14
Review Biological alternatives for termite control: A review Monica Verma, Satyawati Sharma * , Rajendra Prasad Center for Rural Development and Technology, Block III, Indian Institute of Technology, Hauz Khas, New Delhi 110 016, India article info Article history: Received 28 January 2009 Received in revised form 15 May 2009 Accepted 16 May 2009 Available online 11 September 2009 Keywords: Formosan subterranean termites Botanicals Biocontrol agent Bait technology Soil termiticide Chemical fumigation Antifeedant Repellant abstract Termites are a serious menace to both plants and structures. They are the most problematic pest threatening agriculture and the urban environment. They cause significant losses to annual and perennial crops and damage to wooden components in buildings, especially in the semi-arid and sub- humid tropics. Chemical control has been a successful method of preventing termite attack, but the effects of these chemicals are of concern as they create problems for our health and the environment. Biological methods could be suitable alternatives in this regard. The present paper reviews the various methods (physical, chemical, and biological) for termite control. Recent advances and past research done on termite control emphasizing biological methods are reviewed. Biological methods described include botanicals (essential oil, seed, bark, leaf, fruit, root, wood, resin), as well as fungal, bacterial, and nematode approaches. The relationship between chemical structure of active components responsible for termite control and termiticidal activity is discussed. The plants reviewed show good insecticidal properties against termites. These botanicals can be used for termite control singly and in combination. The active component from biomass can be extracted to prepare efficacious and potent biocidal formulations. Ó 2009 Elsevier Ltd. All rights reserved. Contents 1. Introduction ...................................................................................................................... 960 2. Economic losses caused by termites ................................................................................................. 960 3. Biology of termites ............................................................ ................................................... 960 4. Termite classification ...............................................................................................................961 4.1. Characteristics of a few major families of termites ............................................................................... 961 4.1.1. Kalotermitidae (drywood and dampwood termites) ....................................................................... 961 4.1.2. Hodotermitidae (rottenwood termites) .................................................................................. 961 4.1.3. Termitidae .......................................................................................................... 961 4.1.4. Rhinotermitidae (subterranean termites) ................................................................................ 961 5. Termite control ....................................................................................................................961 5.1. Physical methods ............................................................................................................ 961 5.2. Chemical methods .......................................................................................................... 962 5.3. Biological ................................................................................................................... 963 5.3.1. Botanicals .......................................................................................................... 963 5.3.1.1. Plant essential oil ................................................ .......................................... 963 5.3.1.2. Plant extract ............................................................................................... 964 5.3.1.2.1. Leaf .................................................. ........................................... 964 5.3.1.2.2. Root ............................................................................................. 965 5.3.1.2.3. Fruit and seed ................................................................................... 965 5.3.1.3. Wood extract ............................................................................................... 965 5.3.1.4. Resin ...................................................................................................... 965 * Corresponding author. Tel.: þ91 11 26591116; fax: þ91 11 26591112. E-mail address: [email protected] (S. Sharma). Contents lists available at ScienceDirect International Biodeterioration & Biodegradation journal homepage: www.elsevier.com/locate/ibiod 0964-8305/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ibiod.2009.05.009 International Biodeterioration & Biodegradation 63 (2009) 959–972

Biological alternatives for termite control: A review

Embed Size (px)

Citation preview

Page 1: Biological alternatives for termite control: A review

lable at ScienceDirect

International Biodeterioration & Biodegradation 63 (2009) 959–972

Contents lists avai

International Biodeterioration & Biodegradation

journal homepage: www.elsevier .com/locate/ ib iod

Review

Biological alternatives for termite control: A review

Monica Verma, Satyawati Sharma*, Rajendra PrasadCenter for Rural Development and Technology, Block III, Indian Institute of Technology, Hauz Khas, New Delhi 110 016, India

a r t i c l e i n f o

Article history:Received 28 January 2009Received in revised form15 May 2009Accepted 16 May 2009Available online 11 September 2009

Keywords:Formosan subterranean termitesBotanicalsBiocontrol agentBait technologySoil termiticideChemical fumigationAntifeedantRepellant

* Corresponding author. Tel.: þ91 11 26591116; faxE-mail address: [email protected] (S. Sharm

0964-8305/$ – see front matter � 2009 Elsevier Ltd.doi:10.1016/j.ibiod.2009.05.009

a b s t r a c t

Termites are a serious menace to both plants and structures. They are the most problematic pestthreatening agriculture and the urban environment. They cause significant losses to annual andperennial crops and damage to wooden components in buildings, especially in the semi-arid and sub-humid tropics. Chemical control has been a successful method of preventing termite attack, but theeffects of these chemicals are of concern as they create problems for our health and the environment.Biological methods could be suitable alternatives in this regard. The present paper reviews the variousmethods (physical, chemical, and biological) for termite control. Recent advances and past research doneon termite control emphasizing biological methods are reviewed. Biological methods described includebotanicals (essential oil, seed, bark, leaf, fruit, root, wood, resin), as well as fungal, bacterial, andnematode approaches. The relationship between chemical structure of active components responsiblefor termite control and termiticidal activity is discussed. The plants reviewed show good insecticidalproperties against termites. These botanicals can be used for termite control singly and in combination.The active component from biomass can be extracted to prepare efficacious and potent biocidalformulations.

� 2009 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9602. Economic losses caused by termites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9603. Biology of termites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9604. Termite classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .961

4.1. Characteristics of a few major families of termites . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9614.1.1. Kalotermitidae (drywood and dampwood termites) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9614.1.2. Hodotermitidae (rottenwood termites) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9614.1.3. Termitidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9614.1.4. Rhinotermitidae (subterranean termites) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 961

5. Termite control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .9615.1. Physical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9615.2. Chemical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9625.3. Biological . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 963

5.3.1. Botanicals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9635.3.1.1. Plant essential oil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9635.3.1.2. Plant extract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 964

5.3.1.2.1. Leaf . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9645.3.1.2.2. Root . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9655.3.1.2.3. Fruit and seed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 965

5.3.1.3. Wood extract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9655.3.1.4. Resin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 965

: þ91 11 26591112.a).

All rights reserved.

Page 2: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972960

5.3.2. Nematode control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9665.3.3. Bacterial control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9675.3.4. Fungal control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 968

6. Bait technology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9687. Wood treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 968

7.1. Chemical . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9687.2. Nonchemical . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 968

8. Relationship between chemical structure and antitermitic activity of active component . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9699. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 969

Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 969References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 969

Table 1Crop losses, building damage and economic losses caused by termites worldwide.

Country Croplosses (%)

Buildingdamage (%)

Economiclosses/annum(Million US $)

Reference/Source

Australia – – >95.24 www.chem.unep.ch/pops/termites

Brazil – 42.7 – Milano and Fontes,2002

China – 80–90 248.68–292.79 Zhong and Liug, 2002Europe – – 313 www.chem.unep.ch/

pops/termitesIndia 15–25

(Maize crop)– 35.12 Joshi et al., 2005

Japan – – 800 www.chem.unep.ch/pops/termites

Malaysia – 70 –Residential

8–10 Lee, 2002

20 –Industrial10 –Commercial

SouthernAfrica

3–100 – – Mitchell, 2002

Spain – 53.2 – Gaju et al., 2002United

States– – >1000 www.chem.unep.ch/

pops/termites

1. Introduction

Termites are the most problematic pests in the plant kingdomand buildings. There are over 2800 described species of termites,with about 185 considered to be pests. They cause over 3 billiondollars worth of damage to wooden structures annually throughoutthe U.S. (Lewis, 1997). Termites that belong to the familiesHodotermitidae (Anacanthotermes and Hodotermes), Kalotermitidae(Neotermes), Rhinotermitidae (Coptotermes, Heterotermes, andPsammotermes), and Termitidae (Amitermes, Ancistrotermes,Cornitermes, Macrotermes, Microcerotermes, Microtermes, Odon-totermes, Procornitermes, and Syntermes) cause great loss in agri-culture (UNEP Report, 2000). Out of 300 species of termites knownso far from India, about 35 species have been reported damagingagricultural crops and buildings. The major mound-buildingspecies in India are Odontotermes obesus, Odontotermes redemanni,and Odontotermes wallonensis, and the subterranean species areHeterotermes indicola, Coptotermes ceylonicus, C. heimi, Odontotermeshorni, Microtermes obese, Trinervitermes biformis, and Microcerotermesbeesoni (Rajagopal, 2002). Synthetic pesticides remain the primarymethod used to prevent termite attack on wooden structures.However, the persistent use of chemical termiticides is at present ofenvironmental concern and has resulted in the need to search forplant-derived compounds as an alternative for termite control.

2. Economic losses caused by termites

Termites are of the greatest importance in recycling woody andother plant material. Their tunneling efforts help to aerate soil.Termites are an important part of the community of decomposers.They are able to decompose cellulose, the main component ofwood. They are abundant in tropical and subtropical environments,where they help in breaking down and recycling one third of theannual production of dead wood. But they become economic pestswhen they start destroying wood and wooden products of humanhomes, building materials, forests, and other commercial products(Meyer, 2005). Control and repair costs due to Formosan subter-ranean termites in New Orleans, for example, have been estimatedat 300 million dollars annually (Suszkiw, 1998). Termites damageabout 10–30 percent of harvested kernels of groundnut in Mali,Burkina-Faso, Niger, and Nigeria (Umeh et al., 1999). In India, theyare responsible for the loss of 15–25% of maize yield and about 1478million Rupees (Joshi et al., 2005). Crop losses in other countries areshown in Table 1.

3. Biology of termites

Termites (soft bodied, pale in color, with mouth parts for bitingand chewing and utilizing cellulose as a food source) belong to thegroup of insects called Isoptera. They are closely related to

cockroaches (Meyer, 2005) and are long-lived social insects.Termites living in large colonies depend entirely on wood, eitherliving or dead, or the woody tissue of plants, intact or partiallydecayed.

Their colony consists of reproductive forms, sterile workers,soldiers, and immature individuals. The reproductives are of twotypes, primary and supplementary. The primary reproductives, theking and queen, are pigmented and fully developed winged adults.Their role is egg production and distribution by colonizing flights.The queen lays about 3000 eggs a day through its enlargedabdomen (Thompson, 2000). It lives up to 25 years. The eggs areyellowish-white and hatch after 50–60 days of incubation. Thecolony reaches its maximum size in approximately 4–5 years andit may include 60,000 to 200,000 workers. In most termitecolonies there is only one pair of primary reproductives, but whenthey die they are usually replaced by numerous supplementaryreproductives, which are with or without wing pads and areslightly larger and more pigmented then workers. The sterilecastes, the workers and the soldiers, are wingless and usually lackeyes (Myles, 2005). Worker and soldier termites are 6 mm longand pale cream in color; however, the heads of soldiers are muchenlarged (almost half their body length) with noticeable blackjaws. Workers construct the distinctive shelter tubes and collectfood to feed the young and other members of the colony. Soldiertermites are responsible for guarding the colony and its occupants.

Page 3: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 961

Termites continually groom each other to obtain certain secre-tions. These secretions help in regulating the number of individ-uals in the various castes (Philip, 2004). Workers mature in a yearand live up to 3–5 years. Soldiers also mature within a year andlive up to 5 years (Myles, 2005).

Winged reproductives (alates) emerge in a mass nuptial flight inApril and May. These flights are often the first indication of termiteinfestations (Philip, 2004). After a brief flight, alates shed theirwings. Females immediately search for nesting sites with malesfollowing closely behind. When the pair finds a moist crevice withwooden material, they form the royal chamber and lay eggs (Su andScheffrahn, 2000).

4. Termite classification

Termites are classified at the taxonomic rank of order Isoptera.About 2800 termite species are recognized and classified in sevenfamilies (Aanen et al., 2002). These are arranged in a phylogeneticsequence; the first three families are the lower or primitivetermites and the last four are the higher or advanced termites(Table 2).

4.1. Characteristics of a few major families of termites

4.1.1. Kalotermitidae (drywood and dampwood termites)These insects nest in the wood itself and do not require contact

with the soil. They include the western drywood termite (Incisi-termes minor), the forest tree termite (Neotermes connexus), and thepowderpost termite Cryptotermes brevis.

4.1.2. Hodotermitidae (rottenwood termites)These are generally found inhabiting moist wood. Contact with

the soil is not a requirement. This family includes the Pacificdampwood termite (Zootermopsis angusticollis).

Table 2Outline of termite classification.

Family Subfamily Genera

Mastotermitidae Mastotermes darwiniensisKalotermitidae KalotermesHodotermitidae Carinatermitinaea Carinatermes

Lutetiatermitinaea LutetiatermesHodotermitinae Hodotermes

Termopsidae Cretatermitinae CretatermesPorotermitinae PorotermesStolotermitinae StolotermesTermopsinae Termopsis

Rhinotermitidae Archeorhinotermitinaea ArcheorhinotermesCoptotermitinae CoptotermesHeterotermitinae HeterotermesProrhinoterminae ProrhinotermesPsammotermitinae PsammotermesStylotermitinae StylotermesTermitogetoninae TermitogetonRhinotermitinae Rhinotermes

Serritermitidae Serritermes serrifer

Termitidae Apicotermitinae ApicotermesForaminitermitinae ForaminitermesSphaerotermitinae SphaerotermesMacrotermitinae MacrotermesSyntermitinae SyntermesNasutitermitinae NasutitermesTermitinae Termes

a Fossil taxon Engel & Krishna (2004).

4.1.3. TermitidaeThis is the largest family of termites worldwide, but all of the

North American species are of relatively minor importance. Itincludes mound-building termites (Macrotermes spp.) and subter-ranean termites (Odontotermes spp.).

4.1.4. Rhinotermitidae (subterranean termites)These insects build nests in the soil and generally infest wood

that is in contact with the ground. This family includes the mostdestructive species found in the U. S., the eastern subterraneantermite (Reticulitermes flavipes), the western subterranean termite(R. hesperus), and the Formosan subterranean termite (Coptotermesformosanus) (Meyer, 2005).

