termites and microbial biological control strategies
DESCRIPTION
Termitesare very devastating insect pests of agricultural, ornamental crops and dry wood.They are social insect having strong inter-communication, due to which they are very active pests,withboth positive and negative effects on the environment. They are found in every type of soil in the world,and have a broad range of species. Management of termites has been approached with a number of different stretigies, especially chemical pesticides, which have otherenvironmental site impacts. Microbial biological control is defined as the use, and proper adjustment, of natural enemies via microbial organisms, such as; fungi, virus, bacteria, and with the aim of suppression and management of insect populations. A broad range of species, from different groups of microbial organisms, have strong association with termites, and some have been recorded as parasites. Somespecies are currently used as commercial biological control agents of termites.TRANSCRIPT
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
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Research Paper
TERMITES AND MICROBIAL BIOLOGICAL CONTROL STRATEGIES
MUHAMMAD QASIM,
Yongwen Lin, Dalin Fang, Liande Wang*
Insect ecology Lab, Plant Protection College, Fujian Agriculture and Forestry
University, Fuzhou 350002, China
*Corresponding Author
Received 05-07-2015; Revised 22-07-2015; Accepted 25-07-2015
ABSTRACT
Termitesare very devastating insect pests of agricultural, ornamental crops and dry
wood.They are social insect having strong inter-communication, due to which they
are very active pests,withboth positive and negative effects on the environment. They
are found in every type of soil in the world,and have a broad range of species.
Management of termites has been approached with a number of different stretigies,
especially chemical pesticides, which have otherenvironmental site impacts. Microbial
biological control is defined as the use, and proper adjustment, of natural enemies
via microbial organisms, such as; fungi, virus, bacteria, and with the aim of
suppression and management of insect populations. A broad range of species, from
different groups of microbial organisms, have strong association with termites, and
some have been recorded as parasites. Somespecies are currently used as
commercial biological control agents of termites.
Keywords: Termite damage, crops,biological management, fungi, nematodes
Introduction
Termites were reported to be nested
within the Blattaria (Grandcolas, 1994;
Kambhampati, 1995). It is well
established that eusocial termites
evolved from a sub-social ancestor
(Shellman-Reeve, 1997; Thorne,
1997).Termites are hemimetabolous,
social insects and major pests of
different urban and agricultural objects,
such as timber, paper and arables
crops, (Verma et al., 2009; Osipitan and
Oseyemi, 2012), and efficent
decomposers of wood and leaves in
natural systems (Collins, 1981; Noble et
al., 2009). (Korb, 2008b, a).
Termitescomprise four different castes;
king, queen, soldiers and workers
(Suiter et al., 2002), andmature colonies
may contain thousands of individuals
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
34
(Long, 2005), which are Termites are
known to eat faeces, dead termites,
cast-off skin, and debris, and process
these waste materials for building nests
(Song et al., 2006).
There are approximately 3000 species of
termites - including371 which are
considered as pest species - and
comprise eight families, which canbe
divided into two groups on based of
habitat; 1) wood dwelling: i)
Kalotermitidae, ii) Stolotermitidae, iii)
Archotermopsidae, and, 2)
subterranean: i) Hodotermitidae, ii)
Mastotermitidae, iii) Rhinotermitidae, iv)
Stylotermitidae and v) Termitidae
(Krishna et al., 2013). Four of these
families are considered to be
economically important: Kalotermitidae,
Hodotermitidae, Rhinotermitidae and
Termitidae (Legendre et al., 2008).
Kalotermitidae exclusively inhabit wood
(dead, dying and living) and depend on
cellulose, the main structural element
in woody materials (Cabrera and
Scheffrahn, 2011). Hodotermitidae
attacks grasses (Symes and Woodborne,
2010), Rhinotermitidae are largely
subterranean, but invade wood works in
buildings and adjacent trees(Dronnet et
al., 2002), and Termitidae is largest,
and economically most important, both
under the above ground dwellers (Mora
et al., 1996).Four hundred and eighty
six species oftermite have been recorded
in China. These are dominated by
Reticulitermes, Nasutitermes and
Glypptotermes, respectively see Table
(1): as mentioned in below table.
Table 1: Classification of Termites in
China (modified from (Junhong and
Bingrong, 2004) Family Genus Species
Hodotermitidae 1 1
Kalotermitidae 5 36 (Glypototermes) +
28 = 64
Rhinotermitidae 7 111 (Reticulitermes) +
75= 186
Termitidae 31 45 (Nasutitermes) +
190= 235
Total 44 486
Termite as pests
Termitesare a highly devastative and
polyphagous insect pest, which cause
damage to buildings, furniture, plants
and agricultural crops, such as cereals,
pulses, oil crops, sugarcane, vegetables,
fruits and root crops (Table 2). Termites
cause estimated losses of US$22 billion
annualy across the globe(Govorushko,
2011). In China losses attributed to
termites were estimated at US$0.3
billion, in 2004(Junhong and Bingrong,
2004).
