Final Import Risk Analysis Report for Fresh Unshu Mandarin Fruit from Shizuoka Prefecture in Japan

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Timing for infection in the orchard

  • Developing leaves, between 50% and 75% of their final size, are the most susceptible stage for citrus canker infection (Ohta 1967; Canteros 1992). The first disease symptoms of citrus canker usually become visible on new leaves and shoots of unshu mandarin during the growing season (Goto 1962; Koizumi 1977).

  • The appearance of lesions on twigs and fruit in the disease cycle generally occurs only after a certain inoculum level has been reached on leaves (Schubert et al. 2001). A reduction of the pathogen level on leaves reduces the occurrence of the pathogen on fruit (Stall et al. 1982; Goto 1992; Canteros 2004).

  • Koizumi (1972) observed that citrus canker infection is highly dependent on host receptivity. Xanthomonas citri subsp. citri bacteria die relatively quickly in lesions of early infected fruit, as the formation of a phellogen layer acts as a barrier between infected and non-infected tissue suppressing further bacterial infection. In late infections, a combination of physiological changes associated with the ripening of fruit and the drop in temperatures during the autumn and winter period, effectively arrest bacterial development in infected tissue.

  • The time interval for fruit to become naturally infected with the bacterium is limited, as resistance of fruit to citrus canker increases with fruit maturity (Koizumi 1972; Canteros 1992; Graham et al. 1992b). Natural (stomatal) citrus canker infection of unshu mandarin is most severe during the early stages (first two months) of fruit development when fruit is less than 30 mm in size (Goto 1962; Koizumi 1972). Biosecurity Australia officers who visited the designated export areas in 2007 observed that fruit reached this size in mid summer (July). Unshu mandarin fruit become increasingly resistant to infections when they reach 45–50% of their final size (Koizumi 1972; Canteros 1992). In comparison, fruit of less resistant citrus species become resistant at a later growth stage. For example, Citrus natsudaidai (natsudaidai mandarin) becomes resistant when fruit reaches 50 mm in size (Goto 1962), Citrus sinensis cv. Washington Navel (sweet orange) at 68% and Citrus paradisi cv. Duncan (grapefruit) at 85% of their final size (Canteros 1992).

  • For fruit infection to occur, several conditions are required to coincide: the host tissue needs to be in a receptive stage, climatic conditions suitable to release and transfer bacteria need to occur, and sufficient inoculum needs to be available.

  • The minimum inoculum load of X. citri subsp. citri bacteria to cause stomatal infection is about 100 000 cells/ml and for wound infection is about 100 to1000 cells/ml (Goto 1962).

  • Lesions less than a fortnight old contain about 10 000 000 viable X. citri subsp. citri cells per lesion. Lesions more than one month old contained less than 1000 viable X. citri subsp. citri cells per lesion (Timmer et al. 1991).

  • Population levels of X. citri subsp. citri on symptomless fruit of grapefruit, lemon, orange and tangerine ranged from undetectable levels from sprayed low disease orange and lemon plots to between 0 to 1 000 000 X. citri subsp. citri cells per fruit from highly infected, unsprayed grapefruit, lemon and orange plots (Rybak and Canteros 2001). The fruit of all citrus cultivars used in this study were of higher susceptibility to citrus canker than C. unshiu (Koizumi 1976, 1985; Koizumi and Kuhara 1982). Symptomless C. unshiu fruit may be expected to have very low population levels of X. citri subsp. citri in comparison to the citrus cultivars tested by Rybak and Canteros (2001).

Conditions limiting fruit infection in the production area

  • Shizuoka Prefecture is affected by typhoons generally from July to October annually (refer to Table 3.4). Strong winds, during these typhoons, could carry citrus canker bacteria from infected areas along the coastal lowlands inland to the production area.

  • Warm and wet weather, together with wind-driven rain and wind speeds exceeding 8.7 m/s, greatly increase the likelihood of infection (Serizawa et al. 1969).

  • Infection other than through young leaves and young fruit requires wounded tissue, such as caused by mechanical damage or citrus leafminer damage (Goto 1962; Serizawa et al. 1969; Koizumi and Kuhara 1982; Chagas et al. 2001). Pruning of trees in the export areas occurs about March in early spring prior to leaf flush, flowering and fruit set (refer to Chapter 3).