5. Termite control

Although termites are excellent decomposers of dead wood andother sources of cellulose, they become a serious problem whenthey attack dwellings and crops. Therefore, effective methods haveto be found to control them. Different control methods (Fig. 1) havebeen adopted so far and the important ones are discussed below.

5.1. Physical methods

Physical barriers are a very popular method of preventingsubterranean termite attack on wooden structures. Barriers are oftwo types: toxic and nontoxic. Toxic physical barriers include theuse of chemical termiticides in the soil around the structure.Chlorfenapyr (BASF-Phantom) barrier treatment is very effective asit is non-repellent and has delayed toxicity (Rust and Saran, 2006).In Australia, protection of structures from subterranean termiteshas traditionally relied upon the creation of a zone of poisoned soilunder and around the structure to prevent termites gaining accessfrom the ground (Ewart, 2000). Nontoxic physical barriers aresubstances (e.g., sand or gravel aggregates, metal mesh or sheeting)that exclude termites because they are impenetrable, thus acting asphysical/mechanical barriers to prevent termite penetration anddamage to the building. Various types of nontoxic physical barriersare concrete slabs (Lenz et al.,1997), graded particles (sand, crushedrock, granites and basalts, glass), solid sheet material (high-gradestainless steel, marine-grade aluminum, certain plastics) andwoven stainless steel mesh (high-grade stainless steel) (UNEPReport, 2000). Research by the Urban Entomology Program hasshown that coarse sand is an effective physical barrier when at least50% of the particles are between 1.4 and 2.8 mm and no more than25% of the mixture is smaller than 1.4 mm. Graded gravel andstainless steel mesh are a promising alternative to soil treatment.The gravel works on the principle that certain sizes are too small fortermites to pass between and too large to be picked up in termitejaws and used to build tunnels. The size of the gravel therefore hasto be different for different termite species. Stainless steel meshworks in a similar way, in that holes in the mesh are too small fora termite to pass through with the mesh too large for a termite tobite through. The mesh must be laid under the entire foundationand must be exposed above the soil surface all around the house(Morris, 2001). A stainless steel mesh called Termimesh is used inHawaii and Australia as a termite barrier (Grace et al., 1996).

Other physical methods include heat, freezing, electricity, andmicrowaves. Heat treatment is an alternative to chemical fumiga-tion for complete building treatment of drywood termites. Wood-row and Grace (1998) controlled C. brevis by using high-temperaturetreatments. The mean maximum wood core and ambient temper-atures were 55.1 �C and 68.1 �C, respectively. Heat treatment inbuildings is done by first covering the building with nylon tarps andremoving heat-sensitive materials from the building. The water is

Page 4: Biological alternatives for termite control: A review

Termitecontrol

Physical Biological Chemical

Fungal (Mycotoxin)

Bait

Entomopathogenic Nematodes (Termiticidal/

bacterial symbiont) Botanical(Bioactive

constituent)Toxic

Barriers

Non toxic

Heat Electrical Freezing Microwave

Treatments

Bacterial(Toxins)

Fig. 1. Diagrammatic representation of different control measures of termites.

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972962

left running to protect plastic pipes. A large propane heating unit isconnected to the tent by a large flexible hose and turned on. Hot air isblown in and around the structure to heat the walls from both theinterior and exterior. Heat is allowed to reach 45 �C (120 F) for35 min–50 �C (130 F) for 1 h. Then heat is shut off and the tent isremoved (Myles, 2005). The heat tolerance of structure-infestingdrywood termites was studied by Scheffrahn et al. (1997). Doi et al.(1999) studied the effects of heat treatments of wood on the feedingbehavior of C. formosanus shiraki and Reticulitermes speratus. Theyconcluded that termites were more attracted to steam-treated woodthen to dry-heated wood, as steam-treated wood produced somefeeding attractants.

Freezing treatment is not useful for large areas, as it can shatterwindow glass. For this treatment tarps are used for larger areassuch as porches. Liquid nitrogen is pumped into the infested area,chilling it down to �20 F, thus freezing the termites. Later, gas isvented off and the tarps are removed.

Electrical treatment involves the treatment of infested woodenmaterial with electric shock. An Electro-Gun is placed on one side ofthe infested timber, and an electrical shock of low current(w0.5 amp), high voltage (90,000 V), and high frequency (60,000cycles) is passed through the wood and termite galleries and endsat the ground (Myles, 2005). Lewis and Haverty (2000) observedthe lethal effects of electrical shock treatments on the westerndrywood termite, I. minor (Hagen) in intentionally and naturalinfested boards. Termites in the path were killed.

In microwave treatment microwave generators are mountedagainst a wall on a pole one foot apart. Remote switches start thegenerators, and heat generated by the microwaves kills termites.The pole system is then moved to the next wall space to be exposedto the treatment (UNEP Report, 2000).

5.2. Chemical methods

Chemical treatment measures are the most important and mostwidely used to reduce the infestation of termites. Several termiti-cides containing active ingredients: bifenthrin (Makhteshim-Agan-Seizure 100 EC), chlorfenapyr (BASF-Phantom), cypermethrin(Effecticide-Spraykill), fipronil (BASF-Termidor), imidacloprid(Bayer–Gaucho) and permethrin (BASF-Coopex TC Termiticide) areregistered for termite control around the world under variousbrand names. They contain various chemicals such as spinosad(Dow AgroSciences-Tracer), disodium octaborate tetrahydrate(DOT) (Nissus-Tim-Bor), calcium arsenate (Helena-Calcium arse-nate), and chlorpyriphos (Efekto-No Ant) are also being used. Theirchemical toxicity, formulation and application method, as well asdrywood termite behavior and gallery system architecture influ-enced the performance of local chemical treatment (Scheffrahnet al., 1997). When termites were placed on soil treated at�50 ppmwith termiticides, bifenthrin, cypermethrin, and permethrin had

the greatest activity. Soil treated with chlordane, permethrin(<50 ppm), and chlorpyriphos formulations acted more slowly.Fenvalerate (Agrofarm-Agrovate) (<100 ppm) and isofenphosformulations were the least active treatments, as reported by Smithand Rust (1990). At high concentration cypermethrin (100 ppm),fenvalerate (500 ppm), and imidacloprid (1000 ppm) are effectiveagainst subterranean termites (Kuriachan and Gold, 1998). Ahmedet al. (2006a) demonstrated the efficacy of imidacloprid, mono-mehypo, and chlorpyriphos against subterranean termites insugarcane crop and found that chlorpyriphos was the most effective.

The wooden stakes coated with 10% calcium carbonate in gelatinsolution (glue of animal hides), 5% copper sulphate in gelatinsolution and 12% calcium carbonate mixed with 10% zinc oxide insodium silicate solution prevented termite attack in soil up to 2, 4,and 5 years, respectively. The control wooden stakes were found tobe severely damaged by termites within 6 months. Stakes coatedwith Solignum used as a standard wood preservative for compar-ison remained free from termite infestation for a period of 5 years(Roomi et al., 1990). Chromated copper arsenate (CCA) treatment insouthern yellow pine and radiata pine were found to be toxic againstFormosan subterranean termites, C. formosanus (Grace, 1998).

Chemical treatments comprise groomable coating, soil termiti-cide injection, baits, and chemical fumigation. Groomable coatingor trap-treat-release (TTR) is a technique for suppressing or killingsocial insect colonies, particularly those of subterranean termites.The TTR method was developed by Dr. T. G. Myles at the Universityof Toronto. In TTR the toxicant is applied externally to termitebodies as a groomable coating. Cleaning and grooming (licking),a social behavior of termites, results in the ingestion of the pesticideby the grooming individuals. After ingestion, the pesticide is furtherdistributed by mutual feeding behaviors (trophallaxis and procto-deal trophallaxis). Under laboratory conditions, it is possible toachieve extraordinarily high kill ratios among members of thecolony (1 treated termite can kill over 1000 untreated termitesconfined in a petri dish). Under field conditions, it has been esti-mated that 50–100 termites are killed for each termite treated(Myles, 2005).

Soil termiticide injection is used for subterranean termites. Itincludes drilling of the foundation wall/slab and injection oftermiticide below the slab and in the soil in contact with thefoundation (Myles, 2005). Chemical fumigation is usually used fordrywood termite infestation. This strategy is employed to dealwith drywood termites, aerial colonies of subterranean termites,and cases where arboreal species nest inside structures. Itincludes the incorporation of toxic gas inside the structure. All thechemical absorbent materials are removed from the building to befumigated. The whole building is covered with a tent and fumi-gant is pumped into the building. Later the tent is removed andgas is vented off (Myles, 2005). The active ingredients in variousfumigants include carbon dioxide (asphyxiant), methyl bromide

Page 5: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 963

(Landkem-Metabrom), phosphine, sulfuryl fluoride (metabolicpoison). Methyl bromide is a commonly used fumigant. It pene-trates quickly and deeply into materials at normal atmosphericpressure. It exerts its principal toxic effect on the nervous systemof insects (Bond, 1984).However, issues involving the atmosphericozone layer, odor in some household materials after treatment,and long aeration times for fumigated structures have limited theuse of this fumigant (UNEP Report, 2000).

Methyl bromide is an ozone depleting chemical. Under theMontreal Protocol on Substances that Deplete the Ozone Layer andthe Clean Air Act (CAA) the amount of methyl bromide producedand imported in the U.S. was reduced incrementally until it wasphased out in January 1, 2005 (http://www.epa.gov/ozone/mbr/).The Montreal Protocol was revised and signed by 160 countries inSeptember 1997. Developed countries agreed to phase-out the useof the methyl bromide by 2005, with intermediate cuts of 25% by1999, 50% by 2001 and 70% by 2003. Developing countries havea ten-year grace period, phasing out use by 2115, with a freeze onuse in 2002 and a 20% reduction by 2005 (Byron, 1997). Methylbromide breaks down to form bromine, which participates ina series of ozone depleting chemical reactions (Cox et al., 1995;UNEP, 1992). Bromine is 50 times more reactive than chlorine indepleting ozone because it reacts with reservoir chlorine species,freeing the chlorine to react with additional ozone (World Mete-orological Organization, 1994). The United Nations EnvironmentProgramme (UNEP) calculated that methyl bromide had an ODP of0.6, or 60% of CFC-11’s ozone depleting potential, and the atmo-spheric lifetime was calculated at 1.7 years (Mellouki et al., 1992;Solomon et al., 1992). Ozone depletion continues to be a seriousglobal environmental problem. Depletion is linked to rising ratesof skin cancers, eye cataracts and damage to key ecosystems(Byron, 1997)

The fumigation of some foodstuffs with methyl bromide mayresult in the creation of undesirable taints or odours. Theseodours usually persist and in most cases there is no practical wayto remove them. The reason may be the reactions with sulphur orsulphur compounds originally present or added during the pro-cessing of foodstuffs (Bond, 1984). The repeated or excessivefumigation with methyl bromide can develop a sulphury odor.This is due to the methylation of methionine residues in whichthe sulphur atom is expelled in the form of dimethyl sulfide.Dimethyl sulfide has been identified as a cause of this taint(Saxby, 1996).

Although chemical control is a proven means of protection fromtermites, its excessive use is harmful for the environment. Newmethods of termite control are always being developed byresearchers. Plant-derived natural products, entomopathogenicfungi, nematodes, and bacteria are some of the alternativemethods. The use of botanicals as termiticides has been discussedbelow in detail along with other biological alternatives.

5.3. Biological

The excessive use of chemicals is a serious environmentalconcern as target insects develop resistance (Georgiou and Taylor,1986). Therefore, it has become necessary to search for alternativemeans for termite control so that use of these chemicals can beminimized. Plant-derived natural products and biocontrol agentsare promising replacements. These alternative control strategieswere initiated in 1935, when cellulose blocks were treated withcitronellic acid to test against termites (Trikojus, 1935). Botanicalpesticides possess many desirable properties, such as insecticidalactivity, repellency to pests, deterrent to feeding, insect growthregulation and toxicity to agricultural pests (Prakash and Rao, 1986,1987; Prakash et al., 1987, 1989, 1990).

5.3.1. Botanicals5.3.1.1. Plant essential oil. Insecticidal activity of essential oils wasevaluated as early as 1972 (Nakashima and Shimizu, 1972). Someplant essential oils not only repel insects, but also have contactand fumigant insecticidal actions against specific pests (Isman,2000). Various essential oils have been evaluated against termites(Table 2). Repellency and toxicity of essential oils from vetivergrass, cassia leaf, clove bud, cedarwood, Eucalyptus globules,Eucalyptus citrodera, lemon grass, and geranium against Formosansubterranean termites was reported by Zhu et al. (2001a). Vetiveroil has long-lasting activity, and hence has been proven the mosteffective.

Zhu et al. (2001b) reported a component of vetiver grass oil,nootkatone (a sesquiterpene ketone) as a strong repellent andtoxicant to Formosan subterranean termites. Vetiver oil and noot-katone act as an effective barrier to Formosan subterraneantermites and red imported fire ants at concentrations ranging from5 to 100 mg g�1 of sand (Maistrello et al., 2001a; Zhu et al., 2001a,b;Henderson et al., 2005a,b). They act as arrestants, repellents, andfeeding deterrents. Nootkatone negatively affects termites for 12months and is more long-lasting then vetiver oil. (Maistrello et al.,2003). Nootkatone acts as a feeding deterrent that results in almosta complete loss of Pseudotrichonympha grassii koidzumi, the mostimportant flagellate species for cellulose digestion in the Formosansubterranean termite (Maistrello et al., 2001b). Vetiver oil andnootkatone can be used as novel pesticides that can be incorpo-rated into potting media for substrate (soil, wood, and mulch)treatments to reduce the spread of Formosan subterraneantermites (Mao et al., 2006). A study by Nix et al. (2006) providedpreliminary evidence that vetiver grass root mulch treatmentdecreases the tunneling activity and wood consumption ofFormosan subterranean termites and increases their mortality.Vetiver oil can be chemically modified to enrich sesquiterpenonesand other structurally related compounds exhibiting potentinsecticidal activity (Chauhan and Raina, 2006).