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Table2: Crops Attacked by Termites Cereals Maize Brazil (Constantino,
2002), Ethiopia (Cowie et
al., 1990; Wood, 1991),
Ghana (Maayiem et al.,
2012), India (Tomar,
2013), Malawi (Munthali
et al., 1999), Saudi Arabia
(Faragalla and Al Qhtani,
2013), Uganda (Orikiriza
et al., 2012), Zimbabwe
(Thierfelder et al., 2013)
Sorghum Africa (Zida et al., 2011),
India (Srivastava, 1984;
Tomar, 2013), Pakistan
(Ahmed et al., 2004),
Malawi (Nyirenda et al.,
2007), Saudi Arabia
(Faragalla and Al Qhtani,
2013), Uganda (Orikiriza
et al., 2012)
Rice Benin (Togola et al.,
2012a; Togola et al.,
2012b), Brazil (Rouland-
Lefèvre, 2011), Ghana
(Maayiem et al., 2012),
India (Tomar, 2013),
Indonesia (Brown and
Marten, 1986), Nigeria
(Nwilene et al., 2008;
Agunbiade et al., 2009),
Philippines (Reissig et al.,
1986; Acda, 2013)
Barley Ethopia (Taye et al.,
2013), India (Bhanot et
al., 1984; Kharub and
Chander, 2012), Saudi
Arabia (Badawi et al.,
1986), Ethiopia (Kuma et
al., 2011)
Millet China, Ghana (Maayiem et
al., 2012), India (Rathour
et al., 2014), Nigeria
(Mohammed et al., 2014),
Saudi Arabia (Faragalla
and Al Qhtani, 2013),
Sudan (Pearce et al.,
1995), Yemen (Wood et al.,
1987)
Wheat Ethopia (Taye et al.,
2013), India (Rathour et
al., 2014), Pakistan
(Ahmed et al., 2004),
Tanzania (Mwalongo et al.,
1999), Yemen (Wood et al.,
1987)
Pulses Beans Sudan (Pearce et al.,
1995), Tanzania
(Mwalongo et al., 1999),
Zambia (Sileshi et al.,
2009)
Cowpea Ghana (Maayiem et al.,
2012), Nigeria
(Mohammed et al., 2014),
Zambia (Sileshi et al.,
2009)
Pigeon pea China (Rao et al., 2002),
India (Reddy et al., 1992),
Nigeria (Dialoke et al.,
2010; Dasbak et al.,
2012), Uganda (Nahdy et
al., 1994), Zambia (Sileshi
et al., 2008)
Chickpea India (Yadav et al., 2013)
Oil crops Groundnut Australia, Bangladesh
(Biswas, 2014), China,
Ethiopia, Ghana (Maayiem
et al., 2012), India (Gold
and Wightman, 1991),
Malawi (Umeh et al.,
2001), Saudi Arabia
(Faragalla and Al Qhtani,
2013), Uganda (Orikiriza
et al., 2012), Yemen (Wood
et al., 1987)
Sunflower India (Basappa, 2004),
Pakistan (Aslam et al.,
2000), Zambia (Sileshi et
al., 2009)
Soybean Kenya (Terano, 2010),
Tanzania (Bigger, 1966),
Zambia (Sileshi et al.,
2009)
Sesame Ethopia (Taye et al.,
2013), Nigeria
(Mohammed et al., 2014),
Sudan (Pearce et al.,
1995), Yemen (Wood et al.,
1987)
Vegetables Tomato Saudi Arabia (Faragalla
and Al Qhtani, 2013),
Sudan (Pearce et al.,
1995), Yemen (Wood et al.,
1987)
Okra Saudi Arabia (Faragalla
and Al Qhtani, 2013),
Sudan (Pearce et al.,
1995)
Pepper Saudi Arabia (Faragalla
and Al Qhtani, 2013)
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Egg plant Saudi Arabia (Faragalla
and Al Qhtani, 2013)
Cotton Africa, China, India (Tomar, 2013),
Malawi, Pakistan, Sudan, Tanzania,
Uganda, Yemen (Wood et al., 1987),
Zambia (Sileshi et al., 2009)
Root Crops Potatoes Australia, India (Tomar,
2013), Uganda (Orikiriza
et al., 2012)
Yam Ghana (Maayiem et al.,
2012), Nigeria
(Mohammed et al., 2014)
Cassava China (Gui‐Xiang et al.,
1994), Ghana, India (Lal
and Pillai, 1981), Nigeria
(Mohammed et al., 2014),
Zambia (Sileshi et al.,
2009)
Sugarcane Argentina (Constantino, 2002),
