Nativa, Sinop, v. 11, n. 1, p. 115-127, 2023.
Pesquisas Agrárias e Ambientais
DOI: https://doi.org/10.31413/nativa.v11i1.14852
ISSN: 2318-7670
Biological control of termites: a bibliometric and state-of-the-art review
Claudio Brito COÊLHO1, Emmanoella Costa Guaraná ARAUJO2* ,
Iací Dandara dos Santos BRASIL3, Kyvia Pontes Teixeira das CHAGAS3, Thiago Cardoso SILVA3,
Gabriel Agostini ORSO3, Adriano Reis Prazeres MASCARENHAS2, Jhony VENDRUSCOLO2
1Federal Rural University of Pernambuco, Recife, PE, Brazil.
2Federal University of Rondônia, Rolim de Moura, RO, Brazil.
3 PosGraduate Program in Forestry Engineering, Federal University of Paraná, Curitiba, PR, Brazil.
*E-mail: manuguarana@gmail.com
Submission: 01/05/2023; Accepted on 04/10/2023; Published on 04/17/2023.
ABSTRACT: Termites are considered pests and biological control is an environmentally friendly alternative
to reduce pesticide contamination. It was aimed with this study to compile the publications indexed in the
Scopus platform referring to biological control of termites between 1981 and 2019. A total of 143 publications
were found, each of which was read and filtered according to the selection criteria. The studies analyzed were
conducted in 16 countries, with the United States leading the way (44%). A total of 55 termite species and seven
families were recorded in the papers. For the control agents tested, more than 140 species were identified and
classified. Plant insecticides were the most cited, with emphasis on oils and extracts from Azadirachta indica and
Chamaecyparis obtusa. It was noted that most research was conducted on a laboratory scale in the form of
experimental designs. This may limit more comprehensive discussions of the biological termite control agents
tested. Although the use of other control agents is increasing, there is a wide range of insecticides and plant-
derived compounds that can be studied.
Keywords: pesticides; Xylophagous agent; control agents; ecosystem engineers; systematic review.
Controle biológico de cupins: uma revisão bibliométrica e estado da arte
RESUMO: Os cupins são considerados pragas e o controle biológico é uma alternativa ecologicamente correta
para reduzir a contaminação por pesticidas. Objetivou-se com este estudo compilar as publicações indexadas
na plataforma Scopus referentes ao controle biológico de cupins entre 1981 e 2019. Foram encontradas 143
publicações, cada uma delas foi lida e filtrada de acordo com os critérios de seleção. Os estudos analisados
foram realizados em 16 países, com os Estados Unidos liderando (44%). Um total de 55 espécies de cupins e
sete famílias foram registradas nos trabalhos. Para os agentes de controle testados, mais de 140 espécies foram
identificadas e classificadas. Os inseticidas vegetais foram os mais citados, com ênfase em óleos e extratos das
espécies Azadirachta indica e Chamaecyparis obtusa. Foi observado que a maioria das pesquisas foram conduzidas
em escala laboratorial na forma de delineamentos experimentais. Isto pode limitar discussões mais
aprofundadas sobre os agentes biológicos de controle de cupins testados. Embora o uso de outros agentes de
controle esteja aumentando, há uma vasta gama de inseticidas e compostos derivados de plantas que podem
ser estudados.
Palavras-chave: pesticidas; agente Xilófago; agentes de controle; engenheiros de ecossistema; revisão
sistemática.
1. INTRODUCTION
Termites are terrestrial social insects, classified in the
Neoptera superorder, polymorphic and hemimetabolous,
with lengths varying from 3 to 25 mm (CONSTANTINO,
2012; GULLAN; CRANSTON, 2017). Termites are
cosmopolitan but are most often present in Oriental,
Neotropical, and Ethiopian areas, being especially diverse in
tropical forests and savannas (CONSTANTINO, 2012). The
infraorder Isoptera is part of Blattodea order and comprises
nine families: Archotermopsidae, Hodotermitidae,
Kalotermitidae, Mastotermitidae, Rhinotermitidae,
Serritermitidae, Stolotermitidae, Stylotermitidae and
Termitidae (ENGEL, 2011; KRISHNA, 2013).
These insects feed on different forms and sources of
lignocellulosic (alive, dead, or rotten), grasses, hummus,
manure, roots, leaves, stems, and soil detritus
(EGGLETON, 2010; KRISHNA, 2013). Some termites feed
on fungi, by obtaining contaminated material and growing
the fungus inside their nests, feeding on the spores and
mycelium produced (BIGNELL, 2006). Except for a few
arboreal species, termites spend most of their lives building,
foraging, and feeding in or on soil (HOLT; LEPAGE, 2000).
They are known as ecosystem engineers, being especially
important in harsh environments and depleted soils. To
modify the minerals, present in the soil, they dig enormous
galleries and channels that can enhance the stability and
absorption of organic matter (BIGNELL, 2006; GULLAN;
CRANSTON, 2017).
