Import risk analysis:  leafless  
Citrus budwood  for propagation  
 
Biosecurity  New Zealand  Discussion  Paper  No: 2021/….. 
 
 
 
 
 
ISBN No: (contact Publications team)  
ISSN No:  
 
 
 
April  2021 
 
 
Disclaimer  
 
While every effort has been made to ensure the information in this publication is accurate, the Ministry 
for Primary Industries  does not accept any responsibility or liability for error of fact, omission, 
interpretation or opinion that may be present, nor for the consequences of any decisions based on  
this information.  
 
The material contained in the import risk analysis is preliminary and will be updated based on any 
feedback received during consultation on any related import health standards or any furthe r feedback 
that may be provided by internal or external experts.  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Recommended citation:  
MPI (20 21) Import Risk Analysis:  Citrus  budwood  for propagation . Version 1.  April 2021. Ministry for 
Primary Industries, New Zealand.  
 
 
 
 
Ministry for Primary Industries  
PO Box 2526  
WELLINGTON  6140  
 
Email: brand@mpi.govt.nz  
Telephone: 0800 00 83 33  
Facsimile: 04 -894 0300  
 
This publication is also available on the Ministry for Primary Industries  websit e at  
http://www.mpi.govt.nz/news -and-resources/publications/   
 
 
© Crown Copyright - Ministry for Primary Industries  
 
  
i  
 
 
 
 
 
 
 
Import risk analysis: Citrus  (Citrus spp.) budwood  for propagation  
 
 
Version 1 .0 
 
April 2021 
 
 
Approved f or general release  
 
 
 
 
 
 
 
 
 
 
 
Enrico Perotti  
Associate Director,  Animal and Plant Health Directorate  
Biosecurity New Zealand  
Ministry for Primary Industries  
 
 
 
 
 
 
 
 
 
 
 
 
© Crown Copyright - Ministry for Primary Industries  
  
 ii Version information  
 
 
Version number  Comments  Date of approval  
1.0 Peer -reviewed and current at date of 
release  12 April 2021  
   
  
New Zealand is a member of the World Trade Organi zation and a signatory to the Agreement on the 
Application of Sanitary and Phytosanitary Measures (“ the SPS Agreement”). Under the SPS 
Agreement, countries must base their measures on an international standard  or an assessment of the 
biological risks to plant, animal or human health.  
 
This document provides a scientific analysis of the risks associated with the importation of Citrus 
budwood  from all countries.  It assesses the introduction of pathog ens associated with Citrus budwood 
(not assessed as part of the 2016 import risk analysis ) imported from all parts of the world and  
assesse s the potential impacts of those  organisms should they enter and establish in New Zealand. 
The document has been internally and externally peer reviewed and is now released publicly . Any 
significant new science information received that may alter the level of assessed risk will be included 
in a review, and an updated version released.   
 
Contribu tors to this risk analysis  
The following people provided significant input into the development of this risk analysis:  
 
1. Authors  
 
Dr Abigail Durrant    Senior Adviser   MPI New Zealand, Wellington  
Dr Helen Harman    Senior Adviser   MPI New Zealand, Wellingt on 
Melanie Newfield    Manager   MPI New Zealand, Wellington  
Dr Shola Olaniyan    Senior Adviser   MPI New Zealand, Wellington  
Dr Karen Wilson    Senior Adviser   MPI New Zealand, Wellington  
   
2. Internal review  
 
Kaavya Benjamin    Senior Adviser   MPI New Zealand, Wellington  
Dr Allan Burne     Senior Adviser   MPI New Zealand, Wellington  
Dr Stephan Halloy   Senior Adviser   MPI New Zealand, Wellington  
Dr Justyna Paplinska   Senior Adviser   MPI New Zealand, Wellington  
Bruce Philip    Senior Adviser   MPI New Zealand, Wellington  
Dr Charlotte Simmonds   Senior Tech. Writer  MPI New Zealand, Wellington  
 
3. External  review  
 
Dr Claire Sansford   Independent Plant Health Consultant  York, UK  
 
 
   
iii Executive summary  
 
Background  
This import risk analysis (IRA) has been dev eloped in response to a request to review the import 
health standard  (IHS) for germplasm of all Citrus  species listed  in the Plant Biosecurity Index (PBI) . In 
2016 , a review of the IHS was initiated , and a draft IHS was prepared, along with relevant PRAs 
(https://www.mpi.govt.nz/dmsdocument/14338 -Citrus -spp.-nursery -stock -Pest-Risk-Assessment ). This 
current IRA identif ies any new pathogens since the 2016 IRA that meet the criteria for additional 
measures (or anything that was missed, e.g. pathogens may not be new since 2016 but literature may 
not have been found or available).  
 
Objectives  
To ensure that the known biosecurity risk from regulated organisms associated with imported Citrus  
nursery stock is managed appropriately , Biosecurity New Zealand’s  objectives in reviewing the import 
health standard  for germplasm of Citrus  species are to : 
a) identify any pathogens where there are changes in measures in the 2016 import risk analysis 
and where the risk assessment isn’t documented and determine if they meet the criteria for 
additional measures , 
b) identify any  new pathogens since the 2016 import ris k analysis which meet the criteria for 
additional measures (or anything that was missed, e.g. not new since 2016 but literature may 
not have been found or available) , 
c) identify any pathogens which are not listed as requiring additional measures in 3B but ma y 
meet the criteria for additional measures if the minimum requirements are level 3A post -entry 
quarantine , 
d) identify pathogens which are associated with the commodity and may require additional 
measures , and 
e) assess those pathogens using a method that provi des sufficient evidence about the 
biosecurity risks for a robust and transparent decision on whether to apply additional 
measures . 
 
Import risk analysis  methodology  
The import risk analysis process involves three principal stages:  
• Scoping/commissioning  
• Hazard identification  
• Pest risk assessment  
 
Scoping/commissioning  
This involves a detailed project plan with estimated timeframes and approval of that plan. The 
following key questions are ans wered:  
• What are the risk management questions?  
• What is the commodity description?  
• What basic measures will be applied to the commodity?  
 
 
Risk management questions  
General description  Specific questions that the risk manager needs answered in order to make a 
decision. They are based on the commodity description and basic measures 
for that commodity.  
Description specific 
to this Citrus 
budwood IRA  1. Does each assessed pathogen meet the criteria to be a quarant ine 
pest?1 
2. Does each assessed pathogen m eet (or potentially meet) the criteria 
for requiring additional measures (i.e. over and above basic 
measures)?  
 
