Draft Report for the Review of Biosecurity Import Requirements for Fresh Apple Fruit from the Pacific Northwest States of the United States of America

Support for Growth

Draft report for the review of biosecurity import requirements for fresh apple fruit from the Pacific Northwest states of the United States of America

Submission by Apple and Pear Australia Ltd January 2021

Draft report for the review of biosecurity import requirements for fresh apple fruit from the Pacific Northwest states of the United States of America

Submission by Apple and Pear Australia Ltd 21 January 2021

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

Summary

The Draft report for the review of biosecurity import requirements for fresh apple fruit from the Pacific Northwest states of the United States of America (the Review), has been reviewed by APAL and does not meet the benchmark of acceptable international standards for scientific analysis and risk assessment. Founded in places on misinterpreted or outdated science and containing both significant omissions of relevant information, and conflicting arguments, APAL argues that the Review unacceptably understates the risk posed by many of the pests listed.

A full and comprehensive reassessment is required for both the pests for which a full pest risk assessment has been conducted and also for those listed in Appendix A and determined as requiring no further assessment. Furthermore, the proposed mitigation measures are vague, unsupported by data and in some cases conflict with those already in existence for the same pest for other trading partners.

Specifically, APAL considers that the Unrestricted risk estimates for the following species are understated and require reassessment:

• Spider mites (Tetranychus mcdanieli, T. pacificus and T. turkestani) • Apple curculio (Anthonomus quadrigibbus) • Apple fruit moth (Argyresthia conjugella) • Lygus bugs (Lygus hesperus) • Lacanobia fruit worm (Lacanobia subjuncta) • Coprinus and other postharvest fruit rots In addition, the ratings for spider mites, apple curculio, apple fruit moths and lygus bugs are inconsistent with those of Australia’s trading partners, including in some instances the United States (USA) itself. Mitigation measures for fruit moths are in direct conflict with existing Australian Import Biosecurity Conditions for New Zealand (NZ) fruit, and also with Western Australia’s entry requirements.

The ratings and mitigation measures for a number of pests are also inadequately aligned with existing regulations or inadequately evidenced, including those for fire blight, leaf curling midge and European canker.

The Review also notes a number of pests that are absent from Australia but were deemed to not warrant a Risk Analysis. This includes a number of pests which are of major concern in apple production and APAL requires a more detailed explanation as to the reason for their exclusion from further risk analysis. In some cases, these are restricted pests that warrant mitigation measures in the USA but for which Australia sees no need (eg. Plum curculio).

These include:

• Rust mite (Aculus malivagrans) • Apple blister mite (Eriophyes mali) • Plum curculio (Conotrachelus nenuphar) • Apple aphid (Aphis pomi) • Rosy apple aphid (Dysaphis plantaginea) • Double dart moth (Graphiphora augur) • Fisheye rot (Butlerelfia eustacei) • Apple decline (Valsa ceratophora)

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

Introduction

This submission by APAL comprises:

1. General comments that apply throughout the Review. 2. Comments on Chapter 3 and its observations on apple production in the Pacific Northwest (PNW) of the USA. 3. A detailed examination of Chapter 4 with particular consideration of the Unrestricted risk estimates (URE) for those pests that the Department of Agriculture, Water and Environment (the Department) considered did not breach Australia’s Appropriate Level of Protection (ALOP). 4. Consideration of pests that the Department determined were potential quarantine pests (Appendix A) but were not considered further for various reasons. 5. Other potential pests and diseases that were not covered in the Review, but which may pose a quarantine risk for Australia. 6. Proposed mitigation measures and trade.

Wherever possible this submission follows a similar chronological order to that of the Review and relates comments to specific areas. However, where Review content is repeated under several sections, APAL comments have application across multiple areas and pests.

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

1. General comments APAL notes, that in framing this Review, the Department has drawn upon existing policy and evidence presented therein to support many of the arguments relating to risk. Secondly APAL acknowledges that the Department is also constrained for some pests (e.g. fire blight) by the ten-year-old rulings from the World Trade Organisation (WTO) in 2010.

APAL recognises that once policy has been determined it can be difficult to change, however the failure to re-examine or update earlier assumptions risks drawing erroneous conclusions based on flawed, misinterpreted (see General Technical Comments) or outdated science and is an example of the systematic lack of rigour that is so evident in the current Review. With respect to the WTO, ten years have elapsed since the original decision and during that time there have been significant advances in science, orchard and post-harvest practices, and in genomics and diagnostics, all particularly relevant to risk analysis. This raises the question; at what point are such decisions reviewed or updated to reflect subsequent science and how is this process conducted? Furthermore, who has responsibility for ensuring WTO decisions remain contemporary? APAL submits that as the current Review draws heavily upon earlier Pest Risk Analyses that were informed by the WTO ruling these should have been re-examined with reference to contemporary science.

In the current Review for PNW-USA apples, APAL finds substantial flaws that undermine many of the conclusions presented and the resultant Unrestricted risk estimates. The standard of the Review does not meet industry’s expectations of a robust and scientifically vigorous risk analysis.

The major concerns are summarised below:

a) Lack of rigour and consistency including inferences not supported by data and misinterpretation of scientific reports/papers b) Information about pests is not accurately reported and as a consequence the risk for many pests is understated or inadequately assessed c) Incomplete referencing and inadequate follow-up of contemporary science subsequent to the 2008 USA Import Risk Assessment (IRA) d) Lack of understanding of commercial orchard management e) Lack of data to support the efficacy of the standard orchard management protocols in the PNW when applied to meet Australia’s different MRLs f) The equivalencing of risk associated with stone fruit to that from apple has not been justified g) Equivalencing risk management from the USA with that from NZ and China requires better evidence for validity h) Lack of awareness of industry concern regarding certain exotic pests and the biosecurity threat they pose (and the significant eradication costs that would be incurred should they enter the country) i) Inconsistency in categorising risk within and between pests j) Evidence for or against risk is not clearly delineated k) Australia is accepting risks from the USA which the USA does not accept on its own imports l) Inconsistency between international trade and Australian interstate trade requirements.

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

General referencing and administrative comments

The referencing is incomplete and inaccurate, a serious shortcoming that meant that, in considering this Review, a large amount of time had to be devoted to verifying and checking claims made in the Review. From this checking it was found that:

• citations are incorrect when referencing a paper which quotes another paper. This gives the impression that author had made a claim when in fact he/she was merely repeating what someone had said elsewhere. A more correct method in such cases is as follows; Lowe (1993) in Smith and Chapman (1995). • many links provided for references, especially URLs, do not work. A random sample showed more than 50 per cent failed and the date on which they were accessed is not shown. It appears to the reader as though many references were not updated from the earlier (2008) Review and are either no longer available or may have been superseded by more recent publications raising the question of whether the Review is based on the most up-to-date available science. This would appear to be particularly the case for handbooks, manuals, extension materials, personal communications and such like. • remarks attributed to authors do not match the reference provided e.g. Mellot 2019 p. 61 • a number of instances were found where information critical to risk appears to have been overlooked in papers that were cited for other reasons. This conveys the impression of selective quotation. • more supporting evidence around existing measures and their efficacy could have been provided, for example for stone fruit or apple imports, both in terms of regulated and unregulated pests. Simple editorial mistakes also mar the credibility of the document including:

• presenting pests in a different order in different tables and in text (cf. Table 4.1 and 5.1 and text in Ch 4.) • incorrect referencing of Table 3.1 on top of p. 31 where 3.2 is quoted • page 26 paragraph 4 – Pandemis hesperana (sic) is listed in the text but not in Table 3.1 Pests of apple trees in PNW. • should this be Pandemis heparana rather than Pandemis hesperana? • p. 31 Codling moth is a ‘lepidopteran’ not ‘lepidoperan’

General technical comments

Australia’s stance on a number of pests differs from that of other trading partners including even the USA. New Zealand regards spider mites as requiring risk mitigation whereas the Review does not. Similarly, plum curculio is seen as a risk for apple producers in the PNW and there are control measures in place, according to the Review (p. 52). However, the Review finds that no specific control measures need to be applied for imports to Australia. This is is counter-intuitive and at the very least warranted comment from the Department as to reasons for the different stance between Australia and the USA. The Review quotes heavily from risk analyses for other countries, however, fails in these cases to provide sufficient evidence as to why the risk is similar, for example, similarities in pest incidence, weather data, topography, varieties, orchard systems etc. all of which have an influence upon the likely risk posed by a pest. More detail is requested to demonstrate the relevance to the Australian situation of the cited cases.

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

Of particular concern is the equating of risk from stone fruit with that for apples on the basis that they are “morphologically similar” (p. 183). This equivalencing is then often used to transfer ratings from previous stone fruit risk analyses across to those for apples. This is both a false and dangerous equivalence. Apples have a calyx and in some varieties this can be open, making it relatively easy to access the core. Both the calyx and the core provide known refuges for a number of pests and pathogens. Stone fruit have no such external structure.

In checking previous risk analyses a number of instances were detected where cited authors have been misinterpreted in what they wrote, and this has been directly transferred across to this Review. Thus, not only is the earlier risk analysis misinterpreting the science, but this error is used to underpin the findings of the present Review. This then begs the question as to whether any cross-checking of the information occurred and throws doubt upon the validity of the risk ratings in earlier Pest Risk Analyses and the consequent policy. The areas listed above, at the very least, reveal a lack of diligence and rigour and call into question the validity of the entire document. As will be highlighted in assessing individual pests, this has the potential to expose Australia to significant risk of importation of exotic organisms.

For all those pests for which previous ratings exist and are associated with current imports the provision of interception data etc. would provide a greater degree of comfort to Australian horticultural industries as to both the effectiveness of existing measures and also the accuracy of risk estimation.

There is a lack of both clarity regarding the rationale for using data from one species to support expected outcomes in another and consistency in the way this approach is applied in the Review. The Review makes abundant use of data from different species, even genera, on the basis that it is assumed they have similar responses, and in other instances separates organism behaviours from different species. In both cases no or little rationale is provided for what appears to be arbitrary assignment.

There is a great reliance in the Review on waste disposal to remove infected fruit out of circulation and thus minimise risk. There are two issues here and both are germane to risk:

• The first is that many of the organisms are capable of long latency periods and the reason for their inclusion is that the apple fruit may not exhibit obvious symptoms. • The second is that different methods of waste disposal for fruit are attributed for fruit infected by different pathogens and different insect pests. APAL queries the legitimacy of this approach. Arguments are poorly articulated and often contradictory making it difficult to determine whether statements are supportive or contrary to the stated level of risk.

The assignment of risk for pests is inconsistently applied within this document and from other risk analyses and, because the same reasoning is repeated, where this reasoning was initially unsound the same mistake is continually repeated each time the argument is used. The provision of a table clearly setting out the arguments (pro and con) and the degree to which they apply to each pest would make assessment of risk basis more transparent and significantly. As currently constructed the risk discussion sections are confusing, opaque and obfuscate when it comes to determining the outcome.

It is also APAL’s view that the discussion on consequences, where present, and also where previous assessments have been utilised, often understates the impacts based on the evidence cited.

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

2. Chapter 3

APAL is of the view that more current evidence that reflects commercial orchard and post- harvest practices is required before the Department can draw any conclusions regarding the risks and their management through the export pathway. The chapter exposes a serious lack of understanding of commercial orchard practice and it is clear many of the pest control measures mentioned are lifted from home garden texts rather than reflecting commercial orchard practice. Some of these are highlighted below. p. 18 – The Review indicates commercial practices are already in place for fire blight, leaf curling midge and European canker, references Table 3.2 and notes that:

“This approach is consistent with the risk assessment for these three pests in apples from New Zealand (Biosecurity Australia 2011b).” There is little evidence provided to substantiate and equate either the pest levels in the two countries or the efficacy of the controls, particularly as elsewhere in the Review it is acknowledged that there have been serious outbreaks of fire blight in recent years and, as is discussed under the individual pests in this response, these three pests have been difficult to control. APAL was unable to find much discussion in the Review as to the seasonal variation in pest pressure in the PNW or on changes in risk and pest threshold levels. Commercial experience is such that under some conditions it is just not possible to achieve a satisfactory level of control of an individual pest. It would therefore seem prudent to set some thresholds at which risk becomes unacceptable. p. 24 para 2 – States that bees, to provide pollination services, are transported from outside the area (California). Was an assessment conducted to assess the risk of virus transmission through contaminated pollen and hives? Several viruses reported in the PNW have been reported to be pollen transmitted including apple latent virus, tomato ringspot virus, apple mosaic virus.

What measures are in place in the PNW to ensure honey bees/hives that provide pollination services are clean and virus free?

Arthropod pest management

This section appears to be taken from a gardening manual rather than commercial production systems. Many of the treatments which the Review quotes for various pests and diseases are only found under the home garden section of the PNW Pest Management Handbook. The content of this section seriously undermines the credibility of the Review. p. 26 para 4 – Pandemis hesperana (sic) is listed in the Review text but not in Table 3.1 Pests of apple trees in PNW. Presumably this is Pandemis heparana? p. 26 – Granulosis virus is reported in the Review to be used to manage codling moth; The product containing the virus needs to be ingested by the larvae to be effective. According to Australian entomologists (https://extensionaus.com.au/ozapplepearipdm/is-granulosis- virus-effective-in-controlling-cm/ Accessed 11.01.2021), larvae often spit out the first bite of the apple (i.e. the skin where the virus product is located) and then burrow into the apple. How effective is this product in commercial orchards in reducing codling moth and how widely is it used? There are also reports of several types of resistance to granulosis virus in Cydia pomonella. Does this occur in the PNW-USA? Is there any data to verify the effectiveness of the control methods?

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

p. 26 – The fourth paragraph states that broad spectrum insecticides are avoided. How does this reconcile with Table 3.2 where pesticides such as Carbaryl and Azinphos-methyl are mentioned?

The same paragraph states that “heavy rain and cold weather also suppress mite numbers”. How reliable and effective is waiting for heavy rain and cold weather in reducing mite numbers in a commercial orchard? Furthermore, as will be noted under ‘mites’ in the next section, orchard practice is cited in some references as encouraging a population build-up of these mites to help maintain adequate numbers of predatory species. It is difficult to understand from such contradictions as to what the Review is actually stating. p. 26 – Wiman, Stoven & Bush 2019; reference link does not work.

The following examples of arthropod pest management do not appear realistic for a commercial orchard that plans to export fruit. How many commercial, export ready orchards are using these methods, how effective are they and how is efficacy of such methods monitored?

• p. 26 – last paragraph how many growers physically remove egg cases or larvae (p.27) from fruit? • p. 26 – last paragraph; how many growers use a flashlight to hand-pick nocturnal cutworm larvae from their orchards? Is this effective and profitable? • p. 27 – Lacanobia fruit worm larvae “…can be hand-picked when thinning fruit”; are workers trained in identifying the larvae? How efficacious is this in a large-scale commercial orchard? The discussion on p. 27 notes several measures that may mitigate mite populations. Will they be part of any orchard approval program?

Do commercial orchards routinely wash mites from trees with a strong stream of water? If so, does this kill mites, or do they go back up into trees when the water stream has been removed? And what impact does that have on the susceptibility of apple trees and/or fruit to other pests and diseases e.g. via wounding enabling infection by pathogens, wet conditions to encourage pests/diseases? p. 27 para 3 – refers to physically removing codling moth-infested apples; again, how feasible is this in commercial situations? This is reported for small orchards. What is the average size of an orchard that will be exporting apples to Australia and what do they use to manage codling moth? How is it monitored?

Mating disruption is presented as an alternative to physically removing codling moth-infected fruit and as successful when orchards are larger than 10 acres (4ha). What is the size of the orchards that will be exporting apples? Are alternative methods used in orchards that are less than 10 acres in size? What verification/auditing/traceability systems are in place to ensure that the codling moth management systems that are being used are effective. The information presented in the document does not instil much confidence in either of the two methods and further details are requested. p. 27 – The Review states that spider mites can be reduced by avoiding dry and dusty conditions. This raises several questions. How common are dry and dusty conditions in the PNW? How do growers in the PNW avoid dry and dusty conditions? The Review mentions that cover crops are planted to reduce dust. How common and efficacious is this? What are these cover crops and what effect do they have on this pest and other insect populations? Supporting evidence is requested around this.