This indicates that termites require a lot of attention in
the forestry and industrialized timber sectors. Studies indicate
Biological control of termites: a bibliometric and state-of-the-art review
Nativa, Sinop, v. 11, n. 1, p. 115-127, 2023.
116
the damage that termites can cause to solid wood structures
as well as their by-products (BATISTA et al., 2022;
MEDEIROS NETO et al., 2022). In addition, increased
seedling mortality and reduced productivity in Eucalyptus spp.
and Pinus spp. plantations, which are among the most widely
cultivated wood species in the world, is reported
(GOVORUSHKO, 2019; PRASTYANINGSI et al., 2020;
EVANS, 2021). These aspects are fundamental for the
timber market in tropical regions, especially in Brazil, which
stands out worldwide in the area of native and planted forests
with robust tropical timber production (MASCARENHAS
et al., 2021; MEDEIROS et al., 2021).
Overall, only a minority of species are considered pests,
by attacking trees, wooden structures, and crops, causing
substantial damage (BIGNELL et al., 2014; GULLAN;
CRANSTON, 2017). Most insects are classified by the
United Nations Environment Programme (UNEP) as pests
due to the losses caused and whether their removal is
economically beneficial. Beyond organic materials like crops,
forests, and pastures, termites can also significantly damage
structures such as buildings, bridges, and dams, along with
furniture, paper, and food (UNEP, 2003).
The traditional method for pest control consists of
applying insecticides based on synthetic organic compounds.
Among these insecticides, POPs (Persistent Organic
Pollutants) stood out for many years. Although effective in
controlling pests, POPs pose risks to the environment and
human safety, due to their capacity for long-range transport,
bioaccumulation, and bioamplification (UNEP, 2003).
Biological control can be a viable alternative to reduce the
impacts caused by pesticides on the environment. Controlled
application of entomopathogens and botanical insecticides
are examples of control agents with low risk of
contamination. Despite being a topic of interest to
agricultural sciences, few studies have been published on the
biotic mechanisms of pest control.
One of the ways to evaluate the scientific production on
these topics is through a systematic review, evaluating
bibliometric data and the state of the art. A bibliometric
review is by the choice of papers through a database that
brings together publications, making it possible to identify
gaps in knowledge and analyze research trends over time
(DONTHU et al., 2021; ARAUJO et al., 2023). Thus, the
objective of the present study was to compile data presented
by scientific publications stored in the Scopus platform about
the biological control of termites, in addition to carrying out
the state-of-the-art on the subject.
2. MATERIALS AND METHODS
2.1. Bibliometric Review
Using the Scopus (Elsevier) database, we searched under
the terms “termite” and “biological control” in titles,
abstracts, and keywords of publications from 1981 to 2019.
The string generated was: TITLE-ABS-KEY ("termite"
AND "biological control") AND (EXCLUDE (PUBYEAR,
2020, 2021, 2022)). The search generated a list of 143
publications, which were identified and accessed individually
through Google Scholar and other specific indexation
platforms. Every publication was read and filtered, with those
aligned with the following criteria being maintained: 1 –
investigation of biological control of termites, even if it is not
the main theme of the production; and 2 – testing of at least
one agent for biological control of termites, except for review
publications. We considered biological control agents to be:
a) those directly extracted from plants, such as essential oils,
extracts, plant tissue, ashes from plant material, or chemical
compounds isolated from plants; b) agents with
entomopathogenic potentials, such as fungi, bacteria, viruses,
nematodes and acari; and c) predators such as ants and larvae
of various species.
After filtering, the remaining papers were classified by: I)
type of publication; II) year of publication; III) authors; IV)
research institution affiliation; V) funding agency; VI) journal
or other publication; and VII) science area (as in Scopus).
Data were tabulated and graphs generated with spreadsheet
management software.
2.2. State of the Art
Aiming to point out efficient methods for termite
control, as well as possibilities for new experiments in the
area, we conducted a systematic review using the filtered
documents. Information was extracted and divided into: a)
site of collection; b) species of termites collected; c) termite
targets; d) study venue (field x laboratory); e) tested control
agents; and f) application spots.
3. RESULTS
3.1. Bibliometric Review
After screening, 68 articles related to the topic were
identified. The documents are classified by Scopus into four
types: article; review (6%); book chapter (3%); and
conference paper (1%). “Article” was the most numerous
categories, corresponding to 85% of publications.
Considering the whole period of this review (1981-2019), the
number of publications addressing the biological control of
termites was rising but is still low. The peaks were in 2017,
with six publications, and 2004-2005, with five publications
each (Figure 1). There were also periods with no publications
indexed in the Scopus database on the subject (1984 to 1989
and 1991 to 1996), giving an average of 1.74
publications/year.
Figure 1. Publications per year on biological control of termites
(1981- 2019).
Figura 1. Publicações por ano sobre controle biológico de cupins
(1981-2019).
A total of 155 authors participated in the publications
about biological control of termites. Of these authors, those
with the highest number of publications are cited below
(Figure 2A). The integration cluster revels that the three top
authors worked together (Figure 2B).
