Rastrococcus invadens
(fruit tree mealybug)

Pictures

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Identity

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Preferred Scientific Name

• Rastrococcus invadens Williams

Preferred Common Name

• fruit tree mealybug

International Common Names

• English: mango mealybug
• French: cochenille farineuse du manguier

EPPO code

• RASTIN (Rastrococcus invadens)

Summary of Invasiveness

Top of page R. invadens spread very rapidly throughout West Africa after being originally reported from Benin/Ghana. A wide range of indigenous natural enemies were recorded from it, but had very little effect on its populations, which occurred on a wide range of host plants, whereas it is found on a very restricted range of hosts in its area of origin.

Taxonomic Tree

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• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Sternorrhyncha
•                             Unknown: Coccoidea
•                                 Family: Pseudococcidae
•                                     Genus: Rastrococcus
•                                         Species: Rastrococcus invadens

Notes on Taxonomy and Nomenclature

Top of page R. invadens is very close to R. spinosus, and the identities of the two species have been somewhat confused. The species recorded as R. spinosus by Mahmood et al. (1980) as causing damage to mango in Pakistan seems now to be R. invadens (Williams, 1986).

Description

Top of page Adult female pale greenish white, covered with white wax except for a bare area on midline. Length 3.5-4 mm, width 2-2.5 mm. Filaments conspicuous and long, anterior 3.5-6 mm long, posterior 5-8 mm long, lateral 1.5-2.5 mm long (Williams, 1986). Males have not been described in detail yet, but have a single pair of wings and no mouthparts.

On microscopic slides, the anal lobes with their set of setae, the nine segmented antennae, well-developed legs, various pores and cerarii are characteristic (for details see original description by Williams, 1986 and identification key in Williams, 1989).

Distribution

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R. invadens does not seem to cause primary feeding damage to its tree host plants. However, the accumulation of honeydew and, shortly thereafter, development of sooty mould affects the photosynthetic capacity of the plant. Heavily affected plant parts stop growing, and often no new leaves or flowers are produced. In severely affected areas of West Africa, mango production was stopped altogether (Williams, 1986; Agounké et al., 1988; Bokonon-Ganta and Neuenschwander, 1995) before biological control substantially lowered mealybug populations.

Distribution Table

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The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

Hosts/Species Affected

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In the original description by Williams (1986) about 12 plant hosts are mentioned. For Africa, Agounké et al. (1988) listed 45 species of host plants from 22 families attacked by, or harbouring populations of, R. invadens in West Africa, and Biassangama et al. (1991) listed 23 species from Central Africa. Since then, a total of over 100 host-plant species have been found in Africa, particularly where populations of this insect are abundant on the primary host, mango. Not all these hosts could sustain populations of R. invadens.

Host Plants and Other Plants Affected

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Growth Stages

Top of page Flowering stage, Fruiting stage, Vegetative growing stage

List of Symptoms/Signs

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Biology and Ecology

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Biology

R. invadens females produce first-instar larvae, which, under field conditions in tropical Africa, moult within 10-12 days into second instars. The second instar lasts 7-8.5 days, and slight differences can be observed between the sexes. Third-instar males form a cocoon and go through to a fourth instar over 8-11 days; third-instar females take 6.5-8.5 days before moulting to adults. Overall, males take ca 28-31 days from hatching to last moult. The short-lived adult males are capable of mating upon emergence. Females take 25-27 days from hatching to adult emergence. The prereproductive period of the females lasts for 17-18 days. Females survived up to 225 days and laid eggs up to about day 200. These and further life-table parameters are given by Boavida and Neuenschwander (1995a). For R. invadens kept in the laboratory or the glasshouse, longer development times and a shorter reproductive period were found (Willink and Moore, 1988). Up to almost 200 first instars were produced on average during the life time of one female.