  • Unwounded fully expanded leaves and unshu fruit larger than half of their final size are less prone to infection due to the presence of a waxy cuticle (Canteros 1992; Goto 1992). Although fruit infection can occur (Koizumi 1972; Serizawa et al. 1985; Goto 2005), this generally happens in instances of high inoculum pressure with severe bacterial infection of the tree canopy (Serizawa et al. 1985; Goto 1992).

Existing commercial control program

  • MAFF’s unshu mandarin spray calendar (Table 3.5) recommends the use of chemicals to control citrus canker and citrus leafminer. Citrus canker sprays are timed to protect suceptible leaves and small fruit, and citrus leafminer control is timed to coincide with the emergence of larvae feeding on leaves. The use of chemicals would reduce the incidence of both pests in orchards. Chemical usage is not mandatory in the production area.

  • Copper sprays are a standard control measure that reduce the level of citrus canker (Stall et al. 1980; Das 2003; Graham et al. 2004). Copper sprays decrease the number of viable cells of X. citri subsp. citri found on infected plants (Stall et al. 1980). Behlau et al. (2007) and Leite et al. (1987) reported copper treatments reduced the incidence of citrus canker by 43.5% and 90%, respectively. The number of sprays necessary to control citrus canker depends on the susceptibility of the citrus cultivar and on climatic conditions (Kuhara 1978; Leite and Mohan 1990).

Conditions for transport

  • In 2008, MAFF informed Biosecurity Australia that the transport temperatures for fruit shipped from Japan to New Zealand and the USA are 4ºC and 6ºC, respectively. The voyage to these countries takes about two and four weeks, respectively. Bacterial multiplication occurs only above 14ºC (Koizumi 1976, 1985) and transport temperatures are therefore not conducive to the proliferation of citrus canker bacteria. However, citrus canker bacteria survive below zero temperatures during winter in Japan’s most northern citrus growing areas (refer to Table 3.3), which suggests that bacteria are likely to survive transportation at these temperatures.

Volume of trade

  • The expected import volume of unshu mandarin from Japan is estimated to be small, as the total area of the designated export areas (Areas 1–4) consists of only about 25 hectares. Export volumes of fresh unshu mandarin fruit to the USA from these designated export areas averaged a total of 230 tonnes per annum between 1995 and 2005 (APHIS 2006).

The unknown status of citrus canker and its hosts in the production area outside the designated export areas, moderated by the protected position of orchards, and the moderate resistance of unshu mandarin to citrus canker and the expected low volume of imports, support a risk rating for importation of ‘Low’.

Probability of distribution

The likelihood that X. citri subsp. citri will be distributed within Australia in a viable state, as a result of the processing, sale or disposal of fresh unshu mandarin fruit from the production area in Japan, is: VERY LOW.

  • Unshu mandarins would be distributed throughout Australia via wholesale and retail sale. The intended use of the commodity is for human consumption and waste material would be generated.

  • Successful transfer of citrus canker bacteria from infected peel to a host is likely to be limited, considering the following events need to coincide:

    1. Infected fruit peel would need to be discarded in close proximity to a susceptible host

Most fruit waste, including peel, would be disposed of by municipal garbage collection and therefore would be unavailable as a potential infection source. Some waste, of which the majority will be peel, may be discarded in compost bins or heaps. Fruit peel may also be discarded in gardens, along roadsides or within parks and other public places.

Citrus canker hosts, especially species of Citrus, are commonly grown in gardens and some as potted plants throughout Australia. However, citrus cultivation in built-up areas is limited to home gardens, as citrus is rarely used as an amenity plant.

    1. Viable inoculum would need to be present

Citrus canker bacteria can survive on a variety of surfaces including plastics, cloth, wood and metal for up to 48 hours under sun and 72 hours under shade conditions (Graham et al. 2000).

In soil, populations of citrus canker bacteria rapidly decline unless there is replenishment of bacteria from infected inoculum sources (Graham et al. 1989). Hence, there is limited potential for citrus canker bacteria to remain viable away from fruit or a host.