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117
Figure 2. A) The 22 authors with the highest number of publications on the biological control of termites (1981-2019). B) Integration
clusters and main clusters among authors with publications on biological control of termites (1981-2019).
Figura 2. A) Os 22 autores com maior número de publicações sobre controle biológico de cupins (1981-2019). B) Clusters de integração
e clusters principais entre autores com publicações sobre controle biológico de cupins (1981-2019).
Among the 84 institutions with affiliated authors, the
standout was the United States Department of Agriculture
(USDA), with more than 30%, represented by the
Agricultural Research Service (ARS) and Forest Service
(FS) (Figure 3). The United States was the country with the
largest portion of institutions and authors (43%), followed
by Brazil (11%), India (10%), Malaysia (5%), and China
(4%). Identification of institutions/agencies and
nationalities indicates where the subject is being analyzed
the most.
Figure 3. Institutions with numbers of affiliated authors who
published papers on biological control of termites (1981-2019).
Figura 3. Instituições com números de autores afiliados que
publicaram artigos sobre controle biológico de cupins (1981-2019).
Out of the 11 funding agencies presented by Scopus
(Figure 4), the three that funded the most research were
Brazilian governmental agencies, denoting the importance of
public funding for the development of Brazilian research.
Figure 4. Publications on biological control of termites by funding
agencies and institutions, (1981-2019).
Figura 4. Publicações sobre controle biológico de cupins por
agências e instituições de fomento, (1981-2019).
The theme was addressed by 43 journals, with International
Biodeterioration and Biodegradation having the most publications
(9%). Most journals (46%) only published one study. Figure
5 identifies those with at least two documents published
(Figure 5). As for nationalities, there were studies from 14
countries, with 30% of journals being American, 21% British
and 14% Dutch.
There was a huge difference between the nationalities of
journals and authors’ affiliation institutes. Even though less
than 8% of authors were affiliated with European
institutions, more than 55% of studies were published in
journals from Europe. The pattern was the opposite in Asia,
where almost 30% of institutions were based, but
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118
corresponded to less than 7% of publications by nationality
of the journal.
Figure 5. Journals with higher publishing numbers on biological
control of termites (1981-2019).
Figura 5. Periódicos com maior número de publicações sobre
controle biológico de cupins (1981-2019).
Scopus classified studies into 15 categories regarding the
area of science (Figure 6). Areas with the highest occurrence
within publications were: “Agricultural and Biological
Sciences” (48%); “Environmental Science” (17%);
“Immunology and Microbiology” (10%); and “Materials
Science” (7%). This classification is in full accordance with
the subject, as: 1 – The potential of termites as agricultural
and forest pests; 2 – The relevant ecological function
performed by termites in their natural and introduced
habitats; 3 – Biological control methods executed with the
introduction of pathogenic microorganisms, parasites or
through the attack of symbionts present in the guts of
termites; 4 – Especially on urban areas, where the damage
caused by termite attack can have a direct relationship with
the material attacked.
Figure 6. Publications on biological control of termites, classified by
areas of science, according to Scopus (1981-2019).
Figura 6. Publicações sobre controle biológico de cupins,
classificadas por áreas da ciência, segundo Scopus (1981-2019).
3.2. Collection sites
Collections were made in 63 areas. The sites were
described with different levels of specificity. Some articles
gave full description of the area, presenting geographic
coordinates, while some only identified the region where the
collection took place. Some studies were conducted in
multiple collection sites while others focused on a single
collection site. Among the 16 countries, the one with the
most collections was the United States, representing 44%
(Figure 7).
Figure 7. Termite collecting sites by country in publications on biological control of termites (1981-2019).
Figura 7. Locais de coleta de cupins por país em publicações sobre controle biológico de cupins (1981-2019).
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119
3.3. Termite species collected
A total of 55 termite species, from 35 genera and seven
families were counted. Of the 183 reports of termites, 178
identified the isopteran genus and 136 the genus and species.
The families were Rhinotermitidae, Termitidae,
Kalotermitidae, Archotermopsidae, Hodotermitidae,
Stolotermitidae and Mastotermitidae, while the genera were
Coptotermes, Reticulitermes, Nasutitermes, Odontotermes, and
Macrotermes. The most frequent species were Coptotermes
formosanus, Reticulitermes flavipes and Coptotermes curvignathus
(Figure 8).
It is possible to observe a concentration of studies on five
species, representing more than 40% of the studies with
identified species. The genera Coptotermes and Reticulitermes
represented almost 40% of mentions by genus, and 45% of
the studies were on the Rhinotermitidae family. Through the
information gathered, a map was formed representing the
collected species of each country (Figure 9). The diversity of
species was greatest in Brazil, United States and the Asian
continent.
Figure 8. Number of publications on termite biological control
addressing each species.
Figura 8. Número de publicações sobre controle biológico de cupins
abordando cada espécie.
Figure 9. Species collected by country mentioned in publications on biological control of termites (1981-2019).
Figura 9. Espécies coletadas por país citadas em publicações sobre controle biológico de cupins (1981-2019).