Population dynamics

In West Africa, R. invadens has been shown to disperse very well, most likely by humans transporting seedlings from nurseries (Boussienguet and Herren, 1991; see map in Neuenschwander et al., 1994). Population densities were usually higher on young than on old leaves (Boavida and Neuenschwander, 1995a) and differed markedly between individual mango trees. On highly infested mango trees, the pre-reproductive period was shorter and the total offspring production higher than on less-infested trees (Boavida and Neuenschwander, 1995b), indicating the importance of plant genotype on mealybug size and survival. Similarly, large differences in mealybug population levels between different mango trees were reported by Narasimham and Chacko (1991).

Population peaks occurred irregularly, but mainly in the wet season (Agricola et al., 1989; Boavida and Neuenschwander, 1995a), though they often seemed to be more influenced by the plant host than by weather (Matokot et al., 1992). The proportion of male mealybugs showed large and unexplained fluctuations, independently of population density (Boavida and Neuenschwander, 1995a).

In three studies in Africa, namely in Togo, Congo and Benin, population dynamics were heavily influenced by classical biological control. Pest populations crashed within 1-2 years, and local extinction was sometimes observed.

Natural enemies

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Notes on Natural Enemies

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Predators of R. invadens are listed by Agounké et al. (1988), Matokot et al. (1992) and Boavida and Neuenschwander (1995a). Despite this richness in the indigenous fauna, control was eventually achieved only by introduction of Gyranusoidea tebygi, assisted in some foci, mainly towns in Benin, by Anagyrus mangicola. Both parasitoids were described by Noyes (1988, 1990) only after R. invadens had been recognised as a separate species. See Control for further information.

Though G. tebygi is attacked by several indigenous hyperparasitoids in Africa (Agricola and Fischer, 1991; Biassangama et al., 1991; Matokot et al., 1992; Moore and Cross, 1992; Boavida et al., 1995a, b), biological control of R. invadens does not seem to be severely affected. Similarly, levels of parasitism by G. tebygi were reduced in the laboratory by the pathogen Hirsutella cryptosclerotium (Fernández-García et al., 1990), but overall mortality of the mealybug was greater when both agents were acting together (Akalach et al., 1992).

Means of Movement and Dispersal

Top of page Natural dispersal

Young may be carried by wind and gravity. The chances of successful migration would be low, but with large numbers of progeny, at least some successful movement between plants must occur.

Vector transmission

None known, but phoresy probably occurs.

Agricultural practices

It is likely that human transport of seedlings from nurseries was a major cause of spread in West Africa (Neuenschwander et al., 1994). Anecdotal, and unreferenced, information has speculated that original outbreaks occurred at the time of mango improvement schemes after rearing material was supplied to West Africa from India.

Social movement

The tradition of carrying gifts of food, including fruits, must have contributed to local and longer distance migration.

Pathway Vectors

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Plant Trade

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Plant parts not known to carry the pest in trade/transport
Bark
Bulbs/Tubers/Corms/Rhizomes
Growing medium accompanying plants
Roots
True seeds (inc. grain)
Wood

Wood Packaging

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Impact Summary

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Impact

Top of page R. invadens does not seem to be of great economic importance in India. In fact, the species had not been recognized and was mistaken for R. spinosus, before it was accidentally introduced into Africa (Williams, 1986). Wherever this mealybug appeared in Africa it became a pest of prime importance on mango with yield losses estimated at 89% in Benin (Bokonon-Ganta et al., 2002), sometimes on citrus, and on many horticultural crops and shade trees (Agounké et al., 1988; Ivbijaro et al., 1992). Serious infestations resulted in almost complete loss of production whereas lighter attack led to significant reductions in ash content, crude fibre and sugar levels of ripe and unripe fruit (Tobih et al., 2002) and protein, fat and carbohydrate levels (Pitan et al., 2002).

In severely affected areas, mango production was reduced by 89-100% and citrus production was also greatly reduced (Vögele et al., 1991; Agounké et al., 1988; Bokonon-Ganta et al., 1995, 2002).

Environmental Impact

Top of page Large numbers of mealybugs would have been prey for indigenous predators and parasitoids and possibly some lizards and birds. Defoliation of large trees would have had some local impact in terms of increased UV irradiation and probably water erosion of soil immediately under these trees. These components were not studied in depth.