 
 
1A quarantine pest is an organism that is not present in New Zealand (or is present but still represents a biosecurity risk, e .g. is 
capable of vectoring pathogens not present in New Zealand) and is capable of establishing and causing harm in New Zealand. 
For the purposes of this analysis, it also includes diseases.   iv  
 
Commodity description  
General  description  The commodity description defines the form of the commodity that is covered 
by the import health standard , e.g. the commodity species and the countries 
under consideration. The commodity description may also include 
commercial commodity quality specificati ons, e.g. commercial production.  
Description specific 
to this Citrus 
budwood IRA  Citrus budwood ( Citrus bud stick with buds but no leaves). In this case, the 
commodity description does not include any requirements for ‘commercial 
production’ methods to b e used in the production of the budwood.  
 
Minimum  requirements  
General  description  The minimum level of risk management for a particular commodity that all 
exporting countries must  meet . They are not pest -specific but are likely to 
manage, or partially manage, a wide range of pests.  
Basic measures are based on information already known about  the risks  and 
are justified by existing risk assessments .  
Description specific 
to this Citrus 
budwood IRA  Consignments of Citrus budwood imported into New Zealand must:  
1. Comply with the commodity description (e.g. leafless budwood);  
2. Undergo basic measures;  and 
3. Be held in level 3A post -entry quarantine for one growing season . 
These conditions were determined based on the 2016 PRAs.  
 
 
Hazard identification  
A hazard is a pest (including arthropods and pathogens) or disease that is:  
• Not present in New Zealand (or is present but still represents a biosecurity risk, e.g. is 
capable of vectoring pathogens not present in New Zealand  or is under official control ), 
• Has the ability to establish and cause harm in New Zealand, and  
• Is associated with imported risk goods and import pathways.  
 
Hazard identification is the process where, depending on the scope of the import risk analysis , a list of 
pests and diseases  potentially associated with the commodity is c ompiled and then assessed against 
specified criteria, in order to determine which pests or diseases  requir e further assessment. The 
objec tive for hazard identification in this import risk analysis  is to identify any new pathogens , 
nematodes or diseases  since the 2016 IRA (or anything that was missed, e.g. the pest may not be 
new since 2016 but literature may not have been found or available)  that meet the risk evaluation 
criteria for requiring additional measures over and above basic measures.  
 
Because this import risk a nalysis will be used to develop  an import health standard for Citrus spp., the 
hazard identification  needs to consider  pathogens , nematodes or diseases  associated with any Citrus 
spp. listed on the  Plant Biosecurity Index  (PBI 2020). To identify pathogens that potentially meet risk 
evaluation criteria, the hazard identification  focused on the following:  
• Pathogens , nematodes or diseases  that are associated with leafless Citrus budwood of all 
Citrus  species listed on the MPI Plant Biosecurity Index ; 
• Pathogens, nematodes or diseases that are not present in New Zealand  (or are present but 
still represent a biosecurity risk, e.g. they are  capable of vectoring pathogens not present in 
New Zealand , or they are  under official control) ; 
• Pathogens, nematodes or diseases that have traits that indicate that they  may not be 
identified or contained in Level 3A post -entry quarantine.  
 
The hazard identification only identified pathogens (viruses and fungi) that re quired further 
assessment. These are addressed in the Pest Risk Assessment section below and listed in Summary 
Table 1.  
 
As the search sources used were  English language sources and data systems that may not be 
available in all countries,  they are recognis ed as being deficient in information contained in non -
English language publications and countries that hold pest and disease information locally (e.g. not on 
the internet). No effort was made to access or translate non -English language information or to 
research pathogen records in countries with science publication systems  with less digital presence . 
Therefore, while all pathogens identified in the hazard identification are assessed in this import risk  
v analysis , the sources used should not be considered an  adequate representation of pathogens in non -
English language countries or countries with more analogue -based  publication systems.  
 
Pest groups and pest species that did not meet the criteria to require pest risk assessments are listed 
in Appendix 1, along with the rationale for excluding them.  
 
Pest risk assessment  
The purpose of risk assessment is to determine the level of risk that hazard pathogens  (identified at 
the hazard identification  stage as requiring further assessment) present to New Zealand . Specifically, 
the pest  risk assessment concludes whether the pathogen  meets the risk evaluation criteria for 
requiring additional measures over and above the minimum  requirements . 
 
For this import risk analysis,  pathogens  that meet, or potentially meet, the criteria for additional 
measures are those that  cannot be contained in a Level 3A post -entry quarantine facility  and/or 
cannot be detected during one growing season in Level 3A post -entry quarantine . 
 
Some t raits that potent ially indicate additional measure s may be require d include : 
o ability of the pathogen to be latent for long periods (more than one growing season, such as 
fungi that are  endophytic) ;  
o tendency of the pathogen to only show symptoms under certain growing conditions , such as 
when the plants are stressed ; 
o ability of the pathogen to produce wind -dispersed spores.  
 
The PRA addresses the following:  
• Likelihood of entry:  
o the strength or frequency of the association with Citrus budwood  
o the likelihood of en try given the application of minimum requirements  
• Likelihood of establishment:  
o the suitability of the New Zealand environment for the pathogen (including the climate, 
host plants and vectors)  
o conditions necessary for the pathogen to spread  
• The potential i mpacts in New Zealand:  
o economic impacts: on Citrus and other economically important  plants (symptoms on 
individual plants, crop yield, costs of management practices, trade restrictions etc.)  
o environmental impacts: on native plants and ecosystems  
o sociocultural  impacts : plant losses or wider consequences that would affect socially 
importan t plants  
o human health impacts  
Summary Table 1 shows pest species for which PRAs were carried out and the PRA conclusion with respect to the 
requirement for additional measures.  
Pest group  Species considered in the pest risk assessment  (PRA)  PRA conclusion: Are 
the criteria to be 
considered for 
additional measures 
met?  
Fungi  Colletotrichum abscissum  No 
Colletotrichum acutatum  No 
Diaporthe baccae, D. hongkongensis, D. novem  Yes 
Elsino e australis  No 
Erysiphe quercicola, Fibroidium tingitaninum  Some, but not all  
Lasiodiplodia brasiliensis, L. citricola, L. hormozganensis, 
L. iranensis, L. mediterranea, L. mitidjana, 
L. pseudotheobromae, L. subglobosa  Some, but not all  
Phyllosticta citrocarpa  Yes 
Plenodomus tracheiphilus  Some, but not all   vi Pest group  Species considered in the pest risk assessment  (PRA)  PRA conclusion: Are 
the criteria to be 
considered for 
additional measures 
met?  
Virus  Citrus leprosis viruses: Citrus leprosis virus C (CiLV -C), 
Citrus leprosis virus C2  (CiLV -C2), Hibiscus green spot virus 
2, Orchid fleck dichorhavirus [citrus strain], Citrus leprosis N 
dichorhavirus, Citrus chlorotic  spot dichorhavirus, Citrus 
chlorotic spot virus  Yes 
 
