Termites and microbial biological control strategies

ISSN:2395-1079 Available online at http://www.gjms.co.in/index.php/sajms

South Asia Journal of Multidisciplinary Studies SAJMS September2015, Vol. 1, No.-8

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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’s email: [email protected]

*Corresponding Author

Received 10-09-2015; Revised 20-09-2015; Accepted 26-09-

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.

Key words: 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

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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 (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



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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).

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)

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)



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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)

Mulberry China (Kai et al., 2001), Pakistan (Ahmed and Qasim, 2011), Saudi Arabia (Badawi et al., 1986)

Pineapple 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)

Coconut Africa (Rouland-Lefèvre, 2011), China (Tang et al., 2006), Indonesia (Mariau et al., 1992), Indonesia (Mariau et al., 1992), Tanzania (Materu et al., 2013)

ForestPlants 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)

Eucalyptus 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)

Magnolia China (Kai et al., 2001)

Dalbergia 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; Hemachandra et al., 2014), Tanzania (Ndunguru, 2006)

Microbial biological control of termites Termite pest management efforts have been

focused mostly on subterranean and arboreal



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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)



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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 = Philippines (Khan et al., 1993b) NDL = New Delhi

BNG = Bangalore

CBE = Coimbatore

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 Cordycepioideus bisporus (Ochiel et al., 1996)

8 Entomophthora coronata (Yendol and Paschke, 1965)

9 E. virulenta

10 Gliocladium virens ATCC 9645 (Kramm and West, 1982)

11 Gloeophyllum 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 var. acridum (Jarrold et al., 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. fumosoroseus



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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-

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.,



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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,

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



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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. 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



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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 Heterorhabditis sonorensis

Akare KF723798 (Zadji et al., 2014a; Zadji et al., 2014c) Ouere1 KF723799

Ouere2 KF723800

Yokon KF723801

Hessa1 KF723802

Hessa2 KF723803

Aglali KF723804

Zoundomey KF723805

Kissamey KF723806

Aliho KF723807

Azohoue1 KF723808

Azohoue2 KF723809

Kpanroun KF723810

Tankpe KF723812

Kemondji KF723813

Zagnanado KF723814

Kpedekpo KF723815

Akohoun KF723818

Setto1 KF723819

Setto2 KF723820

Setto3 KF723821

Djidja1 KF723822

Djidja2 KF723823

Kassehlo KF723824

Dan KF723825

Avokanzoun KF723826

Ze1 KF723827

Ze3 KF723828

Ze4 KF723829

Ze2

Djidja

2 H. indica Ayogbe1 KF723816

3 Steinernema sp. Bembereke (Zadji et al., 2014b)



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4 S. carpocapsae (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. longicadam D-4-3 (Zhu, 2002)

10 H. bacteriophora (Yu et al., 2006)

11 S. riobrave

12 Neosteinernema longicurvicauda (Nguyen and Smart, 1994)

13 Chroniodiplogaster(Mikoletzkya) aerivora

(Merrill and Ford, 1916; Poinar Jr, 1990)

14 Diplogaster labiate (Pemberton, 1928)

15 H. baujardi (El-Bassiouny and Abd El-Rahman, 2011)

16 Neoaplectana carpocapsae DD-136 (Fujii, 1976)

17 Pseudaphelenchus yukiae (Kanzaki et al., 2009b)

18 P. vindai (Kanzaki et al., 2010)

19 P. sui (Kanzaki et al., 2014)

20 P. scheffrahni

21 Termirhabditis fastidiosus (Massey, 1971)

22 Rhabpanus ossiculum

23 Rhabditis rainai (Carta and Osbrink, 2005)

24 Oigolaimella attenuata (von Lieven and Sudhaus, 2008)

25 Poikilolaimus carsiops (Kanzaki et al., 2011)

26 P. floridensis (Kanzaki et al., 2009a)

27 P. ernstmayri SB346 (Sudhaus and Koch, 2004)

28 Pelodera scrofulata (Tahseen et al., 2014)

29 P. termitis (Carta et al., 2010)

30 Acrobeloides amurensis

31 Panagrolaimus spondyli

32 Pristionchus aerivorus (Christie, 1941)

33 Hartertia gallinarum (Watson and Stenlake, 1965)

34 Caenorhabditis 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.



12

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 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)



13

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 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



14

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, 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



15

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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Termites and microbial biological control strategies

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