Australia, Bangladesh (Alam et al.,
2012), Brazil (Rouland-Lefèvre, 2011),
Chad (Rouland-Lefevre and Mora, 2002),
China (Zeng, 2004), Colombia, Cuba,
India (Tomar, 2013), Kenya, Mexico,
Nigeria (Collins, 1984), Pakistan (Ahmed
et al., 2007), Philippines, Uganda
(Orikiriza et al., 2012), Somalia, Africa,
Sudan
Tobacco Sudan (Pearce et al., 1995), Pakistan
(Shah et al., 2013), Yemen (Wood et al.,
1987)
Table 3: Plants attacked by termites Fruit
Plants
Guava India, Saudi Arabia (Faragalla
and Al Qhtani, 2013)
Coffee Argentina, Brazil (Neves and
Alves, 1999a), Ethopia (Taye et
al., 2013), Ghana (Ackonor,
1997)
Citrus Afghanistan, Algeria, America
(Stansly et al., 2001), Australia,
Ethopia (Taye et al., 2013),
India, Iran, Iraq, Israel, Saudi
Arabia (Faragalla and Al Qhtani,
2013)
Banana Ethopia (Taye et al., 2013),
Hawaii (Lai et al., 1983), Malawi
(Munthali et al., 1999), Saudi
Arabia (Faragalla and Al Qhtani,
2013)
Mango Ethopia (Taye et al., 2013), India
(Tomar, 2013), Hawaii (Lai et al.,
1983), Pakistan (Javaid and
Afzal, 2001), Philippines (Acda,
2013), Saudi Arabia (Faragalla
and Al Qhtani, 2013)
Papaya Hawaii (Lai et al., 1983), Saudi
Arabia (Badawi et al., 1986)
Grapes Australia, India, Saudi Arabia
(Faragalla and Al Qhtani, 2013)
Mulberr
y
China (Kai et al., 2001),
Pakistan (Ahmed and Qasim,
2011), Saudi Arabia (Badawi et
al., 1986)
Pineapp
le
Argentina, Australia, Brazil,
Kenya, Paraguay, Uruguay
Almond Saudi Arabia (Faragalla and Al
Qhtani, 2013)
Litchi China (Gui‐Xiang et al., 1994)
Plum China (Gui‐Xiang et al., 1994)
Palm
Trees
Date
palm
Saudi Arabia (Faragalla and Al
Qhtani, 2013), Sudan (Wood
and Kambal, 1984; Logan and
El-Bakri, 1990), Tunisia, UAE
(Kaakeh, 2006)
Coconu
t
Africa (Rouland-Lefèvre, 2011),
China (Tang et al.,
2006), Indonesia (Mariau et al.,
1992), Indonesia (Mariau et al.,
1992), Tanzania (Materu et al.,
2013)
ForestPla
nts
Rubber
Plant
China (Yan et al., 2001),
Indonesia (Herlinda et al., 2010)
Pine Africa (Wardell, 1987), America
(Little et al., 2014), Australia,
China (Kai et al., 2001),
Pakistan (Javaid and Afzal,
2001)
Eucalyp
tus
Africa (Rouland-Lefèvre, 2011),
Brazil (Constantino, 2002),
Australia (Werner et al., 2008),
China (Gui‐Xiang et al., 1994),
Portugal (Nobre et al., 2009),
Saudi Arabia (Faragalla and Al
Qhtani, 2013), Uganda (Nyeko
and Nakabonge, 2008; Orikiriza
et al., 2012)
Magnoli
a
China (Kai et al., 2001)
Dalbergi
a
China (Kai et al., 2001),
Pakistan (Javaid and Afzal,
2001)
Tea Bangladesh (Ahmed, 2012), China
(Muraleedharan, 1992), India (Gulati et al.,
2006; Singha et al., 2011; Pandey et al.,
2013), Kenya (Adoyo et al., 1997), Sri Lanka
(Danthanarayana and Vitarana, 1987;
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
37
Hemachandra et al., 2014), Tanzania
(Ndunguru, 2006)
Microbial biological control of
termites
Termite pest management efforts have
been focused mostly on subterranean
and arboreal nesters,and have
employed a variety of microbial
biological control agents, including
viruses(Al Fazairy and Hassan, 1988b),
fungi (Sun et al., 2003; Dong et al.,
2007; Dong et al., 2009), bacteria
(Khan, 2006; Devi, 2013), and
nematodes (Wilson-Rich et al., 2007).