   
vii Contents  Page 
 
1 Risk analysis process  1 
1.1 Hazard identification  3 
1.2 Risk assessment  4 
1.3 CASE format as a pilot  4 
1.4 Assessment of uncertainties  5 
1.5 Review and consultation  5 
1.6 Conclusions  of the risk analysis  5 
1.7 References for Chapter 1  6 
2 Scope and objectives  7 
2.1 Scope and approach of this risk analysis  7 
2.2 Commodity description  8 
2.3 Taxonomy of the plant commodity under consideration  10 
2.4 General information related to the likelihood of entry  10 
2.5 General information related to the likelihood of establishment  11 
2.6 General information related to impacts of pests and diseases  14 
2.7 References for Chapter 2  15 
3 Hazard identification  18 
3.1 References for Chapter 3  19 
4 Risk assessment criteria  20 
4.1 Risk management questions  20 
4.2 Criteria and traits for additional measures  20 
4.3 Assessment method  20 
4.4 References for Chapter 4  22 
5 Pest risk assessments: Fungi  23 
5.1 Colletotrichum abscissum  (post -bloom fruit drop)  23 
5.2 Colletotrichum limetticola  (Key lime anthracnose)  27 
5.3 Diaporthe  spp. associated with citrus: Diaporthe baccae , D. hongkongensis  and D. novem  32 
5.4 Elsinoe australis  (sweet orange scab)  47 
5.5 Erysiphe quercicola  and Fibroidium tingitaninum  (powdery mildew of citrus)  52 
5.6 Lasiodiplodia  species associated with disease of Citrus trees  63 
5.7 Phyllosticta citricarpa  (citrus black spot)  88 
5.8 Plenodomus tracheiphilus  (mal secco disease of citrus)  100 
6 Pest risk assessment: Viruses  108 
6.1 Citrus leprosis viruses  108 
Appendix 1: Summary of taxa excluded at hazard identification  121 
6.2 References  126 
Appendix 2: Glossary and Abbreviations  128 
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 1 1 Risk analysis process  
 
The World Trade Organization Agreement on the Application of Sanitary and Phytosanitary Measures 
(the SPS Agreement) states that phytosanitary measures must be supported by risk assessment and 
not maintained without sufficient evidence. That is, to require additional measures , MPI must have 
evidence that a pathogen  would not be sufficiently managed by the application of the minimum 
requirements.  
 
The Biosecurity New Zealand  (BNZ)  process for undertaking an import risk analysis builds on the 
existing international frameworks for risk analysis under the World Organisation for Anim al Health 
(OIE) and the International Plant Protection Convention (IPPC) , and extends the scope , under the 
SPS Agreement , to include all of the values required by the Biosecurity Act (1993 )2. The BNZ process 
and methodology for undertaking an IRA is summarised in Figure 1.  
 
Import risk analys es are used in the development or review of import health standar ds under the 
Biosecurity Act (1993). An import health standard  specifies the requirements  to be met for the effective 
management of risks associated with importing risk goods3. 
 
The Biosecurity Act (1993) requires a chief technical officer to begin the pr ocess of developing an 
import health standard  by: “analysing or assessing the risks associated with importing a class or 
description of goods ”4.  
 
While the Biosecurity Act does not state how the risks are to be assessed or analysed, it does state 
that the chief technical officer must have regard to certain matters when developing  an import health 
standard for recommendation to the Director -General. A number of these are part of an import risk 
analysis , as described by the OIE and IPPC:  
• The likelihood that the goods will import organisms5 
• The nature of the organism s that the goods may import  
• The possible effect on human health, the New Zealand envir onment6, and the New Zealand 
economy of the organism s that the goods may import  
• In relation to requirements proposed for inclusion in an import health standard , the extent to 
which the requirements reduce or manage the likelihood or impacts of adverse eff ects from 
organisms that may be imported on or in association with goods7 
 
An import risk analysis  is also a relevant factor in how a country meets its obligations under the SPS 
Agreement and other agreements such as the Convention on Biological Diversity. Under the SPS 
Agreement, risk management measures either must be based on existing international standards, 
guidelines or recommendations, or must be supported by a scientific justification8. Measures must not 
be maintained without sufficient scientific evidence9. Measures must also not be unnecessarily trade -
restrictive10. In order to meet these ob ligations, the SPS Agreement  requires that measures are based 
on a risk analysis. Under the Convention on Biological Diversity , countries must consider 
environmental impacts in decision -making and prevent the introduction of  alien species that threaten 
ecosystems, habitats and species  and control or eradicate them .  
 
 
2 Biosecurity Act section 24(4)(b)(iii) “…human health, the New Zealand environment, and the New Zealand economy…” As 
defined in section 2(1), environment includes ( a) ecosystems and their constituent parts, including people and their 
communities; and (b) all natural and physical resources; and (c) amenity values; and (d) the aesthetic, cultural, economic, a nd 
social conditions that affect or are affected by any matte r referring to paragraphs (a) to (c).   
3 Section 22, Biosecurity Act 1993  
4 Section 23(1), Biosecurity Act 1993  
5 From section 2(1) , Biosecurity Act 1993:  “organism —(a) does not include a human being or a genetic structure derived from a 
human being:  (b)includes a micro -organism:  (c) subject to paragraph (a), includes a genetic structure that is capable of 
replicating itself (whether that structure comprises all or only part of an entity, and whether it comprises all or only part  of the 
total ge netic structure of an entity):  (d) includes an entity (other than a human being) declared by the Governor -General by 
Order in Council to be an organism for the purposes of this Act:  (e) includes a reproductive cell or developmental stage of an 
organism:  (f) includes any particle that is a prion ” 
6 From section 2(1) , Biosecurity Act 1993, “ environment includes — (a) ecosystems and their constituent parts, including people 
and their communities; and (b) all natural and physical resources; and (c) amenity values; and (d) the aesthetic, cultural, 
economic, and social conditions that affect or are affected by any matter referred to in paragraphs (a) to (c)”  
7 Section s 23(4)(b) and (d) Biosecurity Act 1993  
8 SPS Agreement 1995 , Article  3(1) and (3)  
9 SPS Agreement 1995 , Article 5(7)  
10 SPS Agreement , Article 5(6)  2 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand   
Figure 1: Biosecurity New Zealand  process and methodology for undertaking an import risk 
analysis  
The Biosecurity Act (1993) requires a chief technical officer  to begin the process of developing an 
import health standard  by “analysing or assessing the risks associated with importing a class or 
description of goods ”11. 
While the Biosecurity Act does not  state how the risks are to be assessed or analysed, it does state 
that the chief technical officer  must have regard to certain matters when developing an import health 
standard for recommendation to the Director -General. A number of the  matters  are part o f an import 
risk analysis, as described by the OIE and IPPC:  
• The likelihood that the goods will import organisms12 
• The nature of the organism that the goods may import  
 
