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Insect Sci. Applic. Vol. 21, No. 4, pp. 361 - 368

THE CHEMICAL ECOLOGY OF HOST LOCATION BY PARASITOIDS OF AFRICAN STEMBORERS

LINNET S. GOHOLE^1,2 AND ADELE J. NGI-SONG²

¹Moi University, Department of Crop Production and Seed Technology, P.O. Box 1125, Eldoret, Kenya; ²International Centre of Insect Physiology and Ecology, P.O. Box 30772, Nairobi, Kenya

Accepted 21 November 2001

Code Number: ti01044

ABSTRACT

During foraging, parasitoids of insect herbivores are aided by chemical compounds generally termed 'infochemicals', to locate their hosts. The origin of the infochemicals varies; they may be derived from the herbivore itself or activities related to the biology of the herbivore, the host plant, or from interactions between the plant and the herbivore. This paper reviews the status of research in this area, and presents an account of the infochemicals used by African stemborer parasitoids during foraging, as well as recommending possible areas for further investigation. The information generated has potential for application in behaviour modification of parasitoids species in biological control programmes.

Key Words: infochemicals, volatiles, parasitoids, stemborers, foraging behaviour

RÉSUMÉ

Lors de la recherche de l'hôte les parasitoïdes des insectes herbivores s'orientent grâce à certains composés chimiques volatiles appelés 'infochemicals'. L'origine de ces composés chimiques est variable. Ils proviennent soit de l'hôte lui-même, soit des activités en relation avec la biologie de l'hôte, de la plante hôte, ou de l'interaction entre les deux. Cet article revise le statut des recherches dans ce domaine. Il présente une liste des composés chimiques utilisés par les parasitoïdes des foreurs africains lors de la recherche de l'hôte et suggère des thèmes de recherches futures. Les informations générées ici ont un potentiel d'application dans les programmes de lutte biologique dans le cadre de la modification des comportements des espèces de parasitoïdes.

Mots Clés: infochemicals, volatiles, foreurs, comportement

INTRODUCTION

Lepidopteran stemborers are among the major pests of cereals in Africa, causing yield losses of typically between 20 and 40 percent (Seshu Reddy and Walker, 1990). Several stemborer species attack cereal crops in Africa, but those of major economic importance are listed in Table 1. One control measure being advocated for the control of stemborers is biological control, and several parasitoids, predators and pathogens have been reported as being natural enemies of stemborers (Bonhof et al., 1997; Polaszek, 1998a). The common parasitoids of African stemborers are also listed in Table 1.

Table 1. Major African stemborers and parasitoids attacking them
Stemborer family	Stemborer species	Parasitoid species	Host stage attacked	Host plants