Impact: Biodiversity

Top of page No problems have been reported. In theory the mealybug could cause problems for uncommon mango varieties, but biological control removed that possibility.

Social Impact

Top of page Marked effects on social activity include disruption of village life, often conducted under significant mango trees, animist beliefs as spiritually important trees were attacked, superstitious fears as one generalist predator has a pupal stage which is regarded as bringing bad luck, and the loss of medicinally valuable resources from plants (Vögele et al., 1991). Livelihoods were affected as roadside sales of fruits were reduced, childhood malnutrition was thought to have increased from reduced provision of fruits with high vitamin A and C content and increased fly numbers were believed to have been promoted by excess honeydew, causing nuisance to villagers and tourists (Vögele et al., 1991). Anecdotal information refers to householders destroying trees as a control measure and hotel and religious gardens being spoiled by infestations.

Detection and Inspection

Top of page The species is easily detected and identified either by the conspicuous females sitting openly on the undersides of leaves, often near the mid-rib (Narasimham and Chacko, 1991) or by their characteristic exuviae.

Similarities to Other Species/Conditions

Top of page R. invadens is very close to R. spinosus, and the identities of the two species have been somewhat confused. Field diagnostic characters to differentiate between adults of three mealybug species, including R. invadens, are given by Narasimham (1990).

Prevention and Control

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Biological control by Gyranusoidea tebygi and Anagyrus mangicola has led to satisfactory control of the mango mealybug in Africa. No other interventions were needed, although it must be stressed that, particularly in urban environments, more than 1 year may be needed before low host equilibria are established.

The establishment and spread of G. tebygi in Togo (six releases, Agricola et al., 1989) in Congo (where it appeared without deliberate releases, Matokot et al., 1992), and of the two parasitoids in much of West Africa (a total of 42 releases of G. tebygi and 22 releases of A. mangicola, Neuenschwander, 1989; Neuenschwander et al., 1994) are well documented. The impact, mostly of G. tebygi, was demonstrated by population dynamics studies (Agricola et al., 1989 in Togo; Matokot et al., 1992 in Congo; Boavida and Neuenschwander, 1995a in Benin, Pitan et al., 2000 in Nigeria) and by a parasitoid exclusion experiment by means of sleeves (Boavida et al., 1995b). Similarly, quantitative survey results covering all infested zones in Benin indicated a reduction of R. invadens following the introduction of G. tebygi, a corresponding reduction in sooty mould cover, and an increase in the number of new leaves (Bokonon-Ganta and Neuenschwander, 1995). R. invadens populations invariably crashed during the year following the first introduction or observation of G. tebygi. As the mealybug population was reduced, the number of host plants attacked was also diminished (Boussienguet and Mouloungou, 1993). A first attempt at economic impact analysis was made by Vögele et al. (1991). Subsequently, Bokonon-Ganta et al. (2002) estimated the benefit-cost ratio of the biocontrol project as 145:1 for Benin alone.

In addition to these field studies, both parasitoids were also studied in detail in the laboratory in order to understand their interactions with the host and with each other (Willink and Moore, 1988; Moore and Cross, 1992, 1993; Cross and Moore, 1992; Bokonon-Ganta et al., 1995, 1996; Boavida et al., 1995a). Though there is some niche overlap, the two parasitoids can coexist on the same host population. Initial fears, derived from an early simulation model (Godfray and Waage, 1991), that the addition of A. mangicola to the system could be harmful, were thereby allayed by these studies.