Fungi
A variety of entomopathogenic fungi
(EPF) have been used in the
management of insect pests. Their
environmental persistence makes EPF
an effectivy biological control agent.
Various strains of EPF are effective
against different insect life stages, and
may act as ecto-parasites (infecting
through cuticle contact) or as endo-
parasites, (enter into the body, and
producing toxins). Effective EPF should
fulfil certain fundamental prerequisites,
such as 1) high infectivity for the target
insect, 2) fungal growth and sporulation
must occur at appropriate
temperaturesand under environmental
conditions and 3) EPFs must be
relatively stable(Hänel, 1982b).
A number of EPF strains, which meet
these conditions, have been
recommended against a diversity of
insects, such as Beauveria spp.
(Hypocreales: Cordycipitaceae),
Metarhizium spp. (Hypocreales:
Clavicipitaceae) and Lecanicillium spp.
(Hypocreales: Cordycipitaceae).EPF
fungi (Metarhizium anisopliae, M.
flavoviride, Paecilomyces lilacinus, P.
fumosoroseus and Beauveria bassiana)
were checked by different researchers
against different insect pests and
proved to very good bio-control agents,
such as termites (Neves and Alves,
1999b; Krutmuang and Mekchay, 2005;
Chouvenc et al., 2009a; Chouvenc et al.,
2009b), aphids (Li and Sheng, 2007;
Chen et al., 2008; Ownley et al., 2010),
whiteflies, thrips, mites, lepidopteran
larvae, weevils, grasshoppers (Faria and
Wraight, 2007; Kabaluk et al., 2010)
and mosquitoes (Fang et al., 2011).
Table 4: Pathogenic Fungal Species
associated with Termites # Species Isolate References
1 Aspergillus
sp.
(Pandey et al.,
2013)
2 Aspergillus
flavus
(Henderson, 2007)
3 A. fumigatus (Chai, 1995)
4 Beauveria
bassiana
(Neves and Alves,
1999a)
787 (Jones et al., 1996)
1683
3040
3041
2A3 (Lai et al., 1982)
N-22
T-27
PHP =
Philippin
es
(Khan et al., 1993b)
NDL =
New
Delhi
BNG =
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Bangalor
e
CBE =
Coimbato
re
BPT =
Bapatla
(Andhra
Pradesh)
ATCC
90519
(Wright and Lax,
2013)
ATCC
26037
ATCC
90518
ATCC
26037
(Kramm and West,
1982)
NRRL
3108
BB
79211
5 Conidiobolus
sp.
(Altson, 1947)
6 Conidiobolus
coronatus
(Sajap et al., 1997)
7 Cordycepioid
eus bisporus
(Ochiel et al., 1996)
8 Entomophtho
ra coronata
(Yendol and
Paschke, 1965)
9 E. virulenta
10 Gliocladium
virens
ATCC
9645
(Kramm and West,
1982)
11 Gloeophyllu
m trabeum
(Grace et al., 1992)
12 Hirsutella
thompsonii
F52 (James, 2009)
13 Isaria
fumosorosea
(Wright and Lax,
2013)
14 Metarhizium
anisopliae
(Neves and Alves,
1999a)
346 (Jones et al., 1996)
472
2162
Tonga (Lai et al., 1982)
10B
MM-773
Ga1 (Ahmed et al., 2009)
Ga3
Ga4
NRRL
5530
(Kramm and West,
1982)
15 M. anisopliae
var.
anisopliae
(Khan et al., 1993b)
16 M. anisopliae (Jarrold et al.,
var. acridum 2007)
17 M. anisopliae
var.
dcjhyium
(Dong et al., 2009)
18 M. flavoviride (Wells et al., 1995)
19 M. flavoviride
var. minus
(Khan et al., 1993b)
20 Paecilomyces
lilacinus
(Khan et al., 1993b;
Sharma et al.,
2013) 21 P.
fumosoroseu
s
22 P. cicadae (Chai, 1995)
They rupture the cuticle of insect, to
reach the hemocoel,through
degradation of the cuticle with enzymes,
such as; chitinase, protease and lipase,
which each act on the different
components of the cuticle(Breeding et
al., 2012; Khan et al., 2012).
a- Proteases: Saprophytic fungi
produce prophenol oxidase in the
hemolymph to activate the protein
degrading enzymes proteases,
collagenases, and chymoleastases
(Sheng et al., 2006; Khachatourians
and Qazi, 2008). For this purpose
certain genes are responsible like
conidiation associated genes (cag),
which encode subtilisin-like
proteinase (Pr1) (Small and
Bidochka, 2005) resulting over
expression of phenol oxidase in the
hemolymph leading to the feeding
reduction of insects (St Leger et al.,
1996).