Exposure of infected fruit peel to antagonistic and predatory microorganisms, such as those associated with compost or soil, greatly accelerates bacterial cell death (Koizumi 1972; Goto et al. 1975b). Above-ground, the desiccation of citrus canker bacteria is accelerated by exposure to direct sunlight (Goto 1962, 1992; Graham et al. 2000). Epiphytic bacterial proliferation is epidemiologically insignificant (Timmer et al. 1996b). The available inoculum in or on infected fruit peel diminishes once fruit has been detached from the tree (see point 3, below).

The survival of X. citri subsp. citri bacteria in fruit peel of unshu mandarins was studied in the field during the cool and wet winter period in Japan. Results on the survival of X. citri subsp. citri bacteria were as follows: less than 2 months for specimens buried or left on the ground, 2.5 months for specimens left outdoors but not in contact with the ground, and about 5 months for specimens kept indoors (Koizumi 1972). This suggests a potential for the bacteria to persist in the environment if associated with infected fruit. However, Graham et al. (1989) report that in a study in Florida, USA, citrus canker populations rapidly declined in lesions on fruit on the ground or in infested soil. The proposed import of unshu mandarins into Australia coincides with summer, when climatic conditions would speed up the rate of decomposition.

Fresh citrus canker lesions are the primary source of inoculum, as the rate and number of bacterial cells exuding from infected tissue is higher from fresh than from older lesions (Timmer et al. 1991). Population levels of X. citri subsp. citri in visible lesions are higher than the levels associated with asymptomatic occurrences of bacteria on leaves and fruit (Rybak and Canteros 2001). Therefore, the possible inoculum levels on asymptomatic unshu fruit may be too low to initiate infections.

Xanthomonas citri subsp. citri bacteria die relatively quickly in lesions of early infected unshu fruit due to the formation of suberised tissue (phellogen), which forms a barrier between infected and non-infected tissue to inhibit further bacterial growth and spread (Koizumi 1972). Koizumi also observed that in late infections a combination of physiological changes associated with the ripening of fruit and the drop in temperatures during the autumn and winter period, effectively arrest the development of infected tissue (Koizumi 1972).

Bacteria need to actively ooze from the infected tissues to become available for transfer. This requires the infected tissue (in this instance the peel) to be wet for a minimum of 15 minutes (Goto 1962).

Bacterial proliferation depends on warm (>20ºC) and moist (>1000 mm/annum rainfall during the growing season) growing conditions (Koizumi 1976, 1985; Kuhara 1978). The multiplication of citrus canker bacteria occurs mostly in the margins of expanding lesions on leaves and fruit. Lesions are associated with visible symptom development. Asymptomatic fruit has not yet developed lesions and therefore is unlikely to release bacterial ooze. Multiplication of citrus canker bacteria ceases with abscission of leaves and fruit and with the onset of decomposition (Koizumi 1972; Graham et al. 1989; Goto 1992). There is no evidence that epiphytic bacteria on the surface of fruit persist in adequate numbers to provide sufficient inoculum to cause infection (Timmer et al. 1996b). Neither are there reports in the literature that fruit without visible symptoms at harvest would develop lesions after harvest (Graham et al. 2004).

    1. Free water is necessary to enable the transfer of bacteria from peel to a host

The transfer of bacteria is facilitated by rain splash (Gottwald et al. 1989, 1992). Xanthomonas bacteria, due to their mucilaginous coat, suspend easily in water and disperse in droplets. Wind speeds of more than 8.7 m/s are required to cause stomatal infection, as lower wind speeds rarely result in new infections (Serizawa et al. 1969). However, fresh wounds, such as those caused by the citrus leafminer, remain suitable infection sites without the requirement of pressurised water soaking (Chagas et al. 2001).

    1. Orientation of fruit peel

Fruit peel would have to have to face upwards to enable bacterial release during a wind driven rain event in the direction of an infection court. Bacteria in discarded fruit waste on the ground are less likely to be dispersed by wind or rain than bacteria on trees, because the waste is partly sheltered on the ground.

While host plants are common in commercial and domestic environments in Australia, the following events have to coincide for distribution of the bacterium to occur: warm weather, wind-driven rain, and sufficient citrus canker inoculum. These factors combined support the risk rating for distribution of ‘Very low’.

Probability of entry (importation  distribution)

The likelihood that X. citri subsp. citri will enter Australia and be transferred in a viable state to a susceptible host, as a result of trade in fresh unshu mandarin from the production area in Japan, is: VERY LOW.

