Aleurotrachelus atratus (palm-infesting whitefly)

Identity

Preferred Scientific Name

• Aleurotrachelus atratus

Preferred Common Name

• palm-infesting whitefly

Local Common Names

• Comoros: coconut whitefly
• Seychelles: coconut whitefly

Summary of Invasiveness

The whitefly A. atratus is a highly invasive pest of coconut and ornamental palms (Arecaceae). Before the 1990s this species was only known to feed on coconut from Brazil (Hempel, 1922; Mound and Halsey, 1978), but since 2001 it has been reported widely in the tropics and subtropics on more than a hundred plant species and is known to be invasive in Cape Verde, Comoros, Mauritius, Mozambique and the Seychelles. Mainly thelytokous, it is oligophagous on perennial palms, and has winged adults, all of which allows it to naturalize in new areas after accidental introduction on host plant material. It has also been found on indoor plantings of palms in botanical collections in temperate regions (Malumphy and Tresedar, 2011). The biology, host range and increasing geographical distribution of A. atratus have been studied in detail by Borowiec et al. (2010), and reviewed by Malumphy and Tresedar (2011).

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Sternorrhyncha
•                             Superfamily: Aleyrodoidea
•                                 Family: Aleyrodidae
•                                     Genus: Aleurotrachelus
•                                         Species: Aleurotrachelus atratus

Notes on Taxonomy and Nomenclature

A. atratus is a Neotropical whitefly, originally described by Hempel (1922) from specimens collected from coconut (Cocos nucifera) in Brazil. This species is assigned to the genus Aleurotrachelus in the subfamily Aleurodinae. Aleurotrachelus is one of the largest genera of whiteflies and currently contains 74 species (Martin and Mound, 2007). This genus may need taxonomic revision because it contains species that are probably unrelated morphologically. This genus was sometimes used to place several species of doubtful identity (Martin, 2005).

Description

A. atratus puparia are elliptical, black, 1.0-1.1 mm long with a long marginal white wax fringe and dorsal wax filaments that often completely cover the insect. The puparia often occur in dense colonies that smother the underside of the fronds with puparia, wax secretions and honeydew, on which sooty moulds grow.

The body of A. atratus is dark yellow. All four larval stages of A. atratus are black. The first instars have four pairs of wax plumes excreted by glands at the base of dorsal setae. Each dorsal seta has curving longitudinal grooves that guide the wax flakes as they are secreted from the seta base. When the wax has been removed, each puparium can be seen to have a distinct diagnostic pair of submarginal longitudinal cephalothoracic folds that extend into the abdomen (Malumphy and Tresedar, 2011).

There are no comprehensive diagnostic keys available to Aleurotrachelus, which is one of the largest genera of whiteflies, containing 74 species (Martin and Mound, 2007), several of which are quite unrelated morphologically. Whitefly taxonomy is based on the morphology of the fourth-larval instar, commonly known as the pupa or puparium. A. atratus pupae require slide mounting and examination by a specialist for reliable determination. Photographs of diagnostic morphological characters of a slide-mounted pupa of A. atratus are provided by Streito et al. (2004) and Walker (2008).

The type specimens were collected on coconut in Brazil (Hempel, 1922).

Distribution

A. atratus is native to Brazil, but since the late 1990s it has spread rapidly, probably due to anthropogenic activities such as trade in ornamental palms. It is now found in Africa, North and South America, Central America and the Caribbean, Europe and Oceania.

Distribution Table

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.

History of Introduction and Spread

Before 2001, A. atratus was only reported from Brazil, where it was considered common on coconut palm (Lepesme 1947; Mound and Halsey, 1978). Howard et al. (2001) reported A. atratus as being widely distributed in the Neotropical region (Antigua, Bahamas, Barbados, Bermuda, Brazil, Colombia, Guyana, Nevis, Puerto Rico, Venezuela and Florida, USA), but did not provide the dates that the species was first detected in each country, so it is unclear for how long A. atratus has been expanding its geographical range. As it was already widely distributed by 2001, it is likely to have been spreading for decades before then and was either overlooked or confused with other whitefly species commonly found on palms, most notably Aleurodicus species. A. atratus has since been recorded in many other countries within the Neotropical region (Evans, 2008; Delvare et al., 2008) and has spread into other geographical regions.

