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 July 2015, Vol. 1, No.-6

33

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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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).



35

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



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.,


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



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



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),


2009)

Sesame Ethopia (Taye et al.,

2013), Nigeria




1987)

Vegetables Tomato Saudi Arabia (Faragalla




1987)

Okra Saudi Arabia (Faragalla



1995)

Pepper Saudi Arabia (Faragalla

and Al Qhtani, 2013)



36

Egg plant Saudi Arabia (Faragalla


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,


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



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


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


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,


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


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;



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 =



38

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


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


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-



39

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,



40

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.



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



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



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


17 Enterobacter

cloacae

(Husseneder and

Grace, 2005)

18 Enterobacter

gergoviae


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


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



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,



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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Termites and Microbial Biological Control Strategies