Final Import Risk Analysis Report for Fresh Mango Fruit from India

4.7. Mealybugs [Hemiptera: Pseudococcidae]

Mealybugs impact on plants and commodities by:

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  sucking plant sap through their tubular stylets. If left unchecked, heavy infestations of mealybugs may damage or weaken plants, directly causing premature leaf drop, dieback and even plant death.
  
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  causing indirect damage by injecting toxins or plant pathogens into host plants (such as grapevine leaf roll virus (Pfeiffer and Schultz 1986), mealybug pineapple wilt).
  
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  contaminating fruit with egg sacs, nymphs and adults (UC ANR 2006), or by depositing a waste product, ‘honeydew’, on the leaves and fruit. Honeydew may act as a substrate for sooty mould to grow. Sooty mould may reduce photosynthesis and downgrades fruit quality.
  

The mealybugs of quarantine concern associated with mango fruit are:

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  Planococcus lilacinus – coffee mealybug ^EP
  
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  Rastrococcus iceryoides – downy snowline mealybug
  
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  Rastrococcus invadens – mango mealybug
  
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  Rastrococcus spinosus – Philippine mango mealybug ^EP
  

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  Ferrisia malvastra – Malvastrum mealybug
  
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  Ferrisia virgata – striped mealybug
  

The discussion below largely concentrates on R. invadens as an example of the mealybugs of concern. However, the conclusions reached are valid for all species being assessed.

4.7.1. Probability of entry

Probability of importation

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  These mealybugs have been reported in India on mango (Ben-Dov et al. 2006) affecting leaves, blossoms and fruit (Peña and Mohyuddin 1997; Tobih et al. 2002; Peña 2004; Moore 2004).
  
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  Later instar nymphs and adult females of R. iceryoides usually feed on the tender terminal shoots, inflorescences and fruits, whereas first instar nymphs feed on the undersides of leaves. In severe infestations, all the tender shoots, inflorescences and fruits of mango are infested by different stages of the pest (Rawat and Jakhmola 1970).
  
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  Mangoes packed for export typically consist of the fruit and a very short (approximately 0.3 to 0.5 cm) pedicel attached to the top of the fruit. The morphology of the fruit does not provide any hiding places for the mealybugs. Despite this, mealybugs have been found in mango consignments entering the USA (USDA 2006), proving that they are associated with the fruit pathway.
  
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  Mealybugs are quite small and may be difficult to detect, particularly in low numbers. The common length for adult female mealybugs of most species is approximately 1.5–4 mm long (Akintola and Ande 2006).
  
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  Mealybug infestations may promote the growth of sooty mould on the surface of the fruit. Fruit with sooty mould may be rejected at the point of harvest but symptoms would need to be severe for rejection to occur at this point.
  
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  The normal post-harvest practice of washing fruit to remove sap (Morton 1987) may remove some mealybug species on the fruit at the time of harvest, but the effective removal of all mealybugs may be difficult (Taverner and Bailey 1995).
  
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  However, the detection of mealybugs on arrival of mangoes in the USA (USDA 2006) demonstrates that post-harvest cleaning and washing will not remove all mealybugs and quality control inspectors within the packing house are likely to miss some infested fruit.
  

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  Mealybugs are likely to survive storage and transportation, as shown by the interception of mealybugs on mangoes imported into the USA (USDA 2006).
  
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  Adult females of R. invadens live from 51–110 days; nymphal development is about 28– 30 days for both male and female mealybugs (Moore 2004). Mated adult females of R. iceryoides can live for 13–23 days and unmated females can live for up to 80 days, whereas adult males live for only 1–2 days (Rawat and Jakhmola 1970). There is a high probability that viable female mealybugs present on the fruit at point of export would still be viable on arrival in Australia.
  
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  The optimum temperature for storage of mangoes is approximately 13-14^oC, as storage below this temperature results in chilling injury to the fruit (Lederman et al. 1997; Nair and Singh 2004). Adult female R. iceryoides are known to hibernate overwinter in India (Rawat and Jakhmola 1970). The development of nymphs and other pre-adult stages would be slowed or halted by cool storage.
  