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

p. 27 - Paragraph 4 states that cultural control of lygus bugs is achieved through elimination of weeds that serve as protection and early season food for the insect. How does this differ from the habitat provided by cover crops planted to reduce dust? This would appear to directly contradict the management practices cited in the previous paragraph. p. 27 para 4 – according to the PNW Pest Management Handbook many mites are encouraged up to a point so as to facilitate populations of predatory mites. Clarity is requested around this and its impact upon risk, and also reconciling this with earlier statements in the Review on controlling mite populations. p. 27 – the first paragraph about apple maggots has been copied almost directly from the PNW Pest Management Handbook. Was the information fact checked? The paragraph provides historical information about how apple maggot came to be in the PNW but little information to support the risk assessment. p. 28 – Beers, Antonelli and LaGasa (1997) (the reference link doesn’t work). This is a very old (23 years) reference for a trapping grid. Is more recent information available about trapping grids and the traps used in 2020 or is the same system still being used? p. 28 – Further detail is requested about the current distribution of apple maggot in the PNW to demonstrate efficacy of control measures used. The areas within the PNW where apple maggot is reported to be present are referenced from Yee et al. (2012); this is an eight-year- old reference; has the maggot spread since then? Has this reference been checked against the list of counties currently covered by the current prohibition of fruit movement for apples? If so, is there any change? APAL requests further evidence around the efficacy of current control measures. There has been no evidence presented as to how this pest has behaved since it first appeared in the PNW. According to Bush et al. (2005) apple maggot has spread and infected many parts of the apple growing areas in the PNW. Furthermore, although the reference of Bush et al. (2005), is cited in the Review the information about spread was not. It would also have been far more informative for the Review to have published a distribution map of apple maggot as it currently exists as well as detailing any spread that may have occurred since its arrival in the PNW and also since 2012. p. 28 – At the end of paragraph 2, the Review states “this technique is not effective against high levels of fly populations”. More information is requested around what is used to manage the apple maggot under these conditions. Wiman et al. (2019) (accessed online 8.12.20) It also reports that “a low fly population may not be detected using the traps, so place the trap in a location where there is a history of activity or damage to best represent emergence timing.” More information is requested around how is this managed in commercial orchards to ensure efficacy. p. 29 – Clarification is requested about the definition of what are referred to as ‘commercial fruit’ in the case of commercial cherries, pears and other fruits that are exceptions to the regulations, and how these are treated in comparison to ‘non-commercial’ fruit? p. 31 – The leaf curling midge distribution reference (CABI EPPO 2008; this link does not work) provided in the Review is from 2008; this is 12 years old. More current information is requested about the distribution of apple leaf curling midge in the PNW and if/how it has changed since 2008. This would demonstrate efficacy, or otherwise, of the current control measures used and affect the risk assessment. APAL notes that the midge was first detected in 1991 in Whatcom County (Eddy 2013). Has the geographic range of the midge expanded since then? Again, a map would be of assistance.

The discussion of fire blight management on page 31 requires clarification and further information, specifically:

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

p. 31 et seq. – This data presented in the Review (e.g., Dupont et al. 2019) suggests that fire blight is not controlled very well at all. Dupont et al. (2019) and Dupont (2018, 2020) note losses of US$222m in 2018 due to fire blight and provide management recommendations. We question current data on the level of infection in the PNW compared with NZ. The frequency of outbreaks reported in the PNW are not suggestive of good control. Further information is required about the severity of these outbreaks and what this means for fruit infection and risk and needs to be addressed in risk mitigation measures.

Aćimović et al. (2015) reference Stockwell et al. (2002) to report that in Washington and northern Oregon, economic losses on pome fruits due to fire blight were over $68 million. This (Aćimović 2015) is not cited in the Review. The measures for PNW and NZ management of fire blight need to be examined against a background of disease incidence and severity between the two countries. Resistance to streptomycin, an antibiotic used to manage fire blight, has been reported in the Erwinia amylovora population in the USA. Further information is requested about how this, and the potential of antimicrobial resistance (AMR) developing against other antibiotics used in crop protection, is managed and what is the risk of resistant strains of Erwinia entering Australia. p. 31 – The Review provides information about the frequency of outbreaks for fire blight. Why can this not be provided for the other pests in the Review document? APAL also queries why if levels of fire blight fluctuate to the extent cited then why is there no discussion in the Review about threshold levels and risk? p. 31 – Clarification is requested about the difference between a minor outbreak and a serious outbreak of fire blight? p. 31 – Further information is requested about the implications of 5–10% damage to plants in terms of infectivity, yield and occurrence of the pathogen on fruit? This figure needs to be related to fruit infection or risk to be of value to the risk mitigation assessment. p. 31 – Smith (1999) and Smith (2006); The risk prediction models presented in the Review are out of date. Further searches found that WSU has recently updated the models and included information in Decision Aid. Further information is requested around the uptake, use and impacts on pest incidence and disease severity of these models. pp. 35-38 – This section of the Review discusses packhouse processes and control measures, but little detail is provided about the actual measures themselves. This raises a number of concerns which are of direct relevance for meeting the proposed risk management measures. These include packhouse sanitation, fruit treatment and segregation after grading. As noted earlier the importance of threshold levels and risk has also been ignored. Furthermore, the treatments in the packing shed that are described in the Review are referenced to University publications and further information is requested about how the actual practice was verified against what is stated? p. 36 – The Review cites Washington State University (2018b) that chlorine solutions of 100 ppm are applied to wash apples. Is this concentration what is used in practice? Further information is requested around whether this refers to residual chlorine and whether this concentration of chlorine is effective at killing the pathogen (including their infective propagules) listed in the Review for the contact time that is used. Pathogens and pathogen structures have been shown to differ in their sensitivity to chlorine. Will chlorine concentration and pH monitoring of dump/wash tanks form part of any QA system and would that be auditable?

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

p. 36 – references for post-harvest practices include Kupferman (1996, 2001) – these are very old references; post-harvest technologies have advanced significantly over the last 25 years. Has anything changed in the USA? More information is requested about the current post- harvest technologies and practices (e.g. such as washing, grading of fruit and efficacy in removing pests) in the USA since these publications. p. 36 – More information is requested about how frequently state/federal QC officers and inspectors examine fruit? What are the processes and protocols when fruit does not pass examination? p. 36 – are the treatments applied before or after packing and prior to or during transit? p. 38 – The Review states that “Most packing lines are cleaned and sanitised daily”. Clarification is requested around what defines ‘most’? What are the implications if they are not and how is this monitored? p. 38 – In section 3.6.2 Transport, the reference for Washington State University (2019) does not mention transport to Australia and is irrelevant to the information presented. p. 39 – In this chart (Figure 3) fruit is inspected by ‘in-house’ QC officers. What is the role and involvement of the state and federal inspectors mentioned earlier in the Review (p. 37) compared with the role of the in-house QC officers? p. 40 – Section 3.7.2 Export statistics. Further details are requested about the availability of data for numbers of interceptions of pests/diseases in these exports. This would support the assessment of the effectiveness of control measures that are used in the PNW and what the risk is to Australia.

For most pests/pathogens the Review, when considering likelihood of distribution and establishment, relies heavily on the principle of fruit showing symptoms of being infected/infested by the particular organism. This is a flawed assessment. The asymptomatic behaviour is the reason why a number of these pests are considered risks. Further details are requested about how asymptomatic risk is addressed. Little detail is provided in the document.

APAL notes that there is little detail provided in the Review to indicate how fruit destined for Australia will be managed in the packhouse after grading and packing. Will all fruit be sealed in cartons or will there be loose fruit as well? How will potential post-packing contamination be avoided both for apple-specific pests but also potential hitchhikers such as brown marmorated stink bug (BMSB, Halyomorpha halys). APAL notes that grading and packing will occur at the same time as BMSB is seeking refuge sites for winter hibernation. What measures will be in place to ensure packed pallets and product destined for Australia is quarantined prior to loading to avoid this type of ‘hitchhiker’ pest?

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

3. Chapter 4 Specific pests Comment is generally provided only on those pests/pathogens for which no measures are promulgated as the Department considered that the unregulated risk is believed to meet Australia’s ALOP. A general comment is that where existing measures are quoted why is there little supporting data from quarantine interceptions etc. on imported material? More detail around this may then support the existing or proposed measures.

Spider mites

APAL does not believe the Review adequately demonstrates clear and consistent evidence or associated rationale for assessing spider mites as presenting no risk (Very low) against Australia’s ALOP.

Inconsistent assessment of risk

There appears to be a contradiction around the risk posed by spider mites (rated as Very low) when compared with that for Cenopalpus (flat mite; rated as Low and therefore requires risk mitigation).

• The Review relies on the previous Assessment for stone fruit and yet acknowledges that spider mites can be found on apple fruit and in the same locations as Cenopalpus. • Wiman et al. (2019) consider spider mites to be widespread in the PNW-USA apple production areas and that they can be associated with apple fruit in egg, nymphal and adult life stages (Curtis et al. 1992). Yet, the Likelihood of Entry for flat mites and spider mites is rated as Moderate and Low, respectively, with an URE of Low and Very low (Table 4.28). APAL queries how and why, based on this evidence, the risk assessments for these two pests are different, despite apparently similar biological behaviour. No evidence has been provided as to why the consequences from spider mite establishment in Australia should be rated differently (cf. moderate for Cenopalpus and low for spider mites) to that for Cenopalpus, or how in fact these ratings for consequences were derived at all.

Clarification is also sought on the reason for differences in risk categorisation compared with our trading partners. APAL notes that NZ considers spider mites a risk for stone fruit imports from the USA, but Australia does not. Why, or what is the reason for this difference? At the very least some discussion is merited on this point. In assessing the risk of importation of spider mites on apple fruit, the Review adopts the same rating level as for stone fruit imports into Australia despite noting that: “While principally found on the leaves of host plants, spider mites may also be present and feed on fruit, particularly if population densities are high during harvest (Hoyt & Beers 1993; Mellott 2019; Smith 2001b).” (p. 48) and on p. 49:

“Spider mites present on apples are likely to occupy sheltered positions, such as in the stem attachment and the calyx, and are unlikely to be dislodged from fruit by harvesting and grading activities because of their small size (Wiman, Stoven & Bush 2019).”

Apple & Pear Australia Ltd. Suite G.02, 128 Jolimont Rd, ABN 55 490 626 489 East Melbourne, VIC 3002

Despite these statements the Review largely draws on the assessment from stone fruit which, unlike apples, do not have a calyx cavity in which mites and other pests are known to hide.

No mention is made in the assessment of risk of the fact that many of these mites are encouraged in the orchard to facilitate development of predatory mite populations (PNW Pest Management Handbook, 2019). No evidence has been provided as to why the consequences from spider mite establishment in Australia should be rated differently to that for Cenopalpus (cf. moderate for Cenopalpus and low for spider mite), or how in fact these ratings for consequences were derived at all.

Spider mites readily survive cold temperatures so what measures are in place to reduce the risk of them coming in with fruit? The discussion around cold and survival is vague. While extended cold storage may impact viability, the spider mite eggs are resilient, and the ability to overwinter could allow surviving females to lay additional eggs after arrival (Veerman 1985).

Based upon the morphological differences between apples and stone fruit, and the points noted above, APAL questions the justification for equating the risk to apples with that for stone fruit. For example, in assigning risk ratings a change in the likelihood of distribution to High from Moderate would see Australia’s ALOP exceeded.

The assessment of spider mites arriving on the stone fruit pathway from California etc. is not the same as the Review proposal of apples arriving in Australia from the PNW. Arrivals at different times of the year pose different risks for likelihood of distribution. The evidence for lack of hosts due to arriving in winter (stone fruit) lacks credibility for stone fruit and is not relevant for apples which will arrive in summer when deciduous hosts will be in leaf. In addition, apples, unlike stone fruit, as already noted, have a calyx so offer an opportunity for mite and other small insect ‘hitchhikers’.

APAL would like clarification around this statement p. 195:

“All apple consignments for export to Australia must be inspected by APHIS/US regulatory officials and found free of Cenopalpus pulcher, Phenacoccus aceris, Pseudococcus maritimus, Frankliniella occidentalis and Frankliniella tritici.”

Why are consignments not inspected to be free of all mites not found in Australia? The implication is that other mites such as Tetranchyus spp. would not require treatment.

As well as the situation for NZ (mentioned earlier), it is also significant that the USA requires cold treatment and fumigation for spider mite in apples from Japan see: https://epermits.aphis.usda.gov/manual/index.cfm?action=cirReportP&PERMITTED_ID=105 96847

APAL questions why Australia sees no need for mitigation measures when both the exporters to Australia, (USA & NZ), require mitigation measures for their imports.

The conflicting evidence and morphological differences between apples and stone fruit, as well as inconsistencies in risk mitigation measures compared with Australia’s trading partners, warrant that this section needs reassessment and, on the evidence provided, spider mites would exceed Australia’s ALOP.

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Reference update

As for most other ‘updates’ in the Review since 2008 the additional references quoted are of marginal or of no relevance to risk analysis ratings:

• Dar et al. (2017) looks at mite populations of Tetranchyus turkestani on mulberry in relation to temperature. • Migeon & Dorkeld (2017) is a database on mite species. • Perry (2014) is a paper on the reaction of mite species to fungicides and water stress on grape vines. The relevance of the references raises the questions of whether they are merely quoted to provide a semblance of having updated the Review since 2008?

Apple curculio (Anthonomus quadrigibbus)

An Apple Industry High Priority Pest

The Review finds that apple curculio meets Australia’s ALOP and therefore requires no extra measures to mitigate risk. However, as with spider mites it only takes the risk rating of either importation or distribution to change to High, or establishment to change to a higher level to exceed ALOP.

Arguments to support the conclusion are poorly articulated and it is difficult to determine at times whether the statement is in support or contrary to the conclusion reached.

There are also a number of statements which are purely speculative without any supporting data or are either irrelevant or subject to dispute, for which no correct answer exists: e.g. p. 51 “usually eggs are thought to be laid singly in each cavity of the fruit….”.

Clarification is sought about what ‘usually’ means and what happens in ‘unusual’ circumstances?

On p. 51 the impression is created that Jeger et al. (2018) had provided empirical evidence that apple curculio lays only one egg per fruit:

“….but Jeger (2018) (Sic) confirmed that only one egg is laid per fruit.” whereas in reality the paper quoted (Jeger et al. 2018) is actually a review citing other people’s work. Subtle changes in text or referencing such as this can mislead the reader.

The discussion on p. 55 around likelihood of Establishment is largely speculative and with little substantive evidence and is often contradictory. Clarification and further supporting evidence is requested. The statement such as discarded fruit is “likely to be exposed to direct sunlight”. Further information is requested on what basis this was decided; furthermore, the Review appears to be taking a bet each way (on conditions being dry or wet) without any evidence for either proposition with the following statement: “In summer, discarded fruit is likely to be exposed to outdoor sunlight. Larvae inside discarded infested fruit are unlikely to complete their development before the fruit desiccates under dry conditions, or rots under wet conditions.”

It can equally be argued that there are plenty of areas in Australia which have a mesic environment that does not promote immediate desiccation or rotting.

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Similarly, the Review states “Infested apples will be largely managed through commercial waste systems” – do these systems have direct exposure to sunlight as a process? Further, the number of wild apples on roadsides attests to the number of cores tossed outside car windows whilst cores (which may contain the eggs) are often just discarded by people wherever they are. There is nothing in the data provided to suggest that infested apples will always be recognised by people and discarded appropriately.

