Draft Import Risk Analysis Report for Fresh Apple Fruit from the People’s Republic of China

As indicated, the unrestricted risk for apple blotch has been assessed as ‘low’, which exceeds Australia’s ALOP. Therefore, specific risk management measures are required for this pest.

8. 
   Sooty blotch and flyspeck complex
   
   1. 
      Introduction
      

Sooty blotch and flyspeck (SBFS) are diseases caused by a complex of fungi that colonise the cuticle of apple fruit (Batzer et al. 2005). Sooty blotch appears as dark smudges and flyspeck appears as groups of tiny black spots on the surface of fruit. Although these fungi do not affect the growth and development of the fruit, they cause economic loss to growers because of reduced fruit quality, and market value can be reduced by more than 90 per cent (Batzer et al. 2002; Williamson and Sutton 2000).

Colby (1920) determined that sooty blotch was caused by Gloeodes pomigena (Schwein.) Colby and flyspeck was caused by Schizothyrium pomi (Mont. & Fr.) Arx. Johnson and Sutton (1994) and Johnson et al. (1997) found sooty blotch was caused by three fungi, Geastrumia polystigmatis Batista & M.L. Farr, Peltaster fructicola Eric M. Johnson, T.B. Sutton & Hodges and Leptodontidium elatius (de Hoog) de Hoog. Subsequently, recent studies have found that a range of fungi can cause SBFS. Batzer et al. (2005) using molecular methods to identify the fungi from samples from the midwest of the United Sates, found 30 species caused SBFS lesions on apple fruit in inoculation field trials.

In two recent studies conducted in China, a range of fungi were isolated from apples with SBFS symptoms from orchards in Shaanxi, Shandong, Liaoning, Henan and Yunnan provinces (Zhang 2006; Zhang 2007). These fungi included the following groups:

Dissoconium mali G.Y. Sun, Z Zhang & R. Zhang and Dissoconium multiseptatae G.Y. Sun & Z. Zhang [Anamorphic Mycosphaerellaceae]

Paraconiothyrium sp. [Anamorphic Montagnulaceae]

Passalora sp. [Anamorphic Mycosphaerellaceae]

Peltaster sp. [Dothidiales: Dothioraceae]

Pseudocercospora sp. [Anamorphic Mycosphaerellaceae]

Pseudocercosporella sp. [Anamorphic Mycosphaerellaceae]

Stenella sp. [Anamorphic Mycosphaerellaceae]

Strelitziana mali G.Y. Sun & Z. Zhang [Anamorphic Chaetothyriales]

Stomiopeltis spp. [Anamorphic Micropeltidaceae]

Wallemia longxianensis, Wallemia qiangyangesis and Wallemia sebi (Fr.) Arx [Wallemiales]

Xenostigmina sp. [Anamorphic Mycosphaerellaceae]

Zygophiala liquanensis and Zygophiala taiyuensis [Anamorphic Schizothyriaceae]

In the 2006 study, 18 isolates from apples, in the genera Zygophialia, Wallemia, Dissoconium, Peltaster and Pseudocercosporella, were able to cause SBFS (Zhang 2006). Of the fungi listed above for China, Dissoconium spp., Passalora sp., Peltaster spp., Pseudocercospora spp., Pseudocercosporella spp., Xenostigmina spp. and Zygophiala spp. have been shown to cause SBFS in the United States.

The fungi associated with SBFS in China are anamorphic fungi that disperse by means of conidia. SBFS fungi apparently overwinter on reservoir hosts and apple twigs and fruit in the United States and conidia are spread by wind and rain to developing fruit and new tissues of reservoir hosts in the spring and early summer (Williamson and Sutton 2000). SBFS fungi grow on a wide range of reservoir hosts, including trees, shrubs and vines that are near or bordering orchards (Williamson and Sutton 2000).

As the fungi that are associated with SBFS in China are not known to cause SBFS in Australia, they will be assessed in this pest risk assessment.

The risk scenario of particular relevance to the sooty blotch and flyspeck disease complex is infected fruit with viable inoculum.

