on FAW eggs at the low temperature and humidity of 21 ◦ C × RH
30 % as well as the high temperature and humidity (33 ◦ C × RH 90 %).
Therefore, T. dendrolimi could be a potential candidate for biological
6
Biological Control 179 (2023) 105179
control of FAW among different geographical variations. Trichogramma
mwanzai and T. lutea are two native egg parasitoid wasps of FAW in
Zambia, and T. lutea showed that it parasitized more host eggs than
T. mwanzai (Sun et al., 2021). In this study, we found T. lutea had a wide
temperature adaptation. However, the high humidity could significantly
influence the parasitism ability. Under 33 ◦ C × RH 90 %, T. lutea can’t
parasitize FAW eggs. In addition, both net reproduction rate (R0) and
intrinsic rate of increase (rm) of T. lutea were higher at the lower hu­
midity (Kalyebi et al., 2006). Considering various environmental fac­
tors, T. lutea may be better adapted to the African climate of its
provenance and subsequently play a greater role in FAW management.
Using Trichogramma species as natural enemies for biological control
of economically important agricultural and forest lepidopterous pests
have a long history worldwide and made great achievements (Zang
et al., 2021). In China, among all of the utilized Trichogramma species,
T. dendrolimi is considered to be one of the most successful species, not
only because it is a dominant egg parasitoid in various crop agro­
ecosystems (Luo et al., 2014; Hou et al., 2018) but also it can be effi­
ciently mass-produced on the eggs of the Chinese oak silk moth, A. pernyi
(Zhang et al., 2018; Wang et al., 2020; Zang et al., 2021). In addition, the
results from this study showed that T. dendrolimi performed well on
parasitized FAW eggs with a wide temperature and humidity conditions.
All of these factors indicated that T. dendrolimi is a potential biocontrol
agent for the management of FAW. In the current context of the Belt and
Road Initiative, China-Africa agricultural cooperation is expected to
usher in new development opportunities. We envisage whether
T. dendrolimi can be introduced as a cost-effective biocontrol agent to
control FAW in Africa. Meanwhile, the current study also provided a
useful information for utilizing T. lutea to control FAW at different
environmental conditions. Although laboratory studies can reflect
important biological and ecological characteristics of potential biolog­
ical control agents (Kalyebi et al., 2005b), the performance should also
be evaluated under field conditions before speculating or displacing
species to new environments.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This research was funded by the National Natural Science Founda­
tion of China (32172469), and Program of Introducing Talents to Chi­
nese Universities (111 Program, D20023). ND was supported in part by
the Horizon Europe project ADOPT-IPM (n◦ 101060430)
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