11 Section 23(1) Biosecurity Act 1993  
12 From Section 2(1) Biosecurity Act 1993:  “organism —(a) does not include a human being or a genetic structure derived from 
a human being: (b)  includes a micro -organism: (c) subject to paragraph (a), includes a genetic structure that is capable of 
replicating itself (whether that structure comprises all or only part of an entity, and whether it comprises all or only part  of the 
total genetic stru cture of an entity): (d) includes an entity (other than a human being) declared by the Governor -General by 
Order in Council to be an organism for the purposes of this Act: (e) includes a reproductive cell or developmental stage of a n 
organism: (f) includes  any particle that is a prion ” 
 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 3 • The possible effect on human health, the New Zealand environment13, and the New Zealand 
economy of the organism that the goods may import  
• In relation to risk management measures proposed for inclusion in an IHS, the extent to which 
the measures reduce or manage the likelihood or impacts of adverse effects from organisms 
that may be im ported on or in association with goods14. 
1.1 Hazard identification15 
Hazard identification is the process for identifying pests  and diseases associated with imported risk 
goods and that have the ability to cause harm to New Zealand. The process consists of co mpiling a 
list of potential hazards and then assessing them against criteria to see whether they warrant further  
consideration . The hazard identification answers two different questions:  
• Does the species meet the criteria to be considered a biosecurity ris k or quarantine pest for 
New Zealand?  
• Is the species associated with the commodity that is being assessed?  
 
The criteria for a quarantine pest for New Zealand are derived from the Biosecurity Act and ISPMs 2, 5 
and 11. These criteria are:  
• Is the species pr esent in New Zealand?  
• OR is the species present in New Zealand , but it meets one of the following criteria?  
o The species is under official control.  
o The species is a vector of quarantine pests.  
o There are subspecific taxa (subspecies, varieties, strains , etc.) within the species 
that are an increased risk to New Zealand compared with those already present.  
o There are other factors that would mean that the species may still be of concern in 
associated with imported goods (e.g. increased exposure to people through imported 
goods16). 
• AND does the species have the potential to establish in New Zealand and harm “human 
health, the New Zealand environment, and the New Zealand economy17?” 
 
Association with the commodity is based on:  
• association with the host species or genus;  
• association with the specific parts of the plant;  and 
• whether a particular pest or disease will stay associated with a commodity when it is being 
handled –for example , a large flying insect is unlikely to stay on a piece of fruit when  it is 
picked.  
 
For the haza rd identification:  
a) A list of preliminary hazards must be compiled using the methods documented in the 
plan 
b) Potential hazards must be assessed against criteria which meet relevant International 
Standards and the requirements of the Biosecurity Act 1993  
c) The hazard identification conclusions must be documented and supported by suitable 
evidence  
 
Different approaches may be taken in compiling and presenting the list of potential hazards, 
depending on the information needed for each group of pest or disease . The approach for each group 
is determined during the commissioning process, once the risk management question and risk 
evaluation criteria have been established. The approaches to be used are documented in the plan. 
The specific a pproaches to hazard identification used in this IRA are discussed further in Section 3.  
 
At the end of the hazard identification process, the list of hazards that warrant further assessment may 
be peer reviewed or discussed with risk managers and key stak eholders. The plan will also need to be 
updated if there are other changes, such as a change to the  commodity description or the  methods for 
hazard identification.  
 
13 From section 2(1) Biosecurity Act 1993, “ environment  includes —(a) ecosystems and their constituent parts, including people 
and their communities; and (b) all natural and physical resources; and (c) amenity values; and (d) t he aesthetic, cultural, 
economic, and social conditions that affect or are affected by any matter referred to in paragraphs (a) to (c)”  
14 Section s 23(4)(b) and (d) Biosecurity Act 1993  
15 Under the IPPC, the hazard identification process is known as pest ca tegorisation in ISPM 2 and ISPM 11.  
16 One example is venomous spiders on fresh fruit. Even if the spiders are present in a country, there may be higher likelihood 
of people getting bitten if the spiders are associated with fruit sold at a supermarket.  
17Biosecurity Act 1993  4 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand   
1.2 Risk assessment  
At the end of hazard identification, the list of hazards that require risk  assessment is discussed and 
agreed on by the project team.  
 
A risk assessment evaluates the likelihood of introduction and consequence for a particular hazard, as 
well as the uncertainty in the conclusions. The SPS agreement describes the factors to consider  when 
assessing risk. These factors include:  
• available scientific evidence ;  
• relevant processes and production methods ;  
• relevant inspection, sampling and testing methods ;  
• prevalence of specific diseases or pests ; 
• relevant ecological and environmental conditions ; and  
• potential damage in the event o f the entry, establishment or spread of a pest . 
 
A qualitative approach is suitable for the majority of import risk analyses and is currently the most 
common type of assessment undertaken to support the development and review of import 
requirements. Qualit ative descriptors of likelihood, consequence and uncertainty are used (see 
Chapter 4).  
 
The risk assessment stage of the IRA process:  
a) must be documented and supported by suitable evidence , and  
b) must answer the risk management question by following definiti ons or criteria agreed 
on during commissioning and documented in the plan.  
 
1.3 CASE format as a pilot  
 
As a pilot to improve readability, the pest risk assessments in this project  use the CASE schema. 
Under the CASE schema, the contention  or conclusion  (that is, the answer to the risk management 
question) is presented first, followed by the arguments  supporting this contention and the evidence  
and sources  supporting each argument.  
 
To follow the CASE schema, the pest risk assessments will apply the following basic format:  
 
• Description of the pest/pathogen: This is a sentence or t wo describing the pest or disease  for 
a non -expert, the taxonomy and the other names used.  
 
• Statement: This explains whether or not the pest or disease meets the criteria for additional 
measures (or is a bit marginal or meets  some of  these criteria but not oth ers, partly meets 
criteria, etc .). 
 