2. 
   Probability of entry
   

The probability of entry is considered in two parts, the probability of importation and the probability of distribution, which consider pre-border and post-border issues respectively.

Probability of importation

The likelihood that SBFS fungi will arrive in Australia with the importation of apple fruit: HIGH.

• 
  The fungi causing SBFS occur widely in China, being collected in Henan, Liaoning, Shaanxi, Shandong and Yunnan provinces (Zhang 2006; Zhang 2007).
  
• 
  In south-eastern United States, infection levels of 5–90% occur (Batzer et al. 2002; Williamson and Sutton 2000).
  
• 
  The general incidence of SBFS in the main apple production areas in China is not published but infection rates of 72–86% have been recorded in Yunnan province, with losses from SBFS of 92–95% in some orchards in extreme years (Zhang 2006).
  
• 
  Sooty blotch and flyspeck produce obvious symptoms on apple fruit. Colonies vary from discrete circular colonies to large colonies with diffuse margins (Sutton 1990). Apples with obvious SBFS symptoms will be detected and discarded during the grading operations in the packing house. However, fruit in the early stages of infection or with small colonies may escape detection. Once apples are infected with SBFS fungi, it takes about 20–28 days for symptoms to develop, but they may become visible in 8–12 days under optimal conditions (Sutton et al. 1988).
  
• 
  Sooty blotch and flyspeck can develop in storage and transport. Drake (1970; 1972; 1974) found that when symptomless fruit was stored for 6 months at 0–1 °C, extensive sooty blotch and flyspeck developed when the last fungicide spray was made 8–10 weeks before harvest.
  

The wide distribution of this disease complex in major apple production areas in China and symptomless fruit developing infections during storage and transport, support a risk rating for importation of ‘high’.

Probability of distribution

The likelihood that SBFS fungi will be distributed in Australia as a result of processing, sale or disposal of the commodity: HIGH.

• 
  Imported apple fruit is intended for human consumption in Australia. It is expected that once the apple fruit has arrived in Australia it will be distributed throughout Australia for repacking and/or retail sale. Any infected fruit present may be distributed during these processes.
  
• 
  Individual consumers will distribute small quantities of apples to a variety of urban, rural and wild environments.
  
• 
  SBFS fungi will survive distribution in Australia, as they can develop in storage at 0–1 °C (Drake 1970; Drake 1972; Drake 1974).
  
• 
  Fruit waste, that may include the skin of apple fruit with SBFS colonies, may be disposed of in close proximity to a suitable host plant.
  
• 
  SBFS fungi grow on a wide range of reservoir hosts, including trees, shrubs and vines that are near or bordering orchards (Williamson and Sutton 2000). For example, the host plants of Zygophiala jamaicensis include 120 species in 44 families of seed plants, including Malus, that are found throughout temperate and tropical regions (Zhang 2006; Zhang 2007). These host plants are widely distributed throughout Australia.
  
• 
  The fungi associated with SBFS in China are anamorphic fungi that disperse by means of conidia (Williamson and Sutton 2000). Conidia of these fungi on the surface of SBFS colonies could be spread by wind and wind-blown rain to new tissues of hosts in close proximity to discarded apple waste.
  

The disposal of fruit waste in the environment, the ability of wind and water droplets to transfer spores from the fruit waste to a host and the wide range and distribution of hosts support a risk rating for distribution of ‘high’.

Probability of entry (importation  distribution)

The overall probability of entry is determined by combining the probability of importation with the probability of distribution using the matrix of rules shown in Table 2.2. The likelihood that SBFS fungi will enter Australia as a result of trade in fresh apple fruit from China and be distributed in a viable state to a suitable host: HIGH.

3. 
   Probability of establishment
   

The likelihood that SBFS fungi will establish in Australia based on a comparison of factors in the source and destination areas considered pertinent to their survival and reproduction: HIGH.

• 
  The development of SBFS is favoured by warm temperatures, high rainfall and high humidity (Batzer et al. 2008; Zhang 2006; Zhang 2007).
  