      1. Probability of establishment

The likelihood that X. citri subsp. citri will establish in Australia, based on a comparison of factors in the source and destination areas considered pertinent to its survival and reproduction, is: HIGH.

  • Australia’s diverse citrus industry would be susceptible to citrus canker, specifically the production of highly susceptible citrus such as Citrus sinensis cv. Navel (sweet orange), C. paradisi (grapefruit), C. limon (lemon) and C. aurantifolia (lime).

  • Existing pest management practices are unlikely to have an effect on the establishment of of citrus canker. Chemical control is difficult, as copper fungicides only give limited control, and importance is placed on the prevention of primary infection (Kuhara 1978; Serizawa and Inoue 1983).

  • However, the natural infection period of hosts is limited, as infection is primarily associated with expanding plant tissues such as leaf flushes and early fruit development (90–120 days after flowering) (Koizumi 1981; Gottwald and Graham 1992; Graham et al. 1992b). Resistance of fruit and leaves to citrus canker increases with the development of a waxy cuticula (Canteros 1992; Goto 1992). Alternatively, the pathogen requires wounds as entry sites.

  • Wet, warm weather simultaneously with wind speeds exceeding 8.7 m/s, such as experienced during rain storms, aid in the release of bacteria from infected tissue and their transfer and penetration through stomata or wounds (Serizawa et al. 1969; Gottwald and Graham 1992; Graham et al. 1992a). Intercellular spaces of plant tissues are generally filled with air, but under certain conditions (i.e. wind-driven rain, rainstorms etc) become filled with water. Such water congestion favours infection with bacterial pathogens (Gottwald and Graham 1992). It is recognised that fresh wounds remain suitable infection sites without the requirement of pressurised water soaking (Chagas et al. 2001).

  • Citrus leafminer (Phyllocnistis citrella), which through its leafmining damage aids in the establishment of the pathogen (Gottwald et al. 1997; Chagas et al. 2001), is widely distributed throughout Australia (Herbison-Evans and Crossley 2004).

  • Citrus canker can survive in diseased plant tissues, as long as cells in the vicinity of the lesion remain viable. Overwintering lesions are the most important source of inoculum for the following season (Koizumi 1977).

  • Citrus canker is primarily known to occur in tropical and subtropical climates where high temperatures and rainfall occur at the same time such as in South-east Asia, Pacific and Indian Ocean islands, and South America. It is also reported from drier, more temperate areas in South-west Asia and the Middle East (CAB International 2007).

  • In Australia, an outbreak of citrus canker occurred in the Northern Territory in 1991 and in 1993; official eradication was declared in 1995. A more recent outbreak occurred in Emerald, central Queensland, in late 2004, demonstrating that suitable environments for citrus canker occur in Australia, especially in the northern Australian production areas. This outbreak occurred in an isolated area and eradication was officially announced on 23 January 2009 (IPPC 2009).

  • Broadbent (1992) assessed the potential of citrus canker to cause infection under Australian conditions, evaluating the climatic parameters and leaf flushes at the major citrus growing regions within Australia. Conditions in the tropical (Torres Strait and Darwin) and subtropical (Central Burnett) region in southern Queensland and central New South Wales (Kulnura) citrus growing regions would be suitable for disease development. In the tropics a major growth flush occurs in October, which coincides with the onset of the wet season during summer. Citrus in the Burnett region and around Kulnura flushes in early November when temperature and rainfall are increasing. Conditions may also be suitable at Carnarvon where citrus is grown under irrigation and suitable temperature regimes occur for most of the year.

Past outbreaks of citrus canker in areas of northern Australia, a wide distribution of citrus host plants throughout Australia, and the ability for citrus canker to survive in diseased plant tissues all support a risk rating for establishment of ‘High’.

      1. Probability of spread

The likelihood that X. citri subsp. citri will spread within Australia, based on a comparison of those factors in source and destination areas considered pertinent to the geographic distribution of the pest, is: HIGH.

  • Citrus canker is mostly found on Citrus species and citrus relatives, including Fortunella and Poncirus (PHA 2004a). Cultivated citrus species are widespread in Australia. Native hosts, such as C. glauca, occur widely throughout arid and semi-arid inland eastern Australia from northern Queensland and southern New South Wales to the Flinders Ranges in the west (Mabberley 1998; QDPIF 2006b; APNI 2008). Citrus glauca may provide a host in irrigated inland areas west of the Great Dividing Range (QDPIF 2006b).