“Most of the fruit, other than the core and seed, will be consumed. Domestic consumers may discard remaining apple waste into urban, rural or natural environments. Rotten fruit may be discarded in domestic compost or managed residential waste systems which will go to landfill.” The point is that the fruit may not be rotten but merely have a larva inside or be infected by a fungus and be asymptomatic. Depending upon circumstances the fruit could finish up anywhere.

“Larvae and pupae of A. quadrigibbus are vulnerable to exposure to direct sunlight, and have been reported to die within one hour (Fulton 1928). In summer, discarded fruit is likely to be exposed to outdoor sunlight. Larvae inside discarded infested fruit are unlikely to complete their development before the fruit desiccates under dry conditions, or rots under wet conditions.”

It is also noted that this reference is very old (1928). Is any more recent information available about the susceptibility of A. quadrigibbus to environmental conditions?

Some statements appear to be almost random and APAL is unsure as to why they have been placed in the Review at all. One example is:

“In Australia, depending on the cultivar, apple fruit-setting occurs from October to early November, and harvesting from February to May. Anthonomus quadrigibbus prefers to infest fruits immediately after they set (Crandall 1905; Fulton 1928; Steeves, Lehmkuhl & Bethune 1979).

Clarification is needed on the reason for this statement and what evidence there is to support the contention that larvae would be unable to complete their development? The reliance on all fruit being found in summer or rotting, as has been noted above, is at best questionable.

There are contradictions in the interpretation of literature. For example, p. 55 – it is stated that apple curculio can fly more than 400 m which increases the chances of finding a suitable host, yet on p. 57 – the Review notes that adults are capable of flight but unlikely to migrate far. Clarification is requested around this.

Some of the practices outlined for detecting the pest appear impractical for large export consignments, for example:

• “Visual inspection of host fruit can detect damage symptoms and fruit suspected of being infected can be cut open to find immature stages.” This procedure is only relevant if the pest is suspected. No data has been presented to indicate the effectiveness of this approach. Further information is requested about the post- harvest practices in the US and their efficacy (this also relates back to an earlier comment about advances in post-harvest technologies)? • Then- “during packing house and quality assurance procedures, fruit with visible damage are likely to be detected and discarded.” (p-53) Further evidence is requested around what percentage of fruit are likely to be detected, and what proportion of symptomless but infected fruit are not detected.

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Similarly, the comments on p. 56 around infection routes and control are not evidenced. APAL contends that the most likely infection route in Australia is from metro or peri-urban areas as this is where imported apples are more likely to be purchased and there are a plethora of potential hosts available in these environments. The comment that, “well maintained orchards may reduce the ability of apple curculio to establish” (p-56) is largely irrelevant in this context and does not reflect the real risk. It is also at variance with the statement on p. 54 that the majority of imported apples are likely to be received in major population centres. One would suggest that an existing apple orchardist is probably one of the least likely purchasers of imported apples. Similarly, the comment p. 56 on existing control measures in commercial orchards being likely to mitigate against establishment is pure speculation and unlikely to reflect reality. Evidence needs to be presented to support this statement in the Review.

The discussion on cold temperature survival is confusing. If the response of the pest to cold temperature is deemed to be similar to that of plum curculio, why are similar control measures not mandated for apples as exist in the USA? APAL questions how the Review reconciles its findings for both plum curculio and apple curculio against the following quote:

“Plum curculio, which is very similar in biology to A. quadrigibbus, is regulated on apple and other host produce entering the PNW-USA by applying a mandatory cold treatment at 0°C for a continuous 40 days against the larval stages, as required under the Oregon state administrative rule, 603-052-0030 (Oregon Secretary of State 2019).” The quotation above also merits the question as to why the USA sees plum curculio as warranting special measures, but Australia doesn’t (p. 208).

Any cold treatment for A. quadrigibbus needs to be established for that species and not assume that it will be same as that for another genus. This principle of doubtful equivalence does not hold for other insects so why should it be any different for these species? Further supporting evidence is requested.

Section 4.3.5 presents control measures, incidence information and the importance of the pest from Canada dating back to 1928, 1930 and 1953. Further information is requested about how this is relevant to apple production and risk mitigation in PNW in 2020? Does Quebec supply apples to the PNW for export? The discussion also fails to mention the concern in Jeger et al. (2018) that the species (A. quadrigibbus) may spread to other Rosaceae hosts outside its known range once in the European Union (EU). Reference update

Referencing is generally inappropriate or irrelevant:

• Burke & Anderson (1989) – this is a systematics article; it does not, for example refer to fruit dropping prematurely so fails to support the statement for which it is being cited • Campbell et al. (1989b) (link to reference does not work) - this is a compendium on economic pests of crops etc. that underscores the need for control of A. quadrigibbus. • Jeger et al. (2018) (link to reference does not work) - further searching uncovered Jeger et al. 2018 which was a risk assessment for the EU for this pest and concluded that A. quadrigibbus met the criteria to be a quarantine pest for the EU but was likely to be controlled by existing measures (not specified) for apple pests. This last piece of information (from Jeger et al. 2018) was omitted from the Review.

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APAL submits that the Review has underestimated the risk posed by apple curculio and the confused, and at times contradictory, reasoning together with the recognition by the PNW for measures to control this pest mandate that at the very least the same protocols should be verified and adopted by Australia.

The question also needs to be asked as to why plum curculio was not considered a risk given that the USA does consider it a risk.

Apple leaf curling midge (Dasineura mali)

There is little evidence provided in this Review to indicate that the risk posed by apple leaf curling midge has been adequately assessed. The Review’s finding of an unrestricted risk rating for this pest as Negligible is unacceptable. In coming to this conclusion, the Review largely relies upon the earlier NZ Risk Analysis from 2011 and comes to the same conclusion. Comments obtained by APAL from growers and exporters with NZ experience suggest that leaf curling midge is a very serious pest in NZ.

APAL could find no mention in Mellot (2019) to verify the statement in the Review that:

“D. mali is not recognised as a pest of apple in the PNW states (Mellott 2019).”

The Review notes on p. 62 that D. mali is “…. occasionally associated with export consignments” (from NZ). This rather vague statement about occasional association with NZ exports to the USA provides no supporting evidence or confidence in mitigation measures. How frequently is “occasionally”? APAL queries the extent to which shipments were, or may, have been withheld by pre-clearance inspections in NZ? This is relevant in the light of the next paragraph.

The evidence presented in Ch. 5 suggests that approximately 2.6% of shipments from New Zealand contained apple leaf curling midge. This is at variance with personal communications from apple importers who have indicated that the continual detection of this pest in the calyces of apple fruit is a significant impediment to exporting apples from NZ and in fact has led to the cessation of export of certain varieties. Exporters in NZ have deliberately withheld shipments due to the fact that they have been unable to remove apple midge from calyces in areas of high population pressure such as Hawkes Bay. Australia is thus being protected from the importation of this pest by importer/exporter self-regulation. Some discussion on this aspect in the Review would have greatly assisted the definition of risk and potential mitigation measures.

There are also reports of detection of apple leaf curling midge in apple fruit in the PNW. In California, D. mali has been intercepted by Californian Department of Food and Agriculture’s (CDFA) border stations 89 times since 2009, typically as pupae, on apple fruit from NZ and the PNW (https://blogs.cdfa.ca.gov/Section3162/?tag=apple-leaf-gall-midge; accessed 21.12.20). Basing the risk assessment on NZ practices being acceptable (p. 60) is inadequate and, without a direct comparison of prevalence and orchard practices in the two countries is insufficient. The Unrestricted risk estimate for NZ of Negligible based on commercial practices being implemented is not supported by commercial experience irrespective of commercial control measures being implemented. Negligible is not an appropriate risk rating for this pest. This rating is undermined by the Review itself noting that apple leaf curling midge has been detected in several USA ports on NZ apples and also pre-clearance inspections. This suggests a higher Unrestricted risk estimate than Negligible is more appropriate. Additional, current supporting evidence is requested.

The quote on p. 61 attributed to Mellot (2019) that apple leaf curling midge is not recognised as a pest of the PNW is incorrect. The article by Mellot (2019) is about spider mites not apple leaf curling midge.

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No evidence is presented to justify the statement at the top of p. 62 that:

“The abundance of D. mali in PNW-USA apple orchards, in comparison with those in New Zealand, is expected to be Very low due to the restricted distribution of D. mali in the PNW-USA.” This quotation is immediately followed by the next;

“Furthermore, apples from PNW-USA are subjected to commercial production practices for pest management including monitoring, insecticidal sprays and biological control (Beers 2017; LaGasa 2007).”

What does this mean in the context of risk compared with NZ? Does this mean that practices in the PNW are better at reducing risk than those in New Zealand? Information about the distribution of apple leaf curling midge in the PNW is unclear. The averaging of infestation levels over a region when the pest is only found in certain areas (p. 62, para 1) is not valid and misleading as it tells the reader nothing about the risk posed by individual orchards where the pest is present. Of concern from a risk perspective, is the incidence of apple leaf curling midge in the locations where it occurs in the PNW and how this relates to the incidence in NZ, and implementation of risk mitigation measures.

Similarly, the comment in the same paragraph, that the pest is subject to commercial control is meaningless in the context of the discussion in the preceding two paragraphs in the Review. Presumably it is managed in NZ also, yet they have issues with apple leaf curling midge. No evidence is presented to substantiate the statement that the abundance of apple leaf curling midge in PNW-USA orchards is low (p. 62 last para). The statement that the pest is not recognised as a pest in the PNW is also not strictly true. The Washington State Tree Fruit Protection manual states:

“Apple leaf midge is generally not considered an economic pest of mature apple trees. However, high populations in nurseries or on young trees or top-worked (grafted) stock may stunt growth or kill terminal shoots.”

APAL contends that little evidence is provided to substantiate an Importation risk of Low nor why pests from the US are less likely to be imported (rated Low) than those from NZ where the rating is Moderate. Evidence to validate this is requested. Referencing update

Referencing is once again inadequate:

• p. 61 – Mellott (2019) this reference is on mites and does not mention D. mali. • LasGasa (2007) link does not work • Biosecurity (2011b) link does not work

In order to substantiate the past ratings for this pest more recent papers are cited on p. 61 para 3. Unfortunately, these have nothing or very little to do with the risk posed by this pest and are of little relevance.

Of the papers cited the following is noted:

• Beers (2017) is an article summarising apple leaf curling midge in Washington State University crop protection extension material • He & Wang (2015) is about parasitising of the midge • Lo and Walker (2017) is about regional emergence in NZ • Page-Weir et al. (2018) is on the efficacy of heat treatments to kill cocoons

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• Wearing et al. (2013) is on phenology and IPM • Yuan (2014) is on fruit disinfestation using UV radiation. Are any of these research outcomes now applied commercially to reduce risk? Significantly in the context of risk assessment the occurrence of the pest in the calyx and stem ends of apples is supported in another paper by Lo et al. (2015) which is not referenced in the Review.

Importantly, all these publications mention the role of fruit as a carrier of the pest and it is not unreasonable to expect that this research would not be performed unless there was an identified trade risk from fruit borne cocoons.

Based upon the NZ experience of management of apple leaf curling midge and what is known about the pest, it is submitted that the risk rating of Negligible is inappropriate and that further protocols than those listed are required for this pest if it is to meet Australia’s ALOP. Industry advice is that existing regulations are only working from NZ due to self-regulation so are we to assume that Australia will have a similar reliance on imports from the PNW-USA?

Chaff Scale

Chaff scale is primarily a pest of citrus and apple is not a major host and thus APAL would concur with the assessment on this pest requiring no particular measures. Referencing update

We note however that there are again issues with references that need to be highlighted.

• The URL for Garcia et al. (2020) is not correct and the actual reference is: http://scalenet.info/static/scaledb/flatcat/Diaspididae.htm However, this is only a list of records and one wonders why it was cited as it’s of little relevance to discussion of risk.

• Khadiga et al. (2015) is about citrus trees • What is concerning is that the paper by Masten et al. (2009) actually showed a 6% interception of chaff scale on imported fruits into Croatia. Whilst this was on citrus, the preferred host, this nevertheless is new information and merited comment.

Lygus bugs (Lygus lineolaris)

The risk assessment of lygus bugs lacks rigour and as a consequence fails to address the true risk posed by this pest. The Unrestricted risk assessment rating for lygus bugs on the import pathway is given as Very low. In reaching this assessment the Review draws heavily from the risk assessment for stone fruit from the USA. As mentioned earlier, little or no evidence has been provided as to why the risk from these two commodities (stone fruit and apples) is similar. APAL contends that they are not. For example, in the stone fruit Provisional Import Risk Assessment (IRA) it is noted that:

“All harvested stone fruit is washed and brushed/defuzzed following harvest. These actions would almost certainly remove the highly mobile adults and nymphs, including any that become associated with the fruit after harvest.”

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Whilst this may be the case for stone fruit which have an exterior without cavities, it is not analogous to apples which have a calyx cavity. This difference alone merited a closer analysis of risk. There is no discussion on this difference for this pest and the possibility of lygus bugs hitchhiking in the calyx cavity.

The stone fruit PRA also notes that lygus bugs are polyphagous and yet downplays the risk that they will find suitable hosts if imported. APAL questions this logic and requests clarification here. Referencing update

Lastly the references quoted as being consulted since the stone fruit analysis are, as in most other instances where this has been done in this Review, largely irrelevant and should be noted as such, rather than implying that the existing information is substantiated:

• Allen et al. (2018) is on lygus bugs in cotton and early season control. The relevance of including this is questioned. • Antwi & Rondon (2018) is about molecular identification; are new diagnostic methodologies included in the risk assessment process? • EPPO (2019) has no mention of lygus bugs. • Hagler et al. (2010) looked at feeding preferences of lygus and whitefly on cotton discs and sweet potato, the relevance of which to this IRA is questionable. • Conversely, Cooper & Spurgeon (2019) note that adults can survive periods of 33 days without food and still be reproductive therefore they can probably survive sea freight. This should have been mentioned in the current assessment.

Risk mitigation

Biosecurity NZ requires mitigation measures against L. lineolaris (Suffert et al. 2016) which raises the question as to why Australia sees it differently. It is also included in the European Union’s list of “Pests With Lesser Economic Importance And More Likely To Transfer, Or High Economic Importance But Less Likely To Transfer” (Suffert et al. 2016)

The finding that the Unrestricted risk estimate would not exceed our ALOP cannot be substantiated on the evidence provided.

APAL submits that lygus bugs need to be re-examined for their risk against apples and not based upon that from a morphologically dissimilar genus such as Prunus.

Lacanobia fruit worm (Lacanobia subjuncta)

An Apple Industry High Priority Pest

The Review believes that this pest requires no special risk mitigation measures as the Unrestricted risk estimate is Very low. APAL disputes this rating and notes that many of the arguments to support this proposition are merely supposition at best and without supporting evidence eg. infested fruit falling from tree (p. 81).

Doerr & Brunner (2002) note that Lacanobia feeds on apple fruit and can create a hole as big as a finger. Whilst this is valid for late instar larvae, evidence as to likelihood of finding smaller early instar larvae in apple fruit would be useful. It is noted that larvae can be found in fruit as late as October which is well into harvest season in the PNW-USA. See: https://pnwhandbooks.org/node/7494/print (accessed 16/11/20)

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As for many other pests the potential role of the calyx cavity in importation and distribution is ignored.

Whilst larvae may not be able to develop at low temperature (p. 81) that does equate to survival and does not substantiate the following statement: “Undetected larvae from sorting ……are unlikely to be viable during cold temperature storage and shipment to Australia”.

No evidence has been presented on larvae and cold survival pp. 81-82 and conflating development with survival is both misleading and not scientifically valid. Evidence to support this is requested. This mistake is repeated on more than one occasion in the Review.

Most of the evidence supplied around likelihood of importation supports a rating of moderate unless better evidence can be provided. The discussion on likelihood of distribution is largely speculative with no evidence to support the propositions offered. The role of domestic and urban households and other forms of waste is ignored. If apples are imported and larval development is arrested due to cold (p. 81) then it is more than likely that apples would still contain undetected larvae within the fruit and therefore be asymptomatic. It would therefore not necessarily go to commercial waste. Clarification and supporting evidence around this are requested.