Noctuidae	Busseola	Telenomus busseolae Gahan ^{1, 2}	E	Maize,
	fusca	Telenomus isis Polaszek¹	E	sorghum, millet
	Fuller	Trichogrammatoidea lutea Girault²	E	sugarcane,
		Bracon sesamiae Cameron^{3, 4}	L	wild grasses
		Cotesia sesamiae (Cameron)^{2, 5}	L
		Sturmiopsis parasitica (Curran)^{3, 6}	L
		Pediobius furvus Gahan^{7, 8}	P
		Procerochasmias nigromaculatus (Cameron)^{9, 10}	P
		Tetrastichus atriclavus Waterston⁸	P
	Sesamia	Telenomus busseolae^{1, 11}	E	Maize,
	calamistis	Trichogramma sp.^{12, 22}	E	sorghum,
	Hampson	Cotesia sesamiae^{8, 13}	L	millet,
		Stenobracon rufus (Szépligeti)⁶	L	sugarcane,
		Procerochasmias nigromaculatus^{8, 10}	P	wild grasses
Crambidae	Chilo	Trichogramma sp. near mwanzai Schulten	E	Maize,
	partellus	and Feijen²²		sorghum,
	(Swinhoe)⁺	Telenomus sp.^{14, 15}	E	millet,
		Trichogrammatoidea sp.¹⁶	E	rice,
		Cotesia sesamiae^{5, 17}	L	sugarcane,
		Cotesia flavipes⁺ Cameron^5,18	L	wild grasses
		Sturmiopsis parasitica (Curran)¹⁹	L
		Stenobracon rufus^{6, 20}	L
		Dentichasmias busseolae Heinrich^{21, 22}	P
		Pediobius furvus^{4, 8}	P
		Psilochalchis soudanensis (Steffan)^{14, 17}	P
	Chilo	Trichogramma sp.^{12, 25}	E	Maize,
	orichal-	Cotesia sesamiae^{18, 25}	L	sorghum,
	cociliellus	Stenobracon rufus^{6, 26}	L	sugarcane,
	Strand	Sturmiopsis parasitica^{16, 27}	L	wild grasses
		Pediobius furvus^{16, 24}	P
		Dentichasmias busseolae^{7, 22}	P
		Psilochalchis soundanensis²²	P
	Coniesta	Goniozus indicus Ashmead²⁸	L	Millet
	ignefusalis	Syzeuctus senegalenesis Benoit³³	L
	(Hampson)
Pyralidae	Eldana	Telenomus applanatus Bin and Johnson^{29, 30}	E	Sugarcane,
	saccharina	Bracon sesamiae²⁶	L	maize,
	(Walker)	Cotesia seasmiae ^{8, 31}	L	sorghum,
		Goniozus indicus ³²	L	sedges
		Xanthopimpla stemmator⁺ (Thurnberg)³⁰	P
		Psilochalchis soudanensis⁸	P
	Maliarpha	Telenomus bini Polaszek and Kimani³⁴	E	Cultivated
	separatella	Goniozus indicus²⁸	L	and wild rice
	Ragonot	Chelonus maudae Huddleston²⁰	L
		Venturia jordanae Fitton^{10, 34}	L
		Pristomerus africator Aubert and Shaumar³⁴	L
⁺ Exotic species introduced into Africa
References: 1, Polaszek et al. 1993; 2, Kfir, 1995; 3, Chinwada and Overholt, 2001; 4, Kfir, 1997; 5, Walker, 1994; 6, Milner, 1967; 7, Seshu Reddy, 1989; 8, Mohyuddin and Greathead, 1970; 9, Kfir and Bell, 1993; 10, Zwart, 1998; 11, Bosque-Pérez and Schulthess, 1998; 12, Mathez, 1972; 13, Polaszek and Walker, 1991; 14, Oloo, 1989; 15, Polaszek and Kimani-Njogu, 1998; 16, Mohyuddin, 1990; 17, Kfir, 1990; 18, Overholt et al., 1997; 19, Harris, 1998; 20, Achterberg and Walker, 1998; 21, Mohyddin, 1972; 22, Skovgård and Päts, 1996; 23, Polaszek et al., 1998; 24, Minja, 1990; 25, Ogol et al., 1998; 26, Achterberg and Polaszek, 1996; 27, Greathead, 1990; 28, Polaszek, 1998b; 29, Polaszek and Kimani, 1990; 30, Conlong, 1997; 31, LePelly, 1959; 32, Conlong et al., 1988; 33, Harris, 1962; 34, Polaszek et al., 1994.

PARASITOID FORAGING BEHAVIOUR

Parasitoids search for, locate and successfully parasitise their hosts in a sequence of events that includes host habitat location, host location, host acceptance, and host suitability (Vinson, 1984; Smith et al., 1993). Studies have shown that (mainly volatile) chemical compounds, termed infochemicals, convey information on the likely presence of suitable hosts to parasitoids (Dicke and Sabelis, 1988; Dicke and Vet, 1999).

ROLE OF INFOCHEMICALS IN HOST AND HOST HABITAT LOCATION

Long-range attractants
Plants provide information in the form of volatile chemical cues, which aids parasitoids to locate their hosts at some distance. Many parasitoid species are attracted to volatiles emitted by undamaged host plants; in single-choice olfactometric tests, the stemborer parasitoids Cotesia flavipes Cameron and Co. sesamiae (Cameron) (Hymenoptera: Braconidae) were attracted to 8- to 10-week-old undamaged maize and sorghum plants (Ngi-Song et al., 1996).