For each section of the hazard identification or risk assessment, the following format is then applied:  
 
Contention  (e.g. Given the arguments and evidence below , the pest or disease meets /does not meet  
the criteria to be a quarantine pest for New  Zealand .) 
 
Argument 1  (e.g. The pest or disease  is known/ not known to be present in New Zealand .) 
 
• Evidence  and sources  appear as bullets underneath , unless there is a good reason to use 
paragraphs . 
 
Argument 2  (e.g. The pest or disease  has/does not have the potential to establish and spread in 
New Zealand .) 
 
• Evidence  and sources appear as bullets underneath , unless there is a good reason to use 
paragraphs . 
 
Care has been taken to present the supporting arguments and evidence, along with evi dence that 
includes objections and/or counterevidence.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 5  
 
1.4 Assessment of uncertainties  
The SPS Agreement requires measures to be applie d only to the extent necessary  and to be 
supported by sufficient scientific evidence18. Therefore, i f there is insufficient evidence  indicating that 
an organism meets the criteria requiring additional measures (the risk evaluation criteria), then the 
lack of evidence suggests that it does not meet the criteria to be a hazard (see section 1.3.5). 
However, in some ca ses there may be good reason to consider a pest or pathogen even when 
evidence is insufficient  (e.g. similarity to known pests or pathogens). Following discussion with the 
commissioning team, that pest or pathogen may be assessed further . If there is insuf ficient evidence  
but significant uncertainty, then the decision -maker may apply measures . Under those circumstances , 
the measures are provisional , and certain conditions m ay be required19. 
 
Therefore, documenting significant uncertainty is an essential par t of a risk assessment. Uncertainties 
such as contradictions in the evidence or a lack of evidence are documented in the import risk 
analysis . Where the risk assessment identifies significant uncertainty affecting the conclusion, this is 
indicated  in the c onclusion. The risk management proposal (se e section 1.3.5) considers these risk 
assessments  further . See Chapter 4 for more  information on how uncertainty is documented.   
 
1.5 Review and consultation  
Peer review is a fundamental component of a risk analysis that helps  ensure the analysis is based on 
the most up -to-date and credible information  available .  
 
The import risk analysis  may be reviewed to check that the plan has been followed ; that the IRA is 
based on the best available and most credible information ; that the document is clear and logical ; that 
assumptions are valid ; and that conclusions are consistent with the evidence, with other conclusions in 
the import risk analysis and wi th relevant conclusions in other assessments. The peer review process 
involves relevant experts within MPI and may involve experts from outside MPI, either from 
New Zealand or overseas where necessary. A representative from the team commissioning the impor t 
risk analysis  is included in the peer review process.  
 
The import risk analysis  may be reviewed as a whole or in parts. For example,  it is common that 
individual assessments for pests or pathogens are reviewed by an expert in that group.  
 
For an import risk analysis  peer review:  
a) The import risk analysis  must be reviewed by relevant staff from within MPI, including a 
representative of the team commissioning the import risk analysis , determined by the 
team manager responsible for the import risk analysis . 
b) Individual pest or pathogen assessments should be r eviewed by relevant experts within 
MPI and also subject matter experts and/or relevant stakeholders from outside MPI, 
either from New Zealand or overseas, when the team manager considers it necessary .  
c) All peer review comments must be considered, and if in ternal or external reviewers ’ 
feedback20 is not incorporated into the import risk analysis , the rationale for the 
decision not to include that feedback must be clearly documented  and, where 
necessary, discussed with the reviewer . 
 
1.6 Conclusions  of the risk analysis  
The conclusions of the risk analysis are summarised in a risk management proposal that accompanies 
the draft import health standard  being consulted on. The risk analysis provides additional technical 
detail should submitters wish to s ee a more detailed scientific analysis of the biological risks.  
 
All submissions received from stakeholders  will be analysed and compiled into a review of 
submissions. The import risk analysis , risk management proposal and draft import health standard  will 
be modified where appropriate depending on the outcome of consultation.  
 
18 SPS Agreement 1995, Article 2.2  
19 SPS Agreement 1995, Article 5.7  
20 This point does not apply to corrections to spelling, punctuation or grammar.  6 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand   
 
1.7 References for Chapter 1  
FAO (1995) International Standards for Phytosanitary Measures (ISPM) No. 2. Guidelines for pest risk 
analysis. Secretariat of the International Plant Prote ction Convention, Food and Agricultural 
Organization of the United Nations, Rome.  
FAO (2013) International Standards for Phytosanitary Measures (ISPM) No. 11. Pest risk analysis for 
quarantine pests. Secretariat of the International Plant Protection Conven tion, Food and Agricultural 
Organization of the United Nations, Rome.  
MPI Standard 155.02.06 (2020) Ministry for Primary Industries Standard 155.02.06 Importation of 
Nursery Stock . Available at: https://www.biosecurity.govt.nz/dmsdocument/1152 -Nursery -Stock -
Import -Health -Standard  Accessed 12  November 2020  
PBI (2020) Plant Biosecurity Index (Version: 02.01.00) Ministry for Primary Industries Internal 
databa se.  
WTO (199 5) World Trade Organization (WTO) Sanitary and Phytosan itary Measures Agreement 
(SPS). www.wto.org/english/tratop_e/sps_e/sps_e.htm .  
   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 7 2 Scope and objectives  
 
This import risk analysis (IRA) has been developed in response to a request to review the import 
health standard  (IHS) for germplasm of all Citrus  species listed in the Plant Biosecurity Index from all 
countries. An IRA was completed for this commodity  in 2016 
(https://www.mpi.govt.nz/dmsdocument/14338 -Citrus -spp.-nursery -stock -Pest-Risk-Assessment ). 
 
Biosecurity New Zealand’s objective in reviewing the import health standard  for citrus germplasm is to 
ensure that the known biosecurity risk from pathogens associated with imported Citrus budwood is 
managed appropriately.  
 
The purpose of the import risk analysis is to identify and assess biosecurity risks a ssociated with 
imported leafless Citrus budwood, to inform decisions on risk management. The decisions that this 
import risk analysis  will inform are:  
a. whether any pathogens on Citrus budwood require additional measures, and  
b. whether to remove any pathogens  that do not require additional measures any more in the 
current import health standard , due to new scientific evidence.  
 
The objective of the import risk analysis  is to:  
a. identify any pathogens in the 2016 import risk analysis  for which the measures were c hanged 
without a documented risk assessment;  
b. identify any new pathogens since the 2016 import risk analysis  that meet the criteria for 
additional measures (or anything that was missed, e.g. the pest may not be new since 2016 
but literature may not have been found or available);  
c. identify any pathogens that are not listed as requiring additional measures in Level 3B post 
entry quarantine facilities but may meet the criteria for additional measures if the minimum 
requirements are Level 3A post -entry quarantine;  
d. assess those pathogens using a method that provides sufficient evidence about the 
biosecurity risks, for a robust and transparent decision on whether to apply additional 
measures.  
 