The leaf essential oil of Tagetes erecta rich in (Z)- -ocimene(42.2%) showed significant termiticidal activity. Complete mortalityof O. obesus Rhamb. was observed at a dose of 6 ml/petri-plate of leafessential oil after 24 h of exposure (Singh et al., 2002a). Essentialoils of aerial parts of Maca (Lepidium meyenii) act as a feedingdeterrent to termites. Minor components 3-methoxyphenyl-acetonitrile and benzylthiocyanate showed good activity againstFormosan subterranean termites (Tellez et al., 2002). The essentialoil of catnip, Nepeta cataria (lamiaceae) acts as a barrier to subter-ranean termites R. flavipes (Kollar) and R. virginicus (Banks)(Peterson and Ems- Wilson, 2003). Calocedrus formosana leafessential oil and its main constituent, T-muurolol, caused 100%mortality of C. formosanus at the dosage of 5 mg g�1 (Cheng, 2004).Cheng et al. (2007) reported the antitermitic activity of 11 essentialoils from three species of coniferous tree against C. formosanusshiraki. One-hundred-percent mortality was recorded with dosagesof 10 mg g�1 of heartwood and sapwood essential oil of Calocedrusmacrolepis var. formosana and Cryptomeria japonica and the leafessential oil of Chaemocyparis obtusa var. formosana. Among all,heartwood of C. macrolepis var. formosana exhibited the strongesttermiticidal property. Leaf essential oil from two Melauleucaspecies, gelam and cajupati, were tested for their termiticidalactivity. Gelam oils were rich in compounds with a high boilingpoint and separated into the elemene-rich type and g-terpineneand terpinolene type. Cajupati oils were characterized into threechemotypes according to their 1, 8 cineole contentdhigh, low, ornone. Gelam oils were found to be more effective then cajupati oils(Sakasegawa et al., 2003). Park and Shin (2005) screened 29 plantspecies for termiticidal activities. Of these, 19 showed goodtermiticidal activity. He observed that clove bud oil and garlic oil

Page 6: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972964

had potent antitermitic activity. Three major compounds fromgarlic oil (diallyl trisulphide, diallyl disulfide, and diallyl sulfide)and two major compounds from clove bud oil (eugenol andb-caryophyllene) were tested individually for their insecticidalactivity. Diallyl trisulphide was the most toxic, followed by diallylsulfide, eugenol, and b-caryophyllene.

5.3.1.2. Plant extract. Three species of flagellated protists (Spiro-trichonympha leidyi, Holomastigotoides hartmanni, and P. grassii) arefound in the hindgut of Formosan subterranean termites (Ohkumaet al., 2000). Doolittle et al. (2007) investigated the ability of threenatural products (neem extract, capsaicin, and gleditschia) toreduce the number of microbes (S. leidyi, H. hartmanni, P. grassii, andspirochaetes) present in the hindgut of the Formosan subterraneantermite. Neem extract significantly reduced the population ofP. grassi and spirochaetes and was found to be most potent at 1 ppmconcentration, causing 100% termite mortality. Anthracenes,anthrones, anthraquinones, and xanthones (Rudman and Gay,1963) acts as deterrents, monoterpenoids, alkaloids and hydrocar-bons toxic (Cornelius et al., 1997) and plant flavonoids and relatedcompounds both toxic and antifeedant against termites (Boue andRaina, 2003; Ohmura et al., 2000).

Table 3Effect of essential oils from different parts of plants/trees against termites.

Plant Part Active component

Thujopsis dolabrata var. Hondai Wood b-Thujaplicin and carvacrol

Chamaecyparis pisifera Wood Chamaecynone andisochamaecynone

Cryptomeria japonica Wood b-Eudesmol and cedrolAzadirachta indica Seed LimonoidsChamaecyparis obtuse Endl. Wood Monoterpene, sesquiterpene, and

sesquiterpene alcoholThujopsis dolobrata Siebold Wood ThujopseneTaiwania cryptomerioides Wood Cedrol and a-cadinolVetiveria zizanoides Root Nootkatone (a sesquiterpene alco

and cedrene

Vetiver, cassia, clove,cedarwood, lemon grass andgeranium

Root, leafand bud

Cinnamomum osmophloeum Leaf CinnamaldehydeTagetes erecta Leaf (Z)-ocimeneLepidium meyenii (Walp.) Leaf Benzylthiocynate, 3-

methoxyphenylacetonitrileand b-ionone

Ephedra distachya, E. fragilis,and E. major.

Aerial parts Et benzoate, benzaldehyde,cis-calamenene, E-phytol,n-pentacosane, 6,10,14-trimethylpentadecanone, cis-thujopsene,b-terpineol, eugenol, b-terpineoland Me linoleate

Catnip (Nepeta cataria) – Isomers of nepetalactone

Melaleuca gelam andM. cajuputi

Leaves andtwigs

Elemene, g-terpinene andterpinolene, Monoterpenes,sesquiterpenes, hydrocarbonsand a diterpene

Calocedrus formosana Leaf T-muurololGarlic (Allium sativum) and

clove (Eugenia caryophyllata)Bud Diallyl trisulphide, Diallyl disulph

eugenol, Diallyl sulfide and b-caryophyllene

Australian white cypress,Callitris glaucophyllaThompson et Johnson

Wood Guaiol, a-eudesmol, and b-eudesmcitronellic acid and geranic acid

Chamaecyparis obtusa var.formosana Calocedrusmacrolepis var. formosanaand C. japonica

Heartwood,Sapwood andleaf

Citrus Peel D-limonene

Different parts of a number of plants, such as leaf, flower, fruit,and root, contain some bioactive components and can be used intermite control agents (Table 3).

5.3.1.2.1. Leaf. Hexane and methanol extract of leaves ofJuniperus species have shown termiticidal activities (Adams et al.,1988). A neem insecticide formulation, Margosan-O, containing0.3% azadirachtin and 14% neem oil, was toxic against the Formosansubterranean termite (Grace and Yates, 1992). Detarium micro-carpum possessed strong antifeedant activity when the methanolextract of its leaves was tested against termites. Four clerodanediterpenesd3,13E-clerodien-15-oic acid; 4(18),13E-clerodien-15-oic acid; 18-oxo-3,13E-clerodien-15-oic acid; and 2-oxo-3,13E-clerodien-15-oic aciddwere isolated and found to be effective ata 1% concentration (Lajide et al., 1995a). Sharma et al. (1999)examined six plant species, viz., Acorus calamus, Lantana camara,Parthenium hausteneum, Pongamia glabra, Jatropha curcas, andT. erecta, for their toxic action against O. obesus. Acorus calamusrhizomes, and aerial parts of T. erecta were found to be most toxic.Hexanes, diethyl ether, and ethanol fractions of tarbush (Flourensiacernua) leaves exhibited a high degree of antitermite activity.The hexane fraction contained mostly monoterpenoids, whilethe ethanol fraction volatiles were primarily sesquiterpenoids

Termite Activity/Effect Reference

– Toxic Nakashima andShimizu, 1972

Coptotermes formosanus Toxic Saeki et al., 1973

– Toxic Yatagai et al., 1991Reticulitermes speratus Antifeedant Serit et al., 1992– Toxic Shimanouchi, 1992

– Toxic Yoshida et al., 1998C. formosanus Shiraki Toxic Chang et al., 2001

hol) C. formosanus Shiraki Arrestants, feedingdeterrent, repellentand toxic

Maistrello et al., 2001b;Zhu et al., 2001b;Maistrello et al., 2003;Nix et al., 2006

Formosan subterraneantermite

Repellent and toxic Chen et al., 2002

C. formosanus Shiraki Toxic Chang and Cheng, 2002Odontotermes obesus Mortality Singh et al., 2002aC. formosanus Feeding deterrent Tellez et al., 2002

-2-

– Toxic Kobaisy et al., 2003

R. flavipes (Kollar) andR. virginicus (Banks)

Toxic Peterson and Ems-Wilson, 2003

R. speratus (Kolbe) Toxic Sakasegawa et al.,2003; Kim et al., 2005

C. formosanus Toxic Cheng et al., 2004ide, R. speratus Kolbe Toxic Park and Shin, 2005

ol, C. formosanus Shiraki Repellent Watanabe et al., 2005

C. formosanus Repellent and toxic Cheng et al., 2007

C. formosanus Toxic Raina et al., 2007

Page 7: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 965

(Tellez et al., 2001). Blaske and Hertel (2001) studied the effect ofplant extract formulation on the orientation and survival ofsubterranean termites. The fermented extract from leaves of Musaparadisiaca at 100% concentration prevented termite attack for 50days (Thambidurai, 2002).

Fokialakis et al. (2006) tested 220 crude extracts of plantsnative to Greece and Kazakhstan. Four Echinops species werefound to be active against termites. Eight thiophenes were furtherisolated and tested, with results showing varying degree of ter-miticidal activity. Two compounds, terthiophene and bithiophene,demonstrated 100% termite mortality within 9 days against theFormosan subterranean termite. Soil treated with seeds of With-ania somnifera, Croton tiglium, and Hygrophila articulata disruptedthe bacterial activities in the gut of Microtermes obesi. Seedextracts of Withania somnifera and Hygrophila articulate werehighly toxic in a 6-day period. Areas of tunneling and the numberof bacterial colonies were also reduced at 100% concentration ofW. somnifera and H. articulate (Ahmed et al., 2006b). Lantanacamara var. aculeata leaves were studied for their termiticidaleffects. A 5% chloroform extract was most effective (Verma andVerma, 2006).

5.3.1.2.2. Root. Quinines isolated from the chloroform extract ofthe roots of Diospyros sylvatica were found to be toxic againstO. obesus. The major termiticidal components identified wereplumbagin, isodiospyrin, and microphyllone (Ganapaty et al., 2004).

5.3.1.2.3. Fruit and seed. Hexane extract of Xylopia aethiopicafruits and aqueous methanol extract of the seeds were studied fortheir antifeedant activity against R. speratus workers. The crudeextract at 1% concentration exhibited strong antifeedant activity.Further isolation of hexane extract resulted in six ent-kauranediterpenes. Of all, (-) – Kaur – 16- en-19-oic acid had the strongestantifeedent activity (Lajide et al., 1995b). Escoubas et al. (1995)prepared n-hexane and methanolic seed extract of Aframomummelegueta. Various compounds were isolated and [6] – Gingeroland [6] – Shogoal showed the strongest antifeedant activity.

5.3.1.3. Wood extract. Some woods are resistant to termite attackdue to the presence of some active component as part of theirnatural defense. Researchers exploited this potential and extractedthe active components, testing them against termites. Table 4shows the woods of different tree species and the active compo-nents responsible for termite control. The feeding deterrent activityof sapwood extracts of sugar pine, Pinus lambertiana Dougl., andrelated compounds was determined against the western drywoodtermite, lncisitermes minor (Hagen). The substance 2-iodooctade-canoic acid reduced termite feeding while 2- bromooctadecanoicacid had deterrent activity comparable to that of commercialwood preservatives (Scheffrahn and Rust, 1983). The heartwoodof bald cypress, Taxodium distichum (L.) Rich, has been reported toact as a feeding deterrent against C. formosanus Shiraki. Threefractions were isolated, each containing one major component. Allthe three were structurally related diterpenes. The two mostactive heartwood constituents were identified by GC–MS andNMR as ferruginol and manool, while the third and least active,but most prevalent, compound in heartwood was identified asnezukol (Scheffrahn et al., 1988). Twelve taxa of Juniperus fromthe U.S. were investigated for termiticidal activities of theheartwood, bark/sapwood, and leaves. All taxa exhibited termi-ticidal activities for the fresh heartwood sawdusts. Both hexaneand methanol (sequential) extracts of the heartwoods showedtermiticidal activities (Adams et al., 1988). Four antitermiticcompoundsdcatalponol, epicatalponol, catalponone, and cata-palactonedwere isolated from Catalpa bignonioides heartwood,and catalponol and catapalactone were found to be most effectiveagainst R. flavipes (McDaniel, 1992).

Flavonoids, castillen D and castillen E, isolated from the heart-wood of Lonchocarpus castilloi Standley, showed concentration-dependent feeding deterrent activity, but were not toxic to C. brevis(Walker) (Reyes-Chilpa et al., 1995). Cedrol and cedrene, havingtermiticidal ability, have been isolated from Juniperus procera(Kinyanju et al., 2000). Flavonoids showed antifeedant activityagainst C. formosanus. Toxifolin and quercetin isolated from Japa-nese larchwood might be useful as termite control agents (Ohmuraet al., 1999, 2000). The heartwood of Taiwania cryptomerizoidesexhibited very high antitermitic activity due to the presence ofcompounds cedrol and a-cadinol (Chang et al., 2001). Five plantflavonoidsdgenistein, biochanin A, apigenin, quercetin, andglyceollindwere evaluated for fecundity, mortality, and foodconsumption of C. formosanus Shiraki. Apigenin at 50 mg/primaryreproductive pair proved to be the most toxic, and biochanin A wasmost effective in reducing fecundity. Biochanin A is a promisingphytochemical with the ability to reduce fecundity in primaryreproductives of the Formosan subterranean termite (Boue andRaina, 2003). The crude water extracts of Japanese larchwoodcontaining flavonoids in large quantities exhibited potent termitefeeding deterrent activities (Chen et al., 2004).