3.4. Termite targets and evaluation site (Field x
Laboratory)
More than 30 targets of termite attacks were registered.
These included urban trees, clothing, plastics, paper, and
more frequently structural wood and crops.
The studies used for comparison of the evaluation site did
not include publications categorized by Scopus as “reviews”
or “book chapters”. The experiments were divided between:
experiments that took place in the field, experiments that
took place in a laboratory, or experiments that took place in
both places.
Laboratory experiments represented the vast majority of
studies, with 89%. Simulating the environment of a termite
nest is complex. The cryptic habit of termites, their different
kinds of nests, mechanisms of defense and hygiene, and also
the different kinds of microorganisms that dwell in termite
nests constitute particular habitats for various species.
Among the few studies carried out in the field, only two
reported effective results, one of them through the coating
of a wood piece and the other through spraying of mounds.
3.5. Tested control agents
More than 140 species tested for biological control of
termites were identified and divided into three categories:
pathogens, botanical insecticides, and predators. Botanical
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insecticides were the most cited, also representing the highest
number of species (Figure 10).
Figure 10. Identified species, number of references, and number of
effective species by category of biological control agent.
Figura 10. Espécies identificadas, número de referências e número
de espécies efetivas por categoria de agente de controle biológico.
All told, 24 control agents were utilized more than once.
Also, 11 of these were found to be effective in two or more
studies (Table 1). Among the botanical insecticides, plant oils
and extracts were most frequent. Among the plant sources,
Cupressaceae and Pinaceae were the main families and
Azadirachta indica and Chamaecyparis obtusa were the most cited
species (Figures 11 and 12).
As for pathogens, the most frequent representatives were
fungi and nematodes, particularly the species Metarhizium
anisopliae, Beauveria bassiana and Steinernema carpocapsae (Figures
13 and 14).
Figure 11. Main families utilized to produce botanical insecticides
for termite control.
Figura 11. Principais famílias utilizadas na produção de inseticidas
botânicos para controle de cupins.
Table 1. Effectiveness of tested agents for biological control of termites.
Tabela 1. Eficácia dos agentes testados para controle biológico de cupins.
Control agents
Type
Total applications
Effective applications
Effectiveness (%)
Fungus
33
28
84.9
Beauveria bassiana
Fungus
11
8
72.7
Steinernema carpocapsae
Nematode
6
4
66.7
Heterorhabditis indica
Nematode
5
4
80.0
Serratia marcescens
Bacterial
4
4
100.0
Azadirachta indica
Plant
4
3
75.0
Bacillus thuringiensis
Bacterial
4
3
75.0
Isaria fumosorosea
Fungus
3
3
100.0
Steinernema riobrave
Nematode
3
2
66.7
Heterorhabditis sonorensis
Nematode
2
2
100.0
Jatropha curcas
Plant
2
2
100.0
Figure 12. Number of mentions by the most cited plant species used
to produce botanical insecticides.
Figura 12. Número de menções das espécies vegetais mais citadas
para produção de inseticidas botânicos.
Figure 13. Number of identified species and mentions by group of
pathogens.
Figura 13. Número de espécies identificadas e menções por grupo
de patógenos.
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121
Figure 14. Most mentioned species of pathogens for biological
control of termites.
Figura 14. Espécies de patógenos mais citadas para controle
biológico de cupins.
3.6. Application places
The places were divided into four categories with
applications to substrate being much more frequent than the
others (Figure 15). Effectiveness was superior to 50% for all
the methods used. Overall, the experiments were conducted
in small spaces (commonly Petri dishes). Also, experimental
designs often involved no-choice assays, and even those with
multiple-choice assays did not have ample space. This
reinforces what was pointed out in topic “d”, that the
experimental designs frequently limit the defensive
alternatives for termites and fail to show effective actions of
the tested control agents.
Figure 15. Total and effectiveness of applications by location.
Figura 15. Total e efetividade das aplicações por localidade.
4. DISCUSSION
The survey found several types of publications.
According to Scopus, articles are documents that provide
original research or opinions, which can be published as full
papers in peer-reviewed journals, case reports,
research/technical notes, short communications, and
conference papers, which consist of articles published in the
annals of a conference or symposium (ELSEVIER, 2020).
Publications defined as “Reviews” are those in which there is
significant coverage of previous documents, generally
presenting extended bibliographies and without sections
common to articles, such as “materials and methods” and
“results” (ELSEVIER, 2020). Also, according to Elsevier
(2020), “Book Chapter” is a publication contained in a book
or collection of books.
According to Krishna et al. (2013), studies of termitology
started with classifications published by Linnaeus in the 18th
century and continued with the works of Hagen and Frogatt
in the 19th century, while the leading authors in the 20th
century were Snyder, Emerson, and Grassé. However,
historical records of termites (and the damage caused by
them) date from more than 2200 years ago. Their attack on
dams and dikes was recorded in China (GUI-XIANG et al.,
1994). Research on the biological control of termites started
around 1916, as indicated in the pioneering study of Merril
and Ford, in which parasitic nematodes were found inside
termite heads (PAUL et al., 2018). Since Merril and Ford
discovery, many other biological control agents have been
tested. The oldest one present in this review date to 1981,
conducted by Hänel with the utilization of the fungus
Metarhizium anisopliae (Hänel, 1981).