• 
  The effects of temperature and relative humidity have been studied in vitro for a number of the fungi that cause SBFS. Conidia of Peltaster fructicola germinated from 12 to 24 °C at relative humidities of 95% or above, conidia of Leptodontium elatius germinated from 12 to 32 °C at relative humidities of 97% or above and conidia of Zygophiala jamaicensis germinated from 8 to 28 °C at relative humidities of 96% or above (Williamson and Sutton 2000).
  
• 
  Conditions that would allow the establishment of SBFS fungi on host plants would occur in parts of Australia, especially during periods of wet weather in coastal areas in the warmer months of the year.
  
• 
  Sooty blotch caused by Gloeodes pomigena and flyspeck caused by Schizothyrium pomi have been recorded in New South Wales and Western Australia (APPD 2008; Shivas 1989), which suggests that other SBFS fungi have the potential to establish in Australia.
  

The occurrence of sooty blotch caused by Gloeodes pomigena and flyspeck caused by Schizothyrium pomi in New South Wales and Western Australia and the wide range and distribution of hosts, support a risk rating for establishment of ‘high’.

4. 
   Probability of spread
   

The likelihood that SBFS fungi will spread based on a comparison of the factors in the source and destination areas considered pertinent to the expansion of the geographic distribution of SBFS: HIGH.

• 
  SBFS fungi have a wide range of hosts. For example, the hosts of Z. jamaicensis include 120 species in 44 families of seed plants, including Malus, throughout temperate and tropical regions (Zhang 2006; Zhang 2007). These host plants are widely distributed throughout Australia.
  
• 
  The fungi associated with SBFS in China are anamorphic fungi that disperse by means of conidia (Williamson and Sutton 2000). Conidia of these fungi on the surface of SBFS colonies could be spread by wind and wind-blown rain to new tissues of hosts.
  
• 
  SBFS diseases are favoured by warm temperatures, high rainfall and high humidity (Batzer et al. 2008; Zhang 2006; Zhang 2007).
  
• 
  Conditions that would allow the development and spread of SBFS fungi on host plants would occur in parts of Australia, especially during periods of wet weather in coastal areas in the warmer months of the year.
  
• 
  Sooty blotch, caused by Gloeodes pomigena, and flyspeck, caused by Schizothyrium pomi, have been recorded in New South Wales and Western Australia (APPD 2008; Shivas 1989), which suggests that other SBFS fungi have the potential to spread in Australia.
  
• 
  Distribution of infected fruit via commercial or domestic movement may aid the spread of the SBFS pathogens.
  
• 
  Distribution of infected nursery stock may aid the long distance movement of SBFS fungi to new areas.
  

The dispersal of spores by wind and wind-blown rain, the potential movement of symptomless infected planting materials and the wide range and distribution of hosts, support a risk rating for distribution of ‘high’. Sooty blotch caused by Gloeodes pomigena and flyspeck caused by Schizothyrium pomi have been recorded in New South Wales and Western Australia, further supporting the risk rating of ‘high’ for these fungi.

5. 
   Overall probability of entry, establishment and spread
   

The overall probability of entry, establishment and spread is determined by combining the probabilities of entry, of establishment and of spread using the matrix of ‘rules’ for combining qualitative likelihood shown in Table 2.2.

The overall likelihood that SBFS fungi will enter Australia as a result of trade in the commodity from the country of origin, be distributed in a viable state to suitable hosts, establish in that area and subsequently spread within Australia: HIGH.

6. 
   Consequences
   

The consequences of the establishment of the SBFS fungi recorded on apple fruit in China in Australia have been estimated using the decision rules described in Table 2.3.

Based on the decision rules described in Table 2.4, that is, where the consequences of a pest with respect to one or more criteria are ‘D’, the overall consequences are estimated to be LOW.