However, volatiles from undamaged plants are poor indicators of herbivore presence (Vet et al., 1991; Dicke and Vet, 1999). More useful for parasitoid host location are those volatiles produced by plants in defence to herbivore attack (Turlings et al., 1995), volatiles that are commonly termed herbivore-induced synomones (HIS). Ngi-Song et al. (1996) and Rutledge and Wiedenmann (1999) reported preference for odours from stemborer-infested gramineous plants over odours from uninfested plants by females of both Co. flavipes and Co. sesamiae, suggesting that the damaged plants provided important cues to the searching parasitoids. The volatiles are emitted not only by the damaged tissue but are systemically produced by the whole plant, including undamaged parts (Potting et al., 1995). Among the chemicals produced by herbivore-infested maize plants that are involved in recruiting the larval parasitoid Co. flavipes, are heptanal, (Z)-3-hexenyl acetate, (E)-b -ocimene, linalool and (E)- 4,8-dimethyl-1,3,7-nonatriene, anisole and (E)-b -farnesene (Ngi-Song and Overholt, 1995; Ngi-Song et al., 2000).

Parasitoids are commonly found to learn olfactory cues that are associated with successful host location. Potting et al. (1997) investigated this aspect, but reported that Co. flavipes did not use odour learning in host microhabitat location. There is scope for investigation of this phenomenon with other parasitoids, particularly the solitary parasitoids such as Dentichasmias busseolae and Xanthopimpla stemmator, which have a longer lifespan.

Some plants when damaged produce volatiles that provide information to the foraging parasitoid on the herbivore species attacking the plant (Takabayashi et al., 1991). However, studies by Potting et al. (1993) and Ngi-Song et al. (1996) revealed that Co. flavipes and Co. sesamiae were not able to discriminate between host plants infested by Ch. partellus, Ch. orichalcociliellus, B. fusca and S. calamistis. This would be disadvantageous especially for Co. flavipes whose development is hindered in B. fusca (Ngi-Song et al., 1995). However, the parasitoids were more attracted to plants that had a larger number of stemborers infesting them, probably due to production of larger quantities of volatiles emitted as a result of the injuries (Ngi-Song et al., 1996).

Production of volatiles by non-feeding stages of the herbivore such as the eggs and pupae is negligible or absent (Noldus, 1989), and parasitoids that attack these stages resort to information produced by other stages of the herbivore (information detour) (Vet and Dicke, 1992). In addition, some of them also use host plant volatiles (Romeis et al., 1997). Trichogramma spp. (Trichogrammatidae) have been reported to parasitise the eggs of Ch. partellus, E. saccharina and B. fusca (Skovgård and Päts, 1996; Bonhof et al., 1997); they likely make use of sex pheromones produced by the adult stemborer moths and host plant volatiles to locate the host eggs. Information in area of host location by African stemborer egg parasitoids is still lacking.

Short-range attractants
Having successfully located a suitable habitat, the parasitoids must then find their hosts. Cues from host by-products such as frass, faeces or silk, are generally the most reliable source of information on the presence, identity, availability and suitability of the host to the foraging parasitoid. Although these cues are highly reliable, they are limited by their low detectability (Vet and Dicke, 1992) because they are generally produced in small amounts, and are not very volatile; they tend mainly to act as contact kairomones.

At close proximity, egg parasitoids readily locate their hosts by use of host kairomones such as scales from the host adults' wings or egg-adhesive material (reviewed by Suverkropp, 1997). Once Co. flavipes has found the habitat of its host, it locates the host by using the larval frass, caterpillar regurgitant and holes in the plant's stem (Potting et al., 1997; Ngi-Song and Overholt, 1997). However, when offered frass produced by Ch. partellus, Ch. orichalcociliellus, B. fusca and S. calamistis in a T-tube olfactometer, neither Co. flavipes nor Co. sesamiae was able to discriminate the different stemborers, indicating that these volatiles cannot provide the foraging parasitoid with information on the herbivore species (Ngi-Song and Overholt, 1997).