Identification of the authors of articles of great
importance for bibliometric reviews, since this contributes to
data collection about the subject (SILVA et al., 2020;
ARAUJO et al., 2023). The authors Lax, Osbrink, and Wright
frequently collaborated on each other’s works, making them
the leading research team on the topic (Figure 2). A similar
pattern was found for Wang and Powell, who were co-
authors of four studies presented here. Lax et al. studied the
effects of different control agents, among them fungi,
bacteria, nematodes, and plant extracts on the termite species
Coptotermes formosanus. Wang and Powell targeted C.
formosanus, but also included Reticulitermes flavipes, utilizing the
four previously cited control agents and mites.
Also, Silva et al. (2020) and Araujo et al. (2023) stated that
the identification of institutions/agencies and their
nationalities can contribute to the formation of networks of
institutions and favor the exchange of experiences and
information at different levels, from local to international.
The existence of agencies and mechanisms of funding is of
great importance for the development of scientific research
throughout a region. Hottenrott; Lawson (2014) observed
that academic production is directly affected by funding, not
only on the number of publications but also in the subjects
that are being studied. Areas with significant termite impact
can nevertheless have low academic production on the
subject. Systematic reviews can provide visibility of the
problem and the area.
Termites vary according to habits. Rhinotermitidae are
xylophagous termites commonly living in subterranean nests.
They build large, fast expanding, and diffuse nests in soil or
directly in wood (CONSTANTINO, 2012). Genera are
scattered around the world, especially Coptotermes,
Reticulitermes, and Heterotermes (Bourguignon, 2016). Also
known as the “Formosan subterranean termite”, C. formosanus
is mentioned in the list from the International Union for
Conservation of Nature (IUCN) as “100 of the World’s
Worst Invasive Alien Species”. R. flavipes is also classified as
an invasive species in various countries, such as France
(BAOUDOUIN et al., 2018), Italy (GHESINI et al., 2011),
Pakistan (HASSAN et al., 2017), Germany, Uruguay and
Chile (CONSTANTINO, 2022).
The representatives of the Kalotermitidae family
generally have small colonies do not make direct contact with
soil (CONSTANTINO, 2012). It is a termite basal family and
is dispersed around the globe, with higher numbers in
Oriental and Neotropical zones (Krishna et al., 2013). The
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genera mentioned the most in the articles reviewed were
Cryptotermes and Neotermes, while the most common species
was Cryptotermes brevis. It originated in Peru and Chile, but has
been introduced in a series of other countries in South
America, Europe, Africa, and Oceania (CONSTANTINO,
2022).
Termitidae is the most modern termite family and
corresponds to more than 70% of registered species
(CONSTANTINO, 2022). Their habits and morphology are
varied, normally composed of big colonies and complex
nests, which can be internal or external (CONSTANTINO,
2012). The numbers of species and genera identified in this
review were smaller than those of the Rhinotermitidae. The
most frequent genera were Nasutitermes and Microcerotermes,
with Nasutitermes exitiosus being the most frequent species.
Termites are commonly known for their capacity for
cellulose digestion. This cellulose comes from different
sources, according to each species, and varies from sound
wood to hummus and even fungi (LIMA; COSTA-
LEONARDO, 2007). Although they generally feed on
cellulosic material, the damage caused by termites extends to
other materials as well.
Chouvenc; Su (2010) listed mechanisms that hinder the
biological control of isopterans, pointing out: i) alarm
response/repellency/avoidance behavior; ii) chemical
defense by use of volatile compounds produced by
microorganisms associated with termites; iii) grooming
(cleaning of members and nest); iv) antifungal activity of the
digestive tract; v) humoral immunity; vi) necrophagy
/burial/avoidance of corpses; and vii) competition among
microorganisms.
Observing each point, the utilization of space is an
evident problem. Most isopteran defensive practices are
related to the relocation or isolation of contamination
sources, a practice that is difficult in the small spaces of
laboratories. Therefore, laboratory studies involving
biological control agents of termites mostly consist of tests
of the lethality of the agent (CHOUVENC et al., 2011), since
the simulated environment does not match field conditions.
Botanical insecticides are control agents derived from
plants, and as such, they pose a small risk to the environment
when compared to traditional insecticides (ISMAN, 2014).
The review by Chouvenc et al. (2011), covering studies
from 1960 to 2010, pointed out problems involving the
biological control of termites through the use of fungi,
nematodes, viruses, and bacteria. Some of their observations
were:
1. Reduced experimental protocol, incompatible with the
complex biology of termites. Especially ones developed in
Petri dishes and/or experiments based on no-choice assays,
because they do not provide support for field applications.
2. The data provided were insufficient to define treatment as
effective.
3. High variability of results, suggesting that these
experiments were inconsistent and lacked reliability.