Reasoning for these ratings is provided below:

Criterion	Estimate
DIRECT
Plant life or health	D – Significant at the district level Sooty blotch and flyspeck are two of the most common diseases of pome fruits in many moist, temperate growing regions of the world (Williamson and Sutton 2000). They cause considerable economic loss to growers of fresh market fruit because of reduced fruit quality (Sutton 1990; Williamson and Sutton 2000). In regions with warm, wet and humid conditions in summer when fruit is developing, such as the south-east of the United States and Yunnan Province in China, up to 95% of the crop can be affected by these diseases (Batzer et al. 2008; Zhang 2006; Zhang 2007). In the south-east United States, virtually all of the apple crop would be affected each year if fungicides were not applied. Even with the use of fungicides, losses of 25% or more are reported in individual orchards in some years (Sutton 1990). In Australia, sooty blotch and flyspeck appear to be minor diseases. Sooty blotch, caused by Gloeodes pomigena, has been recorded in New South Wales on apple, peach and orange and in Western Australia on apple (APPD 2008). Flyspeck, caused by Schizothyrium pomi, has been recorded in New South Wales on apple, peach and persimmon and in Western Australia on apple (APPD 2008). However, the entry, establishment and spread of additional species of SBFS fungi from China may increase the importance of these diseases, especially in seasons with high summer rainfall.
Other aspects of the environment	B – Minor significance at the local level Although SBFS fungi have a wide range of host plants, they are unlikely to affect the health of native flora, because they are a complex of fungi that grow on the waxy cuticle of plants (Williamson and Sutton 2000).
INDIRECT
Eradication, control etc.	D – Significant at the district level Control of SBFS is based on a combination of cultural practices, including pruning and bagging and chemical control. It was reported that bagging of fruit significantly reduced the incidence, and severity of these diseases (Zhang 2006; Zhang 2007). Pruning, which facilitates drying, has been shown to reduce disease incidence and severity, especially in the wet season. Proper thinning of fruit is also important. The removal of all nearby reservoir hosts is not always practical, but mowing hedgerows and ditch banks is helpful in reducing the influx of inoculum. Fungicide sprays, applied at 10–14 day intervals, should begin by first or second cover in areas where the diseases are a serious problem. Existing integrated pest management programs may be disrupted due to possible increases in the use of fungicides. Costs for crop monitoring, orchard sanitation, pruning, and fungicides may be incurred by the producer.
Domestic trade	A – Indiscernible at the local level It is unlikely that the entry, establishment and spread of additional SBFS fungi in commercial apple production areas in Australia would result in the implementation of interstate quarantine measures. Sooty blotch and flyspeck have been recorded in New South Wales and Western Australia and no interstate quarantine measures have been put in place for these diseases.
International trade	A – Indiscernible at the local level It is unlikely that the entry, establishment and spread of additional SBFS fungi in commercial apple production areas in Australia would result in the introduction of international quarantine measures. Sooty blotch and flyspeck already occur in Australia and there are no restrictions on the export of Australian fruit because of these diseases. In addition, these diseases are widespread around the world.
Environment	B – Minor significance at the local level Fungicide applications or other control activities including mowing hedgerows and ditch banks to control this disease on susceptible crops would have some impact on the environment.

7. 
   Unrestricted risk estimate
   

Unrestricted risk is the result of combining the probability of entry, establishment and spread with the estimate of consequences. Probabilities and consequences are combined using the risk estimation matrix shown in Table 2.5.

Unrestricted risk estimate for sooty blotch and flyspeck disease complex
Overall probability of entry, establishment and spread	High
Consequences	Low
Unrestricted risk	Low

As indicated, the unrestricted risk for sooty blotch and flyspeck disease complex has been assessed as ‘low’, which exceeds Australia’s ALOP. Therefore, specific risk management measures are required for this pest.

8. 
   Apple scab - Venturia inaequalis
   
   1. 
      Introduction
      

Venturia inaequalis is not present in Western Australia and is a pest of regional quarantine concern for that state.

Apple scab caused by V. inaequalis attacks leaves, petioles, blossoms, sepals, fruits, pedicels and less frequently, young shoots and bud scales. The fungus produces two distinct types of spores, conidia (asexual) and ascospores (sexual) (Biggs 1990). Ascospores released from overwintered leaves and fruit on the orchard floor are the principal source of inoculum in the spring (Ma 2006). The lesions resulting from these infections produce conidia throughout the spring and summer, and serve as secondary inoculum (Biggs 1990; Schwabe 1982). Under favourable conditions, the pathogen attacks the leaves and fruit, causing serious damage.