Three new sesquiterpenes, (4S)-2,6,10-bisaboratrien-4-ol-1-one(1),1,8-epoxy-1(6),2,4,7,10-bisaborapentaen-4-ol (2), and 1-methoxy-4-cadinene (3), have been isolated from the black heartwood ofC. japonica. Compounds 1 and 2 were designated sugikurojinolsA and B, respectively. Compounds 1 and 2 were examined fortermiticidal activity against C. formosanus Shiraki (Arihara et al., 2004).

Heartwood of white cypress pine (Callitris glaucophyllaThompson et Johnson) was investigated for its repellent activityagainst the C. formosanus Shiraki worker. Fraction CY-E2, composedof (�)-citronellic acid, guaiol, a-, a-, and a-eudesmol isomers and anunknown compound, showed the highest statistically significantrepellency (97.8% � 2.2 SEM) of all fractions tested. Bioactivityguided fractionations using high-performance liquid chromatog-raphy led to the isolation of two oxygenated eudesmane-typesesquiterpenes with a-methylene moieties, both termite-repellentcompounds. The isolation of both as ilicic acid methyl ester (IAME)and costic acid from C. glaucophylla heartwood was reported for thefirst time by Watanabe et al. (2005). Heartwoods of Atlantic whitecedar Chamecyparis thyoides; juniper, Juniperus spp.; erisma, Erismaspp.; and ipe, Tabebuia spp. are naturally resistant to R. flavus(Arango et al., 2006). Teak wood is naturally resistant to termiteattack (Roszaini et al., 2006). Heartwood of Caesalpinia echinataLam. is highly resistant to the drywood termite, C. brevis (Silva et al.,2007).

High termiticidal activity was observed for three kinds of woodvinegar made from the mixed wooden chips of C. japonica andPseudotsga menziesii (wood vinegar A), Quercus serrata (woodvinegar B), and Pinus densiflora (wood vinegar C) against R. speratus.Acetic acid, which is the main component of wood vinegar,exhibited high termiticidal acitivity (Yatagai et al., 2002).

5.3.1.4. Resin. Dipterocarp timbers are well known as being resis-tant to biological attack from pests. Shorea robusta has been shownto be highly resistant to the termites M. beesoni and H. indicola (Sen-Sarma, 1963; Sen-Sarma and Chatterjee, 1968). Tables 5 and 6shows the toxic, repellant, and antifeedant effects of resin fromvarious plants. Particleboards constructed from Shorea specieswere also protected from Cryptotermes cynocephalus (Moi, 1980).Dipterocarp woods cause substantial mortality to insects feedingon them. During a 3-month test period, higher mortalitypercentage was observed with termites feeding on Shorea species,while termites feeding on the nondipterocarp Dyera costulatashowed lower mortality percentage (Moi, 1980). Wood resins of thepaleotropical plant family Dipterocarpaceae contain a variety of

Page 8: Biological alternatives for termite control: A review

Table 4Effect of extracts from different parts of plants/trees against termites.

Plant Part Active component Termite Activity/Effect Reference

Adina racemosa Miq. Bark Benzoic acid – Toxic Yaga, 1981Phellodendron amurense – – Reticulitermes speratus Antifeedant Kawaguchi et al., 1989Pinus resinosa, P. strobes,

Carya ovata Mill., Quercusrubra and Acer rubrum

Bark – – Toxic Harun and Labosky, 1985

Neem oil, Azadirachtaindica, A. Juss.

– – R. speratus Kolbe Antifeedant Ishida et al., 1992

Aframomum meleguata Seed Gingerol [5-hydroxy-L-(4-hydroxy-3-methoxyphenyl)decan-3-one]and shogaol [1-(4-hydroxy-3-methoxyphenyl)dec-5-en-3-one]

R. speratus Antifeedant Escoubas et al., 1995

Detarium microcarpum Leaves Clerodane diterpenes, 3,13E-clerodien-15-oic acid, 4(18),13E-clerodien-15-oic acid, 18-oxo-3,13E-clerodien-15-oic acid and 2-oxo-3,13E-clerodien-15-oic acid

R. speratus Antifeedant Lajide et al., 1995a

Xylopia aethiopica Fruits and seeds Diterpenes and amides R. speratus Antifeedant Lajide et al., 1995bAzadirachta indica A. Juss

and Piper guineenseSchum and Thonn

Seed – Microtermes spp., Macrotermesbellicosus Smeathman andM. subhyalinus Rambur

– Umeh and Ivbijaro, 1999

Azadirachta excelsa Leaves, barkextractives andtimber

– Coptotermes curvignathus Antifeedant andinhibitory

Sajap and Aloysius, 2000;Sajap et al., 2006

Moneses uniflora Aerial parts Naphthoquinones, 2, 7- dimethyl-1,4-naphthoquinone and 3-hydroxy-2,7-dimethyl-1,4-naphthoquinone

C. formosanus Toxic Kobaisy et al., 2001

Tarbush (Flourensia cernua) Leaves Monoterpenes and sesquiterpenes Reticulitermes sp. Toxic Tellez et al., 2001Calotropis procera Leaves – Odontotermes obesus – Singh et al., 2002bC. gigantea Leaves – – Repellant Stoll, 2002Musa paradisiaca Leaves – – Repellant Thambidurai, 2002Diospyros sylvatica Root 2-methyl-anthraquinone,

plumbagin, diosindigo, isodiospyrinand microphyllone (quinones)

O. obesus Repellant andtoxic

Ganapaty et al., 2004

Picea glehnii (Sieb. Et Zucc)bark

Stilbene glucosides andisorhapontin (30-methoxy-3,40 , 5-trihydroxystilbene-3-b-D-glucoside)

R. speratus (Kolbe) – Shibutani et al., 2004

Lantana camara var.aculeate

Leaves Triterpenoid, 22 b- acetoxylanticacid

O. obesus Toxic Verma and Verma, 2006;Verma et al., 2005

Withania somnifera, Crotontiglium and Hygrophilaauriculata

Seed and leaf – Microtermes obesi Toxic Ahmed et al., 2006b

Echinops ritro L., E.spinosissimus Turrasubsp. Spinosissimus,E. albicaulis Kar., Kir.and E. transiliensis Golosh

– Thiophenes, 2,20:50 ,200-Terthiophene and 50-(3-buten-1-ynyl)-2,20-bithiophene

C. formosanus Shiraki Toxic Fokialakis et al., 2006

Piper nigrum Seed Guineensine C. formosanus Toxic Meepagala et al., 2006Sophora flavescens Aiton – Alkaloids, matrine and oxymatrine C. formosanus Shiraki Antifeedant and

acute residualtoxicity

Mao and Henderson, 2007

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972966

terpenoids (Bisset et al., 1966, 1967, 1971; Diaz et al., 1966). Freshresins of Anisoptera thurifera appear to protect bee nests fromtermites (Messer, 1984). Dipterocarpus kerrii crude resin and itspurified fractions containing four sesquiterpenoids closely relatedto a-gurjunene are responsible for termiticidal activity againstZootermopsis angusticollus (Richardson et al., 1989). Sesquiterpenes,which occur in many dipterocarps, play an important role indefense against insects (Messer et al., 1990). Chemical componentsdemonstrating insecticidal properties were isolated and identifiedfrom crude resins of four Dipterocarpus species. The most activecompound against Southeast Asian termites (Neotermes spp.) wasalloaromadendrene, followed by humulene, and caryophyllene(Messer et al., 1990). Richardson et al. (1991) identified twouncharacterized sesquiterpenes, 1 and 20, from D. kerrii resin.Sesquiterpene 20 was found to be more toxic then sesquiterpene 1against Neotermes delbergiae. Due to its similarity to a-gurjunene itis referred to as a-gurjunenol.

Guayule resin extracted from Parthenium argentatum Graycontains polyphenols, cinnamyl derivatives, and a variety ofterpenoids (Banigan et al., 1982; Schloman et al., 1983). Thus, it canimpart strength to wood as it is antifeedant, repellent, and toxic totermites (Bultman et al., 1998, 1991; Gutierrez et al., 1999;Nakayama et al., 2001).

5.3.2. Nematode controlTwo families of nematode (phylum Nematoda), Steinernemati-

dae and Heterorhabditidae, are obligate insect parasites (Poinar,1979). Bacterial symbionts Xenorhabdus spp. and Photorhabdus spp.are associated with them (Boemare et al., 1993; Forst et al., 1997).They are widely used in biological control (Gaugler and Kaya, 1990).The infective juvenile stage of the nematode (free-living in soil)infect the insect host; the symbiotic bacteria are released into theinsect hemocoel, causing septicemia and death (Kaya and Gaugler,1993). Trudeau (1989) conducted laboratory tests in which high

Page 9: Biological alternatives for termite control: A review

Table 5Effect of wood extracts from different trees against termites.

Plant Active component Termite Effect Reference

Kalopanax septemlobus Saponins – Toxic Kondo et al., 1963Ternstroemia japonica Barrigenol glycoside (saponin) C. formosanus Toxic Saeki et al., 1968;

Watanabe et al., 1966Inumaki wood, Podocarpus

macrophyllusInumakilactone (bisnorterpenoid) – Toxic Saeki et al., 1970

Callistris L-citronellic acid, D-citronellic acid, L-dihydrocitronellic acid, D-dihydrocitronellicacid, geranic acid, tetrahydrogeranic acid,caprylic acid, pelargonic acid and enanthic acid

R. lucifugus andR. flavipes

Lethal Weissmann andDietrichs, 1975

Pseudotsuga menziesii, Acacia koa, Pinusponderosa, P. lambertiana, Alnusrubra, Juniperus virginiana, Quereusspp., Sequoia sempervirens, Tectonagrandis, Juglans californica and Thujaplicata

– Incisitermes minor(Hagen)

Antifeedant Rust and Reierson, 1977

Hetsuka-nigaki (Adina racemosa) andSendan (Melia azedarach)

Scopoletin and scopolin, nimbolin A andC23H38O5

– Toxic Yaga, 1977 and Yaga,1980

Diospyros virginea L. 7- methyljuglone (5-hydroxy-7-methyl-1-4-naphthquinone)

– Toxic Carter et al., 1978

Torreya nucifera, Thujopsis dolabrata andChamaecyparis formosensis

o- methoxy cinnamaldehyde and torreyal C. formosanus Toxic Ikeda et al., 1978

Ganophyllum falcatum – – Toxic Yazaki, 1982P. lambertiana Dougl. Fatty acids and alpha halogenated compounds I. minor (Hagen) Feeding deterrent Scheffrahn and Rust,

1983Sciadopitys verticillata S. et Z. Isoeugenol mono-Me ether and cedrol – Toxic Yaga and Kinjo, 1986Taxodium distichum Ferruginol, manool, nezukol C. formosanus – Scheffrahn et al., 1988Chamaecyparis obtusa Endl. Diterpenes, T-muurolol and a-cadinol – Toxic Kinjo et al., 1988Juniperus species – – Toxic Adams et al., 1988Port-Orford-cedar, Chamaecyparis

lawsoniana (A. Murr.) Parl.a-terpineol and 3 sesquiterpene alcs., T-cadinol,torreyol (a- cadinol), and a- cadinol

R. flavipes, R. virginicusand C. formosanus

Toxic McDaniel, 1989

Pometia pinnata Saponins – Toxic Ohara et al., 1991Southern catalpa, Catalpa bignonioides

Walt.Catalponol and catalpalactone R. flavipes (Kollar) Toxic McDaniel, 1992

Lonchocarpus castilloi Standley Castilen D and castilen E, flavonoids Cryptotermes Brevis Feeding deterrent Reyes-Chilpa et al.,1995

Cinnamomum camphora (L.) Presl. Camphor – – Hashimoto et al., 1997Juniperus procera – – – Kinyanju et al., 2000Wikstroemia retusa A. Gray wood and

barkHuratoxin and 12a- acetoxy- huratoxin – Toxic Sogabe et al., 2000a

Cryptomeria japonica, Pseudotsgamenzieii, Quercus serrata and Pinusdensiflora

Wood vinegar R. speratus Toxic Yatagai et al., 2002

Cryptomeria japonica Cryptomerione, cubenol, epicubenol, cubebol,and 12-hydroxy-6,7-secoabieta-8,11,13-triene-6,7-dial, T-cadinol, 16-phyllocladanol,sandaracopimarinol, and b-eudesmol

C. formosanus Shiraki Toxic Arihara et al., 2004;Sogabe et al., 2000b

Japanese larchwood, Larix leptolepis Flavonoids C. formosanus Feeding deterrent Chen et al., 2004Australian white cypress, Callitris

glaucophylla Thompson et JohnsonGuaiol, a-eudesmol, and b-eudesmol, citronellicacid and geranic acid

C. formosanus Shiraki Repellent Watanabe et al., 2005

Bangkirai (Shorea laevis) and Merbau(Intsia palembanica)

– Formosan subterraneantermite

– Grace and Torne, 2005

Artocarpus heterophyllus Artocarpin C. formosanus andR. speratus

Toxic Shibutani et al., 2006

Thuja plicata D. don and Chamaecyparisnootkatemis D. Don

– C. formosanus Shiraki Antifeedant Taylor et al., 2006

Brazilian woods Bagassa guianensis(tatajuba) and Erisma uncinatum(cedrinho)

– Nasutitermes sp. Toxic Peres Filho et al., 2006

Myracrodruon urundeuva Lectin Nasutitermes corniger Repellent andtermiticidal

Sa’ et al., 2008

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 967

mortality of R. flavipes (Kollar) termites with nematodes wasobserved. However, experiments with termite species R. tibialis(Epsky and Capinera, 1988) and C. formosanus (Pemberton, 1928)were not successful. Weeks and Baker (2004) studied two species ofentomopathogenic nematode, Heterorhabdidtis bacteriophora(Poinar) and Steinernema carpocapsae (Weiser), in terms of theirsurvivability, detectability, and mortality by the subterraneantermite Heterotermes aureus. Nematode S. carpocapsae proved tobe more potent in causing termite H. aureus mortality thenH. bacteriophora, which could be directly linked to the survivability

of both species. H. aureus had no ability to detect nematodes ofeither species.