4. The concentrations used were too high (above 107). Since
the microorganisms would not be able to maintain that
concentration level in the field, it makes them unavailable for
field trials.
We also observed the same points, particularly the
incomplete experimental protocol of no-choice assays and
Petri dish evaluations. As for the insufficiency of data, some
publications did not present information on the effectiveness
of tested control agents or did not use control treatment.
Other similarities found between this review and that of
Chouvenc et al. (2017) were the concentration of studies on
Coptotermes and Reticulitermes species. Pathogens used were
also similar; fungi and nematodes were particularly frequent,
with Metarhizium anisopliae and Beauveria bassiana being the
most common control agents.
5. CONCLUSIONS
Through parameters utilized in this review, we observed
that the number of publications per year has been growing.
This shows that research interest in the area is increasing.
Authors affiliated with American research centers and
colleges were responsible for the largest share of
publications, but termite attacks were noticed in multiple
points of the globe. Even though the use of other control
agents is rising, the use of entomopathogens is still
predominant. There is a vast set of plant-based insecticides
and compounds that can be tested for the control of termites.
Differences between field conditions and laboratory
conditions can explain the distinct results of each control
agent tested. There is a need to test control methods that
represent nest conditions more accurately.
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ATTACHMENT
Table 2. Titles, authors, journals and access to the 68 publications used on this review.
Tabela 2. Títulos, autores, periódicos e acesso aos 68 trabalhos utilizados na presente revisão.
Title Authors Journal DOI or Link
Diversity, Roles, and Biotechnological Applications
of Symbiotic Microorganisms in the Gut of Termite
Zhou J., Duan J., Gao M.,
Wang Y., Wang X., Zhao K.
Current Microbiology 10.1007/s00284-018-1502-4
Evaluation of the virulence of entomopathogenic
fungus, Isaria fumosorosea isolates against
subterranean termites Coptotermes spp. (Isoptera:
Rhinotermitidae)
Jessica J.J., Peng T.L., Sajap
A.S., Lee S.H., Syazwan S.A.
Journal of Forestry
Research 10.1007/s11676-018-0614-9
Prospects in sustainable control of oil palm pests
and diseases through the enhancement of
ecosystem services - The way forward
Kamarudin N., Seman I.A.,
Masri M.M.M. Journal of Forestry
Research 10.21894/jopr.2019.0030
Potential fungal control of the subterranean termite
heterotermes indicola (Wasmann)
Aihetasham A., Shariq S.,
Qazi J.I.
Pakistan Journal of
Zoology
10.17582/journal.pjz/2018.50.6.2
093.2098
Toxicity Bacillus thuringiensis-based Bio
Insecticide Enriched with Golden Snail Meat Flour
Against Worker and Soldier Castes of Coptotermes
Curvignathus (Isoptera: Termitidae)
Pujiastuti Y. E3S Web of Conferences
10.1051/e3sconf/20186801029
Isolation and characterization of Metarhizium
anisopliae TK29 and its mycoinsecticide effects
against subterranean termite Coptotermes
formosanus
Keppanan R., Sivaperumal
S., Ramos Aguila L.C.,
Hussain M., Bamisile B.S.,
Dash C.K., Wang L.
Microbial Pathogenesis 10.1016/j.micpath.2018.06.040
The diversity of soil fungus in and around termite
mounds of Globitermes sulphureus (haviland)
(blattodea: Termitidae) and response of
subterranean termite to fungi
Guswenrivo I., Nagao H.,
Lee C.Y.
Sustainable Future for
Human Security:
Environment and
Resources
10.1007/978-981-10-5430-3_4
The potential of Isaria spp. as a bioinsecticide for
the biological control of Nasutitermes corniger
Lopes R.D.S., Lima G.D.,
Correia M.T.D.S., da Costa
A.F., Lima E.Á.D.L.A.,
Lima V.L.D.M.
Biocontrol Science and
Technology 10.1080/09583157.2017.1380163
Effects of heartwood extractives on symbiotic
protozoan communities and mortality in two
termite species
Hassan B., Mankowski M.E.,
Kirker G., Ahmed S.
International
Biodeterioration and
Biodegradation
10.1016/j.ibiod.2017.05.023
Mode of infection of metarhizium spp. Fungus and
their potential as biological control agents Aw K.M.S., Hue S.M. Journal of Fungi 10.3390/jof3020030
Microbial Control of Structural Insect Pests Pereira R.M., Oi D.H.,
Baggio M.V., Koehler P.G.
Microbial Control of
Insect and Mite Pests:
From Theory to Practice
10.1016/B978-0-12-803527-
6.00029-9
Quantifications of phytochemicals and biocide
actions of Lawsonia inermis linn. Extracts against
wood termites and fungi
AdedejI G.A., Ogunsanwo
O.Y., Elufioye T.O.
International
Biodeterioration and
Biodegradation
10.1016/j.ibiod.2016.10.026
Control of primary reproductives of Microtermes
spp. in soil treated with Galleria cadavers infected
with Heterorhabditis indica
Mohan S., Upadhyay A.,
Gupta R. Nematology 10.1163/15685411-00003019
Entomopathogenic nematodes for the
management of subterranean termites
Khan M.A., Ahmad W., Paul
B., Paul S., Khan Z.,
Aggarwal C.