The rate at which fruit may desiccate or rot is highly dependent upon a number of factors that are determined by the environment and season at the time fruit is discarded. The Review has not differentiated risk on this basis.

The discussion around heat tolerance is confusing to say the least and contradictory. Not all fruit will be imported in the “hot days of summer” and the last paragraph on p. 82 would indicate that the pest is likely to be unaffected at other times of the year. In addition, the arguments about temperature and survival on p. 82 are misleading. Relying on ambient temperatures to be above 32.5oC to achieve larval mortality in summer is a tenuous risk management strategy.

Lacanobia fruit worm is a high priority pest for the apple and pear industry and, given the nature of its impact, it is difficult to comprehend how the Review determined that the impact at district level for eradication/control is only significant and not major at a district level (E) and similarly for domestic trade. What is even more surprising is that in arriving at its rating for eradication/control the Review notes the difficulty in controlling this pest in Washington State. The Review also notes the ease with which the pest may fly to other hosts and yet this fact was ignored when considering the ability of the pest to spread (pp. 84-85). APAL also notes this is regarded as a pest of concern to the European Union (Suffert et al. 2016). A change of Consequence to E, irrespective of the other ratings for entry, establishment and spread would raise this pest above Australia’s ALOP.

APAL submits that the evidence provided to support the Unrestricted risk estimate for entry establishment and spread is not supported by the speculative nature of the evidence provided whilst that for consequence is contradicted by the arguments presented. Accordingly, this pest warrants reassessment and specific mitigation measures.

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Oriental Fruit Moth (Grapholita molesta)

This is pest of biosecurity concern to Western Australia. It is recognised that oriental fruit moth has already been assessed in other Pest Risk Assessments, but some data on interceptions and its likely threat is requested to support the efficacy of current mitigation measures.

Of concern to APAL is that the proposed measures for fruit moths are not consistent to those that exist in Western Australia for fruit from the eastern states of Australia. This is even more surprising when compared against the import biosecurity conditions for NZ apples into WA which requires mandatory fumigation. APAL questions how or why the situation from the USA should be different?

Post 2008 Literature

As mentioned for other pests, the provision of contemporary references for this species are often of no, or little, relevance.

• Gilligan et al. (2018) goes to a catalogue which only mentions the species in question without any further elaboration particularly in relation to risk. • Graillot et al. (2016) looks at adaptation to granulosis virus that affects codling moth. • Hollingsworth (2019) is about the moth in stone fruit and its methods of control and appears to be an updated extension note. • Yang et al. (2016) looks at population dynamics; what is the relevance of this to the Review? • Zhang et al. (2017) looks at modelling the reproductive system as a means of getting better integrated control. In contrast, Neven et al. (2018) however notes that climate change (warming) climate will make more areas of Washington suitable for fruit moth which will no doubt increase pest pressure. This is important and should have been mentioned in the Review. Furthermore, Zhang et al (2017) noted the increasing problem posed by oriental fruit moth in orchards and this was not mentioned by the Review. Based on existing import biosecurity conditions for NZ, APAL submits that the proposed mitigation strategy which does not mandate fumigation is inadequate for this pest for Western Australia.

Apple fruit moth (Argyresthia conjugella)

Drawing extensively from the existing policy for Japan and China the Review finds that the Unrestricted risk estimate for apple fruit moth at Very low meets Australia’s ALOP. Contradictions exist in the Review’s assessment for this pest.

Compare and contrast the following:

• China IRA: “The risk scenario of concern for A. assimilis is the presence of eggs and larvae on and/or in apple fruit.” • This USA-PNW IRA: “The risk scenario of biosecurity concern is that larval and pupal stages of A. conjugella may be present within mature apple fruit from the PNW- USA.”

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This is not the same risk scenario so why is the same risk assessment used? Furthermore, what is the difference between China and the PNW that changes the risk scenario? This needs to be explained.

On p. 103 it is stated; “The Department has assessed the likelihood of importation of A. assimilis on fresh apple fruit from China as Low (Biosecurity Australia 2010a). However, differences in pest prevalence, climate and horticultural practices between the export areas make it necessary to re-assess the likelihood of importation of A. conjugella associated with the PNW-USA apple pathway.”

The subsequent discussion on importation risk then largely lists risks that increase with importation thus it is difficult to see how a Very low risk of Importation could be determined. apple fruit moth is associated with apple trees and, as the Review acknowledges, it is a severe pest in Scandinavia. The Review implies that the lack of official control measures within the USA is a reason for it not being a pest. However, as the moth is found in both western and eastern USA states why would control measures be applied or justified?

APAL queries why only the risk of importation was re-assessed and no other aspects including consequences. The Review acknowledges that apple fruit moth predates apple seeds but provides little evidence as to the similarity in biology between this species and A. assimilis. APAL was unable to source a copy of Chinese Fruits Vol 3 for a translation but would appreciate a translated copy.

The European Union includes A. assimilis as a pest in its list of “Pests With Lesser Economic Importance And More Likely To Transfer, Or High Economic Importance But Less Likely To Transfer” (Suffert et al. 2016) and, significantly, quotes Biosecurity Australia in reaching its conclusion, noting the significant damage reported in China (up to 80%) in the eighties. However, Biosecurity Australia in using this species as an analogue of A conjugella, has provided an Unrestricted risk estimate of Very low.

APAL queries why the Department is at variance with trading partners in regarding this pest and a number of others in the Review as having an Unrestricted risk estimate of Very low or negligible?

The Review notes that apple fruit moth prefers rowan trees and apples are used as a secondary host, especially in years of low seed set in rowan. Therefore, an important criterion in assessing risk is the extent to which rowan trees are grown in the various countries and in the PNW-USA. This has not been addressed at all in the Review.

The risk assessment for this moth is lacking significantly in detail and completeness, and a more thorough examination is requested.

Post 2008 Literature cited in the Review The more recent references quoted on p. 103 are of little relevance to assessing risk.

• Agriculture Victoria (2019) –This reference is misquoted. Rowan trees are not occasionally grown in Australia (as stated on p. 103) but can be common in places in the southern states. Furthermore, the reference does not mention the words attributed to it and in fact, and more significantly for the Review and assessment of risk of apple fruit moth, this publication assesses the potential of the plant as an invasive species for which it determines that a considerable percentage of Victoria is at risk. • Elameen et al. (2016) is about genetic diversity in populations of Apple fruit moth in Norway.

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• Passini (2015) – it is difficult to see why this was quoted as it is about developing a lab bioassay for volatiles as attractants. Of particular concern is the misinterpretation of papers, which casts significant doubt on the validity of the conclusions drawn on the risk posed by the pest.

Compare the following quotes from the Review: “Studies show that apple is a poor larval host for A. conjugella and the pest develops with difficulty in apples (Furenhed 2006; Kobro et al. 2003)”

With what Furenhed (2006) actually wrote:

“Older studies show that the apple fruit moth has difficulties to develop from apples (Ahlberg, 1927; Edland, 1979), but recent studies prove otherwise (Kobro, 1995). It is even the case that larvae developed from apples are larger than specimens developed in rowan berries (Petersen, pers. com.) The apple fruit moth can reproduce well in apples, and it means that an orchard with a lot of fruit left on the orchard floor can contribute to the pest population the year after (Kobro, 1995).”

It is hard to reconcile what the Review has written with what was actually written in the paper. This needs to be reassessed in the context of what was actually presented in the references cited.

The reference for Ovsyannikova & Grichanov (2008) cannot be accessed from the URL supplied, however accessing the reference at: http://www.agroatlas.ru/en/content/pests/Argyresthia_conjugella/index.html noted that apple fruit moth can cause severe damage to apple which can exceed that caused by codling moth and late apples are damaged most. This again appears to run somewhat contrary to the statements made in the Review.

Misinterpretation of science is unacceptable in a scientific report and calls into question the credibility of the conclusions drawn and also raises questions as to whether the Unrestricted risk estimate for this pest from China of Very low is derived from similar flawed reasoning.

There is a lack of supporting information in the analysis of apple fruit moth and it thus requires a full risk analysis. Any proposed mitigation measures also need to be based upon the actual biology of the pest.

Codling moth (Cydia pomenella)

The mitigation measures proposed for codling moth are at variance with those that exist within Australia for domestic fruit. This not only puts Australian growers at risk, but potentially also at a trade disadvantage through the extension of more favourable treatment to USA producers. APAL does not dispute the findings that mitigation measures are required but does dispute the adequacy of the proposed mitigation measures. to the need to address this discrepancy was noted earlier with respect to oriental fruit moth (G. molesta).

Currently all domestically produced apples must be fumigated before entry to Western Australia where codling moth is not known to occur (https://www.agric.wa.gov.au/ Accessed 21.01.21) However, under the proposed measures suggested in the Review this is an optional condition for apples from the PNW.

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This would lead to the situation whereby apples from the eastern states of Australia, whether produced in Australia or imported, would require disinfestation prior to entry to Western Australia but imported apples from the PNW do not. This is neither consistent nor sensible risk management. Furthermore, it leads by default to a discriminatory trade practice against Australia’s eastern state growers.

APAL notes that Western Australia (WA) has provision for other measures to control fruit moths, but these would be contingent upon a suitable data package being accepted. This has not been adequately clarified in the Review.

Fire blight (Erwinia amylovora)

An Apple Industry High Priority Pest

Fire blight is a disease of particular concern to the apple and pear industry. APAL argues that the Review understates the risk due to:

• Lack of clearly mandated controls • A comparison of New Zealand with USA that is unjustified due to differences in pest prevalence, production practices and climatic conditions • Absence of a detailed comparison of NZ and USA production management • Survival of fire blight in the calyx • Fire blight may exist asymptomatically • Different and changing climatic conditions may increase prevalence of fire blight • Potential for transmission via Mediterranean fruit fly (Medfly) and Queensland fruit fly (Qfly). Lack of mandated control measures

There is a need for clearly mandated controls, threshold levels or other form of check for imports from the PNW. It is noted that for import of fresh apples from New Zealand, orchards registered for export to Australia are required to have in place a fire blight management regime (BAA 2011/14 Attachment A). However, the Review for the USA states that no specific risk mitigation measures are required except for a generic note regarding routine practices. As noted earlier in this submission, insufficient evidence is provided to support the efficacy of these routine practices. What is the justification for a more lenient treatment for USA apples? Further clarification is requested around why the situation for the USA is different to that of New Zealand, given potential differences in pest prevalence, climatic factors, and other variables (see comments below related to p. 109). There are also inconsistencies between Australia’s stance and with other USA trading partners. For example, China requires specific measures for management of fire blight when importing apples from the USA: https://www.aqsiq.net/us-apples.htm (accessed 3.11.20). Discussion in the Review on fire blight understates the true extent of the problem in the PNW and further information is required.

For example, the Review notes (p. 109) that in the most recent assessment of risk for importing apples from New Zealand (Biosecurity Australia 2011b), the Unrestricted risk estimate for E. amylovora was assessed as Very low when certain industry commercial practices were applied, achieving the ALOP for Australia and therefore:

“no specific risk management measures are required for E. amylovora on the PNW-USA apple pathway. Similar in-field controls and packing house measures are routinely applied as part of the PNW-USA apple production system.”

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This is immediately countered by this sentence in the next paragraph (p. 109) which highlights the need to re-assess the likelihood of the importation of E. amylovora due to different conditions between NZ and the USA:

“Differences in pest prevalences (sic) and transport times between exporting areas make it necessary to re-assess the likelihood of importation of E. amylovora with apples on the PNW- USA pathway.” Given that the Review highlights these differences, APAL would argue that the Department cannot rely on New Zealand research to assess the risk of fire blight in apples from the USA.

The statement on p. 116 that PNW-USA orchards adequately manage fire blight is not supported by the evidence presented in the Review relating to fire blight outbreaks e.g. p. 31.

Comments by Dupont (2019), Dupont et al. (2019) and Dupont (2018) on outbreaks of fire blight over recent years would suggest the disease remains a significant issue. “Serious damage to foliage on about 5 to 10% of plants was reported in 1993, 1997, 1998, 2005, 2009, 2012, 2015, 2016, 2017 and 2018 (Dupont et al. 2019).” These outbreaks are not covered in any detail in the Review.

Dupont et al. (2019) also notes that in Washington State in 2018, the cost of managing fire blight was US$37M and estimated the losses due to infection at US$222M. This is significant. As mentioned earlier, Aćimović et al. (2015) quote Stockwell et al. (2002) that “In Washington and northern Oregon, economic losses on pome fruits due to fire blight were over $68 million”. This is not cited in the Review. See also https://portal.ct.gov/CAES/Fact-Sheets/Plant- Pathology/Fire-Blight (accessed 21.01.21) for severity and factors affecting fire blight in the USA.

The earlier 2008 IRA for apples from the USA noted that fire blight was “abundant” in the PNW and yet it is downplayed in this Review. What has changed since 2008 to warrant what appears to be a change of status?

Furthermore, the Review gives the mistaken impression that Temple and Johnson’s (2011) paper (cited on p. 110) was to survey for fire blight: “Surveys showed that 28 of 60 orchards had fire blight symptoms. Disease severity in 21 of those 28 orchards was classified as light (≤1 infected shoot per tree) (Temple & Johnson 2011). The remaining orchards had light to moderate infestations (≥1 to 5 infected shoots per plant”). However, Temple and Johnson (2011) were reporting on verifying the accuracy of Loop-mediated isothermal amplification (LAMP) tests and although the article provided some information on fire blight incidence, it was not a true survey. Of particular concern was their comment that some orchards in the Hood Valley and Columbia Basin experienced significant outbreaks of fire blight and that LAMP detected fire blight in a number of orchards for which there were no visual symptoms. This comment by Temple & Johnson was not mentioned in the Review. Other published work also notes the likelihood that Fire blight can exist asymptomatically (Tancos et al. 2017). Tancos et al. (2017) is not cited in the Review. Further supporting evidence is requested on what has changed in the PNW to manage fire blight.

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The effect of changing climatic conditions

In contending that the risk from fire blight has been underestimated, APAL also notes the following: Low temperature is cited as a reason for a likely low primary infection of blossoms and Smith (2001b; this URL link does not work) is cited (p. 110). However, Smith (2001) wrote:

“Fire blight in the Pacific Northwest was once rare. The weather during bloom is generally too cool (68°F or less daily) for primary blossom infections. Most infections take place on blossoms that appear after petal-fall. These “side blooms” or “secondary blooms” appear on the apple tree shortly after bloom as the weather begins to warm, usually during May, while weather is warm but not hot. These late blossoms are much more common on modern varieties growing on modern rootstocks.”

This statement by Smith (2001) would seem to indicate that fire blight infection is more common than it ‘once’ was and APAL asks what role changing climate may have on the incidence of warm days in spring. For example, temperature maxima for April 2020 show that the daily maxima exceeded 20oC on 15 days (https://www.wunderground.com/history/monthly/us/wa/wenatchee/KEAT/date/2020-4; Accessed 31.10.20).

Given the ongoing climate change and erratic weather conditions, there is a need to review the incidence of fire blight taking into account changing climatic data. For example, Horner et al. (2019) noted that with higher temperatures due to climate change there was increasing pressure in New Zealand from fire blight.

Further, Slack et al. (2019) found E. amylovora populations can infect and grow at daily temperature averages below current forecasting minimums and there could be significant growth at lower night-time temperatures. It is noted that neither Slack et al. (2019) nor Horner et al. (2019) were consulted for the Review.

Post 2008 Literature

A number of references of relevance to the risk assessment were located that post-date the WTO ruling. Several of these were not used by the Review or misinterpreted. As already mentioned in relation to other pests, where scientific report findings are misinterpreted, there is a risk that misleading conclusions can be drawn.

For example, on p. 110 Elkens et al. (2015) is quoted as finding:

“… that close to the petal-fall stage of primary bloom, the number of flowers susceptible to infection begins to decline rapidly.”