5.3.3. Bacterial controlSome rhizobacterial species are known to produce and excrete

hydrogen cyanide (HCN) into the rhizophere. Release of HCN byrhizospheric bacteria into the soil can be toxic to subterraneananimals. HCN-producing Pseudomonas aeruginosa has been shownto have lethal effects on nematodes (Darby et al., 1999; Gallagherand Manoil, 2001). HCN-producing rhizobacteria could be useful

Page 10: Biological alternatives for termite control: A review

Table 6Effect of resin from plants/trees against termite.

Plant Termite Effect Reference

Dipterocarpuskerrii

Zootermopsisangusticollus(Hagen)

Toxic Richardson et al.,1989

Dipterocarpusspecies

Neotermes Toxic Messer et al.,1990

Parthenium argentatumGray (Guayule)

C. formosanusand Heterotermessp.

Repellantand antifeedant

Bultman et al.,1991, 1998

D. kerrii Neotermesdalbergiae

Toxic Richardson et al.,1991

P. argentatum,P. argentatum �P. tomentosumand Castela emoryi

R. flavipes Antifeedant Gutierrez et al.,1999

P. argentatum Gray Reticulitermesspp.

Toxic Nakayama et al.,2001

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972968

for termite control by introducing them into termite mounds,thereby localizing cyanide production and minimizing potentialdeleterious effects on other soil fauna. Nonparasitic rhizobacteriathat produce harmful metabolites might facilitate the biocontrol oftermites. Three different species of HCN-producing rhizobacteria,Rhizobium radiobacter, Alcaligenes latus, and Aeromonsa caviae weretested for their potential to kill O. obesus. The three bacterial specieswere found to be effective in killing the termites under in vitroconditions (Devi et al., 2006).

5.3.4. Fungal controlBiocontrol with pathogenic fungi is a promising alternative to

chemical control of termites. The entomopathogenic fungi playa significant role in integrated pest management (Carrunthus et al.,1991), and fungal pathogens have been known for a long time. DeGeer (1776, 1782) was the first to describe the fungus that attackshouseflies. Approximately 750 species (56 genera) of fungi havebeen isolated from insects, many of which offer great potential pestmanagement. The pathogenicity of a fungus toward insects isdependent upon a complex relationship between the ability of thefungus to germinate on the cuticle, its ability to penetrate thecuticle, and the ability of the insect’s immune system to preventfungus growth. Strains of fungus pathogenic for one particular hostspecies may not show the same growth characteristics and path-ogenicity in another insect species (Huxham et al., 1989). Beauveriabassiana (Balsamo) Vuillemin has been shown to be highly patho-genic to many insect species in both temperate and tropical regions(Stranes et al., 1993). The fungus Metarhyzium aniospliae (Bio Blast)is a biological control agent that requires special application andhandling techniques. Ivermectin is a metabolite produced bya fungus, Streptomyces avermitilis. Sublethal concentrations ofivermectin decrease the food consumption, tunneling, and fightingcapacity of C. formosanus workers (Mo et al., 2006).

6. Bait technology

Baiting is the most recent method of termite pest control. It isenvironmentally sound and utilizes very small amounts of insecttoxicants. In bait technology termite colonies can be eliminated bythe use of toxic or nontoxic baits. Bait is a wood or a cellulosematrix favored by termites that is impregnated with a slow-actingtoxic chemical or nontoxic substance such as fungal spores,mycelium (that grows through termite cuticle and utilizes entiretermite body) and infective stages of nematodes (which carrybacterium which produces toxins lethal to termites). Termiteworkers were exposed to lethal dose of desirable food bait inside

bait stations. Bait stations are placed into soil at intervals aroundthe building. Termite workers feed upon the bait and transfer it toother colony members by grooming or trophallaxis, eventuallyreducing or eliminating the entire colony. Bait consumption bytermites depends on bait design, with termites preferring largerbaits over smaller ones (Evans and Gleeson, 2006). Termites are notsite-specific, but rather, they forage among various food sites,which results in the bait being encountered by many colonymembers. The toxicant must be slow acting because termites tendto avoid sites where sick and dead termites accumulate. Successfultermite baiting needs proper monitoring and maintenance of thestations. Baits are often used in sensitive environments. A numberof baits have been marketed to control termites, with bait productscontaining ingredients such as diflubenzuron, chlorflurazuronhexaflumuron, triflumuron (Bayer–Alsystin 480 SC), sulfluramid,noviflumuron, disodium octoborate tetrahydrate, arsenic trioxide,fipronil, and hydramethylnon. Among them, hexaflumuron is themost popular bait toxicant. Foraging of Coptotermes curvignathuscould be eliminated by using a bait matrix containing hexa-flumuron (Sajap et al., 1999). Fipronil bait consisting of straw pulpand white sugar was evaluated against field colonies of Odonto-termes formosanus (Huang et al., 2005). Su (2005) concluded thatnoviflumuron bait caused higher mortality than did fipronil andthiamethoxam (Syngenta-Cruiser). Osbrink et al. (2005) observedthat imidacloprid did not reduce termite population effectively, andwas therefore not suitable as a liquid bait model.

7. Wood treatment

7.1. Chemical

Chemical treatment of wood to prevent termite attack isa common and effective method. Enoki et al. (1990) treated thewood blocks of buna (Fagus crenata), sugi (C. japonica), and aka-matsu (P. densiflora) with butylene oxide and triethylamine toincrease their termite resistance. Maistrello et al. (2001b) demon-strated that wood treated with disodium octaborate tetrahydrateinduced high termite mortality and almost complete loss of flagel-lates. Chromated copper arsenate (CCA) is commonly used as a woodpreservative against termites, but due to its negative environmentaleffects they are formulated as copper borate, water-borne coppernaphthanate, and N0 N-naphthaloylhydroxylamine. Arango et al.(2006) compared the natural durability of wood species with thesepreservative treatments and came to the conclusion that thesewoods inhibit termite damage as effectively as preservative treat-ments. Nowadays, borate-based multi-component biocide systemsare being used. Multi-component systems combining a borate basesupplemented with either 0.1% azole or 0.5% thujaplicin performedwell against various fungi and the subterranean termite R. flavipes(Kollar). They are nontoxic, nonvolatile, odorless, hypoallergenic,and able to provide long-term protection (Clausen and Yang, 2007).

7.2. Nonchemical

Researchers are studying various nonchemical, plant-basedpreservatives to replace chemical treatment of wood for termitecontrol. Sharma et al. (1990) treated the woods of Pinus longifoliaand Mangifera indica with Ricinus communis and Azadirachta indicaoil to protect against termite infestation. They found R. communisoil superior to A. indica oil. The non-rubber-producing extract(resin) of the guayule bush (P. argentatum Gray) acts as a potentialwood protectant. Wood treated with guayule resin was not attackedby termites of the genus Coptotermes and Heterotermes during 33and 45 months of exposure in the Panamanian rain forest, respec-tively (Bultman et al.,1991). Plant essential oils are considered a safe

Page 11: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 969

and effective replacement for chemical preservatives (Palmer et al.,2001). Vetiver oil and nootkatone (a component of vetiver oil) canalso be used in wood treatments. Nootkatone acts as feedingdeterrent to termites (Maistrello et al., 2001a, 2003). Kartal et al.(2006) screened various essential oils and extracts from plants fortheir ability to inhibit termite attack, and all the formulations wereeffective against subterranean termite attack. The researcherssuggested that essential oils be developed as potential woodpreservatives.

8. Relationship between chemical structure and antitermiticactivity of active component

Scheffrahn and Su (1987) investigated the structural relationshipsof 2-haloalkanoic acids and their esters as antitermitic agents.Unhalogenated acids had little effect on C. formosanus mortality andwood consumption as compared to 2-brominated acids, which weresignificantly more toxic and resulted in diminished feeding on woodby termites. Methyl esters of haloacids had a variable effect onantitermitic activity that may have been related to carbon-chainlength. 2-Iodooctadecanoic acid and ester treatments were moretoxic and less fed upon than 2-bromo compounds, which, in turn,were more active than their 2-chloro analogs. Methyl, ethyl, andisopropyl-2-halooctadecanoates were equally or more toxic thantheir respective haloacids. Noviflumuron (Dow Agrosciences-RecruitIII AG Termite bait; C14H9ClF9N2O3), bistrifluron (C16H7ClF8N2O2),hexaflumuron (Dow Agrosciences-Recruit AG Termite bait;C16H8Cl2F6N2O3), and diflubenzuron (Crompton-Dimilin SC 48Forestry; C17H7Cl2F2N2O3) all are slow-acting insect toxicants used intermite baits. Noviflumuron is more potent and has faster activity. Itcaused higher R. speratus mortality as compared to haxaflumuronand diflubenzuron (Karr et al., 2004; King et al., 2005). Bistrifluronshowed a faster speed of action against C. formosanus than hexa-flumuron (Kubota et al., 2006). Hexaflumuron is superior to diflu-benzuron as a bait toxicant against both C. formosanus and R. flavipes(Su and Scheffrahn, 1993). This suggests that the antitermitic activityof these toxicants increases as the number of fluorine moleculesincreases in the chemical structure of these toxicants. Ohara et al.(1991) synthesized saponins by chemical reactions and also isolatedthem from Pometia pinnata wood to investigate the relationshipbetween chemical structure and antitermitic activity. He found outthat the saponins with two sugar chains had no antitermitic activitywhile those having a single sugar chain showed good results. Resultsare the same for naturally isolated saponins. The longer the sugarchains the weaker their antitermite activity. Ohmura et al. (1997)synthesized triterpenoid saponins (methyl oleanolate glycosides) toinvestigate the same. Methyl oleanolate-3-yl b-D-glucoside andmethyl oleanolate-3-yl b-D-cellobioside showed the greatest anti-feedant activity with R. speratus, and the activity decreased accordingto the lengthening of the chain of the sugar moiety. Because themolecular hydrophilicity increases with the increasing amounts ofsugar residues, it is assumed that adequate polarity is necessary toreveal the antitermitic activities of triterpenoid saponins. Thesestudies suggest that the number of sugar chains, halogenation andcarbon-chain length in the chemical structure of the active compo-nent are the factors affecting the antitermitic activity.

9. Conclusion

This review explains the termite control options used nowadaysand in the past. The chemical method of control is the most popularand effective. But the deleterious effect of chemicals on our envi-ronment cannot be ignored. Therefore, for the safety of livingbeings and the environment, we should search for ecologically safealternatives and exploit the potential of the nonchemical measures

that have been studied by other researchers. The plants investi-gated by different workers having strong termiticidal activity canbe further used individually and in combination. The activecomponent responsible for termite control can be extracted toprepare potent biopesticidal formulations. Few studies relate thestructure of the active component with antitermitic activity andenable us to explore the chemical structure of active componentsprior to their testing on termite species. Plant extracts could beexploited to develop new wood preservatives. Further field-levelstudies are required to use these botanicals as commercialtermiticides.

Acknowledgement

The first author gratefully acknowledges financial assistance forresearch provided by the Indian Institute of Technology, Delhi,India.

References

Aanen, D.K., Eggleton, P., Rouland-Lefevre, C., Guldberg-Froslev, T., Rosendahl, S.,Boomsma, J.J., 2002. The evolution of fungus-growing termites and theirmutualistic fungal symbionts. Proceeding of National Academy of Sciences ofthe United States of America 99, 14887–14892.

Adams, R.P., McDaniel, C.A., Carter, F.L., 1988. Termiticidal activities in the heart-wood, bark/sapwood and leaves of Juniperus species from the United States.Biochemical Systematics and Ecology 16, 453–456.

Ahmed, S., Mustafa, T., Riaz, M.A., Hussain, A., 2006a. Efficacy of insecticides againstsubterranean termites in sugarcane. International Journal of Agriculture andBiology 8, 508–510.

Ahmed, S., Riaz, M.A., Shahid, M., 2006b. Response of Microtermes obesi (Isoptera:Termitidae) and its gut bacteria towards some plant extracts. Journal of Food,Agriculture and Environment 4, 317–320.

Arango, R.A., Green III, F., Hintz, K., Lebow, P.K., Miller, R.B., 2006. Natural durabilityof tropical and native wood against termite damage by Reticulitermes flavis(Kollar). International Biodeterioration & Biodegradation 57, 146–150.

Arihara, S., Umeyama, A., Bando, S., Imoto, S., Ono, M., Yoshikawa, K., 2004. Threenew sesquiterpenes from the black heartwood of Cryptomeria japonica.Chemical & Pharmaceutical Bulletin 52, 463–465.

Banigan, T.F., Verbiscar, A.J., Weber, C.W., 1982. Composition of guayule seeds,leaves, and wood. Journal of Agriculture and Food Chemistry 30, 427–431.

Bisset, N.G., Diaz, M.A., Ehret, C., Ourisson, G., Palmad, M., Patil, F., Pesnelle, P.,Streith, J., 1966. Etudes chimio-taxonomiques dans la famille des dipt-grocarpacges–II. Phytochemistry 5, 865–880.

Bisset, N.G., Diaz-parra, M.A., Ehret, C., Ourisson, G., 1967. Etudes chimio-tax-onomiquesdans la famille des diptdrocarpacees–iii. Phytochemistry 6,1395–1405.

Bisset, N.G., Chavanel, V., Lantz, J.-P., Wolff, R.E., 1971. Constituants sesquiterpe-niques et triterpeniques des rdsines du gem’e shorea. Phytochemistry 10,2451–2463.

Blaske, V.U., Hertel, H., 2001. Repellent and toxic effects of plant extracts onsubterranean termites (Isoptera: Rhonotermidae). Journal of Economic Ento-mology 94, 1200–1207.