The m inimum risk managemen t requirements for this import risk analysis  are based on the import risk 
analysis  completed  in 2016.  
 
2.1 Scope and approach of this risk analysis  
 
For the purpose s of this IRA, the risk evaluation criteria are based on the minimum intervention 
considered s ufficient to manage pest risk s on leafless budwood that does not com e from approved 
offshore facilities . These interventions are  referred to as the minimum requirements. The import risk 
analysis process aims to determine which pathogens m ight not be manage d by minimum 
requirements and therefore require additional measures. T he following minimum requirement  for 
leafless budwood of Citrus spp. was proposed in the 2016 risk management proposal : 
 
• one growing season in Level 3A post -entry quarantine (PEQ)  
 
The pests that the risk management question applies to are pathogens  (viruses, viroids, bacteria, fungi 
and oomycetes ), as well as diseases of unknown aetiology and nematodes. Insects and mites will not 
be assessed in the import risk analysis,  because they  are currently  managed by insecticide and 
fungicide treatments before plants enter post -entry quarantine , as required under the Importation of 
Nursery Stock Standard (MPI Standard 155.02.06) . Therefore, review ing the risks of these pests are 
not in scope . 
 
Pathogens that meet, or potentially meet, the criteria for additional measures are those that:  
1. are associated with leafless Citrus budwood of all Citrus  species listed on the MPI Plant 
Biosecurity Index  
2. are not present in New Zealand (or is present but still represents a biosecurity risk, e.g. is 
capable of vectoring pathogens not present in New Zealand or is under official control)  
3. have traits which indicate that they cannot be contained in a Level 3A post entry quarantine 
facility  and/or be detected during one growing season in Level 3A post entry quarantine  
 8 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  One growing season in Level 3A post -entry quarantine may not reduce the risk of the following types 
of pathogens (for example ): 
• Pathogen s that can be latent for long periods (more than one growing season , such as fungi 
that can be endophytic ) 
• Pathogen s that  only caus es symptoms under certain growing conditions, such as when the 
plants are stressed  
• Pathogen  that can rapidly produce wind -dispersed s pores  
• Pathogens that are vector -transmitted, if there are vectors present in New Zealand, and if the 
vectors are small and mobile enough to enter a 3A post -entry quarantine facility, acquire the 
pathogen and then leave  the facility.  
 
Pathogens that meet the criteria above will undergo a risk assessment that considers the following 
factors:  
a. The strength or frequency of the association with Citrus germplasm; and  
b. The extent to which the minimum requirements will reduce the risk; and  
c. the suitability of the environment in New Zealand for the pathogen (including climate, host 
plant(s) availability, ability to spread and available vectors; and  
d. The economic, environmental, social and cultural  impact on New Zealand ( Citrus and other 
plants, including native s pecies); and  
e. The impact on human health.   
 
 
2.2 Commodity description  
 
The commodity for the IRA is leafless budwood21 of all Citrus  species (including Fortunella and 
Poncirus ) as listed  on the Plant Biosecurity Index  (PBI) , from all countries . Although Citrus  species 
don’t generally have a leafless dormancy period, cuttings have the leaves removed before importation.   
 
Table 1 puts the risk associate d with Citrus germplasm in the wider context  of relative risks of different  
commodities, pathways and plant species. The information in the general commodity risk assess ment 
and the section on the exposure of pests and diseases will be used in the IRA when assessing the risk 
of pests that may meet the criteria for additional measures. Further detail is given in subsequent 
sections.  
 
Table 1: Gener al commodity risk explanation  
Question  Factors to consider  
What is the relative risk associated with the 
commodity class?  Germplasm is the highest risk commodity class overall 22. This is 
because plants are grown from germplasm in conditions designed to 
maximise the survival and growth of the plants. As a result, conditions 
are also maximised for the associated pests and pathogens to 
establish.  
What is the relative risk associated with the 
type of material making up the commodity?  Leafless bu dwood are in the middle of the scale for relative risks 
associated with germplasm. This is because the greater the number of 
plant parts and the greater the size of the individual pieces of material 
imported, the greater the number and type of organisms an d 
diseases  that can be associated with the material. Whole plants and 
cuttings with leaves on , have a greater number of associated species. 
Tissue culture is similar to cuttings in terms of viruses, viroids, 
diseases of unknown aetiology and some bacteria,  but has fewer 
species of associated fungi, oomycetes and other bacteria.  
How likely is the c ommodity to carry pests and 
diseases  which can establish in New Zealand?  Citrus  is native to, and grown commercially in, areas overseas that 
have a similar climate to New Zealand, for example parts of China, 
Japan and Australia. It is also grown in areas that are less similar to 
New Zealand.  Citrus is therefore intermediate in terms of risk 
 
21 Budwood is a  portion of a stem or branch (aerial plant parts only) with a vegetative b ud(s) used in propagation for budding or 
grafting  
22 ISPM 32 https://www.ippc.int/static/media/files/publication/en/2016/01/ISPM_32_2009_En_2015 -12-22_ PostCPM10 
InkAmReformatted.pdf   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 9 Question  Factors to consider  
likelihood  – it is higher than species grown in very specific climates, 
for example , mango, but lower than temperate species, for example , 
cherries.  
 
Citrus  is grown commercially and in home gardens in New Zealand , 
although wild records are rare23. Therefore,  associated pests and 
diseases , including those that are host -specific, are likely to come into 
contact with host plants in New Zealand.   
How likely is the commodity to carry pests 
which cause major impacts in New Zealand? 
What are the values associated with the 
commodity species and the related species in 
New Zealand?  The pests and diseases  associated with Citrus budwood  may affect 
many different host plants in New Zealand. However, the likelihood 
that particular hosts will be affected may be dependent on how closely 
related those hos ts are to Citrus. There is a strong relationship 
between how closely related plant species are and how likely they are 
to share pests and diseases  (Gilbert and Webb 2007).  Therefore, the 
host plants most likely to be affected by pests and diseases  carried on 
Citrus germplasm are Citrus species. The next most likely are 
members of the same family (Rutaceae). There are both native 
(Melicope and Leionema ) and introduced ornamental (e.g. Choisya, 
Coleonema ) genera of the Rutaceae family in New Zealand. Some 
pests and diseases  associated with Citrus affect a wide range of other 
species, for example , some fungi.  
 