Xanthopimpla stemmator, a pupal parasitoid of stemborers, is guided to the microhabitat of its host by larval frass (Hailemichael et al., 1994). Mohyuddin (1972) reported the same for D. busseolae, a pupal parasitoid of Ch. partellus. The frass plays an important role because Ch. partellus pupae stay in the plant at the area of damage, unlike cases where the late instars move to different locations for pupation. The odour associated with the host pupa is also attractive to the parasitoid. Apart from chemical cues, sound and vibrations also aid in the location of concealed pupal hosts (Wäckers et al., 1998).

SHORTFALLS AND FUTURE PROSPECTS

Information on the volatile stimuli involved in the host-searching behaviour by parasitoids of African stemborers is limited. The few studies so far done in this area are summarised in Table 2. Information on the long-range volatiles that aid pupal parasitoids to locate the habitat of their hosts is also still lacking. There is a need to generate such information, as there is a current interest in using this type of parasitoids for the biological control of cereal stemborers. Such information could allow the manipulation of the environment to influence the foraging behaviour of the parasitoids. Little is known about the chemical composition of host frass, which is also very attractive to the parasitoids.

Table 2. Cases of infochemical use by African stemborer parasitoids to locate their hosts
Parasitoid species	Host	Host plant	Infochemical type	Reference
Egg parasitoids
Trichogramma sp.	Bf, Cp, Co	Sorghum, maize	Host sex pheromone	No known examples
			(kairomone)
			Moth scales	Ochiel, 1989
			(kairomone)
Larval parasitoids
Cotesia flavipes	Cp, Co,	Maize,	Herbivore-induced	Ngi-Song et al., 1996; Ngi-Song and Overholt, 1997;
	Sc, Es	sorghum,	synomones,	Potting et al., 1993, 1995;
		Napier grass	frass kairomones	Rutledge and Wiedenmann, 1999
Cotesia sesamiae	Cp, Bf, Sc	Maize,	Herbivore-induced	Ngi-Song et al., 1996; Ngi-Song and
		sorghum,	synomones,	Overholt, 1997; Rutledge and
		Napier grass	frass kairomones	Wiedenmann, 1999
Sturmiopsis	Cp, Bf	Maize, sorghum	Larval frass	Smith et al., 1993
parasitica			(kairomones)
Pupal parasitoids
Dentichasmias	Cp	Maize, sorghum	Larval frass	Mohyuddin, 1972
busseolae			(kairomones)
Xanthopimpla	Cp, Es	Maize, sorghum	Larval frass, host	Hailemichael et al., 1994
stemmato	r		odours (kairomones)
Bf , Busseola fusca; Co, Chilo orichalcociliellus; Cp, Chilo partellus; Es, Eldana saccharina; Sc, Sesamia calamistis.

One way to achieve improved parasitisation rates on stemborers is through habitat management. Diversification of cropping systems is a strategy that is being investigated for its potential to enhance the activity of biological control agents. Companion crops have been reported to produce attractants, which eventually led to higher parasitism rates in the main crop. For instance Khan et al. (1997a), reported increased parasitism of stemborers by the parasitoid Co. sesamiae in a maize - molasses grass intercrop. They attributed this phenomenon to volatiles produced by the molasses grass (non-host plant), which attracted the parasitoids, particularly the compound (E)-4,8-dimethyl- 1,3,7-nonatriene, which is a known chemical cue for stimulating parasitism. Volatiles from the molasses grass were also found to repel stemborer moths, leading to fewer eggs being oviposited in the intercrop as compared to the maize monocrop (Khan et al., 1997b). In addition to this a trap crop Sudan grass or Napier grass planted around the intercrop arrested the repelled stemborers. However, caution must be exercised in habitat management because in some instances, volatiles from companion crops have been shown to mask attractive volatiles or disrupt the whole foraging process (Costello and Altieri, 1995; L. Gohole, unpubl. data).

Research efforts should also go towards elucidating the chemical composition of crops developed for resistance to insect pests. The knowledge on the interaction between such plants and biological control agents is important for guiding efforts at integrating the two pest control strategies. So far, little has been done in this area.