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  There are both chemical and biological options for mealybug control. Mealybugs have been detected on imported mango fruit in the USA (USDA 2006), showing that they can survive some existing pest management procedures.
  

Probability of distribution

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  A range of plants, widely distributed, abundant, native and/or cultivated in Australia, including Acacia, Citrus, Malus, Mangifera, Musa and Vitis, can act as hosts for these pests (Ben-Dov et al. 2006).
  
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  Juvenile mealybugs are able to move about within the host tree, and can be dispersed by wind, visiting insects and birds, and on clothing (Hely et al. 1982).
  
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  Long range dispersal of mealybugs can also occur by the movement of adults and nymphs with fresh vegetative material.
  
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  Crawlers are small and less robust than adult females, but they can be dispersed onto other plants up to several hundred metres by wind (Rohrbach et al. 1988). Adult females are wingless and need to be carried onto hosts by wind or vectors such as other insects or people.
  

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  Mangoes would be distributed for sale to multiple destinations in Australia.
  
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  Mealybugs would need to survive transportation and storage. Although cold storage may impact the survival of mealybugs, some mealybugs are likely to survive storage and distribution as temperatures employed are commonly approximately 13-14^oC (Lederman et al. 1997; Nair and Singh 2004).
  
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  Mango will presumably be shipped all over Australia, so a portion of the pests that enter the country are likely to reach areas of host abundance.
  

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  The intended use of the commodity is human consumption but waste material will be generated (e.g. skins of fruit, overripe fruit, blemished or damaged fruits). Immature stages may complete development on discarded waste.
  
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  While mealybugs have limited mobility, adult females and juveniles are able to crawl between host plants in infested areas (Meyerdirk et al. 2001) and so could migrate from waste fruit to any adjacent vegetation.
  
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  Adult males of R. invadens are winged, fragile and do not live for more than several days. They detect females through pheromones and are able to fly to them in order to mate (Grimes and Cone 1985). Rastrococcus iceryoides males are also winged but fragile and do not live for more than 1–2 days (Rawat and Jakhmola 1970; Grimes and Cone 1985).
  

Probability of entry (importation x distribution)

4.7.2. Probability of establishment

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  These mealybugs are capable of surviving and reproducing on a wide host range (Agounke et al. 1988; Ivbijaro et al. 1992; Ben-Dov et al. 2006). Host species of these mealybugs are widespread in cities, towns and horticultural production areas throughout Australia.
  
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  Rastrococcus invadens is highly polyphagous, infesting about 45 species in 22 families (Agounke et al. 1988) including fruit trees, shade and ornamentals, cereal and tubers (Ivbijaro et al. 1992).
  
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  In Pakistan, R. spinosus is considered an important pest of mangoes and has also been recorded on oleander, banana, guava, orange and other plants (Mahmood et al. 1980).
  

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  These mealybugs are distributed in a range of geographic regions (Williams 2004, Ben-Dov et al. 2006), some of which are climatically similar to parts of Australia.
  
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  Many mealybugs are considered invasive and have become established after introduction to new environments. For example, Planococcus lilacinus is native to the Afrotropical region (Miller et al. 2002) and now has a wider distribution, excluding Australia (Ben-Dov 1994). Rastrococcus invadens is of South-East Asian origin, but is now established in western Africa. The mango mealybug was accidentally introduced into western Africa in the early 1980s and became a major pest of various ornamental and fruit trees (Agounke et al. 1988; Boavida et al. 1995).
  
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  Six species of Rastrococcus are reported in Australia, demonstrating the suitability of climatic conditions for at least some species of this genus (Ben-Dov et al. 2006).
  
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  Climatic factors and identity of the host plant influence a number of aspects of the life history of R. invadens (Moore 2004). The number of days for each developmental stage is influenced by both host plant and temperature (Moore 2004). The population density of R. invadens decreases during rainy seasons and peaks during the dry season (Boavida and Neuenschwander 1995).
  