 

References

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Agounke D, Agricola U, Bokonon-Ganta HA, 1988. Rastrococcus invadens Williams (Hemiptera, Pseudococcidae), a serious exotic pest of fruit trees and other plants in West Africa. Bulletin of Entomological Research, 78(4):695-702

Agricola U, 1991. Biologie der Obstbaumschmierlaus Rastrococcus invadens Williams (Homoptera: Pseudococcidae) und ihre biologische Bekampfung durch Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae) in Togo. PhD Thesis. Institut fur Phytopathologie und angewandte Zoologie, Gieáen, 124 pp

Agricola U, Agounke D, Fischer HU, Moore D, 1989. The control of Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) in Togo by the introduction of Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae). Bulletin of Entomological Research, 79(4):671-678

Agricola U, Fischer HU, 1991. Hyperparasitism in two newly introduced parasitoids, Epidinocarsis lopezi and Gyranusoidea tebygi (Hymenoptera: Encyrtidae) after their establishment in Togo. Bulletin of Entomological Research, 81(2):127-132

Akalach M, Fernandez-Garcia E, Moore D, 1992. Interaction between Rastrococcus invadens (Hom.: Pseudococcidae) and two natural enemies. Entomophaga, 37(1):99-106

Akintola AJ, Ande AT, 2009. Life history and behaviour of Rastrococcus invadens Williams on Ficus thonningii in Nigeria. Australian Journal of Crop Science, 3(1):1-5. http://www.cropj.com/Akintola_January2009_1_5.pdf

Biassangama A, Fabres G, Moussa JB, 1991. The presence in Congo of Gyranusoidea tebygi (Hymenoptera: Encyrtidae), parasitoid of Rastrococcus invadens (Hom.: Pseudococcidae). Bulletin de la Societe Entomologique de France, 96(2):209-211

Boavida C, Ahounou M, Vos M, Neuenschwander P, Alphen JJMvan, 1995. Host stage selection and sex allocation by Gyranusoidea tebygi (Hymenoptera: Encyrtidae), a parasitoid of the mango mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae). Biological Control, 5(4):487-496; 26 ref

Boavida C, Neuenschwander P, 1995. Influence of host plant on the mango mealybug, Rastrococcus invadens. Entomologia Experimentalis et Applicata, 76(2):179-188

Boavida C, Neuenschwander P, Herren HR, 1995. Experimental assessment of the impact of the introduced parasitoid Gyranusoidea tebygi Noyes on the mango mealybug Rastrococcus invadens Williams, by physical exclusion. Biological Control, 5(1):99-103; 24 ref

Boavida C, Neuenschwander P, Schulthess F, 1992. Spatial distribution of Rastrococcus invadens Williams (Hom., Pseudococcidae) in mango trees. Journal of Applied Entomology, 114(4):381-391

Bokonon-Ganta AH, Alphen JJMvan, Neuenschwander P, 1996. Competition between Gyranusoidea tebygi and Anagyrus mangicola, parasitoids of the mango mealybug, Rastrococcus invadens: interspecific host discrimination and larval competition. Entomologia Experimentalis et Applicata, 79(2):179-185; 46 ref

Bokonon-Ganta AH, Groote Hde, Neuenschwander P, 2002. Socio-economic impact of biological control of mango mealybug in Benin. Agriculture, Ecosystems & Environment, 93(1/3):367-378; 27 ref

Bokonon-Ganta AH, Neuenschwander P, 1995. Impact of the biological control agent Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae) on the mango mealybug, Rastrococcus invadens Williams (Homoptera: Pseudococcidae), in Benin. Biocontrol Science and Technology, 5(1):95-107

Bokonon-Ganta AH, Neuenschwander P, Alphen JJMvan, Vos M, 1995. Host stage selection and sex allocation by Anagyrus mangicola (Hymenoptera: Encyrtidae), a parasitoid of the mango mealybug, Rastrococcus invadens (Homoptera: Pseudococcidae). Biological Control, 5(4):479-486; 27 ref

Boussienguet J, Herren HR, 1991. Introduction et dynamique de dispersion de la cochenille du manguier, Rastrococcus invadens Williams (Homoptera: Pseudococcidae) au Gabon. Memoirs de la Societe royale belge en Entomologie, 35:363-367

Boussienguet J, Mouloungou J, 1993. Demographic pressure and food choice in Rastrococcus invadens, a pest of mango recently introduced to Africa (Homoptera, Pseudococcidae). Bulletin de la Societe Entomologique de France, 98(2):139-148