Boemere, N.E., Akhurst., R.J., Mourant, R.G., 1993. DNA relatedness between Xen-orhabdus spp. (Enterobacteriacae), symbiotic bacteria of entomopathogenicnematodes, and a proposal to transfer Xenorhabdus luminescens to a new genus,Photorhabdus gen. Nov. International Journal of Systematic Bacteriology 43,249–255.

Bond, E.J. 1984. Manual of fumigation for insect control. FAO Plant Production andProtection Papers 54, online at http://www.fao.org/docrep/x5042e/x5042E08.htm.

Boue, S.M., Raina, A.K., 2003. Effects of plant flavonoids on fecundity, survival, andfeeding of the Formosan subterranean termite. Journal of Chemical Ecology 29,2575–2584.

Bultman, J.D., Gilbertson, R.L., Adaskaveg, J., Amburgey, T.L., Parikh, S.V., 1991. Theefficacy of guayule resin as a pesticide. Bioresource Technology 35, 197–201.

Bultman, J.D., Chen, S.-L., Schloman Jr., W.W., 1998. Antitermitic efficacy of the resinand rubber in fractionator overheads from a guayule extraction process.Industrial Crops Production 8, 133–143.

Byron, J. 1997. End for methyl bromide. Pesticides News 38, pp 9, online at http://www.pan-uk.org/pestnews/Issue/pn38/pn38p9.htm.

Carrunthus, R.I., Sawer, A.J., Hural, K., 1991. Use of fungal pathogens for biologicalcontrol of insect pests. In: Sustainable Agriculture Research and Education inthe Field. National Academy Press, Washington DC, USA, pp. 336–339.

Carter, F.L., Garlo, A.M., Stanely, J.B., 1978. Termiticidal components of woodextracts: 7-methyl-juglone from Diospyros virginiana. Journal of Agriculture andFood Chemistry 26, 869–873.

Page 12: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972970

Chang, S.-T., Cheng, S.-S., Wang, S.-Y., 2001. Antitermitic activity of essential oils andcomponents from taiwania (Taiwania cryptomerioides). Journal of ChemicalEcology 27, 717–724.

Chang, S.-T., Cheng, S.-S., 2002. Antitermitic activity of leaf essential oils andcomponents from Cinnamomum osmophleum. Journal of Agricultural and FoodChemistry 50, 1389–1392.

Chauhan, K.R., Raina, A.K., 2006. Modified vetiver oil: economic biopesticide. ACSSymposium Series 927, 210–218. Natural Products for Pest Management.

Chen, F., Zhu, B.R.C., Henderson, G., Fei, H., Laine, R., Wang, X., 2002. Termiticidalactivity of essential oils against the formosan subterranean termite. Abstracts ofPapers, 224th ACS National Meeting, Boston, MA, United States, August 18–22,2002.

Chen, K., Ohmura, W., Doi, S., Aoyama, M., 2004. Termite feeding deterrent fromJapanese larchwood. Bioresource Technology 95, 129–134.

Cheng, S.-S., Wu, C.-L., Chang, H.-T., Kao, Y.-T., Chang, S.-T., 2004. Antitermitic andantifungal activities of essential oil of Calocedrus formosana leaf and itscomposition. Journal of Chemical Ecology 30, 1957–1967.

Cheng, S.-S., Chang, H.-T., Wu, C.-L., Chang, S.-T., 2007. Anti-termitic activities ofessential oils from coniferous trees against Coptotermes formosanus. BioresourceTechnology 98, 456–459.

Clausen, C.A., Yang, V., 2007. Protecting wood from mould, decay, and termites withmulti-component biocide systems. International Biodeterioration & Biodegra-dation 59, 20–24.

Cornelius, M.L., Grace, J.K., Yates, J.R., 1997. Toxicity of monoterpenoids and othernatural products to the formosan subterranean termite (Isoptera: Rhinotermi-tidae). Journal of Economic Entomology 87, 705–708.

Cox, R.A., Rattigan, O.V., Jones, R.L., 1995. Laboratory studies of BrO reactions ofinterest for the atmospheric ozone balance. In: Bandy, A.R. (Ed.), The Chemistryof the Atmosphere: Oxidants and Oxidation in the Earth’s Atmosphere. RoyalSociety of Chemistry, Cambridge, pp. 47–64.

Darby, C., Cosma, C.L., Thomas, J.H., 1999. Lethal paralysis of Caenorhabditis elegansby Pseudomonas aeruginosa. Proceedings of National Academy of Science UnitedStates of America 96 (15), 202–215. 207.

De Geer, C., 1776. Memories Pour Servita ‘L’ this toriededs insect, vol. 5. Hassel berg,Pierre, Stolkholm.

De Geer, C. 1782. Aabhandlungen, Zen Geschit der Insekten (Translated fromGerman by J.A.E.Goeze).

Devi, K.K., Seth, N., Kothamasi, S., Kothamasi, D., 2006. Hydrogen cyanide-producingrhizobacteria kill subterranean termite Odontotermes obesus (Rambur) bycyanide poisoning under in vitro conditions. Current Microbiology 54, 74–78.

Diaz, M.A., Ourisson, G., Bisset, N.G., 1966. Etudes chimio-taxonomiques dans lafamille des dipterocarpacaes–I. Phytochemistry 5, 855–863.

Doi, S., Kurimoto, Y., Ohmura, W., Ohara, S., Aoyama, M., Yoshimura, T., 1999. Effectsof heat treatments of wood on the feeding behaviour of two subterraneantermites. Holzforschung 53, 225–229.

Doolittle, M., Raina, A., Lax, A., Boopathy, R., 2007. Effect of natural products on gutmicrobes in Formosan subterranean termite, Coptotermes formosanus. Interna-tional Biodeterioration & Biodegradation 59, 69–71.

Engel, M.S., Krishna, K., 2004. Family-group names for termites (Isoptera). AmericanMuseum Novitates 3432, 1–9.

Enoki, A., Tanaka, H., Yoshioka, S., Fuse, G., 1990. Fungal and termite resistance ofetherified wood and its dimensional stability. Kinki Daigaku Nogakubu Kiyo 23,25–32.

Epsky, N., Capinera, J.L., 1988. Efficacy of the entomogenous nematode Steinernemafeltiae against a subterranean termite, Reticulitermes tibialis (Isoptera: Rhino-termitidae). Journal of Economic Entomology 81, 1313–1317.

Escoubas, P., Lajide, L., Mizutani, J., 1995. Termite antifeedant activity in Aframomummeleguata. Phytochemistry 40, 1097–1099.

Evans, T.V., Gleeson, P.V., 2006. The effect of bait design on bait consumption intermites (Isoptera: Rhinotermitideae). Bulletin of Entomological Research 96,85–90.

Ewart, D.M., 2000. Termite barriers for new construction in Australia (Isoptera).Sociobiology 37, 379–388.

Fokialakis, N., Osbrink, W.L.A., Mamonov, L.K., Gemejieva, N.G., Mims, A.B.,Skaltsounis, A.L., Lax, A.R., Cantrell, C.L., 2006. Antifeedant and toxicity effects ofthiophenes from four Echinops species against the Formosan subterraneantermite, Coptotermes formosanus. Pest Management Science 62, 832–838.

Forst, S., Dowds, B., Boemare, N., Stackebrandt, E., 1997. Xenorhabdus and Proto-rhabdus spp.: bugs that kill bugs. Annual Review Microbiolology 51, 47–72.

Gaju, M., Notario, M.J., Moral, R., Alcaide, E., Moreno, T., Molero, R., de Roca, C.B.,2002. Termite damage to buildings in the Province of Cordoba. Spain Sociobi-ology 40, 75–85.

Gallagher, L.A., Manoil, C., 2001. Pseudomonas aeruginosa PAO1 kills Caenorhabditiselegans by cyanide poisoning. Journal of Bacteriology 183, 6207–6214.

Ganapaty, S., Thomas, P.S., Fotso, S., Laatsch, H., 2004. Antitermitic quinones fromDiospyros sylvatica. Phytochemistry 65 (9), 1265–1271.

Gaugler, R., Kaya, H.K. (Eds.), 1990. Entomopathogenic Nematodes in BiologicalControl. CRC Press, p. 365.

Georgiou, G.P., Taylor, C.E., 1986. Factors influencing the evolution of resistance.In: National Research Council O/S Committee on Strategies for the Manage-ment Pesticide Resistance Pest Population (Ed.), Pesticide Resistance Strate-gies and Tactics for Management. National Academy Press, Washington, DC,pp. 167–169.

Grace, J.K., 1998. Resistance of pine treated with chromated copper arsenate to theformosan subterranean termite. Forest Products Journal 48, 79–82.

Grace, J.K., Yates III, J.R., Tome, C.H.M., Ohino, R.J., 1996. Termite-resistantconstruction: Uses of a stainless steel. Mesh to exclude Coptotermes formasanus(Isoptera: Rhinotermitidae). Sociobiology 28, 365–372.

Grace, J.K., Torne, C.H.M., 2005. Resistance of the Indonesian woods bangkirai(Shorea laevis) and Merbau (Intsia palembanica) to formosan subterraneantermite attack. Sociobiology 45, 503–509.

Grace, J.K., Yates, J.R., 1992. Behavioural effects of a neem insecticide on Copto-termes formosanus (Isoptera: Rhinotermitidae). Tropical Pest Management 38,176–180.

Gutierrez, C., Gonzalez-Coloma, A., Hoffmann, J.J., 1999. Antifeedant properties ofnatural products from Parthenium argentatum, P. argentatumn � P. tomentosum(Asteraceae) and Castela emoryi (Simaroubeaceae) against Reticulitermesflavipes. Industrial Crops and Products 10, 135–140.

Harun, J., Labosky, P.J., 1985. Antitermitic and antifungal properties of selective barkextractives. Wood and Fiber Science 17, 327–335.

Hashimoto, K., Ohtani, Y., Sameshima, K., 1997. Termiticidal activity and its trans-verse distribution in camphor (Cinnamomum camphora) wood. MokuzaiGakkaishi 43, 566–573.

Henderson, G., Heumann, D.O., Laine, R.A., Zhu, B.C.R., Chen, F., 2005a. Extracts ofvetiver oil as a repellent and toxicant to ants, ticks, and cockroaches. U.S. PatentNo. 6, 906,108 (14) June 2005.

Henderson, G., Heumann, D.O., Laine, R.A., Zhu, B.C.R., Chen, F., 2005b. Vetiver oilextract as termite repellent and toxicant. U.S. Patent No. 6,890,960 (10) May 2005.

Huang, Q.-Y., Lei, C.-L., Xue, D., 2005. Field evaluation of fipronil bait againstsubterranean termite Odontotermes formosanus (Isoptera: Termitidae). Journalof Economic Entomology 99, 455–461.

Huxham, L.M., Samueli, K.D.Z., Hele, J.B., McCorkindale, N.J., 1989. In vivo and invitro assays for pathogenicity of wild type and mutant strains of Meta-rhizium anisopliae for three insect species. Journal of Invertebrate Pathology53, 143–151.

Ikeda, T., Takahashi, M., Nishimota, K., 1978. Antitermitic components of Kaya wood,Torreya nucifera Sieb. et Zucc. Mokuzai Gakkaishi 24, 262–266.

Ishida, M., Serit, M., Nakata, K., Juneja, L.J., Kim, M., Takahashi, S., 1992. Severalantifeedants from neem oil, Azadirachta indica A. Juss., against Reticulitermessperatus kolbe (Isoptera: Rhinotermitidae). Bioscience, Biotechnology andBiochemistry 56, 1835–1838.

Isman, M.B., 2000. Plant essential oils for pest and disease management. CropProtection 19, 10603–10608.

Joshi, P.K., Singh, N.P., Singh, N.N., Gerpacio, R.V., Pingali, P.L., 2005. Maize in India:Production Systems, Constraints, and Research Priorities. D.F. CIMMYT, Mexico,p. 22.

Karr, L.L., Sheets, J.J., King, J.E., Dripps, J.E., 2004. Laboratory performance andpharmacokinetics of the benzoylphenylurea noviflumuron in eastern subter-ranean termites (Isoptera: Rhinotermitidae). Journal of Economic Entomology97, 593–600.

Kartal, S.N., Hwang, W.-J., Imamura, Sekine, Y.Y., 2006. Effect of essential oilcompounds and plant extracts on decay and termite resistance of wood. Holzals Roh- und Werkstoff 64, 455–461.

Kawaguchi, H., Kim, M., Ishida, M., Ahn, Y.-J., Yamamoto, T., Yamaoka, R.,Kozuka, M., Goto, K., Takahashi, S., 1989. Several antifeedents from Phello-dendron amurense against Reticulitermes speratus. Agricultural and BiologicalChemistry 53, 2635–2640.

Kaya, H.K., Gaugler, R., 1993. Entomopathogenic nematodes. Annual Reviews ofEntomology 38, 181–206.

Kim, J.H., Liu, K.H., Yoon, Y., Sornnuwat, Y., Kitirattrakarn, T., Anantachoke, C., 2005.Essential leaf oils from Melaleuca cajuputi. Acta Horticulturae 680, 65–72.Proceedings of WOCMAP III: The IIIrd World Congress on Medicinal andAromatic Plants, 2003.

King, J.E., Demark, J.J., Griffin, A.J., 2005. Comparative laboratory efficacy of novi-flumuron and diflubenzuron on Reticulitermes flavipes (Isoptera: Rhinotermiti-dae). Sociobiology 45, 779–785.

Kinjo, K., Doufuku, Y., Yaga, S., 1988. Termiticidal substances from the wood ofChamaecyparis obtusa Endl. Mokuzai Gakkaishi 34, 451–455.

Kinyanju, T., Gitu, P.M., Kamau, G.N., 2000. Potential antitermite compounds fromJuniperus Procera extracts. Chemosphere 41, 1071–1074.