Allelochemicals can also be artificially introduced into the cropping system. Altieri et al. (1981) showed that when extracts from Amaranthus sp. were sprayed on a range of cropping systems, parasitisation of Heliothis zea Boddie (Lepidoptera: Noctuidae) eggs by Trichogramma sp. became higher. However, to be effective, these attractants must lead the parasitoids to their proper hosts. In this regard, it might be prudent to concentrate on volatiles that are released naturally by plants under herbivore attack. Research should be directed towards developing plants that have high emission rates of the herbivore-induced synomones even at low herbivore infestation levels. This attribute can be enhanced through plant breeding or through genetic engineering for the traits of interest (Cortesero et al., 2000).

Elsewhere researchers have demonstrated the role played by herbivore-induced synomones (HIS) in repelling conspecific female moths (Kessler and Baldwin, 2001; De Moraes et al., 2001), thus deterring female oviposition on previously damaged plants. These studies provide new insights into the role of chemical cues in mediating tritrophic interactions, which can also be investigated in the African stemborer control context. The repelling volatiles can also be isolated and introduced into the agroecosystem to repel ovipositing moths.

Currently, some of the volatiles known to recruit parasitoids are being evaluated for potential application in monitoring the establishment and dispersal of the introduced parasitoid Co. flavipes (E. Ngumbi, unpubl. data). Field trials on the use of these compounds to enhance stemborer parasitisation rates are needed. Kimani and Overholt (1995) demonstrated that Co. flavipes responded to pheromones from conspecific individuals of the opposite sex. It might be possible to isolate the pheromones and use them to attract, especially parasitoid females, into a cereal crop field so as to enhance parasitisation of stemborers.

We conclude that there remains a wide scope for research into the foraging behaviour of African stemborer parasitoids. Studies into this area will provide tools to better focus and achieve the control of pest cereal stemborers.