From which the Review concluded:

“The decline in the number of susceptible flowers would therefore result in a concomitant decline in the number of potential calyx infestations.” Whereas what was actually written by Elkens (2015) was:

“The pathogen detection data indicate that copper sanitation may add value to a fire blight management program by delaying the increase of epiphytic populations of E. amylovora in flowers to the late stages of the bloom period, at which time the number of susceptible flowers declines rapidly.”

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This is not the same as what is quoted from Elkens (2015) and it is unclear from the quote as to whether susceptibility changes or because it is nearing the end of bloom there are just fewer flowers. A full reading of the paper implies the latter.

It would appear that only the abstract of this paper was read. In the first instance the paper concerns pears not apples. Furthermore, Elkens (2015) noted that copper sanitation could causes skin russeting in apples and pears and was therefore not popular. Elkins (2015) also noted that:

“Overall, epiphytic populations of E. amylovora on flowers were detected rarely at midbloom (6% of samples) but commonly at petal fall (44% of samples)”.

Elsewhere in the same paper Elkens (2015) notes that there was a rapid increase in detection of fire blight between full bloom and petal fall. Notwithstanding that the study by Elkens referred to pears, this additional information gives a different impression to that provided in the Review.

The discrepancy between inference drawn in the Review and underlying reference is also evident in the use of Johnson (2014). The Review, quoting Johnson (2014) and Temple and Johnston (2011) creates the impression that fire blight does not have enough inoculum for infection (p. 110):

“… between 100,000 (105) and one million (106) cells of E. amylovora are needed on a flower to achieve infection. Fire blight of apple appears frequently to be an inoculum-limited disease, with pathogen populations in floral washes from inoculated fields averaging 5.2 x 103 colony forming units (cfu) per flower.”

However, Johnson (2014) also noted that cells multiply on stigmas and this is temperature dependant. The latter information is pertinent but was not considered in the Review.

It would appear that only the abstract of Temple & Johnson (2011) was read as the figure quoted in the Review of 5.2 x 103 cfu per flower refers only to washes from three experimental orchards and is not based on any epidemiological study. As previously mentioned, Temple & Johnson’s (2011) paper is about validating a LAMP method for fire blight detection, so is of questionable relevance. Incidence data is secondary to the main purpose of the study and as a result can in no way be expected to provide a true survey of fire blight incidence and infection in either time or space. The authors also noted that there were some inconsistencies between their results and those predicted from various heat accumulation models such as the Cougar Blight Model, cited elsewhere in the Review (p. 110) as a tool for fire blight management.

The inference in the Review that practices outlined in manuals or handbooks are standard industry practice is also of concern (p. 111). Whilst manuals may describe what should be done, what is of concern from a biosecurity perspective is what is done in actual practice and the efficacy of that practice. Supporting data of the efficacy of actual practices is required. p. 111 – It is stated that mature fruit do not have enough starch to sustain multiplication of fire blight. APAL was unable to source this information from the references cited (Paulin 2010 and WTO 2010) both of which appear to be the outcome from the WTO deliberations. p. 111 – It is stated that there is accumulated evidence suggesting survival of fire blight on mature fruit is minimal. Unfortunately, there is no citation or provision of this accumulated evidence to support this statement.

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The structure of the arguments presented in the Review is such that headings do not always reflect the content of the text underneath. For example, much of the discussion on pp. 112 and 113 which is supposed to consider the survival of the bacteria in the calyx mostly considers fruit surfaces. This results in the actual risk being understated.

Ordax et al. (2009) noted that many of the studies on calyx survival of E. amylovora are flawed and underestimate the level of E. amylovora in calyces. In a study on survival Ordax et al. (2009) noted the following: “The risk of E. amylovora dissemination through mature fruit transport, although low, has been demonstrated, and should be considered in pest risk assessments.”

Further discussion in this paper notes:

“This study has demonstrated that E. amylovora can survive in the calyx environment of mature apple fruit and cope with the starvation and desiccation conditions present, maintaining its culturability (sic) and⁄or adopting the VBNC state depending on the inoculum dose, temperature, copper presence and time elapsed after the inoculation.”

Ordax et al. (2009) also noted that cold temperatures ameliorate the protective effect of copper and significantly, that E. amylovora cells in the VNBC state could recover their pathogenicity upon contact with host material.

This last finding is significant.

This research by Ordax et al. (2009) appears to contradict the statement in the Review (p. 116 para 5; quoted below):

“It has also been documented that the calyx is an unsupportive environment for E. amylovora, potentially because of the lack of required nutrients and moisture. Extended times under cold storage and transport to Australia are anticipated to further reduce the numbers of viable bacteria in fruit calyces.”

Much of the paper by Ordax et al. (2009) that demonstrates survivability of fire blight in the calyx is not quoted in the Review.

Given this conflict, APAL requests that further work be undertaken on the survivability of fire blight in the calyx. It would also be beneficial to understand if the paper by Ordax et al. (2009) was used by the WTO in their determinations on fire blight.

Vectors of the fire blight bacterium

Of particular concern to Western Australia, due to the presence of Medfly, is also a finding reported by Ordax et al. (2015) that fire blight can be vectored by Medfly, surviving in the gut for up to eight days and on the body for 28 days. This warrants the question as to whether the bacterium can also survive in the gut of Qfly which is present in the eastern states of Australia?

Fire blight and asymptomatic fruit

A number of the studies on fire blight note that asymptomatic fruit may have E. amylovora inoculum and that the amount carried can be quite low but still enough to be a source of infection (see Ordax et al. 2009 and Lopez 2010).

We were unable to locate the comment attributed to Ordax (2010b):

“There is no evidence that E. amylovora enters a VBNC state in apples under field conditions; when VBNC detection was specifically attempted, no E. amylovora VBNC or culturable cells could be detected on symptomless apples harvested from infected trees (Ordax et al. 2010b).”

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But it conflicts with the findings of Ordax et al. (2009) already noted above that Erwinia cells in the VNBC state could recover their pathogenicity upon contact with host material.

The Review also does not mention the use of rootstocks to manage fire blight. Does this form part of a systems approach in the PNW? How effective is this? Has the Risk assessment taken into account the very limited use of resistant rootstock in Australian production systems? Of particular importance in this context is the degree to which tolerant rootstocks may mask the presence of fire blight thus under expressing the true extent of infection and consequent risk in some orchards. The discussion on fire blight fails to accurately reflect the current state of knowledge and certainly does not justify the conclusion that the Unrestricted risk estimate meets Australia’s ALOP. This necessitates that this section be reassessed and rewritten. At the very least there needs to be some boundaries set around infection levels, orchard management programs and protocols and risk which this Review has not considered.

It is also not difficult to obtain an overall Unrestricted risk estimate of Low for this organism and thus exceed Australia’s ALOP. Noting the conditions that exist around NZ imports for fire blight, the Review would have been enhanced had it provided detailed discussion and comparison between NZ and USA production, management and other practices and at the very least required a similar level of management as that required for NZ imports.

Coprinus rot (Coprinopsis psychromorbida)

The Review rates the Unrestricted risk estimate for Coprinus rot as Negligible. APAL disputes this rating due to similar issues that were raised when addressing the section on insect pests and fire blight: selective presentation of evidence, lack of rigour and inconsistencies in risk ratings.

Reliance on a single survey that did not look at the occurrence of latent pathogens.

The assessment of post-harvest fungal rots in the Review relies heavily on a single survey that sampled decayed fruit from packing sheds (Kim and Xiao 2008).

APAL argues that reliance on this study in the Review has an inbuilt bias. The authors made isolations based on “the pathogen signs and morphology of fungi under a microscope if sporulation or fruiting bodies of the pathogens were present on decayed fruit”. Several of the post-harvest pathogens listed in the report (e.g. Coprinus, Truncatella, Neonectria) are latent with symptoms developing during storage. By selectively sampling decayed fruit and isolating from lesions, Kim & Xiao selected for pathogens that were already symptomatic on the fruit. The study did not look at the occurrence of latent pathogens. Relying on this reference for assessment of risk of latent post-harvest pathogens risks failing to consider the full range of post-harvest pathogens that may actually occur. The Review (p. 120) states that for Coprinus rot:

“Infections of fruit usually remain asymptomatic at harvest but become apparent after an extended period of storage”.

In this case, the methodology used in the Kim and Xiao survey would not have detected Coprinus. This is likely to affect the risk of importation assessment (currently Low). The Review (p. 120) then states that: “Symptomless fruit infected with C. psychromorbida may be distributed…”

The overall likelihood of entry is determined to be ‘Low’. The evidence used to support this indicates to the contrary.

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In summary:

• Symptoms may not have developed by the time of harvesting, and there is a possibility that symptomless infected fruit may be harvested, stored and packed for export. • Symptoms occur most frequently in apple fruit that has been stored for extended periods. • Apples can remain asymptomatic for six to seven months in commercial storage. Most of the evidence around the risk of importation supports a higher risk rating and is in places contradictory so that it is not clear how the risk assessment was determined. APAL has concerns around the efficacy of post-harvest treatments (p. 119):

“High pressure washing and chlorine dipping at concentration of 100ppm or more are standard procedures in packing houses in the PNW-USA (Washington Apple Commission 2018). These procedures are effective in removing or devitalising micro-organisms from the surface of fruit (Beuchat 1999)”

Then in the following dot point:

• “High pressure-washing and sanitation measures are unlikely to affect the viability of infections of the pathogen within fruit.” Which of these statements is correct?

Furthermore, if the pathogen is present within symptomless fruit how effective are the high pressure washing or chlorine dip procedures as a treatment?

APAL also notes that the Beuchat (1999) reference is a review paper of treatments to mitigate food borne illnesses associated with a range of bacterial contaminants (e.g Listeria, Salmonella). This reference is irrelevant to the assessment. The efficacy of chlorine treatment against fungal structures and bacterial structures is very different. Furthermore, chlorine as a sanitiser relies on contact – how effective is it at penetrating the fruit to kill Coprinus or other latent pathogens inside the fruit?

The ability of C. psychromorbida to grow in cold storage (p. 121) also raises concerns about the efficacy of post-harvest treatments.

In the case of Coprinus rot, the pathogen is reported as “occurring on apple and pear fruit including those stored for extended periods (Spotts 1990b)”.

Symptoms can develop at temperatures between -1 and 2 and it can spread between fruit even during cold storage. ℃ The Review notes that Coprinus rot is “….often mistaken for bullseye rot”. A clear process is required to ensure that these rots will be identified correctly during inspections. The Unrestricted risk estimate for bull’s eye rot is rated as Very low but impacted by the same deficiencies in rationale for assessment highlighted for Coprinus rot. What assurance is there that these different rots will be correctly identified during inspections? If the two rots are often confused, then this needs to be reflected in risk ratings for the two species.

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Disposal of infected fruit is not properly assessed

The disposal (already mentioned earlier in this response) of fruit affected by Coprinus rot is assessed in the Review as likely to be via commercial or domestic systems, and discarded fruit is likely to enter municipal waste systems. With the number of wild apple (and other fruit) trees growing alongside roads and train lines this seems an unrealistic assumption (there are several websites and blogs dedicated to ‘feral fruit’ see for example https://aboutregional.com.au/feral-fruit-between-coast-cooma-canberra-delicious-and-part- of-history/ and https://roadsidefruittrees.weebly.com/blog). Depending upon the extent of the rot - and noting that it may also be asymptomatic - a reliance on infected material all going to commercial waste is unrealistic, and therefore understates the associated risk. The Review states that during summer, hot dry conditions are likely to limit the growth of the fungus from discarded fruit or packing materials. Yet the fungus is reported to be able to form sclerotia to survive adverse conditions such as hot summers (Spotts et al. 1981), and these can serve as propagules if they come into contact with host material. Traquair et al. (1987) report from Spotts et al. (1981) that “Although sclerotial production was not observed for the apple isolate causing Coprinus rot, black sclerotia were observed on the wood of storage crates infested with this fungus on pears in Oregon. Sclerotia are likely to be significant survival propagules and sources of infection. Sterol inhibitors and dithiocarbamates were shown to reduce mycelial growth of the Coprinus sp. and, ziram applied to trees before harvest was shown to control Coprinus rot in stored fruit (Spotts et al. 1981).”

Spotts 1981 report:

"Black sclerotial patches were observed on inoculated pear wood after 12 wk." [in their inoculation trial]

And, also from Spotts (1981)

"Hanna (1939) reported the production of sclerotia in cultures by the Coprinus identified then as C. urticicola from wheat and nettles at 10oC. Production of sclerotial patches by the pear Coprinus supports this observation. These structures may be significant in the survival of the fungus on crating materials used in cold storage of fruit."

More information is requested about what measures are in place to minimise this risk.

The Review indicates that the fungus can infect a variety of hosts, many of which are “common and abundant in Australia” and that it grows rapidly under temperate conditions (these occur typically around Melbourne and Sydney) and that it can survive on living and dead material, including even horse manure. The importance of the urban and peri-urban fringe was noted earlier in this submission as the most likely place of introduction. However, this has been largely ignored for almost all pests and pathogens when considering distribution, establishment and spread. The Review also notes (p. 120):

“In Australia imported apples will be stored and transported under cold storage at 0° to 2°C (Good Fruit Grower Magazine 2014; Iowa State University Extension and Outreach 2008; Kupferman 1996; University of Maine 2020)”

None of these references mention export of apples to Australia and as such do not support the statement being made in the Review.

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However, as this fungus is able to survive cold temperatures (as are many of the fungi – particularly post-harvest fungi - listed in the document) the effectiveness of cold storage as a risk mitigation measure needs to be examined more thoroughly.

Dispersal mechanisms listed for the fungus are unclear or unsupported The Review states (p. 121) that “…the only known dispersal mechanism for this fungus from fruit is by mycelia.” This is not supported by any references. However, according to Gaudet et al. (1990) “The presence of monokaryons suggested that a sexual fruiting stage may be involved in the dissemination of this fruit rot pathogen but, to date, a fruiting body has not been associated with FRLTB [Fruit rot low temperature basidiomycete] strains."

Here, again, what is written in the Review does not completely accord with the attributed source.

It is difficult to reconcile a rating of ‘Low’ for distribution when most of the arguments in this section (pp. 120-22) argue the converse. With the exception of fruit displaying obvious symptoms all other points in this section point to a high likelihood of distribution.

The relevance to the Review’s risk assessment of the following references is questioned. None of the references cited to support the point that “Harvested apples are normally cold-stored at 0° to 2°C” mention importation of apples to Australia although they all indicate survivability at low temperatures. The following points are noted:

• The Iowa State University Extension and Outreach (2008) describes how “Storing apples at home is convenient and, if done properly, can be economical. Home- grown fruit that may otherwise go to waste can be stored for several months.” The Publication includes tips on harvesting and storing home-grown apples. The relevance of this to the risk assessment of imported apples from the PNW needs to be addressed. • The Good Fruit Grower magazine 2014 reference outlines trials to determine post- harvest storage conditions for Honeycrisp apples; it appears that only the title of the article may have been read: “How to harvest and store WA 38 (Cosmic Crisp®) apples”. • We were unable to access Kupferman (1996) • Similarly, the University of Maine reference provides general storage advice with no reference to the storage and transport of imported apples in Australia. The Review states: “Coprinus rot occurs in the PNW in apple orchards at low incidence”. The references provided to support this statement do not provide specific data on the incidence of this rot in apple orchards or packing sheds.

• Spotts (1990b) – A Compendium reference that has in fact been updated; a second edition is now available and states that the disease has been found sporadically in the PNW on apples and pears. • Willett (1989) – reference link does not work. • APAL questions whether the listing of a pest in handbooks is a good indication of incidence? • As mentioned at the beginning of the discussion on Coprinus rot, the fruit collected in surveys of Kim & Xiao (2008) were selected only if they had decay symptoms and thus was biased toward symptomatic fruit. Changing climatic conditions will also change the severity and incidence of pests.