Introductions

Risk of Introduction

A. atratus is a highly invasive pest of palms that has spread widely in tropical and subtropical regions. It has also been found on indoor plantings in botanical collections in temperate regions. Mainly thelytokous, since only a few males have been found to date (Borowiec et al., 2010), it is oligophagous on perennial palms, and has winged adults, all of which allows it to naturalize in new areas after accidental introduction on host plant material (Malumphy and Tresedar, 2011). Although adult A. atratus are winged, they are small and fragile, and relatively poor fliers. Long distance (international) dispersal is most likely to have resulted from the trade of infested ornamental palms for planting; for example, A. atratus has been intercepted at US ports of entry on palms originating from the Caribbean (Evans, 2008), and in the UK on palms and palm foliage from the Caribbean and Central America, respectively (Malumphy and Tresedar, 2011). The eggs and early-instar larvae are small and very difficult to detect during plant health inspections. The eggs and larvae are only found on foliage, and therefore the trade in palm seeds poses a negligible risk.

Habitat List

Hosts/Species Affected

A. atratus has been recorded feeding on 114 host plant species belonging to five families. Most (96%) hosts are palms in the family Arecaceae. Coconut is the most commonly reported host. A. atratus is occasionally recorded on non-palm hosts, including two highly important crops, citrus and aubergine. The significance of A. atratus on non-palm hosts, however, is unclear (Malumphy and Tresedar, 2011).

Host Plants/Plants Affected

Symptoms

The upper surfaces of infested palm fronds often exhibit chlorosis and/or necrosis. The undersurfaces of infested fronds will be covered in dense patches of black puparia covered in conspicuous white wax secretions. The foliage, stems and fruit may be covered with sticky honeydew which serves as a medium for the growth of sooty moulds. Large whitefly infestations may cause wilting and the plant may lose vigour; consequently, there may be a decrease in fruit production.

Symptoms List

Biology and Ecology

Reproductive Biology

The development of A. atratus involves six stages: egg, four larval instars and adult. A. atratus is mainly parthenogenetic (thelytoky) but some rare males were found in Réunion and Mayotte (Borowiec et al., 2010). Its development takes around 48 days to develop from egg to adulthood at 25-27°C (Borowiec et al., 2010). It is multivoltine and will breed continuously if environmental conditions are suitable.

Climate

Natural Enemies

Notes on Natural Enemies

Several parasitoids (Chalcidoidea, Aphelinidae) have been recorded from A. atratus: Cales noacki Howard, Encarsia cubensis Gahan, Encarsia brasiliensis (Hempel) (= hispida De Santis), Encarsia lanceolata Evans and Polaszek, Encarsia nigricephala Dozier, Eretmocerus cocois Delvare and Eretmocerus desantisi Rose (Borowiec et al., 2010; Evans and Polaszek, 1997, 1998; Delvare et al., 2008; Noyes, 2012). Moreover, Borowiec et al. (2010) recorded a new species of Encarsia on A. atratus in Réunion island. After molecular and morphological investigations, this species appeared to be Encarsia basicincta Gahan (N. Borowiec, unpublished data). Among these parasitoids, E. cocois is to date the only one recorded exclusively on A. atratus (Borowiec et al., 2010; Delvare et al., 2008). Chilocorus nigritus (Fabricius) (Coleoptera: Coccinellidae) has also been recorded as a natural enemy of A. atratus (Beaudoin-Ollivier et al., 2004).

Means of Movement and Dispersal

Natural Dispersal (Non-Biotic)

Adult A. atratus are winged and capable of flight, but are small, delicate and relatively poor fliers.

Accidental Introduction

Palm trees are present worldwide, and because of their great appeal as ornamentals, their trade has increased considerably in recent years. It is most likely that long distance (international) dispersal of A. atratus has resulted from the spread of infested palms in trade. A. atratus has been intercepted at US ports of entry on palms originating from the Caribbean (Evans, 2008), and in the UK on palms and palm foliage imported from the Caribbean and Central America, respectively (Malumphy and Tresedar, 2011).