b- Chitinases: The cuticle is mainly
composed of chitin, which is
degraded by endo and exo-chitinases
through the breaking of N-
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Acetylglucosamine (Kubota et al.,
2004), produced by certain fungi
releasing chitinolytic enzymes (St
Leger et al., 1996; Valadares-Inglis
and Peberdy, 1997), which are
encoded by a chitinase gene (Chit1)
(Screen et al., 2001), chitinase gene
(Chi2) (Baratto et al., 2006) and B.
bassiana chitinase gene (Bbchit1)
(Fang et al., 2005).
Fungicide application on the symbionts
of Macrotermitinae was tested by (El-
Bakri et al., 1989). Death of the
symbiont blocks the assimilation of
foraged food by the termite and the
whole colony dies. Erpacide® 450T and
490T were effective against
termites(Rouland-Lefevre and Mora,
2002).
Field efficiency of fungi (Metarhizium
anisopliae and Beauveria bassiana)
along with imidacloprid was tested to
control termites, which control more
than 80% population but alone fungi
was not much effective (Neves and
Alves, 1999b; Krutmuang and Mekchay,
2005; Lenz, 2005). Five fungal
pathogens (B. bassiana, M. anisopliae,
M. flavoviride, Paecilomyces lilacinus
and P. fumosoroseus) were tested
against O. obesus (Rambur), and
observed thattermites were very
susceptible to all types of fungi (Khan et
al., 1993a; Chouvenc et al., 2009a;
Chouvenc et al., 2009b). While
Aspergillus sp. TK (Pandey et al., 2013)
and Isariafumosorosea(Wright and Lax,
2013)caused prompt mortality by
growing on the termite colony and
worker caste become more susceptible
due to extensive exposure as compared
to other individuls.
It is essential to understand the
parasitization mechanism as well as
interaction between EPF and host
insect, because if both have no proper
interaction, then this strategy goes to
fruitlessness for the management of
insect pests. Each type of fungi has
certain range of mortality against its
susceptible host insects due to their
cuticle structural composition, because
they have to penetrate the cuticle.
Pathogenicity of fungi initiates from
attachment of the fungus in the form of
conidia or blastospores, to the cuticle of
its host, and through certain hydrolytic
alteration in the host body, it germinate
and grow along the surface of host
body, followed by penetration into
cuticle intersections, in addition to
affecting the mating ability of insects
directly or indirectly (Zheng et al.,
2011; Xiao et al., 2012). These fungi
after selection their host cuticle, make
specific linkage with the surface of
insect, and pass through the surface to
yield certain enzymes on various body
fragments, depending upon the
chemical composition of those segments
(Jarrold et al., 2007), which play a role
to decompose lipid bodies,
proteinaceous constituents, chitin
sheets and other ester bindings of
insect body, as well as produce
distinctive bodies within the host body,
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
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which disrupt the insect physique,
resulting in casualty of insects (St.
Leger, 1995; Holder et al., 2007; Pedrini
et al., 2013).
EPF infect the termites by damaging its
integument, which followed by
deterioration of host metabolites
through toxic products, leading to
tissue knocking down, and end with the
death of host organism (Yendol and
Paschke, 1965; Hänel, 1982a). The
mode-of-action, of EPF against termites,
includes disease development in the
following way, which resulted with
mortality of termites, as described by
(Hänel, 1982a; Roberts and Humber,
1984; Leger et al., 1991):
1. Conidial attachment to the
insect body
2. Conidial germination
3. Penetration into cuticle
4. Fungal growth in the
haemocoel
5. Toxin production
6. Host death
But, some termites, like Reticulitermes
sp. and Coptotermes sp., have ability to
remove entomopathogenic fungi from
their body with the help of their
antenna as well as mutual grooming
(Yanagawa et al., 2008, 2009) and some
offensive secretions (Hamilton et al.,
2011), so it is very crucial to be
acquainted with the adaptation of fungi
on the surface besides virulence,
otherwise application of fungi goes to all
in vain.