Pests and diseases  that are associated with Citrus but affect other 
members of the family have the potential for environmental impacts as 
well a s impacts on amenity values. The native genera Melicope and 
Leionema do not occur overseas in regions where Citrus is native or 
cultivated, e.g. Hawaiian Islands, across the Pacific to tropical Asia 
and Australia. Ornamentals in the family Rutaceae, such a s Choisya, 
Coleonema are widely grown around the world. Therefore, many 
common Citrus pests and diseases  have had the opportunity to switch 
hosts onto these genera. This means that, if pests of Citrus have not 
been recorded on these genera overseas, they a re less likely to affect 
members of these genera in New Zealand.  
 
Citrus  is an important crop in New Zealand. The New Zealand citrus 
industry comprises around 1,600 hectares located in  the Bay of 
Plenty, Gisborne and Northland regions. In 2019, the domest ic and 
export sales of fresh citrus fruit were $58.5 million and $12 million, 
respectively (Plant & Food Research 2019).  
 
What is the level of knowledge about the pests 
associated with the commodity and related 
species in New Zealand and overseas?  Citrus  is a well-known  crop that is widely cultivated. Thus, there are 
reliable literature sources for some pests and pathogens associated 
with Citrus across a wide range of countries/continents. There is likely 
to be less information on native R utaceae in New Zealand and 
abroad.  
Conclusion  There is a high risk associated with the importation of Citrus spp. for 
propagation. However, the risk is lower than for commodities that may 
be more temperate in their distribution  or that have many related 
native and economically important plant species in New Zealand (e.g. 
Prunus and Malus ). 
 
 
23 Allan Herbarium 
https://nzflora.landcareresearch.co.nz/default.aspx?selected=NameDetails&TabNum=0&NameId=0BDA3A5C -4DA1 -4289 -
9B8B -C0B3B3A7A6D6  10 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  2.3 Taxonomy  of the plant commodity under consideration  
The taxonomy of citrus fruit species is unclear because of a long history of cultivation and 
hybridisation. The cu rrent wide diversity of commercial citrus fruits is derived from four ancestral 
species  (see, for example , Barrett and Rhodes 1976; Nicolosi  et al. 2000;  Wu et al. 2018 ). Some of 
the lesser -known types (such as yuzu) also have parentage of other species. The ancestral species 
are believed to include : 
• Citrus maxima (pomelo)  
• Citrus reticulata (ancestral mandarin)  
• Citrus medica (citron)  
• Citrus micrantha (small -flowered papeda)  
 
All main  commercial citrus are hybrid s involving parentage of those four species. The hybrids include 
both natural and deliberate crosses. As well as hybridising freely, many types of citrus have 
adventitious  or nucellar  embryony (where one or more vegetative embryo forms from cells of  the 
nucellus of the ovule) (i.e. apomixis  (Zhang et al. 2018) ). 
 
As a result of this complex history, there are various  names applied to different types of fruit , and 
many are only known by their common or trade name . Whether a plant is considered a hybrid,  or a 
species is a taxonomic  question not  necessarily relevant to the question of biosecurity risk.  
 
In 2002 , INRA -CIRAD24 published a review of all known cultivars, varieties, hybrids and species of 
Citrus in cultivation from around the world ( INRA -CIRAD 2002). The review lists  all of the Citrus that 
were then known by the two  major  Citrus naming systems published by Tanaka and Swingle.  While 
INRA -CIRAD (2002) will not contain more recent Citrus cultivars or varieties, the list is the most recent 
attempt to produce a coherent description of the cultivated Citrus complex (see Table 2). Although the 
complexity of  the Citrus taxonomy presents difficulties when it comes to categorising and grouping 
commodities for fresh produce IHSs, this is not a significant issue for this IRA which considers all 
Citrus species listed in the PBI (PBI 2020).  
 
Table 2: List of common Citrus commodities based on the Swingle naming system, using INRA -CIRAD (2002).  
Citrus species (or hybrids)  Synonyms  Common names  
Citrus aurantiifolia (Christ.) Swingle  Citrus limettioides  Lime, Sweet lime, Key lime, 
Mexican lime  
Citrus aurantium L.  Sour orange  
Citrus latifolia (Yu. Tanaka) Tanaka   Tahitian lime  
Citrus limon (L.) Burum.f.  Citrus limonia, Citrus meyeri  Lemon, Meyer lemon  
Citrus maxima (Burman) Merr.  Citrus grandis  Pomelo, Pummelo  
Citrus medica L.   Citron  
Citrus paradisi McFad.  Citrus hassaku  Grapefruit, Hassaku  
Citrus reticulata L.  Citrus unshiu, Citrus deliciosa  Mandarin, Tangerine, Unshu  
Citrus sinensis (L.) Osbeck  Citrus iyo  Orange, Iyokan  
Citrus reticulata  × Citrus paradisi    Tangelo  
Citrus reticulata × Citrus sinensis   Tangor, Satsuma  
 
 
2.4 General information related to the likelihood of entry  
2.4.1  Pathway description  
Because the scope of the import risk analysis includes  all growing conditions and production methods, 
the import risk analysis  need s to consider  pathogens that occur in some ecological and environmental 
conditions  and not others.  
 
While it is reasonable to consider that obviously diseased plants would not be used as a source of 
germplasm, many pathogens are not visible on the plant  surface . Several  of the pathogens discussed 
have obvious symptoms on leaves, flowers , or fruit, but not stems. Plants infected with such 
pathogens are unlikely to be used as a sourc e of budwood  by commercial growers using known 
source plants. However , infected plants may be used for other purposes, such as for breeding 
 
24 Station de Recherche Agronomique, Institut National de la Recherche Agronomique - Centre International de Recherche et 
d’aide au Développement (INRA -CIRAD)   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 11 programmes , or budwood  may be harvested from plants that have not been observed over a long 
period of time.  
 
The import risk analysis  therefore co vers several  pathogens with a limited distribution or infrequent 
association with Citrus  or pathogens that have obvious symptoms during at least part of the year. 
These pathogens have a much lower likelihood of being present in Citrus  nursery stock than more 
widespread Citrus  pathogens ; however , they cannot be ruled out as a risk , given the import risk 
analysi s scope.  
 
In a Level 3 A post-entry quarantine  facilit y, all water leaving the facility must be decontaminated using 
a method proven to kill plant pathogens . The facility must  have vents screened with insect -proof mesh 
with a maximum aperture of 0.2  mm, must be monitored for insects and must be built in such a way 
that no plants are within 1  m of the facility (MPI 2019 ). Additionally, plants are inspected  for signs of 
disease twice a week during active growth and once a week during dormancy (MPI 2019 ). If found, 
any symptoms are diagnosed and controlled . Therefore, if symptoms are due to fungal infection, spore 
production will be  minimised.  
 