  • An infected host plant is rarely killed by citrus canker and infected host tissue can provide an inoculum source contributing to the spread of the pathogen for many years (Gottwald et al. 2001; Schubert et al. 2001).

  • Xanthomonas bacteria, due to their mucilaginous coat, suspend easily in water and disperse in droplets. The bacterium can spread over short distances by rain, irrigation, wind and contaminated harvesting and packing boxes and other equipment (Pruvost et al. 1999; Graham et al. 2000; Gottwald and Graham 2000). Weather events such as thunderstorms, tornadoes, tropical storms and hurricanes contribute to medium to long distance spread from the original source of infection (Gottwald et al. 2000, 2001, 2002b; Gottwald and Irey 2007). Overhead and spray irrigation contribute to in-field spread of the pathogen (Pruvost et al. 1999).

  • A study of the spread of citrus canker bacteria under typhoon conditions was carried out in Japan (Serizawa et al. 1969). Satsuma seedlings (C. unshiu) at a distance of 5.7 m from a highly infected, young citrus tree showed signs of infection when a typhoon incurred precipitation of about 70 mm of rain/day and wind speeds between 12.0 and 17.3 m/s for about 4 hours to the study area. The disease generally developed in wounds or injuries caused by leafminer (Phyllocnistis citrella). Lower wind speeds (i.e. that of 8.7 m/s) rarely resulted in new infections (Serizawa et al. 1969).

  • In Florida in the USA, eradication of all citrus canker hosts within 1900 ft (579 m) from an infection source was not sufficient to contain the spread of the pathogen in areas affected by hurricanes. This subsequently led to the abandonment of the citrus canker eradication campaign in Florida (USDA 2006). The 1900 ft rule was based on research that indicated that in most instances inoculum forms infection foci that would be contained within this distance (Gottwald et al. 2000). Extrapolations on the spread of the pathogen by hurricane storm fronts in the Florida region indicate that the pathogen may have spread under such conditions as far as 17.9 km from the infection source (Gottwald et al. 2000, 2001, 2002b).

  • Experience from Argentina has shown that citrus canker spreads swiftly under subtropical conditions and was known to occur in all areas of north-eastern Argentina within about 10 years of its first detection. This included infection of even isolated citrus trees in urban areas (Canteros 2000).

  • The tropical and subtropical environments in Australian citrus production areas would favour the spread of citrus canker (Broadbent 1992).

  • An industry contingency plan for citrus canker incursions has been developed. However, monitoring for citrus canker would only commence from the time of detection. Hence the bacterium may have already spread widely.

Suitable climatic conditions, specifically in northern Australia, the wide distribution of citrus host plants throughout Australia and the fact that infected plants are not naturally killed and could provide an inoculum source for many years, all support a risk rating for spread of ‘High’.

      1. Probability of entry, establishment and spread

The likelihood that X. citri subsp. citri will be imported as a result of trade in fresh unshu mandarin fruit from the production area in Japan, be distributed in a viable state to a susceptible host, establish and spread within Australia, is: VERY LOW.

      1. Consequences

Assessment of the potential consequences (direct and indirect) of X. citri subsp. citri for Australia is: HIGH.


Estimate and rationale


Plant life or health

Impact score: F – significant at the national level

Citrus canker decreases the marketability of fresh table fruit by causing skin blemishes and can drastically decrease yields by causing premature fruit drop and severe defoliation (Kuhara 1978). It is one of the most economically damaging diseases of citrus worldwide (PHA 2004a).

Once the pathogen has caused infection of a host, it cannot be eliminated from the tree by chemical or other treatments (Stall et al. 1987). Eradication of infected and exposed host plants is general practice.

After establishment, the pathogen disperses rapidly by wind-driven rain, flooding, overhead irrigation, water run-off, contaminated tools, machinery, hands, shoes or clothing. The spread of the disease is rapid. Citrus canker spread swiftly throughout north-eastern Argentina within 10 years from its first detection. This included isolated citrus trees in urban areas (Canteros 2000).

The disease would cause most damage in tropical and subtropical regions of Australia where favourable conditions for the establishment and spread of citrus canker occur year round. An outbreak of citrus canker in the larger production areas in south-eastern Australia could lead to the complete loss of production for a number of years. Replanting and full fruit production could only be re-achieved, assuming that eradication would be successful.