Cross AE, Moore D, 1992. Developmental studies on Anagyrus mangicola (Hymenoptera: Encyrtidae), a parasitoid of the mealybug Rastrococcus invadens (Homoptera: Pseudococcidae). Bulletin of Entomological Research, 82(3):307-312

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

Fernandez-Garcia E, Evans HC, Samson RA, 1990. Hirsutella cryptosclerotium sp. nov., an entomopathogen of the mealybug pest, Rastrococcus invadens, in West Africa. Mycological Research, 94(8):1111-1117

Germain JF, Laplace D, Devarieux A, Boavida C, 2015. First records of the mealybug Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) in French Guiana and the Americas. Zootaxa, 3905(3):447-450. http://www.mapress.com/zootaxa/2015/f/z03905p450f.pdf

Godfray HCJ, Waage JK, 1991. Predictive modelling in biological control: the mango mealy bug (Rastrococcus invadens) and its parasitoids. Journal of Applied Ecology, 28(2):434-453

Hala N, Kehe M, Allou K, 2004. Incidence of the mango mealy bug Rastrococcus invadens Williams, 1986 (Homoptera; Pseudococcidae) in the Ivory Coast. (Incidence de la cochenille farineuse du manguier Rastrococcus invadens Williams, 1986 (Homoptera; Pseudococcidae) en Côte D'ivoire.) Agronomie Africaine, 16(3):29-36. http://www.ajol.info/viewarticle.php?jid=7&id=46416&layout=abstract

Han SH, Ndiaye AB, Hemptinne JL, 2007. Host-plants and predators of Rastrococcus invadens Williams, 1986, newly introduced in Dakar area, Senegal (Hemiptera, Pseudococcidae). (Plantes-hôtes et prédateurs de la Cochenille farineuse du Manguier Rastrococcus invadens Williams, 1986, nouvellement introduite à Dakar, Sénégal (Hemiptera, Pseudococcidae).) Bulletin de la Société Entomologique de France, 112(1):121-125

IPPC, 2008. [English title not available]. (Cochenille du manguier (Rastrococcus invadens) en 1995.) IPPC Official Pest Report, No. SN-1/3. Rome, Italy: FAO. https://www.ippc.int/IPP/En/default

Ivbijaro MF, Udensis N, Ukwela UM, Anno-Nyako FV, 1992. Geographical distribution and host range in Nigeria of the mango mealy bug, Rastrococcus invadens Williams, a serious exotic pest of horticulture and other crops. Insect Science and its Application, 13(3):411-416

Lohr B, 1984. Bericht uber einen Kurzzeitaufenhalt in Togo zur Untersuchung einer Schmierlausgradation im Obstbau. Internal report of the 'Deutsche Gesellschaft fur Technische Zusammenarbeit (GTZ), Eschborn, Germany, 23

Mahmood R, Mohyuddin AI, Kazimi SK, 1980. Rastrococcus spinosus (Robinson) (Homoptera: Pseudococcidae) and its natural enemies in Pakistan. Proceedings of the 1st Pakistan Congress of Zoology, 30 April -- 1 May, 1980, Quaid-i-Azam University, Islamabad Zoological Society of Pakistan ?Islamabad Pakistan, 291-294

Matokot L, Reyd G, Malonga P, le Ru B, 1992. Dynamique des populations de Rastrococcus invadens Williams (Homptera: Pseudococcidae) au Congo; Influence de l'introduction accidentelle du parasitoide asiatique Gyranusoidea tebygi (Hymenoptera: Encyrtidae). Entomophaga, 37:123-140

Moore D, Cross AE, 1992. Competition between two primary parasitoids, Gyranusoidea tebygi Noyes and Anagyrus mangicola Noyes, attacking the mealybug Rastrococcus invadens Williams and the influence of a hyperparasitoid Chartocerus hyalipennis Hayat. Biocontrol Science and Technology, 2(3):225-234