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The Review in unclear as to the host status of Coprinus psychromorbida. In various places it notes that it is a pest of apple and pears, a pest of forage legumes and winter cereals (p. 118), then as a post-harvest pest of pear (p. 119), is only listed as pest of pear in the PNW-USA (p. 119), can infect most apple cultivars (p. 119) then a wide variety of hosts (p. 121) occurs in low incidence in the PNW in apples (p. 120) mainly a pest of pear and numerous hosts in Australia (p. 124). This lack of clarity and consistency does not instil confidence in the subsequent risk assessment.

APAL notes that NZ lists C. psychromorbida as one of the regulated pests for pears from Oregon. This warrants the question as to why Australia has a different view and why this was not explored in the Review, particularly given the emphasis on the NZ export protocols in the current PNW-USA Review. The Review (p. 121) is unclear about the mode of spread between hosts stating that

“Transfer to a new host by vegetative mycelia is unlikely.”

Then:

“Asexual morphs of the fungus such as mycelia are only capable of spreading through direct contact (Gaudet, Kokko & Sholberg 1990).” And:

“If the fungus were to reach a new potential host, infection could occur through growth of mycelia.”

The contradictions in these statements need to be addressed. Further, clarification is required on whether the use of ‘fungus’ in the last quote mean only mycelia or any life form of the fungus?

Sclerotia of Coprinus have been reported (information not presented in the Review) on the wood of storage crates infested with the fungus on pears in Oregon (Spotts et al. 1981) who reported that:

“Sclerotia are likely to be significant survival propagules and sources of infection.”

What is the potential for Coprinus rot to be present on storage crates and packing material from the PNW?

In regard to the discussion on the establishment and spread within Australia, conflicting reasoning is presented. This first citation indicates that parts of Australia are suitable for the survival of Coprinus rot, while the second that it is less likely.

“Coprinopsis psychromorbida occurs in western Canada (including Alberta and British Columbia) and the USA (including Alaska and the PNW) (Farr & Rossman 2009; Smith 1981; Traquair 1980, 1987; Willett et al. 1989). Environments with climates similar to these areas exist in colder parts of temperate south-eastern and south-western Australia (Peel, Finlayson & McMahon 2007), suggesting that these parts of Australia are likely to be suitable for survival of C. psychromorbida (Bureau of Meteorology 2018).”

Then:

“The restricted distribution of C. psychromorbida to climates with cold winters suggests it is less likely to establish in many regions of Australia. For example, California is a large pear producing area in the USA (University of California 2017) and has a warm Mediterranean climate (Weather Atlas 2020) typical of pome fruit producing areas in Australia such as the Goulburn

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Valley in Victoria (Bureau of Meteorology 2018). There are no reports of C. psychromorbida associated with Californian pome production.”

Given the lack of clarity, this section on likelihood of Entry, Distribution and Establishment needs to be reassessed and rewritten. Similar comments can be made around the discussion on pp. 123-24.

Phacidiopycnis rot (Discula pyri)

The Review accords the Unrestricted risk for Phacidiopycnis rot as Very low.

From APAL’s perspective, the majority of the evidence provided is more relevant to pears than apples. Xiao and Boal 2002, 2004a, 2004 b and 2005c, and others, all refer to research conducted on pears. In particular, the evidence to support the claim that D. pyri is unlikely to be associated with apples from PNW relies on pear data.

APAL questions on what basis it was determined that the organism has only a “...rare association with apple fruit…”? (p. 129). Additional evidence/data is required to confirm how closely the risk and biology of Phacidiopycnis rot in pears equates to apples. Further data is also required about the incidence and severity of Phacidiopycnis rot in apples in the PNW.

The points listed in the Review (p. 128), despite largely quoting studies that focused on pears, illustrate the risk of symptoms developing (on pears) at a later date in storage:

“Discula pyri causes infections which are initially asymptomatic but are likely to be detected in early storage.”

“Infections of the stem - and calyx - ends …usually take place in the orchard with symptoms developing during storage”, and,

“Symptoms of infections with D. pyri are first observed after approximately three months in storage and increase with time”.

What do these findings mean for apples in storage and the risk of introduction of the pest?

The Review states that the fungus is more common on pears in the PNW, and “Conidia from pear cankers may also provide a source of inoculum for apple infections”. More data is required on the likelihood of cross-infection from pears to apples. Related to this, in assessing risk, is the extent to which pear trees are grown in close proximity to apples in the PNW-USA. The Review also indicates that crab apples may provide a source of inoculum for apple infection. What measures are in place to manage this risk?

Increasing prevalence of D. pyri Of concern to APAL is that D. pyri is reportedly becoming more prevalent in the PNW. The Review states that “Since 2002, fruit surveys have not detected D. pyri to any significant level on apple”. However, the author cited (Amiri 2020) actually reports that:

“Recent surveys have confirmed that these rots continue to be an emerging threat in the PNW and will require future management attention”.

This implies that the rot is becoming more frequent or more severe. Given the increasing level of detection and the need for future management attention, the risk assessment of Very low needs to be reviewed. Further evidence of the actual incidence and severity of D. pyri on apples is required, rather than relying on data from pears.

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Many of the general concerns already raised regarding the assessment for post-harvest rots in the previous section on Coprinus rot are also relevant here. The Review reports that a 2017 survey found D. pyri to cause 3.9% and 6.7% of pear decay in Washington and Oregon respectively (Ali et al. 2018) and that fruit surveys since 2002 have not detected the fungus “to any significant level” on apple. What is a significant level? The Kim & Xiao (2006) referenced in this section relies on a 2003 survey that sampled decayed apples and as a result has sample bias issue as mentioned earlier regarding sampling of symptomatic fruit. Because of this, the evidence as to prevalence of D. pyri in apples in the PNW needs to be revisited. The reference link for Xiao (2007) did not work, but we located: https://treefruitresearch.org/report/sphaeropsis-rot-in-apple-2/ which refers to Sphaeropsis rot.

US imports rejected entry into Israel due to D. pyri The Review notes that a number of pear consignments have been rejected entry to Israel due to presence of D. pyri. Further clarification is required around this statement as to incidence, number and temporal trend, and how this may impact on apples, including, as mentioned above, cross-infectivity between pears and apples.

The arguments relating to likelihood of Importation largely rest on unsubstantiated statements that the frequency of this pest on apples is low. As discussed above, this argument relies purely on pear research and sampling of only symptomatic apple fruit. Evidence as to prevalence of D. pyri in apples in the PNW must be located and comprehensively reassessed before making any assessments based on this assertion. Furthermore, most of the evidence on p. 128 of the Review would suggest that as a result of the time taken to develop symptoms post-harvest, that if present, the fungus is likely to be imported.

Also of concern is the ability of D. pyri to develop under cold storage conditions:

“Post-harvest infections by D. pyri were observed to take three to four months to develop at 0°C” (p. 127; NB. Data presented is from pears; what happens to apples in cold storage?).

The Review states that “The longer the period that apples from the PNW-USA are in cold storage before export to Australia, the more likely it is that infected fruit will express symptoms. Symptomatic fruits are likely to be detected and discarded before export.”

How long are fruit likely to be stored prior to export? Given that symptom development can take as long as three to four months, is this a reliable strategy for reducing risk? If storage time is seen as a risk mitigating factor by increasing the likelihood of detection, then it would seem logical to set some parameters around storage.

The same references (p. 129) are included in this section with regard to how the apples will be cold-stored and transported in Australia as were presented for Coprinus rot above (Good Fruit Grower, Iowa State etc.). The use of these references has the same inherent faults as already outlined in the discussion under Coprinus rot above.

The Review states that “Early symptoms of D. pyri are similar to those of grey mould (Xiao 2006) which may make early detection of the disease on stored fruit difficult in Australia.” This is a concern for risk of distribution and importation. Of concern is how the disease will be distinguished during inspections and how retailers and consumers will differentiate the disease if they come across rotten fruit. Also, of concern is that Xiao 2006 is cited in the Review, yet it refers to symptoms on pears rather than apples. What do the early symptoms of D. pyri look like on infected apples?

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Unfortunately, as for Coprinus rot, the evidence cited to support the risk ratings under Importation, Distribution, Establishment and Spread is confused and generally supports a higher risk than that assigned, in particular the ability of the species to survive cold temperatures and to be asymptomatic with long latent periods.

APAL submits that as with Coprinus rots this species needs a reassessment and that the assigned risk is not supported by the evidence provided.

Bull’s eye rot (Neofabraea malicorticis and N. perennans (Western Australia))

Neofabraea malicorticis is an Apple Industry High Priority Pest; N. perennans is a High priority pest for Western Australia.

The Unrestricted risk estimate for these two species is assessed as Very low, despite both fungi being acknowledged in the Review to be widely distributed in North America resulting in significant costs to orchardists.

Neofabraea malicorticis (Syn.Cryptosporiopsis curvispora) was assessed in the IRA for apples from China as having an Unrestricted risk estimate of Very low and no specific risk measures are required.

Neofabraea perennans has not been assessed previously, however the Review ascribes similar biology to both species quoting Pscheidt & Ocamb (2019). This reference (PNW Pest Management Handbook) treats the species separately but notes that the two diseases are “somewhat similar”. No further clarification is provided as to what this statement means particularly with respect to biology and epidemiology. Further clarification is required about what is meant by this.

However, APAL notes that:

The Review does identify differences between the two species:

“In the PNW-USA, N. malicorticis is very common in the humid areas west of the Cascades Range, while N. perennans commonly occurs in the drier areas east of the Cascades (Dugan, Grove & Rogers 1993; Grove 1990a; Kienholz 1939).”

This difference in preferred/conducive environmental conditions and how it may have an impact upon the risk of importation and establishment potential in Australia warrants further clarification by the Department, including from where apples are sourced for export. Australia has both humid and drier areas that would accommodate establishment and spread of either species.

As with almost every other potential pest/pathogen in this Review the same weaknesses in substantiation identified in previous sections are evident in the assessment of Bull’s eye rot and, again the conclusion is reached that the risk assessment as currently performed is inadequate.

As with other post-harvest fungi assessed in the Review, these fungi are able to survive cold temperatures thus it is difficult to envisage cold storage as a risk mitigation measure. Furthermore, the fungi are not killed by cold storage, but this can delay onset of symptoms. Symptoms are reported to appear on fruit after several months of storage.

The level of risk is not supported by a full reading of the available references, as evidenced by the examples presented below.

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The Review of the latest literature dismissed Aguilar et al. (2018) as not containing new information that would change risk settings. However, Aguilar et al. (2018) referenced quarantine issues related to these two pathogens following export of USA apples to China and this is not mentioned in the Review:

“Recently, efforts to expand existing trade relations between the U.S. and The People’s Republic of China were curtailed for a 2-year period due to the detection of quarantine pathogens on apple shipments originating from Washington State (WSDA 2014). Identification of post-harvest pathogens causing Sphaeropsis rot (Sphaeropsis spp.), speck rot (Phacidiopycnis washingtonensis), and bull’s-eye rot (Neofabraea spp., Phlyctema sp.) during the summer of 2012 resulted in a temporary suspension of apple fruit trade between the two nations (Wheat 2013). By 2014, a bilateral trade agreement was reached and access to the Chinese market was reinstated with the stipulation that Washington growers and packers abide by phytosanitary guidelines and shipment inspections to prevent further spread of post-harvest pathogens and other important pests (Heping 2015; Warner 2014).”

APAL requests information as to what these phytosanitary guidelines and inspections entail, what changes were made to reduce the risk of this occurring again, and how might they relate to trade with Australia.

Aguilar et al. (2018) also stated that:

“In addition to posing a quarantine concern, bull’s-eye rot has been a major post-harvest disease of apples and pears grown in the PNW for over a century (Cordley 1900)” and

“While all four fungi commonly occur in the PNW, only P. vagabunda N. kienholzii, and N. perennans have been documented in the major pome fruit production districts of central and eastern Washington (Spotts et al. 2009).”

The paper also states that: “Despite the importance of bull’s-eye rot as a major post-harvest disease, little has been published relating to effective control of the causal fungi through application of chemical fungicides registered for pome fruit production in the U.S.”

This last point is significant as it notes that diseases may be important but can still be little studied and hence have little published information.

Based upon these quotes, APAL asks how the reference for Aguilar et al. (2018) could be dismissed as not containing new information of relevance to risk ratings?

The severity of the disease in the PNW also seems to be underrated in the Review see: http://treefruit.wsu.edu/crop-protection/disease-management/apple-anthracnose/ (Accessed Nov 2020).

Post 2008 literature Garton et al. (2016) is dismissed in the Review as containing no new information. However, in reference to N. malicorticis this article states “Growers in the maritime Pacific Northwest have reported removing 2-5% of trees each year and in some cases entire orchard blocks to prevent the spread of cankers.”. This same article also mentions other Neofabraea species that cause symptoms on apple that are not considered in the Review (these species are addressed at the beginning of this section). Infection incidence is reported as exceeding 50% (Garton et al. 2016). These figures are significant and APAL requests how they can be reconciled with a Consequence rating of Low?

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Neofabraea malicorticis (as Cryptosporiopsis kienholzii) was previously assessed for the risk assessment for China where its Unrestricted risk estimate was assessed as Very low.

There is little detail provided on how the ratings for entry, establishment and spread and consequences were assessed – other pests have much more detail provided. Based upon the evidence provided and the conflicts therein the rating of Very low is inappropriate and requires reassessment. The Review has also not included Aguilar et al. (2019) in its risk establishment for bull’s eye rot. This study, which investigated the timing of infection of these two fungi, should be considered relevant to the risk assessment.

There is little evidence provided to indicate that basing the current assessment on the China IRA is appropriate. What are the levels of incidence of the pathogen in China and how do they compare with PNW-USA? APAL also notes that, in China, Neofabraea is a pest of concern and that China has stopped imports in the past from the USA (mentioned above) and Poland (https://www.freshfruitportal.com/news/2017/03/22/chinese-authorities-detect-neofabraea- fungus-polish-apple-shipment/ Accessed Nov 10 2020).

As previously highlighted, APAL again notes inconsistencies in the Review on the methods of fruit disposal and queries the rationale behind waste disposal decisions throughout the Review. For example, fruit with bull’s eye rot may be discarded in compost or the natural environment which differs to fruit disposal suggested for other rots mentioned elsewhere. T

The evidence cited above also suggests that the rating consequences as Low is inappropriate.

The Unrestricted risk estimate for this pest does not reflect the risk based upon either the evidence provided or that from extra evidence cited above. APAL believes that this assessment needs to be redone.

European Canker (Neonectria ditissima)

The assessment concludes that ‘When routinely applied industry commercial practices such as in-field controls and packing house sanitation are taken into consideration, the Unrestricted risk estimate for N. ditissima on apples from the PNW-USA pathway has been assessed as Negligible, which achieves the ALOP for Australia. Therefore, no specific risk management measures are required for N. ditissima on the PNW-USA apple pathway.’

As for the fire blight analysis, the Review draws heavily on the NZ assessment (Negligible) however there is little evidence provided to justify the comparability of the two countries and in fact the Review notes that there are differences (p. 142). The discussion on European canker has similar issues as those highlighted previously for fire blight in this submission.

For example, on p. 143:

“The disease is found primarily in high rainfall areas of Oregon along the coast and Willamette Valley, and rarely in southern, central or eastern parts of the state (PNW Handbooks 2019a). Neonectria ditissima has also been reported at low prevalence in apple orchards in Washington, which is the major apple production state (Grove 1990b; Kim & Beresford 2012; Shaw 1973). and

The three major apple production areas in Oregon are the Willamette Valley (western Oregon), the Mid-Columbia Valley and Milton-Freewater area (Oregon State University 2020), with the highest production coming from Umatilla in eastern Oregon. The major apple production areas

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in Washington, based on USDA-NASS (2006) and Washington Apple Commission (2020b) are located in the eastern foothills of the Cascade mountains.”

Furthermore, on the same page: “There are no known reports of N. ditissima causing apple fruit rots in the major production areas of PNW-USA.”