Citrus relatives are widely distributed in Australia and some of these species have been shown to be susceptible to citrus canker when inoculated under field and laboratory/greenhouse conditions (Peltier and Frederich 1920, 1924; Reinking 1921). However, extensive surveillance in the recent citrus canker outbreak area at Emerald in Australia did not detect citrus canker on the native species Citrus glauca that occurred in areas where infection levels were high (QDPIF 2007a).

Other aspects of the environment

Impact score: A – indiscernible at the national level

There are no known direct effects on the environment.


Eradication, control etc.

Impact score: E – significant at the regional level

Monitoring and surveillance will result in extra costs to citrus growers and eradication is an expensive option. Expenditure on the citrus canker eradication campaign in Emerald, central Queensland, which commenced in July 2004, was estimated to be about $A20 million (QDPIF 2007b). More than 500,000 citrus trees and other hosts were removed (QDPIF 2006a, 2007b). Citrus canker was declared eradicated from the Emerald region on 23 January 2009 (IPPC 2009). As of this date, Australia is free from citrus canker.

The USA government spent US$100 million on an attempted eradication of citrus canker from 1996–1999 in Florida. In 2000, the program was broadened to US$145 million (Schubert et al. 2001) before the United States Department of Agriculture stopped funding in early 2006, declaring citrus canker in Florida ineradicable (DOACS 2006).

In areas where citrus canker has become established, highly susceptible citrus varieties, such as grapefruit (C. paradisi), lemons (C. limon) and sweet oranges (C. sinensis), particularly Navel oranges, will have reduced economic viability due to the requirement for multiple bacterial sprays per year to maintain yields and quality (Gottwald et al. 2001; Schubert et al. 2001).

A change in production systems is also likely to be required such as the introduction of drip irrigation, increased orchard hygiene, regular sanitation of workers, machinery and tools and the likely establishment of windbreaks (Schubert et al. 2001).

Domestic trade

Impact score: E – significant at the regional level

The presence of X. citri subsp. citri in commercial production areas would have a significant effect on interstate trade due to the increased needs for surveillance, certification and disinfestation. Restrictions to trade are likely to significantly impact domestic markets. Furthermore, the removal of commercial citrus trees would lead to the complete loss of production in some regions for some years until replanting and full fruit production would be re-achieved.

The presence of citrus canker would prevent plant nurseries from selling or moving citrus canker host plants to regions free from the pathogen.

The citrus industry is Australia’s largest horticultural industry. The industry had a farm gate value of more than A$400 million per year over the past decade; 60% of the overall farm gate value derives from domestic sales (ACG 2006, 2007).

Whilst the direct costs associated with the citrus canker eradication campaign in Emerald were about $A20 million (QDPIF 2007b), the indirect costs to the industry, associated industries, marketers and to the public (consumers) as a whole were much larger, but no specific data is available.

International trade

Impact score: E – significant at the regional level

The presence of X. citri subsp. citri in commercial production areas of citrus commodities would have a significant effect on international trade due to limited access to overseas markets where this pest is absent. Australia currently exports 20% of fresh citrus commodities to markets that are free from citrus canker (PHA 2004a).

Australia’s citrus industry consists of a number of discrete production areas. Experience from the citrus canker outbreak in Emerald in 2004 has shown that a number of trading partners prohibited the import of citrus fruit or demanded additional assurances for trade to resume.

Citrus exports generated over A$150 million dollars for the 2004/05 financial year, which is about 40% of the gross farm gate value (ACG 2006). Export trade of about A$30 million dollars could be affected in an event of a citrus canker outbreak.

Whilst the direct costs associated with the citrus canker eradication campaign in Emerald was about $A20 million (QDPIF 2007b), the indirect costs to the industry and associated industries and marketers involved in international trade exceeded the direct costs, but no specific data is available.

Environmental and non-commercial

Impact score: C – significant at the local level

Additional control activities would be required to control citrus canker on native host plants, which include species within Citrus and other genera (QDPIF 2006b). Experience from the citrus canker eradication campaign in Emerald showed that control of suspected native hosts (such as Citrus glauca) was labour intensive. The impact on the environment is likely to be significant at the local level and of minor significance at the district level.

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