Kobaisy, M., Tellez, M.R., Osbrink, W.L., 2001. Antitermite naphthoquinones fromMoneses uniflora. Abstracts of Papers, 222nd ACS National Meeting, Chicago, IL,United States, August 26–30, 2001.

Kobaisy, M. Tellez, M.R. Khan, I.A. Schaneberg, B.T., 2003. Essential oil compositionof three Italian species of Ephedra. Abstracts of Papers, 226th ACS NationalMeeting, New York, NY, United States, September 7–11, 2003.

Kondo, T., Kurotori, S., Teshima, M., Sumimoto, M., 1963. Termiticidal substancefrom Kalopanax septemlobus wood. Nippon Mokuzai Gakkaishi 9, 125–129.

Kubota, S., Shono, Y., Matsunaga, T., Kunio, T., 2006. Laboratory evaluation ofbistrifluron, a benzoylphenylurea compound, as a bait toxicant against Copto-termes formosanus (Isoptera: Rhinotermitidae). Journal of Economic Ento-mology 99, 1363–1368.

Kuriachan, I., Gold, R.E., 1998. Evaluation of the ability of Reticulitermes flavipusKollar, a subterranean termite (Isoptera: Rhinotrmitideae) to differentiatebetween termiticide treated and untreated soils in laboratory tests. Sociobi-ology 32, 151–166.

Lajide, L., Escoubas, P., Mizutani, J., 1995a. Termite antifeedant activity in Detariummicrocarpum. Phytochemistry 40, 1101–1104.

Lajide, L., Escoubas, P., Mizutani, J., 1995b. Termite antifeedant activity in Xylopiaaethiopica. Phytochemistry, 1105–1112.

Page 13: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972 971

Lee, C.-Y., 2002. Subterranean termite pests and their control in the urban envi-ronment in Malaysia. Sociobiology 40, 3–9.

Lenz, M., Schafer, B., Runko, S., Glossop, L., 1997. The concrete slab as part ofa termite barrier system: response of Australian subterranean termites to cracksof different width in concrete. Sociobiology 30, 103–118.

Lewis, V.R., 1997. Alternative control strategies for termites. Journal of AgriculturalEntomology 14, 291–307.

Lewis, V.R., Haverty, M.I., 2000. Lethal effects of electrical shock treatments to thewestern drywood termite (isopteran: kalotermitidae) and resulting damage towooden test boards. Sociobiology 37, 163–183.

Maistrello, L., Henderson, G., Laine, R.A., 2001a. Efficacy of vetiver oil and nootka-tone as soil barriers against formosan subterranean termite (Isoptera: Rhino-termitidae). Journal of Economic Entomology 94, 1532–1537.

Maistrello, L., Henderson, G., Laine, R.A., 2001b. Effects of nootkatone and a boratecompound on formosan subterranean termite (Isoptera: Rhinotermitidae) andits symbiont protozoa. Journal of Entomological Science 36, 229–236.

Maistrello, L., Henderson, G., Laine, R.A., 2003. Comparative effects of vetiver oil,nootkatone and disodium octaborate tetrahydrate on Coptotermes formosanusand its symbiotic fauna. Pest Management Science 59, 58–68.

Mao, L., Henderson, G., Bourgeois, W.J., Vaughn, J.A., Laine, R.A., 2006. Vetiver oiland nootkatone effects on the growth of pea and citrus. Industrial Crops andProducts 23, 327–332.

Mao, L., Henderson, G., 2007. Antifeedant activity and acute and residual toxicity ofalkaloids from Sophora flavescens (Leguminosae) against formosan subterra-nean termites (Isoptera: Rhinotermitidae). Journal of Chemical Ecology 100,866–870.

McDaniel, C.A., 1989. Major termiticidal components of heartwood of Port-Orford-cedar, Chaemecyparis lawsoniana (A. Murr.) Parl. Material Organism 24, 1–15.

McDaniel, C.A., 1992. Major antitermitic components of the heartwood of southerncatalpa. Journal of Chemical Ecology 18, 359–369.

Meepagala, K.M., Osbrink, W., Ballew, A., Lax, A.R., Duke, S.O., 2006. Natural productbased amides against Formosan subterranean termites (Coptotermes for-mosanus). Abstracts of Papers, 232nd ACS National Meeting, San Francisco, CA,United States, Sept. 10–14, 2006.

Mellouki, A., Talukdar, R.K., Schmoltner, A., Gierczak, T., Mills, M.J., Solomon, S.,Ravishankara, A.R., 1992. Atmospheric lifetimes and ozone depletion potentialsof methyl bromide and dibromomethane. Geophysical Research Letters 19,2059–2062.

Messer, A.C., 1984. Chalicodoma pluto: the world’s largest bee rediscovered livingcommunally in termite nests (Hymenoptera: Megachilidae). Journal of KansasEntomological Society 57, 165–168.

Messer, A., McCormick, K., SunjayaHagedorn, H.H., Tumbel, F., Meinwald, J., 1990.Defensive role of tropical tree resins: antitermitic sesquiterpenes from South-east Asian dipterocarpaceae. Journal of Chemical Ecology 16, 3333–3352.

Meyer, J.R., 2005. Isoptera. Department of Entomology. NC State University. onlineat. http://www.cals.ncsu.edu/course/ent425/compendium/termites.html.

Milano, S., Fontes, L.R., 2002. Termite pests and their control in urban Brazil.Sociobiology 40, 163–177.

Mitchell, J.D., 2002. Termites as pests of crops, forestry, rangeland and structures inSouthern Africa and their control. Sociobiology 40, 47–70.

Mo, J., Wang, Z., Song, X., Guo, J., Cao, X., Cheng, J., 2006. Effects of sublethalconcentration of ivermectin on behaviour of Coptotermes formasanus. Sociobi-ology 47, 687–696.

Moi, L.C., 1980. A new laboratory method for testing the resistance of particleboards to the drywood termite Cryptotermes cynocephalus. Malaysian Forestry43, 350–355.

Morris, P.I., 2001. Integrated control of subterranean termites: the 6s approach.Proceedings of the American Wood Preservers Association 96, 93–106.

Myles, T.G., 2005. Termite biology, Urban Entomology Programme, online at http://www.utoronto.ca/forest/termite/termite.htm.

Nakashima, Y., Shimizu, K., 1972. Antitermitic activity of Thujopsis dolabrata varHondai. III. Components with a termiticidal activity. Miyazaki Daigaku Noga-kubu Kenkyu Hokoku 19, 251–259.

Nakayama, F.S., Vinyard, S.H., Chow, P., Bajwa, D.S., Youngquist, J.A., Muehl, J.H.,Krzysik, A.M., 2001. Guayule as a wood preservative. Industrial Crops andProducts 14, 105–111.

Nix, K.E., Henderson, G., Zhu, B.C.R., Laine, R.A., 2006. Evaluation of vetiver grassroot growth, oil distribution, and repellency against formosan subterraneantermites. Horticultural Science 41, 167–171.

Ohara, S., Kato, A., Hayashi, Y., Itou, Y., 1991. Chemical structure and biologicalactivity of saponins. Baiomasu Henkan Keikaku Kenkyu Hokoku 27, 54–73.

Ohkuma, M., Ohtoko, K., Iida, T., Tokura, M., Moriya, S., Usami, R., Horikoshi, K.,Kudo, T., 2000. Phylogenetic identification of hypermastigotes, Pseudo-trichonympha, Spirotrichonympha and Holomastigotoides, and parabasaliansymbionts in the hindgut of termites. Journal of Eukaryotic Microbiology 47,249–259.

Ohmura, W., Ohara, S., Kato, A., 1997. Synthesis of triterpenoid saponins and theirantitermitic activities. Mokuzai Gakkaishi 43, 869–874.

Ohmura, W., Doi, S., Aoyama, M., Ohara, S., 1999. Components of steamed and non-steamed Japanese larch (Larix leptolepis (Sieb. et Zucc.) Gord.) heartwoodaffecting the feeding behavior of the subterranean termites, Coptotermesformosanus Shiraki (Isoptera: Rhinotermitidae). Holzforschung 53, 569–574.

Ohmura, W., Doi, S., Aoyama, M., Ohara, S., 2000. Antifeedant activity of flavonoidsand related compounds against the subterranean termite Coptotermesformosanus Shiraki. Journal of Wood Science 46, 149–153.

Osbrink, W.L.A., Cornelius, M.L., Lax, A.R., 2005. Effect of imidacloprid soil treat-ments on occurrence of formosan subterranean termites (Isoptera: Rhino-termitidae) in independent monitors. Journal of Economic Entomology 98,2160–2168.

Palmer, A.S., Stewart, J., Fyfe, L., 2001. The potential application of plant essential oilas natural food preservative in soft cheese. International Journal of FoodMicrobiology 18, 463–470.

Park, I.L.-K., Shin, S.-C., 2005. Fumigant activity of plant essential oils and compo-nents from garlic (Allium sativum) and clove bud (Eugenia caryophyllata) oilsagainst the Japanese termite (Reticulitermes speratus kolbe). Journal ofAgricultural and Food Chemistry 53, 4388–4392.

Pemberton, C.E., 1928. Nematodes associated with termites in Hawaii, Borneo andCelebes. Proceedings of the Hawaiian Entomological Society 7, 147.

Peres Filho, O., Dorval, A., Duda, M.J., Moura, R.G., 2006. Nasutitermes sp. (Isoptera,Termitidae) response to extracts from four Brazilian woods. Scientia Forestalis/Forest Sciences 71, 51–54.

Peterson, C.J., Ems- Wilson, J., 2003. Catnip essential oil as a barrier to subterranean(Isoptera: Rhino-termitideae) in the laboratory. Journal of Economic Ento-mology 96, 1275–1282.

Philip, H., 2004. Biology and Control of the Subterranean Termite. Pest ManagementFactsheet 98–01, online at http://www.agf.gov.bc.ca/cropprot/termite.htm.

Poinar Jr., G.O., 1979. The Natural History of Nematodes. Prentice Hall, EnglewoodCliffs, NJ.

Prakash, A., Rao, J., Pasalu, I.C., Mathur, K.C., 1987. Rice Storage and Insect PestManagement. B.R. Publishing Corp, New Delhi. 337.

Prakash, A., Rao, J., Gupta, S.P., Binh, T.C., 1989. Evaluation of certain plant productsas paddy grain protectant against angoumois grain moth, Sitotorga cerealla Oliv.Journal Nature Conservation 1, 7–13.

Prakash, A., Rao, J., Tewari, S.N., Gupta, S.P., 1990. Rice agro-ecosystem managementby pesticides and its consequences. In: Verma, S.R. (Ed.), Growth Development &Natural Resource Conservation. Natcon Publication, Nature Conservators Indiapp. 131–137.

Prakash, A., Rao, J., 1986. Evaluation of plant producs as antifeedents against the ricestorage insects. Proceedings of Symposiul Residue & Environmental Pollution,201–205.

Prakash, A., Rao, J., 1987. Use of chemicals as grain protectants in storage ecosystemand its consequences. Bulletin Grain Technology 25, 65–69.

Raina, A., Bland, J., Doolittle, M., Lax, A., Boopathy, R., Folkins, M., 2007. Effect oforange oil extract on the formosan subterranean termite (Isoptera: Rhino-termitidae). Journal of Economic Entomology 100, 880–885.

Rajagopal, D., 2002. Economically important termite species in India. Sociobiology41, 33–46.

Reyes-chilpa, R., Viveros-rodriguez, L.N., Gomez-garibay, Z.F., Alavez-solano, D.,1995. Antitermitic activity of lonchocarpus castilloi flavonoids and heartwoodextracts. Journal of Chemical Ecology 21, 455–463.

Richardson, D.P., Messer, A.C., Greenberg, S., Hagedorn, H.H., Meinwald, J., 1989.Defensive sesquiterpenoids from a dipterocarp (Dipterocarpus kerrii). Journal ofChemical Ecology 15, 731–747.

Richardson, D.P., Messer, A.C., Newton, B.A., Lindeman, N.I., 1991. Identification andpreparation of antiinsectan dienols from dipterocarpus kerrii tree resins. Journalof Chemical Ecology 17, 663–685.

Roomi, M.W., Shah, A.H., Anwarullah, M., Hussain, M., 1990. Studies on the controlof subterranean termites by inorganic pesticides. Ariz. Schaidlingskde.,Pflanzenschutz, Umwehschutz 63, 50–52.

Roszaini, K., Salmiah, U., MohdDahlan, J., 2006. Natural resistance of timbers to attack:laboratory evaluation of the resistance of Malaysian wood against coptotermescurvignathus (Holmgren). Journal of Institute of Wood Science 17, 178–182.

Rudman, P., Gay, F.J., 1963. Causes of natural durability in timber. X. Deterrentproperties of some three-ringed carboxylic and heterocyclic substances to thesubterranean termite, Nasutitermes extiosus. C.S.I.R.O. Div. Forest Prod.,Melbourne. Holzforschung 17, 21–25.

Rust, M.K., Reierson, D.A., 1977. Using wood extracts to determine the feedingpreferences of the western drywood termite, incisitermes minor (hagen).Journal Chemical Ecolology 3, 391–399.

Rust, M.K., Saran, R.K., 2006. Toxicity, repellency, and transfer of chlorfenapyragainst western subterranean termites (Isoptera: Rhinotermitidae). Journal ofEconomic Entomology 99, 864–872.

Saeki, I., Sumimoto, M., Kondo, T., 1968. Antitermitic substance of Ternstroemiajaponica wood. III. Biological tests of the antitermitic substance. MokuzaiGakkaishi 14, 110–114.

Saeki, I., Sumimoto, M., Kondo, T., 1970. Termiticidal substances from the wood ofPodocarpus macrophyllus. Holzforschung 24, 83–86.

Saeki, I., Sumimoto, M., Kondo, T., 1973. Termiticidal substances from the wood ofChamaecyparis pisifera. Holzforschung 27, 93–96.