Moore D, Cross AE, 1993. Biological control of the fruit tree mealybug, Rastrococcus invadens Williams; single or multiple introduction? Acta Horticulturae, 341:433-441

Moussa JB, Matile-Ferrero D, 1988. Sur la presence du nouveau ravageur, Rastrococcus invadens Williams en Republique Populaire du Congo (Hemiptera, Coccoidea, Pseudococcidae). Bulletin de la Societe Entomologique de France, 93:2

Narasimham AU, 1990. Field diagnostic characters of some Rastrococcus species (Homoptera: Coccoidea: Pseudococcidae) occurring in India. Oriental Insects, 24:259-265

Narasimham AU, Chacko MJ, 1988. Rastrococcus spp. (Hemiptera: Pseudococcidae) and their natural enemies in India as potential biocontrol agents for R. invadens Williams. Bulletin of Entomological Research, 78(4):703-708

Nébié, K., Nacro, S., Otoidobiga, L. C., Somda, I., 2018. Host plants of the mango mealybug Rastrococcus invadens Williams (Homoptera: Pseudococcidea) in western Burkina Faso. International Journal of Agriculture and Environmental Research, 4(4), 891-901. http://www.ijaer.in/2018files/ijaer_04__69.pdf

Neuenschwander P, 1989. Biocontrol of mango mealybug. IITA Research Briefs, 9:5-6

Neuenschwander P, Boavida C, Bokonon-Ganta A, Gado A, Herren HR, 1994. Establishment and spread of Gyranusoidea tebygi Noyes and Anagyrus mangicola Noyes (Hymenoptera: Encyrtidae), two biological control agents released against the mango mealybug Rastrococcus invadens Williams (Homoptera: Pseudococcidae) in Africa. Biocontrol Science and Technology, 4(1):61-69

Noyes JS, 1988. Gyranusoidea tebygi sp. n. (Hymenoptera: Encyrtidae), a parasitoid of Rastrococcus (Hemiptera: Pseudococcidae) on mango in India. Bulletin of Entomological Research, 78(2):313-316

Noyes JS, 1990. A new species of Anagyrus (Hymenoptera: Encyrtidae) from India attacking Rastrococcus invadens (Homoptera: Pseudococcidae), a pest of mango and citrus in West Africa. Bulletin of Entomological Research, 80(2):203-207

Pitan OOR, Akinlosotu TA, Odebiyi JA, 2000. Impact of Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae) on the mango mealybug Rastrococcus invadens Williams (Homoptera: Pseudococcidae) in Nigeria. Biocontrol Science and Technology, 10(3):245-254; 16 ref

Pitan OOR, Mwansat G, Akinyemi SOS, Adebayo OS, Akiniosotu TA, 2002. Effect of mango mealybug and sooty mould attack on mango and the impact of the released Gyranusoidea tebygi Noyes on yield. Fruits (Paris), 57(2):105-113

Tobih FO, Omoloye AA, Ivbijaro MF, Enobakhare DA, 2002. Effects of field infestation by Rastrococcus invadens Williams (Hemiptera: Pseudococcidae) on the morphology and nutritional status of mango fruits, Mangifera indica L. Crop Protection, 21(9):757-761; 25 ref

Vogele JM, Agounke D, Moore D, 1991. Biological control of the fruit tree mealybug Rastrococcus invadens Williams in Togo: a preliminary sociological and economic evaluation. Tropical Pest Management, 37(4):379-382

Williams DJ, 1986. Rastrococcus invadens sp. n. (Hemiptera: Pseudococcidae) introduced from the Oriental Region to West Africa and causing damage to mango, citrus and other trees. Bulletin of Entomological Research, 76(4):695-699

Willink E, Moore D, 1988. Aspects of the biology of Rastrococcus invadens Williams (Hemiptera: Pseudococcidae), a pest of fruit crops in West Africa, and one of its primary parasitoids, Gyranusoidea tebygi Noyes (Hymenoptera: Encyrtidae). Bulletin of Entomological Research, 78(4):709-715

Distribution Maps

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