This not only contradicts the previous quotations but study by Kim & Xiao (2008) is biased toward symptomatic fruit as already highlighted. APAL re-iterates that this study cannot be taken as an indication of incidence as it only considered symptomatic fruit and the main risk is from asymptomatic fruit.

However, what is even more troubling is that the other reference quoted to justify the statements about incidence (Amiri 2020) has nothing to do with European canker. The following, on p. 144, is then presented when discussing how likely the pathogen is to be imported:

“These conditions are unlikely to occur in the exporting region. The lack of reported fruit infections recorded in the PNW-USA supports this assessment of limited potential for fruit infection.”

This is not only contradictory to earlier statements on p. 143 but also warrants the question as to whether areas where the pathogen is present will be excluded from export, particularly the Willamette Valley, which is a significant production area? Furthermore, if there is a lack of reporting, what measures are in place to ensure the biosecurity risks are minimised?

Also, of concern is that Neonectria ditissima has a latent phase and can persist in fruit and twigs for long periods of time without visible symptoms and as the Review acknowledges, only develops during storage (p. 141). This means the pathogen is protected from disinfection strategies and is difficult, if not impossible, to detect during grading and inspection. How would asymptomatic infections be managed at the border?

The Review indicates that in-field fungicide applications for canker control are conducted before autumn rains. Unfortunately, there is no evidence as to the efficacy of control methods used. Xu and Robinson (2010) found that apple fruit were most susceptible to infection up to four weeks after pollination (with 50% of fruit infected when inoculated up to four weeks after full bloom). The susceptibility decreased initially until approximately two months after full bloom and then increased gradually until harvest. According to the article by Xu and Robinson (2010) the application of in field fungicides at the time of autumn rains is not when the fruit is at its most susceptible. Thus, APAL queries as to whether infield fungicide applications are applied at the most appropriate/efficacious time in the PNW? Was this investigated by the Department during field visits? Evidence provided to reach the conclusions for European canker in the Review is often poor, outdated (eg. APHIS 2007a – pers. Comm), misinterpreted, inappropriate or contradictory. The following are examples:

• McCartney (1967) (cited on p. 143) reported losses of 10–60 per cent for susceptible cultivars such as Delicious, Golden Delicious, Jonathan, Rome Beauty and Tomkins King in California however this information has been omitted from the Review and furthermore no information is provided on the susceptibility of cultivars that may be exported to Australia. • This same report is cited to present climatic conditions (for California) and draw conclusions for the production areas of the PNW but the information about fruit infection presented in the paper is ignored.

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• The Review also states “Fruit infection is rare, only occurring when there is unusually high summer rainfall (McCartney 1967; Nichols & Wilson 1956).” These references are very old and apart from potential change to climatic conditions over the last 50+ years would not appear to be true. Xu and Robinson (2010) report that “Overall, the incidence of fruit rot was influenced more by fruit maturity at the time of inoculation than by duration of wetness”. APAL asks whether occurrence of the pathogen and the infection of fruit has changed since the 1950s and 1960s and what role the changing climate has had on changes to infection including host susceptibility/physiology and pathogen infectivity. Further evidence around this is requested.

APAL queries the rationale for comparing the climate in the PNW to California? They are not the same. California is largely classified as Hot-Summer Mediterranean whilst the PNW is Cold Summer Mediterranean or Oceanic (Koeppen Climate Types) see: https://upload.wikimedia.org/wikipedia/commons/5/54/US_50_states_K%C3%B6ppen_with_ territories.png (Accessed 17 Nov 2020).

In addition, the climatic modelling by Beresford & Kim was reported in 2011. How relevant is this model under a changing climate scenario and to what extent is it validated for the present?

Have climatic events and conditions changed in the PNW to change the prediction in the model? The model was based on the absence of data around incidence of Neonectria in the USA. Since the model’s construction was based on pre-2011 USA distribution have there been any changes in the range of Neonectria in the USA? If so, has the model been adapted? Absence of data is not a strong basis for a model.

The Review states that existing in-field, harvest and post-harvest practices for production handling and packing will greatly reduce the chance of infected apples being exported. What these practices are is not disclosed nor is any evidence presented to show that they do what is claimed. APAL requests further information on these.

The timing and method of infection also affects the development of the fruit rot in storage (cited in the Review: Swinburne 1971, Brown pers comm. 2006) and this is overlooked in the Review’s assessment. The Review also does not consider the possibility of infection post- harvest (for this species or post-harvest pathogens generally). APAL asks will there be any guidelines as to monitoring the washing and dipping tanks of packing lines for post-harvest diseases?

Xu and Robinson (2010) report that the rot, which is often found at the fruit stalk end, is difficult to spot on the grading line, but becomes obvious during marketing leading to rejection of fruit consignments. Surely this increases the risk of infected apples being imported to Australia. This piece of information from Xu & Robinson was omitted from the Review. APAL would also like clarification about whether Neonectria can be found in the pedicel/fruit stalk wood of the apple.

The Review refers to fungicides used in the orchard (and chlorine 100 ppm) in the packhouse being used to control Neonectria. Research in UK has shown that even the most stringent fungicide programs only reduce canker incidence (Cooke, 1999; not referenced in the Review) and this approach does not seem to prevent the fungus from invading the trees (causing cankers which, as cited in the Review, provide the inoculum for fruit infections). Cooke also reports on the efficacy of the timing of fungicide application on the development of post- harvest rots. Similar challenges can be demonstrated in other crops. The effectiveness of control programs in the PNW-USA is not addressed in the Review.

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APAL also questions how fungicide application is effective when the fungus is latent within the fruit. Where the fungus is present within asymptomatic fruit it would be protected from surface disinfestation as well as remaining undetected during inspection.

Spores are readily produced on infected fruit providing strong potential for spread. Is there any evidence that 100 ppm chlorine is sufficient to kill conidia of Neonectria? The fact that spores are very ‘unlikely’ to survive cold storage and transport from PNW to Australia because they do not germinate below 6oC again equates survival with growth. They are not the same. Evidence needs to be provided that spores are killed by low temperatures.

The comment about high pressure washing, and chlorine and the Beuchat (1999) reference has been addressed earlier. This reference is for food borne pathogens of humans.

APAL notes that whilst varietal susceptibility is variable, our understanding is that no variety is resistant to the disease. APAL also notes that pear is susceptible and has been shown to be affected in the PNW. The proximity of pear orchards to apples, potential for cross-infection and the potential risk need to be explored.

The rationale for the Very low rating for likelihood of distribution is unclear both in this and the previous assessment for NZ. Plenty of evidence is available that asymptomatic fruit can carry the fungus. Post 2008 Literature

Dubin and English (1975) is incorrectly referenced and the article referenced does not relate to the content as written in the Review. The Review appears instead to be referring to the article by the same authors entitled: ‘Effects of Temperature, Relative Humidity, and Desiccation on Germination of Nectria galligena Conidia’ that can be found here: https://www.apsnet.org/publications/phytopathology/backissues/Documents/1975Articles/ Phyto65n05_542.PDF

(Accessed 20 Nov 2020).

As has been highlighted for every other pest/pathogen, much of the additional literature, cited as consulted since the previous Review, is not relevant, of marginal relevance to risk, or its relevance has been overlooked.

• Amponsah et al. (2015) – is on susceptibility of different wounds to infection; why this was dismissed as irrelevant is questionable. • Farr & Rossman (2019) – this a database. • Kim & Beresford (2012) – is a climatic model and is cited a number of times. • Walter et al. (2016) – considers how many conidia are required for infection and is not discussed further in the Review. • Wenneker et al. (2017), however, is about methods of detection for latent infection which would seem pertinent when considering the risk of importation of the pathogen on fruit particularly noting the findings of Edwards (2006) which are discussed below but not utilised in the Review. See https://www.horticulture.com.au/globalassets/hort-innovation/historic- reports/investigating-the-current-state-of-knowledge-worldwide-regarding- neonectria-galligena-ap05029.pdf (accessed 22.11.20).

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Furthermore, the Review of new literature has missed some relevant recent publications, some of which would affect the risk assessment ratings, including:

• Xu and Robinson (2010) - report on the effect of fruit maturity and wetness on the susceptibility to infection of apple fruit by N. galligena (Syn. N. ditissima) finding that rot development was influenced more by fruit maturity at the time of inoculation than by the duration of the wetness period. They also report that young fruit were more susceptible to infection (50 % of fruit infected when inoculated up tofour weeks after full bloom), and susceptibility decreased initially until around two months after full bloom and then increased until harvest (refer also to p. 41 of this response). • Gomez-Cortecero et al. (2016) – report on susceptibility of apple varieties and the basis for resistance. • Plante et al. (2002) – a study on the genetic diversity of the fungi in North America. • Xu et al. (1998) – reports on the effect of environment and wound age on infection by N. galligena. Edwards (2006) investigated the current state of knowledge worldwide regarding Neonectria galligena and noted that:

“There is no method for detecting symptomless infections, particularly latent infection in fruit. This seriously limits the development of strategies to mitigate against entry of N. galligena via imported fruit.”

APAL questions how this statement can be reconciled with the Review’s rating for importation and also for detection at the border? As has been noted earlier in this submission how will asymptomatic infections be detected upon arrival?

Saville (2017) and Saville (2014) noted in the UK that up to 10% of trees can be lost annually due to canker and infections occurring during flowering time and this can result in fruit rots which either develop in orchard as eye rot or remain asymptomatic and only develop post- harvest. Post-harvest losses can be as high as 10% of stored fruit.

With respect to the risk mitigation in section 5.1.3: “the Department recognises that the current industry commercial practices in PNW are similar to the IPM practices for these pests applied for apples from NZ. The Department proposes that these controls are appropriate to manage the risk by Neonectria ditissima from PNW-USA consignments.”

APAL is unable to comment on the veracity of this statement as little information is provided to indicate what these practices are. Similarly, more detail is requested about what the in-field controls are? Table 3.2 and Figure 3 provide little detail.

The pathogen has an extensive host range that would have serious implications for not only horticultural crop production, but also for forestry, amenities horticulture and urban landscapes in Australia. It is noted from the NZ (2011) IRA that Consequences were assessed as Low and the environmental impact as Significant at the local level, however much of the discussion on impact and eradication suggested a higher level of Consequence. APAL questions the rating on Consequences and notes that this may change the risk rating for this pest. Consequences can be severe, see: https://www.stuff.co.nz/business/farming/7517825/Canker-threatens-apple-orchards (Accessed 17 Nov 2020)

APAL submits that the entire section on European canker requires a more rigorous approach and therefore a reassessment that accurately captures and reflects current knowledge and risk.

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Truncatella leaf spot (Truncatella hartigii)

The Review notes that Truncatella was not detected in the survey by Kim and Xiao (2008) conducted in 2003–2005. As has been noted earlier this study selected only symptomatic fruit meaning that it is of limited value in determining incidence of latent pathogens. Truncatella has also been reported in seeds. APAL notes Kim and Xiao (2008) did not attempt to isolate from seeds of any fruit collected. Can data be provided to assess the risk of Truncatella being present in seeds?

APAL notes that from the China assessment: “Very low risk of importation largely due to absence of records” and queries whether this is a valid deduction. Whilst it could be argued that the degree to which a pest is a problem may be reflected in the amount of information available, this does not follow that this reflects risk. There are also limited records from the US.

APAL notes that it is difficult to assess the consequences of entry, establishment and spread because there is little information available.

APAL notes, again, the confusion about fruit disposal identified in other sections in the Review and discussed above. In this section, apple fruit is described as being disposed of by composting or in the natural environment where the fungus may spread to other hosts. How are consumers to differentiate between infected apples to dispose of their fruit accordingly? Post 2008 Literature

APAL questions the relevance to risk of the recently reviewed literature:

• Farr and Rossman (2020): Database – this is a huge volume from the American Phytopathological Society that lists fungi on plant products in the USA. The Department has stated it reviewed the literature but does not share any of the information identified about the fungus on apple, if there was any. • Fatima (2019) – APAL was unable to access this document. • Ivanová (2016) – this article reports on the similarity of and differences between the fungi Pestalotiopsis funerea and Truncatella hartigiipaper that damage needles on Pinus. Unless there is cross-infectivity from Pinus to apples, the relevance is questioned. • Pusz et al. (2015) – airborne fungi in a cattle barn of a dairy farm in Poland. How is this relevant to apples from PNW? Do they bring in manure from Poland? For a pathogen that is considered by the Review as being of minor or very minor importance, a very detailed description of symptom development post-harvest is provided. What is the reference for this description?

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Viruses

Apple scar skin viroid

This is also known as pear fruit crinkle, dapple apple, Japanese pear fruit dimple and pear rusty skin. This viroid is of concern because it can be seed-borne as well as in the fruit. Given the number of trees growing by roadsides, there is a risk of the viroid establishing in Australia.

The Review has not made the case for similarity of risk with that from China.

The Review notes that trees of tolerant apple cultivars may not express symptoms for many years after infection and fruit may be asymptomatic. Of particular significance here is the extent to which tolerant cultivars that do not express symptoms are likely to be imported. Further information around this is requested. To support the same risk estimate on Importation as that from China the Review needs to establish how much similarity there is in the likely varietal mix to be imported from the PNW- USA and that from China.

It is clear that risk is strongly dependent upon the percentage of symptomless and hence tolerant fruit that are imported. This has not been established. It would also be useful to know the extent of measures in the PNW to test if trees are infected with the virus to ensure fruit that is exported is not carrying it? Have any surveys been conducted?

The Review also notes that the virus can survive cold storage, thus it is difficult to see how a risk of importation assessment of Moderate can be justified as many of the arguments advanced in the Review do not support such a position.

This section does not adequately cover the various risk criteria and apart from Importation has provided no additional information on the other risk criteria, relying instead on those for apples from China.

Based upon the evidence provided in the Review and the lack of scrutiny around the issues raised by APAL above, it is submitted that the Unrestricted risk estimate of Very low is not supported and requires reassessment.

For example, if the risk of importation was raised to High, then the Unrestricted risk estimate would be raised from Very low to Low.

Post 2008 Literature The comment about references quoted as supplementary to the earlier 2008 Draft as adding no new information is misleading.

• The EFSA PLH Panel et al. (2019) is a risk analysis for the EU and notes that this viroid: “ASSVd meets all the criteria evaluated by EFSA to qualify as a Union quarantine pest with the possible exception of the criterion of absence from the EU territory.”

• Pscheidt and Ocamb (2019) – the reference link opens to a page in the PNW Pest Management Handbook in which the section on this viroid is only briefly summarised with other information.

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• Walia et al. (2014) is an identification guide on herbaceous plants whilst Walia et al. (2015) notes that whitefly can transmit DNA of this viroid. Why is this not considered relevant to risk? In assessing risk from the virus there is little discussion in the Review as to the potential of arthropod species to vector viruses. Was this considered and what was the outcome?

Summary (4.29)

Having considered the evidence provided for the Unrestricted risk estimates APAL contends that the ratings for those pests assessed in Ch. 4 are in large part not supported, and in fact when the cited data is accessed it does not accord with the summary provided in the Review. The overall impression is of a lack of rigour that is reflected in citation errors, inability to access URLs and either incomplete or unsupported representation of the science with important pieces of evidence overlooked. Consequently, APAL considers that the Unrestricted risk estimates for the following species are understated and require reassessment:

• Spider mites • Apple curculio • Apple fruit moth • Lygus bugs • Lacanobia fruit worm • Coprinus and other post-harvest fruit rots.

In addition, the ratings for spider mites, apple curculio, apple fruit moths and lygus bugs are inconsistent with those of our trading partners including in some instances the USA.

Mitigation measures for fruit moths do not correspond with existing import biosecurity conditions for NZ fruit, nor the Western Australia entry requirements. As noted earlier, the requirement for appropriate data packages, as part of any systems approach, that would be acceptable to WA needs clarification.