The successful reproductive strategy of these pests relies on the longevity and egg-laying ability of the adult female, the mobility of the short-lived adult male, the ability of the crawlers to disperse via crawling, vectors or wind, and their ability to locate new hosts.

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  Mealybug species reproduce either sexually or parthenogenetically (Grime and Cone 1985). For mealybugs that reproduce sexually, male mealybugs must locate a female for a population to establish. Male mealybugs are small, non-feeding insects with a short life span, usually just a few days. Adult males are winged but are weak flyers (Grimes and Cone 1985). Female mealybugs release a pheromone to attract males for mating (Grimes and Cone 1985).
  
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  Rastrococcus iceryoides is known to reproduce sexually, and mating must occur if viable eggs are to be produced (Rawat and Jakhmola 1970). On mango, fertility of R. iceryoides has been found to range from 450–585 eggs per female (Rawat and Jakhmola 1970).
  
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  Unmated females of R. iceryoides live for up to 80 days whereas mated females live for 13–23 days. Adult males live for only 1–2 days and start copulating soon after they emerge (Rawat and Jakhmola 1970).
  
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  Development time of R. invadens is influenced by the host plant. Experiments on mango, figs, frangipani and citrus showed that mango-fed nymphs had the highest survival and shortest development rate while the development time of citrus-fed nymphs was the longest (Moore 2004).
  
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  Rastrococcus invadens is capable of producing eight generations a year in India (Moore 2004). The entire life cycle of R. invadens can be completed in 31-84 days (Peña et al. 1998).
  

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  Controls in place for other pests of economic concern may reduce the likelihood of establishment of mealybugs in agricultural ecosystems. However, many hosts available in Australia are present in urban and suburban areas as well as in unmanaged environments. Therefore, it is likely that there would be little overall barrier to the establishment of these mealybugs in Australia.
  

4.7.3. Probability of spread

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  These mealybugs have been reported from a number of environments. For example Rastrococcus invadens is widespread throughout the tropics and subtropics (Ben-Dov et al. 2006). There are similar environments in Australia.
  

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  Rastrococcus invadens is capable of producing eight generations per year in India (Moore 2004). After second and subsequent generations of mealybugs have become established on commercial, household and wild host plants, mealybugs are likely to persist and to spread progressively over time. This spread would be assisted by wind dispersal, vectors and the movement of plant material.
  
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  Due to the limited distance mealybugs can move by crawling or wind dispersal, natural barriers such as deserts, mountains or large areas where hosts are not present would limit the ability of these mealybug species to disperse between some areas.
  
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  Mealybugs may be dispersed within and between orchards with the movement of personnel, infested plant material or by wind dispersal (Hely et al. 1982; Tobih et al. 2002).
  
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  The crawler stage is the most active stage and is responsible for both active and passive dispersal. Crawlers can survive only a day without feeding and once they insert their style to feed they generally remain anchored permanently (CUES 2007). Selection of an appropriate feeding site is critical for subsequent development. Mortality is generally highest during the first instar and failure to settle is considered to be one of the major mortality factors for many species.
  

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  Movement of infested planting material or produce has been reported as the probable way by which some mealybug species have been introduced to other countries (Tobih et al. 2002).
  
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  Adults and nymphs are likely to be moved with plant commodities, as shown by the interception of mealybug species in the USA on imported mango fruit (USDA 2006).
  

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  Several natural enemies attack R. invadens including encyrtid parasitoids (Anagyrus mangicola and Gyranusoides tebygi) (Moore 2004; Tobih et al. 2002). These species are both endophagous parasitoids, specific to R. invadens (Boavida et al. 1995). They are not present in Australia.
  

4.7.4. Overall probability of entry, establishment and spread

The overall probability that mealybugs will be imported as a result of trade in mango fruit from India, be distributed in a viable state to a susceptible host, establish and spread within Australia, is: MODERATE.

4.7.5. Consequences

4.7.6. Unrestricted risk estimate