REFERENCES

Achterberg C. van and Polaszek A. (1996) The parasites of cereal stemborers (Lepidotera: Cossidae, Crambidae, Noctuidae, Pyralidae) in Africa, belonging to the family Braconidae (Hymenoptera: Ichneumonoidea). Zoologische verhandelingen 304, 1 - 123.
Achterberg C. van and Walker A.K. (1998) Braconidae, pp. 137 - 185. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Altieri M. A., Lewis J. W., Nordlund D. A., Gueldner R. C. and Todd J. A. (1981) Chemical interactions between plants and Trichogramma wasps in Georgia soybean fields. Protection Ecol. 3, 259 - 263.
Bonhof M. J., Overholt W. A., van Huis A. and Polaszek A. (1997) Natural enemies of cereal stemborers in East Africa: A review. Insect Sci. Applic. 17, 19 - 35.
Bosque-Pérez N.A. and Schulthess F. (1998) Maize: West and Central Africa, pp. 11 - 24. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Chinwada P. and Overholt W. A. (2001) Natural enemies of maize stemborers on the highveld of Zimbabwe. African Entomol. 9, 67 - 75.
Conlong D. E. (1997) Biological control of Eldana saccharina Walker in South African sugarcane: Constraints identified from 15 years of research. Insect Sci. Applic. 17, 69 - 78.
Conlong D. E., Graham D. Y. and Hastings H. (1988) Notes on the natural host surveys and laboratory rearing of Goniozus natalensis Gordh (Hymenoptera: Bethylidae), a parasitoid of Eldana saccharina Walker (Lepidoptera: Pyralidae). Proc. S. Afr. Sugar Technol. Assoc. 58, 168 - 172.
Cortesero A. M., Stapel J. O. and Lewis W. J. (2000) Understanding and manipulating plant attributes to enhance biological control. Biol. Control 17, 35 - 49.
Costello M. J. and Altieri M. A. (1995) Abundance, growth rate and parasitism of Brevicoryne brassicae and Myzus persicae (Homoptera: Aphididae) on broccoli grown in living mulches. Agric. Ecosyst. Environ. 52, 187 - 196.
Dicke M. and Sabelis M. W. (1988) Infochemical terminology: should it be based on cost-benefit analysis rather than origin of compounds. Func. Ecol. 2, 131 - 139.
Dicke M. and Vet L. E. M. (1999) Plant-carnivore interactions: evolutionary and ecological consequences for plant, herbivore and carnivore, pp. 483 - 520. In Herbivores Between Plants and Predators (Edited by H. Olff, V. K. Brown and R. H. Drent). Blackwell Science, Oxford.
De Moraes C. M., Mescher M. C. and Tumlinson J. H. (2001) Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410, 577 - 580.
Greathead D. J. (1990) Utilization of natural enemies of Chilo spp. for management in Africa. Insect Sci. Applic. 11, 749 - 755.
Harris K. M. (1962) Lepidopterous stemborers of cereals in Nigeria. Bull. Entomol. Res. 53, 139 - 171.
Harris K. M. (1998) Diptera, pp. 265 - 281. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Hailemichael Y., Smith Jr. J. W. and Wiedenmann R. N. (1994) Host- finding behaviour, host acceptance and host suitability of the parasite Xanthopimpla stemmator. Entomol Exp. Appl. 71, 155 - 166.
Kessler A. and Baldwin I. (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291, 2141 - 2144.
Kfir R. (1990) Parasites of the spotted stalk borer Chilo partellus (Lepidoptera: Pyralidae) in South Africa Entomophaga 35, 403 - 410.
Kfir R. (1992) Seasonal abundance of stemborer Chilo partellus (Lepidoptera: Pyralidae) and its parasites on summer grain crops. J. Econ. Entomol. 85, 518 - 529.
Kfir R. (1995) Parasitoids of the African stemborer Busseola fusca (Fuller) (Lepidoptera: Noctuidae) in South Africa. Bull. Entomol. Res. 85, 369 - 377.
Kfir R. (1997) Natural control of the cereal stemborers Busseola fusca and Chilo partellus in South Africa. Insect Sci. Applic. 17, 61 - 67.
Kfir R. and Bell R. (1993) Intraseasonal changes in populations of the African maize stemborer Busseola fusca (Fuller) (Lepidoptera: Noctuidae) in Natal, South Africa. Rev. Zool. Afr. 107, 543 - 553.
Khan Z. R., Ampong- Nyarko K., Chiliswa P., Hassanali A., Kimani S., Lwande W. Overholt W. A., Pickett J. A., Smart L. E., Wadhams L. J. and Woodcock C. (1997a) Intercropping increases parasitism. Nature 388, 631 - 632.
Khan Z. R., Chiliswa P., Ampong-Nyarko K., Smart L. E., Polaszek A., Wandera J. and Mulaa M. A. (1997b) Utilisation of wild gramineous plants for the management of cereal stemborers in Africa. Insect Sci. Applic. 17, 143 - 150.