Nematodes
Entomogenous nematodes (EPNs) were
assessed against termites in laboratory
and field conditions, and these EPNs
prevented the activity of termites in
laboratory and field (Mauldin and Beal,
1989b). In laboratory experiments, it
was observed that four EPNs were
capable of killing termites. Nematodes,
Steinernema riobrave, caused more than
80% mortality of termite, Heterotermes
aureus and Gnathamitermes perplexus
on sand assays. But, R. flavipes was
less susceptible to all nematodes (Yu et
al., 2006). Termiteswere tested by EPNs
in laboratory, and observed thatfour
nematode strains (S. riobrave, S.
carpocapsae, S. feltiae and
Heterorhabditis bacteriophora) were
effective against subterranean termite,
H. aureus causing higher mortality of
termites (Yu et al., 2008). Similarly EPN,
S. riobrave, was very active against
termites, H. aureus. ComparablyS.
riobrave was also effective against R.
flavipes, C. formosanus and H. aureus,
causing mortality 75-91% as well as it
was also effective in field conditions (Yu
et al., 2010). While, in the presence of
imidacloprid, the parasitism of S.
carpocapsae and H. bacteriophora
improved synergistically against
termites (Manzoor, 2012).
The EPNs invade different body
structures of termites, such as; nervous
tissue, muscle tissue fat body, salivary
gland and sternal gland. Parasitism of
termites was highly perceptible in
Egyptian laboratories and field by H.
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
41
baujardi and H. indica(El-Bassiouny
and Abd El-Rahman, 2011). While,
thirty isolates of H. sonorensis and H.
indica were recorded from Benin, which
shown off their pathogenicity against
termites, causing high mortality, as well
as these isolates were resistant to heat,
desiccation and anaerobic conditions
(Zadji et al., 2014a; Zadji et al., 2014b,
c). As well as, termites were susceptible
to entomopathogenic nematodes in the
field of wheat and pearl millet crops,
due to which crop production was
increased (Rathour et al., 2014).
There were eighty three EPNs
nematodes species updated, which were
able to parasitize insect pests during
2001 all over the world (Grewal et al.,
2001), but it was observed that the
focus on the application of nematodes
has been increased progressively, and
up to now 34 EPNs species, along with
more than thirty different isolates, have
been recorded from the whole globe
which are parasitic relationship with
termites, and being used for the
management of termites, as described
in the below table.
Table 5: Termite parasitic nematodes
species # Species Isolate Accession
#
Reference
1 Heterorha
bditis
sonorensi
s
Akare KF723798 (Zadji et al.,
2014a; Zadji et
al., 2014c)
Ouere1 KF723799
Ouere2 KF723800
Yokon KF723801
Hessa1 KF723802
Hessa2 KF723803
Aglali KF723804
Zoundo
mey
KF723805
Kissame
y
KF723806
Aliho KF723807
Azohoue
1
KF723808
Azohoue
2
KF723809
Kpanrou
n
KF723810
Tankpe KF723812
Kemond
ji
KF723813
Zagnana
do
KF723814
Kpedekp
o
KF723815
Akohou
n
KF723818
Setto1 KF723819
Setto2 KF723820
Setto3 KF723821
Djidja1 KF723822
Djidja2 KF723823
Kassehl
o
KF723824
Dan KF723825
Avokanz
oun
KF723826
Ze1 KF723827
Ze3 KF723828
Ze4 KF723829
Ze2
Djidja
2 H. indica Ayogbe1 KF723816
3 Steinerne
ma sp.
Bember
eke
(Zadji et al.,
2014b)
4 S.
carpocaps
ae
(Divya and
Sankar, 2009)
5 S. glaseri (Murugan and
Vasugi, 2011)
6 S. feltiae
Filipjev
(Mauldin and
Beal, 1989a; Yu
et al., 2006) 7 S. bibionis
8 H.
heliothidis
9 S.
longicada
m
D-4-3 (Zhu, 2002)
1
0
H.
bacterioph
ora
(Yu et al., 2006)
1
1
S.
riobrave
1 Neosteiner (Nguyen and
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
42
2 nema
longicurvic
auda
Smart, 1994)
1
3
Chroniodi
plogaster(
Mikoletzk
ya)
aerivora
(Merrill and
Ford, 1916;
Poinar Jr, 1990)
1
4
Diplogaste
r labiate
(Pemberton,
1928)
1
5
H.
baujardi
(El-Bassiouny
and Abd El-
Rahman, 2011)
1
6
Neoaplect
ana
carpocaps
ae
DD-136 (Fujii, 1976)
1
7
Pseudaph
elenchus
yukiae
(Kanzaki et al.,
2009b)
1
8
P. vindai (Kanzaki et al.,
2010)
1
9
P. sui (Kanzaki et al.,
2014)
2
0
P.
scheffrahn
i
2
1
Termirhab
ditis
fastidiosu
s
(Massey, 1971)
2
2
Rhabpanu
s
ossiculum
2
3
Rhabditis
rainai
(Carta and
Osbrink, 2005)
2
4
Oigolaimel
la
attenuata
(von Lieven and
Sudhaus, 2008)
2
5
Poikilolai
mus
carsiops
(Kanzaki et al.,
2011)
2
6
P.
floridensis
(Kanzaki et al.,
2009a)
2
7
P.
ernstmayr
i
SB346 (Sudhaus and
Koch, 2004)
2
8
Pelodera
scrofulata
(Tahseen et al.,
2014)
2
9
P. termitis (Carta et al.,
2010)
3
0
Acrobeloid
es
amurensis
3 Panagrolai
1 mus
spondyli
3
2
Pristionch
us
aerivorus
(Christie, 1941)
3
3
Hartertia
gallinaru
m
(Watson and
Stenlake, 1965)
3
4
Caenorha
bditis sp.