Plant, Soil and Microbes:
Volume 1: Implications
in Crop Science 10.1007/978-3-319-27455-3_16
Variation in subterranean termite susceptibility to
fatal infections by local Metarhizium soil isolates Denier D., Bulmer M.S. Insectes Sociaux 10.1007/s00040-015-0394-6
Behaviour and ecological impacts of termites:
Fecundity investigations in mounds Wako S.E. Ekologia Bratislava 10.1515/eko-2015-0008
Foraging activity of the subterranean sand termite,
psammotermes hybostoma (Desneux) and its
associated fungus metarhizium anisopliae under
natural environmental conditions in El-Fayoum
governorate, egypt
Abd El-Latif N.A., Solaiman
R.H.A. Egyptian Journal of
Biological Pest Control www.cabdirect.org/cabdirect/abs
tract/20153131034
Insecticidal activities of Cunninghamia konishii
Hayata against Formosan subterranean termite,
Coptotermes formosanus (Isoptera:
Rhinotermitidae)
Cheng S.-S., Lin C.-Y., Chen
Y.-J., Chung M.-J., Chang S.-
T.
Pest Management
Science 10.1002/ps.3673
Coêlho et al.
Nativa, Sinop, v. 11, n. 1, p. 115-127, 2023.
125
Characterization of biocontrol traits of
heterorhabditid entomopathogenic nematode
isolates from South Benin targeting the termite pest
Macrotermes bellicosus
Zadji L., Baimey H., Afouda
L., Moens M., Decraemer
W.
BioControl 10.1007/s10526-014-9568-9
Application of bait treated with the
entomopathogenic fungus Metarhizium anisopliae
(Metsch.) sorokin for the control of
microcerotermes diversus Silv.
Cheraghi A., Habibpour B.,
Mossadegh M.S. Psyche (London) 10.1155/2013/865102
Horizontal transmission of the entomopathogen
fungus metarhizium anisopliae in microcerotermes
diversus groups
Cheraghi A., Habibpour B.,
Mossadegh M.S., Sharififard
M. Insects 10.3390/insects3030709
Antitermitic activity of plant essential oils and their
major constituents against termite Odontotermes
assamensis Holmgren (Isoptera: Termitidae) of
North East India
Pandey A., Chattopadhyay
P., Banerjee S., Pakshirajan
K., Singh L.
International
Biodeterioration and
Biodegradation 10.1016/j.ibiod.2012.09.004
When subterranean termites challenge the rules of
fungal epizootics Chouvenc T., Su N.-Y. PLoS ONE 10.1371/journal.pone.0034484
Effect of lectins from Opuntia ficus indica cladodes
and Moringa oleifera seeds on survival of
Nasutitermes corniger
Paiva P.M.G., Santana
G.M.S., Souza I.F.A.C.,
Albuquerque L.P., Agra-
Neto A.C., Albuquerque
A.C., Luz L.A., Napoleão
T.H., Coelho L.C.B.B.
International
Biodeterioration and
Biodegradation 10.1016/j.ibiod.2011.05.008
Subterranean termite prophylactic secretions and
external antifungal defenses Hamilton C., Lay F., Bulmer
M.S. Journal of Insect
Physiology 10.1016/j.jinsphys.2011.05.016
Potential of Metarhizium anisopliae and Beauveria
bassiana in the control of tea termite Microtermes
obesi Holmgren in vitro and under field conditions
Singha D., Singha B., Dutta
B.K. Journal of Pest Science 10.1007/s10340-010-0328-z
Apparent synergy among defense mechanisms in
subterranean termites (Rhinotermitidae) against
epizootic events: Limits and potential for biological
control
Chouvenc T., Su N.-Y. Journal of Economic
Entomology 10.1603/EC09407
A novel strain of Steinernema riobrave (Rhabditida:
Steinernematidae) possesses superior virulence to
subterranean termites (Isoptera: Rhinotermitidae)
Yu H., Gouge D.H.,
Shapiro-Ilan D.I. Journal of Nematology www.ncbi.nlm.nih.gov/pmc/artic
les/PMC3380470/
Infectivity of Metarhizium anisopliae
(Deuteromycotina: Hyphomycetes) isolates to the
arboreal termite Odontotermes sp. (Isoptera:
Termitidae)
Balachander M., Remadevi
O.K., Sasidharan T.O.,
Sapna Bai N.
International Journal of
Tropical Insect Science 10.1017/S1742758409990294
Evaluation of metarhizium anisopliae var.
anisopliae (Deuteromycotina: Hyphomycete)
isolates and their effects on subterranean termite
coptotermes curvignathus (Isoptera:
Rhinotermitidae)
Hoe P.-K., Bong C.-F.J.,
Jugah K., Rajan A.
American Journal of
Agricultural and
Biological Science 10.3844/ajabssp.2009.289.297
Biological alternatives for termite control: A review
Verma M., Sharma S., Prasad
R.