Pathway Causes

Pathway Vectors

Plant Trade

Impact Summary

Impact

A. atratus feeds on palms that are of economic, amenity and environmental importance.

Economic Impact

Both the larval stages and adults of A. atratus damage plants directly by feeding on the foliage. The removal of sap reduces plant vigour, causes chlorosis and premature leaf drop and reduces yields. Large infestations of whitefly, in combination with other stress factors such as lack of water, may result in the death of palms. Indirect damage is caused by the excreted honeydew that serves as a medium for the growth of sooty moulds, which hinder photosynthesis and gas exchange, and reduce yields. The highly conspicuous flocculent white wax that covers dense groups of pupae and the sooty moulds reduce the aesthetic appearance and market value of ornamentals and crops. Plants growing below infested palms also become covered in sticky honeydew, sooty mould and wax. The honeydew attracts ants, flies and other insects which can be a nuisance.                                                                                  

A. atratus is most economically significant as a pest of coconut; for example, in Grand Comoro 90% of coconut palms were severely infested by the whiteflies A. atratus and Paraleyrodes bondari Peracchi, and A. atratus accounted for 90% of the whiteflies found (Streito et al., 2004). The sooty mould that develops on the honeydew excreted by whiteflies significantly affects coconut palm growth and yields. Heavy whitefly infestations have even resulted in death of the palms. The economic impact is substantial, with annual lost earnings for producers estimated at 3-5 million euros. Crops growing under infested coconut, such as vanilla, banana, physic nut and guava, are also damaged (Beaudoin-Ollivier et al., 2004).

A. atratus attacks many ornamental palms commonly planted in tourist areas, such as the Canary Islands and Seychelles, and therefore has the potential to impact tourism (Borowiec et al., 2010).

Environmental Impact

A. atratus feeds on 17 palm species that are listed in the IUCN red list (Borowiec et al., 2010), and therefore has the potential to be detrimental to biodiversity, particularly in more vulnerable island ecosystems.

Threatened Species

Social Impact

There appears to be no specific data published on the social impact of A. atratus; however, the whitefly is an economic pest of coconut and has reduced earnings in the Comoros Islands (Streito et al., 2004), where coconut is traditionally used in many areas of life (such as food, agroforestry and the construction of traditional houses). It has the potential to cause a significant social impact, as coconut is a staple food source for many people in the tropics and subtropics, and plays a role in culture and religion in some countries in Africa (e.g. Comoros Islands) and Asia.  

Risk and Impact Factors

Impact mechanisms

• Herbivory/grazing/browsing

Impact outcomes

• Damages animal/plant products
• Host damage
• Negatively impacts agriculture
• Negatively impacts animal/plant collections
• Negatively impacts forestry
• Negatively impacts livelihoods
• Negatively impacts tourism
• Negatively impacts trade/international relations
• Reduced amenity values
• Reduced native biodiversity
• Threat to/ loss of endangered species
• Threat to/ loss of native species

Invasiveness

• Abundant in its native range
• Benefits from human association (i.e. it is a human commensal)
• Fast growing
• Gregarious
• Has high reproductive potential
• Highly adaptable to different environments
• Highly mobile locally
• Proved invasive outside its native range
• Reproduces asexually
• Tolerant of shade

Likelihood of entry/control

• Difficult to identify/detect as a commodity contaminant
• Difficult to identify/detect in the field
• Difficult/costly to control
• Highly likely to be transported internationally accidentally

Diagnosis

Aleurotrachelus is one of the largest genera of whiteflies and currently contains 74 species (Martin and Mound, 2007). There are no comprehensive keys available for the identification of Aleurotrachelus species and the genus may be polyphyletic (Martin, 2005). Whitefly taxonomy is based on the morphology of the fourth-larval instar, known as the pupa or puparium. A. atratus should be identified by an experienced entomologist by comparing slide-mounted pupae with verified voucher specimens. Photographs of diagnostic morphological characters of a slide-mounted A. atratus pupa are provided by Streito et al. (2004) and Walker (2008).