(Handoo et al.,
2005)
Bacteria
Bacteria were used as biological agent
for the management of termites. Fifteen
bacteria were used to control termite, C.
formosanus. Serratia marcescens
caused 100% mortality of termites
(Osbrink et al., 2001b). Three different
types of rhizobacteria were used as
biocontrol agents against O. obesus in
laboratory conditions. These
rhizobacteria showed potential to kill
termites due to hydrogen cyanide
production(Devi et al., 2007). Bacteria,
Pseudomonas fluorescens, were
evaluated against termites, which
blocked respiratory system of termite by
producing hydrogen cyanide. Bacteria
caused mortality of termite though
inhibiting respiration (Devi and
Kothamasi, 2009).The pathogenicity of
bacterial strains like, B. thuringiensis
subsp. israelensis was assessed against
termites, M. beesoni, and observed that
they caused higher mortality at low
concentrations under laboratory
conditions (Singha et al., 2010).
A bacteriumPseudomonas aeruginosa, is
not harmful to termites, and form good
association, but proves a synergistic
opportunity against termites in the
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
43
presence of lufenuron, as well as
virulence of B. thuringiensis increased
along with lufenoron (Henderson et al.,
2014). On the other hand, an enzyme,
chitin deacetylase, isolated from B.
licheniformis HSA3-1a, and applied on
termites to test the pathogenicity of
bacterium, which hydrolyze the skin,
resulting high mortality of termites
(Natsir and Dali, 2014). Similarly the
pathogenicity of Bacillus subtilis and
Serratia marcescens, was much
operative against termites (Omoya and
Kelly, 2014).
Termito-Pathogenic Bacterial Species
Bacterial bodies are being used for
management of termites earlier than
1960s, which shown very determined
results against termites. Efficiency of
bacterial pathogens may be accelerated
by the warm, humid environment of the
colony, trophollaxis, as well as their
grooming contact with nest mates
(Grace, 1994). Up to now, there have
been twenty eight bacterial species
recorded against termites, as mentioned
in the following tabular chart.
Table 6: Bacterial Pathogens # Species Isolate Reference
1 Acinetobacter
calcoacet/
baumannii
(Osbrink et al., 2001a)
2 Aeromonsa caviae (Devi et al., 2007)
3 Alcaligenes latus
4 Bacillus cereus (Khucharoenphaisan
et al., 2012)
5 B. licheniformis HSA3-
1a
(Natsir and Dali,
2014)
6 B. subtilis (Omoya and Kelly,
2014) 7 B. megaterium
8 B. sphaericus (Toumanoff, 1966)
9 B. thuringiensis
subsp. alesti
10 B. thuringiensis
subsp. israelensis
(Wang and
Henderson, 2013)
11 B. thuringiensis
subsp.
thuringiensis
12 Burkholderia
cepacia
(Devi, 2013)
13 Candida utilis (Khucharoenphaisan
et al., 2012)
14 Citrobacter sp. VA53 (Harazono et al., 2003)
15 Citrobacter freundii (Omoya and Kelly,
2014)
16 Corynebacterium
urealyticum
(Osbrink et al., 2001a)
17 Enterobacter
cloacae
(Husseneder and
Grace, 2005)
18 Enterobacter
gergoviae
(Osbrink et al., 2001a)
19 Escherichia coli (Khucharoenphaisan
et al., 2012)
20 Photorhabdus
luminescens
(Shahina et al., 2011)
21 Pseudomonas
aeruginosa
(Khucharoenphaisan
et al., 2012)
22 P. fluorescens CHA0 (Devi and Kothamasi,
2009)
23 Rhizobium
leguminosarum
(Devi, 2013)
24 R. radiobacter (Devi et al., 2007)
25 Serratia
marcescens
(Osbrink et al., 2001a)
26 S. marcescens
27 Staphylococcus
aureus
(Khucharoenphaisan
et al., 2012)
28 Xenorhabdus
nematophila
(Hiranwrongwera et
al., 2007)
Viruses
The efficacy of nuclear polyhedrosis
virus isolated from Spodoptera littoralis
(Lepidoptera: Noctuidae) has been
tested against Kalotermes flavicollis
(Isoptera: Kalotermitidae) under
laboratory conditions. Though the virus
attachs various body parts, such as the
gut, nervous system, sexual organs and
hypodermis (Al Fazairy and Hassan,
1993), mortality rage has been
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
44
determined to be not significant,
ranging 64-90%, against any caste of
termite (Al Fazairy and Hassan, 1988a).