Sajap, A.S., Aloysius, F., 2000. Effects of leaf extracts of Azadirachta excelsa onCoptotermes curvignathus (Isoptera: Rhinotermidae). Sociobiology 36, 497–503.

Sajap, A.S. Amit, S., Welker, J., 1999. Evaluation of Hexaflumuron for Controlling theSubterranean Termite Coptotermes curvignathus (Isoptera: Rhinotermitidae) inMalaysia. pp. 429–433.

Sajap, A.S., Lardizabal, M.L.T., Ahmad, F.B., Sahri, M.H., 2006. Feeding response ofsubterranean termite, Coptotermes curvignathus (Isoptera: Rhinotermitidae) toAzadirachta excelsa (Meliaceae) extractives and its timber. Sociobiology 48,447–455.

Sakasegawa, M., Hori, K., Yatagai, M., 2003. Composition and antitermite activitiesof essential oils from Melaleuca species. Journal of Wood Science 49, 181–187.

Page 14: Biological alternatives for termite control: A review

M. Verma et al. / International Biodeterioration & Biodegradation 63 (2009) 959–972972

Saxby, M.J., 1996. Food Taints and Off-flavour, second ed. Blackie Academic &Professional, London/New York, pp 54.

Sa, R.A., Napoleao, T.H., Santos, N.D.L., Gomes, F.S., Albuquerque, A.C.,Xavier, H.S., Coelho, L.C.B.B., Bieber, L.W., Paiva, P.M.G., 2008. Induction ofmortality on Nasutitermes corniger (Isoptera, Termitidae) by Myracrodruonurundeuva heartwood lectin. International Biodeterioration & Biodegradation62, 460–464.

Scheffrahn, R.H., Hsu, R.-C., Su, N.-Y., Huffman, J.B., Midland, S.L., Sims, J.J., 1988.Allelochemical resistance of bald cypress, Taxodium distichum, heartwood to thesubterranean termite, Coptotermes formosanus. Journal of Chemical Ecology 14,765–776.

Scheffrahn, R.H., Su, N.Y., Busey, P., 1997. Laboratory and field evaluation of selectedchemical treatment and field evaluation of selected chemical treatment forcontrol of drywood termites (Isoptera: Kalotermitidae). Journal of EconomicEntomology 90, 492–502.

Scheffrahn, R.H., Rust, M.K., 1983. Drywood termite feeding deterrents in sugar pineand antitermitic activity of related compounds. Journal of Chemical Ecology 9,39–55.

Scheffrahn, R.H., Su, N.Y., 1987. Structure/activity relationships of 2-haloalkanoic acidsand their esters as antitermitic agents against formosan subterranean termites(Isoptera: Rhinotermitidae). Journal of Economic Entomology 80, 312–316.

Schloman, W.W., Hivley, R.A., Krishen, A., Andrews, M.A., 1983. Guayule byproductevaluation: extract characterization. Journal of Agriculture and Food Chemistry31, 973–976.

Sen-Sarma, P.K., 1963. Studies on the natural resistance of timbers to termites. I.Observations on the longevity of the test termite Heterotermes indicola Wasm.in the saw dust from forty common Indian timbers. Indian Forestry Bulletin(N.S.) Entomolology 220, 1–3.

Sen-Sarma, P.K., Chatterjee, P.N., 1968. Studies on the natural resistance of timbersto termite attack. V. Laboratory evaluation of the resistance of Indian wood toMicrocerotermes beesoni Snyder (Termitidae, Amitermitinae). Indian Forestry94, 694–704.

Serit, M., Ishida, M., Nakata, K., Kim, M., Takahashi, S., 1992. Antifeedency potencyof neem (Azadirachta indica) extractives and limonoids against termite (Retic-ulitermes speratus). Journal of Pesticide Science 17, 267–273.

Sharma, S., Vasudevan, P., Madan, M., 1990. Insecticidal value of castor (Ricinuscommunis) against termites. International Biodeterioration 27, 249–254.

Sharma, R.N., Tare, V., Pawan, P., 1999. Toxic action of some plant extracts againstselected insect pest and vectors. Pestology 23, 30–37.

Shibutani, S., Samejima, M., Doi, S., 2004. Effects of stilbenes from bark of Piceaglehnii (Sieb. Et Zucc) and their related compounds against feeding behaviour ofReticulitermes speratus (Kolbe). Journal of Wood Science 50, 439–444.

Shibutani, S., Yusuf, S., Doi, S., 2006. Anti-termite (Isoptera) component fromArtocarpus heterophyllus heartwood. Sociobiology 47, 711–720.

Shimanouchi, N., 1992. Distillation of the essential oil of Hinoki (Chamaecyparisobtusa Endl.). Gakujutsu Kiyo - Kochi Kogyo Koto Senmon Gakko 36, 121–126.

Silva, A.C., Monteiro, M.B.B., Brazolin, S., Lopez, G.A.C., Richter, A., Braga, M.R., 2007.Biodeterioration of brazilwood Caesalpinia echinata Lam. (LeguminosaedCae-salpinioideae) by rot fungi and termites. International Biodeterioration &Biodegradation 60, 285–292.

Singh, G., Singh, O.P., Lampasona, M.P., Cesar, A.N., 2002a. Studies on essential oils.Part 35: chemical and biocidal investigations on Tagetes erecta leaf volatile oil.Flavour and Fragrance 18, 62–65.

Singh, M., Lal, K., Singh, S.B., 2002b. Effect of calotropis (Calotropis procera) extracton infestation of termite (Odontotermes obesus) in sugarcane hybrid. IndianJournal of Agricultural Sciences 72, 439–441.

Smith, J.L., Rust, M.K., 1990. Tunneling response and mortality of the westernsubterranean termite (Isoptera: Rhinotermitidae) to soil treated with termiti-cides. Journal of Economic Entomology 83, 1395–1401.

Sogabe, A., Kinjo, K., Abe, F., Yamauchi, T., Yaga, S., 2000a. Termiticidal substancesfrom the wood and bark of Wikstroema retusa A. Gray. Mokuzai Gakkaishi 46,47–53.

Sogabe, A., Kinjo, K., Abe, F., Yamauchi, T., Yaga, S., 2000b. Termiticidal substancesfrom heartwood of Cryptomeria japonica D. Don. Journal of Japan WoodResearch Society 46, 124–131.

Solomon, S., Mills, M., Heidt, L.E., Pollock, W.H., Tuck, A.F., 1992. On the evaluation ofozone depletion potential. Journal of Geophysical Research 97, 825–842.

Stoll, G., 2002. Indigenous Agriculture News 4: 3.Stranes, R.L., Liu, L., Marrane, P.G., 1993. History, use and future of microbial

insecticides. American Entomologist 39, 83–91.Su, N.-Y., 2005. Response of the formosan subterranean termites (Isoptera: Rhino-

termitidae) to baits or nonrepellent termiticides in extended foraging arenas.Journal of Economic Entomology 98, 2143–2152.

Su, N.-Y., Scheffrahn, R.H., 1993. Laboratory evaluation of two chitin synthesisinhibitors, hexaflumuron and diflubenzuron, as bait toxicants against formosanand eastern subterranean termites (Isoptera: Rhinotermitidae). Journal ofEconomic Entomology 86, 1453–1457.

Su, N.-Y., Scheffrahn, R.H., 2000. Formosan Subterranean Termite. University ofFlorida. online at. http://creatures.ifas.ufl.edu/urban/termites/fst.10htm.

Suszkiw, J., 1998. The formosan termite: a formidable foe. Agricultural Research 46,4–9.

Taylor, A.M., Gartner, B.L., Morell, J.J., Tsunoda, K., 2006. Effect of heartwoodextractive fractions of Thuja plicata and Chamaecyparis nootkatensis on wooddegradation by termites or fungi. Journal of Wood Science 52, 147–153.

Tellez, M., Estell, R., Fredrickson, E., Powell, J., Wedge, D., Schrader, K., Kobaisy, M.,2001. Extracts of flourensia cernua (l): volatile constituents and antifungal,antialgal, and antitermite bioactivities. Journal of Chemical Ecology 27, 11.

Tellez, M.R., Khan, I.A., Kobaisy, M., Schrader, K.K., Dayan, F.E., Osbrink, W., 2002.Composition of the essential oil of Lepidium meyenii (Walp.). Phytochemistry 61,149–155.

Thambidurai, S., 2002. Indigenous Agriculture News 1: 9.Thompson, G., 2000. Termites. Tropical Topics News Letter No. 64, Tropical Savanna,

Australia.Trikojus, V.M., 1935. Some synthetic and natural antitermitic substances. Australian

Chemical Institute Journal Proceeding 2, 171–176.Trudeau, D., 1989. Selection of entomophilic nematodes for control of the

eastern subterranean termite, Reticulitermes flavipes (Kollar) (Isoptera:Rhinotermitidae). 93 pp. Master’s thesis, University of Toronto, Toronto,Ontario, Canada.

Umeh, V.C., Waliyar, F., Traore, S., Egwurube, E., 1999. Soil pests of groundnut inWest Africa-species diversity, damage and estimation of yield losses. Interna-tional Crops Research Institute for the Semi-Arid Tropics (ICRISAT), B.P. 320Bamako, Mali. Insect-Science-and-its-Application 19, 131–140.

Umeh, V.C., Ivbijaro, M.F., 1999. Effects of termite damage to maize of seed extractsof Azadirachta indica and Piper guineense in farmers fields. Journal of Agricul-tural Science 133, 403–407.

United Nations Environment Programme 1992. Montreal Protocol AssessmentSupplement, Methyl Bromide: Its Science, Technology, and Economics.Synthesis Report of the Methyl Bromide Interim Scientific Assessment andMethyl Bromide Interim Technology and Economic Assessment.

UNEP/FAO/Global IPM Facility Expert Group on Termite Biology and Management,2000. Finding alternatives to persistent organic pollutants (POPs) for termitemanagement, online at www.chem.unep.ch/pops/termites/termite_ch4.htm.

Verma, S.K., Verma, R.K., Saxena, K.D., 2005. Termiticidal triterpenoid from leaves ofLantana camara var. aculeate. Journal of the Institution of Chemists (India) 77,23–25.

Verma, R.K., Verma, S.K., 2006. Phytochemical and termiticidal study of Lantanacamara var. aculeata leaves. Fitotrapia 77, 466–468.

Watanabe, N., Saeki, I., Sumimoto, M., Kondo, T., Kurotori, S., 1966. Antitermiticsubstance of Ternstroemia japonica wood. Mokuzai Gakkaishi 12, 236–239.

Watanabe, Y., Mihara, R., Mitsunaga, T., Yoshimura, T., 2005. Termite repellentsesquiterpenoids from Callitris glaucophylla heartwood. Journal of WoodScience 51, 514–519.

Weeks, B., Baker, P., 2004. Subterranean Termite (Isoptera: Rhinotermitidae)Mortality Due to Entomopathogenic Nematodes (Nematoda: Steinernematidae,Heterorhabditidae). University of Arizona College of Agriculture. 2004 Turfgrassand Ornamental Research Report, online at. http://cals.arizona.edu/pubs/crops/az1359/.

Weissmann, G., Dietrichs, H.H., 1975. Termiticidal activity of the extractives fromCallitris and their structural relations. Holz als Roh- und Werkstoff 33, 54–56.

Woodrow, R.J., Grace, J.K., 1998. Field studies on the use of high temperatures tocontrol Cryptotermes brevis (Isoptera: kalotermitdae). Sociobiology 32, 27–49.

World Meteorological Organization, 1994. Scientific Assessment of OzoneDepletion: 1994. Global Ozone Research and Monitoring, Geneva. ProjectNo. 37.

Yaga, S., 1977. The termiticidal substances from the wood and bark of Adina race-mosa Miq. Mokuzai Gakkaishi 23, 594–600.

Yaga, S., 1980. On the termite-resistance of okinawan timbers. VI. Termiticidalsubstances from Melia azedarach L. Mokuzai Gakkaishi 26, 494–498.

Yaga, S., 1981. Termiticidal substance from the bark of Adina racemosa Miq. and itsderivatives. Mokuzai Gakkaishi 27, 592–596.

Yaga, S., Kinjo, K., 1986. Termiticidal substances from Sciadopitys verticillata S. et Z.Mokuzai Gakkaishi 32, 720–723.

Yatagai, M., Miyazaki, Y., Morita, S., 1991. Extractives from Yakusugi bogwood andtheir termiticidal activity and growth regulation effects on plant seeds. For.Prod. Res. Inst., Tsukuba, Japan. Mokuzai Gakkaishi 37, 345–351.

Yatagai, M., Nishimoto, M., Ohira, K.H.T., Shibata, A., 2002. Termiticidal activity ofwood vinegar, its components and their homologues. Journal of Wood Science48, 338–342.

Yazaki, Y., 1982. Termiticidal extracts from the wood of Ganophyllum falcatum B1.Holzforschung 36, 249–253.

Yoshida, S., Morita, Y., Narita, K., Okabe, T., 1998. Termiticidal efficacy of neutral oilobtained from Aomori hiba. Tennen Yuki Kagobutsu Toronkai Koen Yoshishu40, 311–315.

Zhong, J.H., Liug, L.L., 2002. Termite fauna in China and their economic importance.Sociobiology 40, 25–32.

Zhu, B.C.R., Henderson, G., Chen, F., Fei, H., Laine, R.A., 2001a. Evaluation of vetiveroil and seven insect-active essential oils against the formosan subterraneantermite. Journal of Chemical Ecology 27, 1617–1625.

Zhu, B.C.R., Henderson, G., Chen, F., Maistrello, L., Laine, R.A., 2001b. Nootkatone isa repellent for formosan subterranean termite (Coptotermes formosanus).Journal of Chemical Ecology 27, 523–531.