The risk scenario of particular relevance to V. inaequalis is that associated with scabby growth on the surface of mature fruit and ‘pin-point’ lesions that are not visible.

Venturia inaequalis was assessed in the Final Import Risk Analysis Report for Apples from New Zealand (Biosecurity Australia 2006a). In that assessment, the overall probability of entry, establishment and spread was assessed to be ‘high’ using a semi-quantitative method and the consequences were assessed to be ‘moderate’. As a result, the unrestricted risk was assessed to be ‘moderate’ and specific risk management measures were determined to be necessary.

Biosecurity Australia considers that the potential volume of apple fruit imported from China would be similar to that from New Zealand and that the potential infection level of apple fruit by V. inaequalis would also be similar. Therefore, the existing policy for V. inaequalis is proposed for the importation of apple fruit from China as the unrestricted risk estimate is considered to be the same.

2. 
   Unrestricted risk
   

Unrestricted risk is the result of combining the probability of entry, establishment and spread with the estimate of consequences. Probabilities and consequences are combined using the risk estimation matrix shown in Table 2.5.

Biosecurity Australia considers the unrestricted risk of V. inaequalis through the importation of apple fruit from China is the same as the risk of this pathogen through the importation of apple fruit from New Zealand. Therefore, the existing policy for V. inaequalis has been adopted for the importation of apple fruit from China.

Unrestricted risk estimate for apple scab
Overall probability of entry, establishment and spread	High
Consequences	Moderate
Unrestricted risk	Moderate

As indicated, the unrestricted risk for apple scab has been assessed as ‘moderate’, which exceeds Australia’s ALOP. Therefore, specific risk management measures are required for this pest.

8. 
   Apple scar skin and apple dapple – Apple scar skin viroid
   
   1. 
      Introduction
      

Apple scar skin and apple dapple are diseases caused by Apple scar skin viroid (ASSVd), which is sometimes called the apple dapple viroid or the pear rusty skin viroid. The diseases deface the fruit and the fruit may remain small and hard and develop an unpleasant flavour. The severity of disease depends on the cultivar and the duration of infection. In severe cases in susceptible cultivars, the fruit is affected by scarring, necrosis and cracking. Some apple cultivars may develop leaf roll or leaf epinasty symptoms (Koganezawa et al. 2003).

ASSVd is a small circular nucleic acid molecule. ASSVd also infects pears and apricots (Koganezawa et al. 2003; Zhao and Niu 2008) and it spreads systemically through trees. Latent symptomless infection of pear by ASSVd is common in China and pear trees are considered to be a source of inoculum for apple trees (Koganezawa et al. 2003; Kyriakopoulou et al. 2003). The viroid is persistent and may have a long incubation (latency) period. Pears and apples may be infected for several years before symptoms become apparent, with symptoms increasing each year after onset in susceptible cultivars (Desvignes et al. 1999).

ASSVd has been found in apple fruit, seed, anthers, petals, receptacles, leaves, bark and roots (Hadidi et al. 1991). Viroid nucleic acids have been found in seeds from apples in the seed coat, subcoat, cotyledon and embryo (Kim et al. 2006). ASSVd is spread by grafting and budding, infected rootstocks and contaminated equipment and tools (Grove et al. 2003; Hadidi et al. 1991). It is also transmitted naturally between trees by an unknown mechanism (Koganezawa et al. 2003; Kyriakopoulou and Hadidi 1998). Transmission by root to root contact has been proposed and may involve natural root grafting (Desvignes et al. 1999).

The possibility of the importation and establishment of ASSVd was considered in an IRA for pears from China and the potential for establishment and spread from the fruit pathway was assessed as not feasible (Biosecurity Australia 2005b) because seed transmission had not been reported at the time. However, seed transmission was recently shown to occur (Kim et al. 2006). The new findings indicate that the viroid can be transmitted through the infected seeds of fruit from infected trees.

The risk scenario of particular relevance to apple scar skin viroid is infected seeds in symptomless fruit.

The assessment of the apple scar skin viroid presented here builds on the existing policy and takes into account information on seed transmission.

2.