Detection and Inspection

Eggs and larvae of A. atratus occur on the underside of palm fronds, and when abundant they are highly conspicuous due to the flocculent white wax which covers the pupae. Adult whitefly may be found on both upper and lower surfaces of palm fronds. The upper surfaces of infested fronds often exhibit chlorosis or necrosis. Infested palms may also exhibit wilting and a covering of sticky honeydew and associated sooty moulds.

However, field identification of A. atratus is unreliable as there are similar species with black pupae in the genus Aleurotrachelus and other genera such as Aleurotulus, Aleurolobus and Tetraleurodes.

Similarities to Other Species/Conditions

Field identification of A. atratus is unreliable as there are similar species with black pupae in the genus Aleurotrachelus, as well as in other genera. Colonies of A. atratus are covered in flocculent white wax and may be confused with other whitefly species that are also common on palms.

The symptoms of A. atratus on palms (chlorosis and/or necrosis) can also be caused by scale insects.

Adult A. atratus resemble those of the cosmopolitan glasshouse whitefly (Trialeurodes vaporariorum), but the body of T. vaporariorum is cream to pale yellow, compared with the dark yellow body of A. atratus.

Prevention and Control

Cultural Control and Sanitary Measures

Cultural control and sanitary measures targeted at A. atratus in a glasshouse at a botanical garden in the UK have included pruning out the worst-infested leaves and, sometimes, the removal of whole plants. On some of the important specimen plants the leaves were washed by hand and wiped with alcohol (Malumphy and Tresedar, 2011).

Biological Control

Biological control measures targeted at A. atratus in a glasshouse at a botanical garden in the UK have included introductions of Amblyseius swirskii Athias-Henriot (Mesostigmata: Phytoseiidae), Chilocorus nigritus Fabricius (Coleoptera: Coccinellidae) and Eretmocerus eremicus Rose and Zolnerowich (Hymenoptera: Aphelinidae) to areas of high whitefly infestation. No evidence, however, has been observed of any of these biological control agents being effective against A. atratus.

The parasitoid Eretmocerus cocois was found to effectively parasitize populations of A. atratus in Guadeloupe (Neotropics) and in the Indian Ocean islands of Réunion and Mayotte (Delvare et al., 2008), and was introduced to Ngazidja (Comoros Islands) for the biological control of the whitefly by CIRAD and the Agriculture, Fisheries and Environment Research Institute (INRAPE) in the Comoros within the Crop Protection Network for the Indian Ocean (PRPV). The parasitoid proved an effective biocontrol agent of A. atratus (Cave, 2008), and may be introduced to the Seychelles (Hobson, 2012).

Chemical Control

Chemical treatments targeted at A. atratus in a glasshouse at a botanical garden in the UK have included applications of maltodextrin and pyrethrin in the spring and summer, and applications of acetamiprid, deltamethrin, pymetrozine, pyrethrin, spiromesifen and thiacloprid in the winter. These treatments were only partially successful; one of the main difficulties was achieving an even application of the pesticides, which was made difficult by the height of the plants and the shape of the palm leaves (Malumphy and Tresedar, 2011).

References

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Borowiec N, Quilici S, Martin J, Issimaila MA, Chadhouliati AC, Youssoufa MA, Beaudoin-Ollivier L, Delvare G, Reynaud B, 2010. Increasing distribution and damage to palms by the Neotropical whitefly, Aleurotrachelus atratus (Hemiptera: Aleyrodidae). Journal of Applied Entomology, 134(6):498-510. http://www.blackwell-synergy.com/loi/jen

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Links to Websites

Contributors

07/08/13 Original text by:

Chris Malumphy, Central Science Laboratories, UK

Distribution Maps

• = Present, no further details
• = Evidence of pathogen
• = Widespread
• = Last reported
• = Localised
• = Presence unconfirmed
• = Confined and subject to quarantine
• = See regional map for distribution within the country
• = Occasional or few reports

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