The risk estimates and mitigation measures for a number of pests are also inadequately aligned with existing regulations or inadequately evidenced including those for fire blight, leaf curling midge and European canker.

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Ch 5 Pest Risk Management

There are a number of factors which need to be taken into account when considering the measures proposed by the Review for controlling and managing pests particularly in-field controls, orchard surveillance and control and systems approaches. Of significance here is that chemical control methods for pests in the USA have significantly higher maximum residue levels (MRLs) than those permissible in Australia. Whilst the need for compliance with Australia’s food laws is mentioned in 5.5, how will the Department determine the efficacy of what is being performed in the USA where MRLs and withholding periods may differ?

Some examples of MRLs are shown below:

Chemical APVMA FSANZ USA abamectin 0.01 0.01 0.02 acetamiprid 0.2 0.2 1 boscalid 2 2 3 captan 10 10 25 diazinon 0.5 0.5 0.5 Dithiocarbamates (ziram) 3 3 7 imidacloprid 0.3 0.3 0.5 phosmet none 1 10 pyraclostrobin 1 1 1.5 spinetoram 0.1 0.1 0.2

Under such circumstances will the approved methods conform to Australian food safety and MRL levels and meet the standards required by Australia? Thus, this comment on (p.182, para 3) relating to standard USA commercial practice is potentially unreliable.

“In addition to PNW-USA’s existing commercial production systems and packing house operations for apples, specific pest risk management measures are proposed to achieve the ALOP for Australia.

A complete comparison of MRLs reveals that for approximately 40% of the permitted pesticides and fungicides available for apples, the MRLs in the USA are higher (sometimes by an order of magnitude) than in Australia.

Interception data from NZ and China is also presented on p. 182 and shows a 2.6% frequency for apple leaf curling midge from NZ. APAL’s earlier comments relating to the difficulties in managing this pest are pertinent here. The statement that stone fruit ‘are morphologically similar’ to apples is incorrect; stone fruit do not have a calyx cavity nor a potentially open core (ovary). Thus, to ascribe similar risk for pests in common on this basis is invalid in many cases.

Due to the lack of detailed information, it is difficult to make many specific comments on proposed amelioration measures although some notes are made below many of which apply across all the pest species mentioned. 47

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In reviewing the proposed mitigation strategies for both pests that exceed Australia’s ALOP and those deemed to meet it APAL notes there is an almost complete lack of quantitative evidence to support either category.

The Review offers the following; “The existing pest management practices in place for apple leafcurling midge in PNW-USA that are comparable to those of the Integrated Pest Management program for New Zealand apples were considered sufficient to reduce the risk.” (p. 187)

“The department recognises that the current industry commercial in-field control and packing house practices to manage the risk by Erwinia amylovora in the PNW-USA are similar to those of Integrated Pest Management practices for these pests applied for apples from New Zealand. The department proposes that these in-field controls applied with pack house sanitation processes are appropriate to manage the risk by Erwinia amylovora on apple consignments for export from the PNW-USA to Australia.” (p. 188)

“The department recognises that the current industry commercial in-field control and packing house practices to manage the risk by Neonectria ditissima in the PNW-USA are similar to those of Integrated Pest Management practices for these pests applied for apples from New Zealand. The department proposes that these in-field controls applied with pack house sanitation processes, are appropriate to manage the risk by Neonectria ditissima on apple consignments for export from the PNW-USA to Australia.” (p. 189)

It appears confidence in the PNW-USA systems approach stems largely from the existence of the NZ pathway. Whilst APAL acknowledges the commercial practices in NZ may provide effective management for these pests, it is unacceptable to presume that a ‘comparable’ system in the PNW-USA would have the same outcome since the pest-pressure, varieties grown, climate, in-field management and commercial operations are not identical. The Review offers no evidence that research has been undertaken to quantitatively compare each NZ control measure to the PNW-USA setting, or to identify the impact a series of ‘small’ differences might have on cumulative efficacy. The Review notes that existing pest management practices in the US are comparable to those of the NZ Integrated Pest Management program. What these may be is not specified other than a somewhat vague mention of insecticides in Table 3.2. Similar comments about the efficacy of these ‘controls’ apply to those above for apple maggot and most other pests/pathogens.

The description in Table 3.2 does not accord with that from the Washington State Tree Fruit guide: http://treefruit.wsu.edu/crop-protection/opm/apple-leafcurling-midge/

It should also be noted that NZ considers its farm-management practices unique Intellectual Property and closely guards this knowledge as a production advantage. Therefore, it seems surprising to suggest that the PNW-USA uses the same techniques since the NZ industry regards their operations a trade-sensitive. This reinforces our concern that the systems are likely to have as many differences as similarities.

APAL would like clarification about what the Review means by ‘systems approach’ as a number of the control options listed separately would also be applicable under a systems approach, thus what extra technique/technology is included under systems approach that is not already covered in the types of control measures already mentioned?

For serious pests of concern – such as apple leaf curling midge, fire blight, European canker, moths and post-harvest rots, systems approaches should be underpinned with rigorous, scientific quantitative data showing how a series of specific measurable actions in a specific

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environment can cumulatively produce an outcome. Assuming experiences with other trading partners will be replicated when applied in a different commercial system that operates in a different geography is not reasonable or scientifically sound.

APAL requests the Department consider the world-leading and recently published Systems Approach research conducted by CSIRO. This research provides a framework for quantitative analysis of Systems Approaches and can take into consideration a range of actions designed to reduce exposure to pests, evaluate host vulnerability, and consider infestation rates (Van Klinken et al. 2020). APAL does not specifically object to a systems approach but insists the Department seek quantitative evidence in line with the CSIRO research to prove it works in the PNW-USA context. This is essential for industry confidence in the pathway.

Inspections & exclusions

It is unclear from the Review how import inspections will be managed, particularly with regards to sampling rates and the application of a ‘risk-based’ inspection model. Given the many inconsistencies in the science presented by the Review, APAL is not confident with the proposed mitigation measures and is seeking to understand the inspection regime in greater detail. The last line of biosecurity defence is import inspection and so the breadth and frequency of these inspections is vital information. It is also unclear how non-compliant exporters are managed with regards to exclusion periods and what evidence they would be required to provide before being re-admitted to the export program.

APAL also notes that for asymptomatic organisms end-point inspection is meaningless and asks how this will be managed?

Apple maggot (Rhagoletis pomonella) is an Apple Industry High Priority Pest and APAL is also intrigued in the differences in consequence from this pest that range from low through moderate to high in previous risk assessments for various Rhagoletis spp.? Such inconsistencies warrant more detailed explanation as it is difficult to understand how where a pest comes from may affect the ultimate consequences from its establishment in Australia.

The statement on p. 186 that apple maggot is under official control in the PNW-USA is not strictly true as it is only under official control for prescribed counties where it is deemed to be absent.

Whilst it is noted that a number of counties or parts thereof are regulated with respect to the importation of fruit or material considered hosts of apple maggot, for those counties not covered by this regulation there would appear to exist open pathways from other parts of the US for the importation and establishment of many other pests not currently found in the PNW. The question of open pathways has not been addressed within the Review. APAL questions why, particularly as many of Australia’s trading partners express concern over the same principle within Australia?

Tension between biosecurity and human health policies

There is an awkward intersection between biosecurity and human health policies in the Review. Several mitigation strategies openly acknowledge the PNW-USA relies on chemicals and antibiotics that are not available for crop protection in Australia and which industry has been actively discouraged from seeking to register because of government concerns regarding anti-microbial resistance.

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There is inconsistency in the policy position of APVMA/FSANZ and DAWE with the former discouraging the adoption of human antibiotics in horticultural production and the latter proposing to accept their use as a permissible pest-management option for imported product.

It is difficult to reconcile why different rules should apply for domestic and foreign producers when antimicrobial resistance (AMR) is acknowledged as a shared global issue, irrespective of where the antibiotics are used. Why are Australian producers asked to meet a higher standard than foreign producers who want to export to the Australian market? It is even more difficult to reconcile how allowing an import pathway that permits the use of human antibiotics accords with the Australian Government’s ‘whole-of-government’ response to Antimicrobial Resistance that specifically states:

‘Antimicrobial resistance (AMR) is a serious global issue that needs our urgent action. Australia’s response recognises that AMR affects human and animal health, agriculture, food and the environment. Our response involves action across all of these sectors. The Council of Australian Governments has endorsed the new National AMR Strategy – 2020 and Beyond. This endorsement recognises that addressing AMR is a matter of national importance.’ https://www.amr.gov.au/ (viewed 15/1/21)

Although the Department’s mandate is to manage biosecurity concerns, it is unreasonable to approve pathways that knowingly contradict a whole-of-government position on such a serious issue as anti-microbial resistance. The approval of an import pathway that permits the use of human antibiotics as part of normal commercial orchard practice is not acceptable when this identical practice is not permitted and actively discouraged by multiple levels of government in Australia.

Currently, the Review essentially endorses the use of antibiotics in orchards because it accepts them as suitable control measures for pests in PNW-USA even though APVMA/FSANZ have suggested they have unacceptable human health implications when used in domestic apple production. The combined effect of these two separate Australian Government policy settings is to disadvantage Australian producers.

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Pests not considered worthy of detailed Risk Analysis from Appendix A

This section will consider data from Appendix A and examine, in the light of evidence presented and that available from other sources, whether there are further pests that warrant a Risk Assessment. The Review’s reasons for not performing a full pest risk assessment suffer from the same flaws that plague the rest of the document; inaccurate citing/quoting, lack of evidence, inappropriate references and a consequent unwarranted diminishment of risk. p. 198 - Fruitflies - The Review notes that the PNW-USA is considered free of Fruit flies (except Apple maggot). APAL’s comments regarding open pathways merit discussion about the potential for exotic fruit fly importation.

Mites

It is noted that these are regarded as quarantine pests in NZ and require mitigation measures, but this is not the case for Australia; why not?

Although a number of species are not known to occur in the PNW-USA the fact that there are open pathways and that their damage profiles are often very similar it is submitted that a more thorough analysis is required than the rather cursory treatment, particularly in relation to the potential for travel via the calyx. p. 199 - Aculus malivagrans The potential for this pest to be on the pathway is not adequately addressed as neither the reference of Vidovic et al. (2014) (which is mostly a taxonomic study) nor that of Keifer (1952) adequately address the risk of mites being transferred in the calyx. Furthermore, there is no mention of this mite in the paper by Keifer (1952) although a number of rust mite species are mentioned for a range of other plant taxa.

On this basis this assessment needs to be reconsidered. p. 201 - Eriophyes mali There is no evidence presented to substantiate the statement that it is unlikely to be on importation pathway and it is noted to attack fruit. A Pest Risk Assessment is required for this pest. p. 208 - Plum curculio – Despite requiring risk mitigation measures in the US this pest is dismissed as not requiring Risk assessment for Australia. APAL questions why this should be the case?

Aphids

Similar comments apply here regarding assessments. URLs for references cited in the Review in many cases do not work, and statements attributed to particular authors are not always accurate. p. 214 - A. pomi – This requires a risk assessment as the summary provided does not accord with that from the PNW Pest Management Handbook. The pests feeds directly on fruit especially green and yellow varieties and fruit may or may not be marked, according to the PNW Pest Management Handbook 2020. The potential for spread via the calyx also needs addressing. pp. 215 &216 - URLs do not work for Western box elder bug or Rosy apple aphid. The comments on Rosy apple aphid are copy and pasted directly from the earlier Risk Analysis (this may explain why URLs do not work). This information is outdated, and the comments and

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assessment should reflect more current knowledge. This pest needs to be reassessed against current knowledge.

Other arthropods p. 219 - Fiebereilla florii; APAL cannot find the reference for Swenson (1974) and there is no mention of feeding habits in Van Steenwyk et al. (2006). It is noted that this pest is a vector for a number of serious virus and phytoplasma diseases affecting fruit tree crops including cherries and stone fruit (See Tedeschi & Alma (2006), Van Steenwyk et al. (2006)). Although the Review notes this pest occurs in the ACT it is suggested that on the basis of the minimal evidence presented and its importance as a vector of disease that a full Risk Assessment be performed. p. 220 - Brown Marmorated Stink Bug (BMSB)

As both a serious pest of apple and a known hitchhiker, BMSB warrants some form of pest risk analysis or mitigation measures. There is no discussion within the Review on this pest. It is known to seek shelter in autumn for hibernation; it is present in the PNW and is found in apple orchards. Pallets or bins awaiting use or already stacked awaiting shipment can potentially provide such niches. APAL suggests that there needs to be some form of mitigation measure to prevent accidental transport on apple consignments destined for Australia. This form of hitchhiking is not addressed in the Department’s separate review of this species. p. 240 – Double dart moth. The reference for Kimber (2009) is not for double dart moth, The URL for Fauske (2007) does not work although further searching found the document quoted and this, along with the reference for Mazzei et al. (2008), fail to mention feeding as described in Appendix A, only describing host plants. Therefore, on this basis a more thorough appraisal of the risk posed by this species is warranted. p. 242 – Hedya nubiferana; mis-quoting of both LaGasa (1996) and Ovsyannikova & Grichanov (2005a) although in this case it probably does not affect the recommendation for no risk assessment required. It nonetheless emphasises the lack of rigour in this document. p. 243 – Hyalophora cecropia; neither of the references cited mention leaves, only that the species feeds on apples. This species warrants further clarification and information.

Hyphantria cunea; the URL link provided fails for Douce (2003) and that for APHIS is no longer available, presumably copied from the earlier Review. This species needs updating. p. 249 – Pandemis cerasana; The URL links provided did not work however the reference was sourced here: http://www.agroatlas.ru/en/content/pests/Pandemis_ribeana/index.html Accessed on 5 Nov 2020

Like many Tortricidae these are significant pests on a wide range of taxa. There is no discussion in the references quoted as to how late in the life cycle of the fruit the larvae may infest, and as to whether or not they may therefore be transported within the fruit asymptomatically. Further information is required around this aspect before these pests can be dismissed as a threat. p. 260 – Yponomeuta padella; The reference quoted makes no mention of feeding on apple leaves. A more recent reference (2013) notes that this is a pest of apple but there is no evidence it feeds on fruit; http://download.ceris.purdue.edu/file/3163 (Accessed 5 Nov 20)

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Thus, whilst there is no further need for additional risk analysis the question is again asked as to why the most up to date information was not sourced, rather than copying and pasting out of date and inaccurately quoted references. https://pnwhandbooks.org/plantdisease/host-disease/apple-malus-spp-virus-diseases p. 269 – APAL questions why Butlerelfia eustacei was not assessed if this fungus has been isolated from stems of healthy apples after harvest. This raises the question ‘Does this infect stems or petioles?’. The difference is significant from a risk perspective. The fungus causes Fisheye rot. How “rare” is this post-harvest rot? Further information about its prevalence in the PNW is requested. It has been listed in the Compendium of apple and pear diseases which was previously used in the Review as a measure of importance/significance of pests to the USA apple industry. At what point does a species merit consideration?

Similar points can be made for other fungi in Appendix A including: p. 285 – In the Potential to be on the pathway column for Mucor mucedo, it is mentioned that Mucor rot of apples in the PNW is caused only by M. piriformis. Presumably, M. piriformis is not included in the assessment because it is present in Australia? p. 303 – the Review lists several Valsa species but omits Valsa ceratospora which is listed as a contributing pathogen to apple decline by Harper (2020):

http://treefruit.wsu.edu/article/apple-decline/

This pest should be included in the Review’s assessment of risk. p. 306 – Apple stem grooving virus: The document states that this virus is present in Western Australia, yet the Western Australia Agriculture department states that it is a ‘Declared Pest – prohibited in Western Australia and Absent in the state. Further clarification is required. https://www.agric.wa.gov.au/organisms/111525 p. 306 – Apple stem pitting virus: The document states that this virus is present in Western Australia, yet the Western Australia Agriculture department states that it is a ‘Declared Pest – prohibited in Western Australia and Absent in the state. Clarification is requested. https://www.agric.wa.gov.au/organisms/121392

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