Kimani S. W. and Overholt W. A. (1995) Biosystematics of the Cotesia flavipes Cameron complex (Hymenoptera: Braconidae): Interspecific hybridisation, sex pheromone and mating behaviour studies. Bull. Entomol. Res. 85, 379 - 386.
LePelley H. (1959) Agricultural Insects of East Africa. East African High Commission. 307 pp.
Mathez F. C. (1972) Chilo partellus Swinh., C. orichalcociliellus Strand (Lep.: Crambidae) and Sesamia calamistis Hmps (Lep.: Noctuidae) on maize in the Coast Province, Kenya. Mitt. Schweiz. Gesellschaft 45, 267 - 289.
Milner J. E. D. (1967) Final report on survey of the parasites of graminaceous stemborers in East Africa. Commonwealth Institute of Biological Control (unpublished).
Minja E. M. (1990) Management of Chilo spp. infesting cereals in Eastern Africa. Insect Sci. Applic. 11, 489 - 499.
Mohyuddin A. I. (1972) Distribution, biology and ecology of Dentichasmias busseolae Heinr. (Hym., Ichneumonidae), a pupal parasite of graminaceous stemborers (Lep., Pyralidae). Bull. Entomol. Res. 62, 161 - 168.
Mohyuddin A. I (1990) Biological control of Chilo spp. in maize, sorghum and millet. Insect Sci. Applic. 11, 721 - 732.
Mohyuddin A. I. and Greathead D. J. (1970) An annotated list of the parasites of graminaceous stemborers in East Africa with a discussion of their potential in biological control. Entomophaga 15, 241 - 247.
Ngi-Song A. J. and Overholt W. A. (1995) Host selection by Cotesia flavipes and Cotesia sesamiae (Hymenoptera: Braconidae): an example of tritrophic relationship in a grass-stemborer parasitoid system, pp. 172 - 181. In Intergrating Biological Control and Host Plant Resistance. Proceedings of a CTA/IAR/IIBC Seminar 9 - 14 October 1995, Addis Ababa, Ethiopia.
Ngi-Song A. J., Overholt W. A. and Ayertey J. N. (1995) Suitability of African gramineous stemborers for development of Cotesia flavipes and C. sesamiae (Hymenoptera: Braconidae). Environ. Entomol. 24, 972 - 984.
Ngi-Song A. J., Overholt W. A., Njagi P. G. N., Dicke M., Ayertey J. N. and Lwande W. (1996) Volatile infochemicals used in host and host habitat location by Cotesia flavipes Cameron and Cotesia sesamiae Cameron (Hymenoptera: Braconidae), larval parasitoids of stemborers on graminae. J. Chem. Ecol. 22, 307 - 323.
Ngi-Song A. J. and Overholt W. A. (1997) Host location and acceptance by Cotesia flavipes and C. sesamiae (Cameron) (Hymenoptera: Braconidae), parasitoids of African gramineous stemborers: Role of frass and other host cues. Biol. Control 9, 136 - 142.
Ngi-Song A. J., Njagi P. G. N., Torto B. and Overholt W. A. (2000) Identification of behaviourally active components from maize volatiles for the stemborer parasitoid Cotesia flavipes Cameron (Hymenoptera: Braconidae). Insect Sci. Applic. 20, 181 - 189.
Noldus L. P. J. J. (1989) Chemical espionage by parasitic wasps. How Trichogramma species exploit moth sex pheromone systems. PhD thesis, Wageningen Agricultural University.
Ochiel S. (1989) Biology of Trichogramma species near exigum Pinto and Platner (Hymenoptera: Trichogrammatidae) on some lepidopterous hosts in South Nyanza. M.Phil. thesis. Rivers State University of Science and Technology, Port Harcourt, Nigeria.
Ogol C. K. P. O., Spence J. R. and Keddie A. (1998) Natural enemy abundance and activity in a maize-Leucaena agroforestry system in Kenya. Environ. Entomol. 27, 1444 - 1457.
Oloo G. W. (1989) The role of local natural enemies in population dynamics of Chilo partellus (Swinh) (Pyralidae) under subsistence farming systems in Kenya. Insect Sci. Applic. 10, 243 - 251.
Overholt W. A., Ngi-Song A. J., Omwega C. O., Kimani-Njogu S. W., Mbapila J., Sallam M. N. and Ofomata V. (1997) A review of the introduction and establishment of Cotesia flavipes Cameron in East Africa for biological control of cereal stemborers. Insect Sci. Applic. 17, 79 - 88.
Polaszek A. and Kimani S. W. (1990) Telenomus species (Hymenoptera: Scelionidae) attacking eggs of pyralid pests (Lepidoptera) in Africa: A review and guide to identification. Bull. Entomol. Res. 80, 57 - 71.