International
Biodeterioration and
Biodegradation 10.1016/j.ibiod.2009.05.009
Anti termite activity of Jatropha curcas Linn
biochemicals Singh N., Sushilkumar Pestology 10.4314/jasem.v12i3.55498
Interaction between the subterranean termite
Reticulitermes flavipes (Isoptera: Rhinotermitidae)
and the entomopathogenic fungus Metarhizium
anisopliae in foraging arenas
Chouvenc T., Su N.Y.,
Elliott M.L. Journal of Economic
Entomology
10.1603/0022-
0493(2008)101[885:IBTSTR]2.0.C
O;2
Non-traditional approaches to subterranean
termite control in buildings Nobre T., Nunes L. Wood Material Science
and Engineering 10.1080/17480270801945413
Susceptibility and behavioral responses of the
dampwood termite Zootermopsis angusticollis to
the entomopathogenic nematode Steinernema
carpocapsae
Wilson-Rich N., Stuart R.J.,
Rosengaus R.B. Journal of Invertebrate
Pathology 10.1016/j.jip.2006.11.004
Resistance of the termite, Coptotermes formosanus
Shiraki to Metarhizium anisopliae due to grooming
Yanagawa A., Shimizu S. BioControl 10.1007/s10526-006-9020-x
Effect of natural products on gut microbes in
Formosan subterranean termite, Coptotermes
formosanus
Doolittle M., Raina A., Lax
A., Boopathy R.
International
Biodeterioration and
Biodegradation 10.1016/j.ibiod.2006.06.023
Biological control of termites: a bibliometric and state-of-the-art review
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Chroniodiplogaster formosiana sp. n. (Rhabditida:
Diplogastridae) from Chinese populations of
Odontotermes formosanus Shiraki (Isoptera:
Termitidae)
Poinar Jr. G., Meikle W.,
Mercadier G. Journal of Nematology https://www.ncbi.nlm.nih.gov/p
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Estimating tree resin dose effect on termites Qian L., Ryu S. Environmetrics 10.1002/env.761
Evaluation of an entomopathogenic fungus,
Paecilomyces fumosoroseus (Wize) Brown and
Smith (Deuteromycota: Hyphomycetes) obtained
from Formosan subterranean termites (Isop.,
Rhinotermitidae)
Meikle W.G., Mercadier G.,
Rosengaus R.B., Kirk A.A.,
Derouané F., Quimby P.C.
Journal of Applied
Entomology
10.1111/j.1439-
0418.2005.00976.x
Differential susceptibility of subterranean termite
castes to entomopathogenic nematodes
Mankowski M.E., Kaya
H.K., Grace J.K., Sipes B.
Biocontrol Science and
Technology 10.1080/09583150400016951
Pathogenicity of paecilomyces lilacinus and
metarhizium anisopliae on microcerotermes sp.
termites (isoptera: Termitidae) [Patogenicidad de
paecilomyces lilacinus y metarhizium anisopliae
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Ana Isabél Gutiérrez G.,
Yamillé Saldarriaqa O.,
Sandra Uribe S., Zuluaqa A
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Revista Colombiana de
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Pathogenicity of Metarhizium anisopliae var.
anisopliae and Metarhizium anisopliae var. acridum
on Nasustitermes coxipoensis (Holmgren)
(Isoptera: Termitidae) [Patogenicidade de
Metarhizium anisopliae var. anisopliae e
Metarhizium anisopliae var. acridum sobre
Nasutitermes coxipoensis (Holmgren) (Isoptera:
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Albuquerque A.C., Pereira
K.C.A., Cunha F.M., Veiga
A.F.S.L., Athayde A.C.R.,
Lima E.A.L.A.
Neotropical Entomology
10.1590/S1519-
566X2005000400008
A strain of the fungus Metarhizium anisopliae for
controlling subterranean termites
Wright M.S., Raina A.K.,
Lax A.R.
Journal of Economic
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Termite feeding deterrent from Japanese larch
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Author Contributions:
C.B.C. - methodology, investigation or data collection, statistical
analysis and writing (original draft); E.C.G.A. - conceptualization,
methodology, investigation or data collection and writing; I.D.S.B.
- conceptualization, methodology, investigation or data collection,
statistical analysis and writing; K.P.T.C. - methodology,
investigation or data collection and writing (proofreading and
editing); T.C.S. - conceptualization, methodology, investigation or
data collection, statistical analysis and writing (original draft,
proofreading and editing); G.A.O - methodology, data collection
and statistical analysis. A.R.P.M. - statistical analysis, validation, and
writing (proofreading and editing); J.V. – statistical analysis,
validation and writing (proofreading and editing); All authors read
and agreed to the published version of the manuscript.
Funding:
Not applicable.
Institutional Review Board Statement:
Not applicable.
Informed Consent Statement:
Not applicable.
Data Availability Statement:
Study data can be obtained by request to the corresponding author,
via e-mail.
Conflicts of Interest:
The authors declare no conflict of interest.