Problems and stratigiesof microbial
biological control Agents
There are many environmental factors,
which affect pesticidal potential of
microbial biological agents. There is also
hindrance that they are being used in
bulk concentrations, whereas chemical
pesticides are very effective in very low
amount. There are two main problems
with microbial biological agents.
Inactivation
Environmental factors deteriorated the
persistence of biopesticides. Sunlight
causes inactivation of Bt cell due to
absorbance resulting in loss of
insecticidal activity (Cohen et al., 1991).
Rainfall deteriorated the persistence of
biopesticides on foliage due to washing
(Behle et al., 1997). Twenty percent of
Bt biopesticide degraded due to 3 cm of
rain. Out of 10ºC-30ºC temperature
range, the persistence of Bt was
degraded by heat due to high
temperature and reduced feeding of
insects due to low temperature (Ignoffo,
1992). Neem products, having
triterpenoids are deteriorated when
sprayed on plants due to sun light
(Johnson et al., 2003; Barrek et al.,
2004). Similarly virus is also sensitive to
ultraviolet radiation (Kienzle and Elder,
2003; Arthurs and Lacey, 2004), since
there is need of virus spray at 7-10 days
interval.
Leaching
There is another big issue of
microbial pathogens, that they move
from one part of the soil, and become
sediment on other places in the soil,
resulting in the contamination of
ground water, and ultimately, these
water resources become detrimental to
other living beneficial bodies in the soil
(Craun et al., 1994; Wang et al., 2013).
These pathogenic bodies (bacteria and
viruses) migrate from upper surface to
lower layers of soil by leaching process,
which is supported by certain cracks in
the soil as well as worm holes. After
application of these pathogenic bodies
into the soil, they absorb into water via
dispersion and filtration, which become
sedimentation at specific distance from
the applied surface (Corapcioglu and
Haridas, 1984; Abu-Ashour et al., 1994;
Amin et al., 2013; Martins et al., 2013).
After leaching, these microbes
accumulate in the ground water, which
ultimately taken up by plants, and
caused certain disorders in the plant
structures. Thus, these pathogenic
microbes become hazardous for both
plant as well as animal life, causing a
number of diseases (Bradford et al.,
2013).
Conclusion
Almost three hundred and seventy
species of termite have been identified
as pests of staple, vegetables, industrial
crops, fruits and buildings. The damage
of termites is more serious in sandy
loam, loamy sand and alluvial soils,
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South Asia Journal of Multidisciplinary Studies SAJMS July 2015, Vol. 1, No.-6
45
andtermite’s damage increases with the
height of crop.Termite management
tactics change with the passage of time.
Initially the control of termite was on
anecdotal basis; many farmers in Asia
and Africa had been using plant
extracts neem, wild tobacco, dried
chilies, callotrops and wood ash, for
controlling and repelling termites. The
emergence of organochlorines replaced
the use of plant extracts. However
concern over health; carcinogenic
effects and persistency of
organochlorine insecticide has led to
almost total ban on their use.
Biocontrol agents, having high potency,
in the management of termites have
much importance with regards of
environment. But these agents may be
effective against certain species not all
termite species, as well as less
persistence in the environment.But the
combination of different biological agent
along with certain plant extracts.
A large number of microbial organisms
are too much effective against termites,
which are being used for management.
These microbes have great affinity the
termite colonies, in different
environments. Thus, certain species
specific microbes might be exploited
against termites, such as in some
conditions ceratin fungal bodies are
more effective, as compared to bacterial
or nematode applications, while on the
other hand, the efficiency of these
microbes against termites has proved
very promising specific castes, like some
microbes were observed solely attacking
workers and some against reproductive
castes. So, it is very feasible and fruitful
to utilize microbial biological agents
after studying their biology against
termite.
But, on the othe other hand, there are
some problems with the usage of such
pathogenic microbes, that they become
inactive in certain harsh conditions.
Moreover, these microbial bodies have
some leaching problems, which become
source of contamination of ground
water, and caused certain water borne
diseases in animals. So, it is necessary
to minimize the leaching proportions of
the pathogenic bodies.
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