Polaszek A. and Walker A. K. (1991) The Cotesia flavipes species complex: Parasitoids of cereal stemborers in the tropics. Redia 74, 335 - 341.Polaszek A., Ubeku J. A. and Bosque-Pérez N. A. (1993) Taxonomy of Telenomus busseolae species complex (Hymenoptera: Scelionidae) egg parasitoid of cereal stemborers (Lepidoptera: Noctuidae, Pyralidae). Bull. Entomol. Res. 83, 221 - 226.
Polaszek A., Fitton M. G., Bianchi G. and Huddleston T. (1994) The parasites of the African white rice borer, Maliarpha separatella Ragonot (Lepidoptera: Pyralidae). Bull. Entomol. Res. 84, 65 - 90.
Polaszek A. (Ed.) (1998a) African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control. CAB International, Wallingford, 530 pp.
Polaszek A. (1998b) Bethylidae, pp. 133 - 135. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Polaszek A. and Kimani-Njogu S. W. (1998) Scelionidae, pp. 259 - 264. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Polaszek A., LaSalle J. and Jongema Y. (1998) Chalcidoidea, pp. 191 - 203. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.
Potting R. P. J., Osae-Danso F., Overholt W. A. and Ngi-Song A. J. (1993) Host selection in Cotesia flavipes, parasitoid of tropical stemborers. Proc. Exp. Appl. Entomol., N.E.V. Amsterdam. 4, 47 - 52.
Potting R. P. J., Overholt W. A., Osae-Danso F. O. and Takasu K. (1997) Foraging behaviour and life history of the stemborer parasitoid Cotesia flavipes. J. Insect Behav. 10, 13 - 29.
Potting R. P. J., Vet L. E. M. and Dicke M. (1995) Host microhabitat location by stemborer parasitoid Cotesia flavipes: The role of herbivore volatiles and locally systemically induced plant volatiles. J. Chem. Ecol. 21, 525 - 539.
Romeis J., Thomas S. G. and Zebitz C. P. W (1997) Volatile plant infochemicals mediate plant preference of Trichogramma chilonis. J. Chem. Ecol. 23, 2455 - 2465.
Rutledge C. E. and Wiedenmann R. N. (1999) Habitat preferences of three congeneric braconid parasitoids: Implications for host-range testing in biological control. Biol. Control 16, 144 - 154.
Seshu Reddy K. V. (1989) Sorghum stem borers in Eastern Africa, pp. 33 - 40. In International Workshop on Sorghum Stemborers. 17 - 20 Nov. 1987. ICRISAT, Patancheru, India.
Seshu Reddy K. V. and Walker P. T. (1990) A review of the yield losses in graminaceous crop caused by Chilo spp. Insect Sci. Applic. 11, 563 - 569.
Skovgård H. and Päts P. (1996) Effects of intercropping on maize stemborers and their natural enemies. Bull. Entomol. Res. 86, 599 - 607.
Smith J. W., Wiedenmann R. N. and Overholt W. A. (1993) Parasites of Lepidopteran Stemborers of Tropical Gramineous Plants. ICIPE Science Press, Nairobi. 81 pp.
Suverkropp B. S. (1997) Host-finding behaviour of Trichogramma brassicae in maize. PhD Thesis, Wageningen Agricultural University.
Takabayashi J., Noda T. and Takahashi S. (1991) Plants produce attractants for Apanteles kariyai, a parasitoid of Pseudaletia separata: cases of 'communication' and 'misunderstanding' in parasitoid-plant interactions. Appl. Entomol. Zool. 26, 237 - 243.
Turlings T. C. J., Loughrin J. H., McCall P. J., Röse U. S. R., Lewis W. J. and Tumlinson J. H. (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl. Acad. Sci. USA. 92, 4169 - 4174.
Vinson S. B (1984) How parasitoids locate their hosts: a case of espionage, pp. 325 - 348. In Insect Communication (Edited by T. Lewis). Academic Press, London. 414 pp.
Vet L. E. M., Wäckers F. L. and Dicke M. (1991) How to hunt for hiding hosts: The reliability-detectability problem in foraging parasitoids. Neth. J. Zool. 41, 202 - 213.
Vet L. E. M. and Dicke M. (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37, 141 - 172.
Wäckers F. L., Mitter E. and Dorn S. (1998) Vibrational sounding by the pupal Pimpla (Coccygomimus) turionellae: An additional solution to the reliability- detectability problem. Biol. Control 11, 141 - 146.
Walker A. K. (1994) Species of Microgastrinae (Hymenoptera: Braconidae) parasitizing lepidopterous cereal stemborers in Africa. Bull. Entomol. Res. 84, 421 - 434.
Zwart K. W. R. (1998) Ichneumonidae, pp. 205 - 264. In African Cereal Stemborers: Economic Importance, Taxonomy, Natural Enemies and Control (Edited by A. Polaszek). CAB International, Wallingford.