A summary of the import pathway of leafless Citrus budwood into New Zealand from non -MPI 
accredited facilities is given in Figure 2.    
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Figure 2: Summary of the pathway for the import of leafless Citrus budwood from non -MPI accredited facilities  
 
2.5 General information related to the likelihood of establishment  
 
2.5.1  Exposure  
When a pathogen arrives in a new area, it usually needs to find or come into contact with a growing 
host plant in order to establish. In the case of nursery stock, imported plant material is  maintained in a 
habitat favourable  for plant growth and is likely to be multiplied up to substantial numbers. Promoting  
the survival and per sistence of the plant material also promotes the survival and persistence of the 
associated pathogens. The process of a pathogen coming into contact with a growing host plant is 
termed “exposure” in MPI risk assessments. Previous import risk analyse s for ger mplasm, such as 
Actinidia  tissue culture (MPI 2018) , have determined  exposure to have a high likelihood with low 
uncertainty, regardless of the pathogen type being assessed. P est risk assessment s for Citrus  nursery 
12 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  stock (MPI 2016) similarly reported a hig h likelihood for exposure for all assessed pathogens. 
Exposure has therefore not been assessed for individual pathogens in this import risk analysis . 
 
2.5.2  New Zealand climate s 
New Zealand in general exhibits a mid -latitude oceanic temperate climate (Cfb temper ate with 
maritime climate in the K öppen classification (K öppen 1936 ; Rubel and Kottek 2010) ). Annual 
precipitation varies substantially due to topography, from dry eastern and inland areas to very high 
precipitation (on a global scale) in  areas of the West  Coat  areas25. The driest New Zealand climates 
barely reach a conventional water deficit on average (although they can do so in extreme years and 
months). The New Zealand climate ‘space’ can be visualised  as a three -dimensional simplified climate 
niche ( Figure 3 ). This represents the average monthly temperature and precipitation for each month 
of the year for 42 New Zealand climate stations.  
 
 
Figure 3: Climate niches of New Zealand. Thin grey lines: average monthly temperature ( 1981–2010) for 42 
New Zealand climate stations (data from NIWA (2020) ). Each polygon is composed of the 12 months of 
the year. Small black ellipse: average conditions for those 42 sites. Large ellipse: 95% inclusive ellipse.  
 
As a consequenc e of being a small land  mass in a large ocean, New Zealand has  relatively low 
diurnal and seasonal temperature fluctuations (equable climate). Rainfall is close to evenly distributed 
between summer and winter. These features are similar in equatorial climates. However, there can be 
relatively rapid variations between days as large weather systems alternate over the oceans.  
Unlike many northern hem isphere continental climates with reliable lengthy warm and cold periods, a 
small temperature variation in a mild oceanic climate means a more significan t change in the number 
of days crossing threshold degrees , which may in some cases restrict the ability  of some organisms to 
establish. This feature is also common to sma ller land masses and mountains of the southern 
hemisphere, which is why , globally , some of the most similar climate conditions to New Zealand are in 
the montane regions of the Andean Yungas  cloud forests and grasslands (Halloy et al. 2008) . This is 
reflected in high morphological similarities of adaptions (Halloy and Mark 1996).  
Together with tussock grasslands, temperate rainforests are the global biome  most represented in 
New Zealand. The  northernmost  areas of New Zealand are subtropical, with an ability to grow a range 
of subtropical plants.  
 
25 This summary is written with crop pests and diseases in mind, focusing on the climate in inhabited and cultivated areas of 
New Zealand. Rainy outliers (e.g. Milford and Mt Cook) and high mountain climates are not considered, as they represent 
extremes wit h relatively low human and agricultural activity.  
050100150200250300
-10 0 10 20 30precipitation, monthly (mm)
temperature, average monthly (oC) 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 13 The northern part of New Zealand is the most climatically suitable for the establishment of new pests 
and pathogens from sub -tropical  or tropical cl imate s, due to the c limate suitability of th is area. The 
area includes Kaitaia, Kerikeri, Whangarei, Auckland and Tauranga. Auckland and Tauranga  contain 
large, active seaports .  
2.5.3  Distribution of Citrus in New Zealand  
Citrus  species are native to  the warmer temperate climates of the world , and most parts of New 
Zealand’s coastal environments are ideal for them as long as they are sheltered.  Mature trees are 
either flowering or fruiting and commonly doing both together. The genus Citrus is widespread 
throughout the country with households commonly having Meyer lemon trees in their gardens. If 
conditions allow, other species of Citrus can be found growing in home gardens. Citrus × aurantium L. 
(sour orange) and C. × limon, especially cv. ‘Meyer’ (Meyer le mon), C. reticulata Blanco 
(mandarin/tangerine/satsuma) and C. sinensis (orange) , are very commonly grown in warmer North 
Island areas. The Bearss cultivar of Tahitian lime, C. × latifolia cv. (Yu . Tanaka)  Tanaka , is also 
common and will also grow in coole r areas of the North Island. Nevertheless, on the New Zealand 
mainland , no Citrus spp. has been reliably reported in the wild.   
The main citrus-growing areas of New Zealand are the Northland, Auckland, Bay of Plenty and 
Gisborne region s (Plant and Food Re search  2019). Most commercial production takes place in the 
Gisborne and Northland regions, followed by Auckland, Bay of Plenty and Hawke’s Bay, with much 
less in other regions through out the North Island and in parts of the South Island (Plant and Food 
Research  2019).   
The northern part of New Zealand is the most climatically suitable for the establishment of new pests , 
pathogens  and vectors  from sub -tropical  or tropical climate s. The area includes Kaitaia, Kerikeri  and 
Whangarei (Northland) , Auckland, and Tauranga (Bay of Plenty).  
Climate in the regions where citrus is grown  commercially : 
• Northland: Kerikeri is an orcharding town , with many varieties of Citrus  fruit grown there. 
Avocado s, kūmara, macadamia s and tamarillos are the other main cr ops grown there 
(HortResearch 2005; Plant and Food Research 2010). This is a sub -tropical zone, with warm 
humid summers and mild winters. Typical summer daytime maximum air temperatures range 
from 22 °C to 26 °C, but seldom exceed 30 °C. Winter daytime maximu m air temperatures 
range from 12 °C to 17 °C (NIWA 2008).  
• Auckland: This region produces a variety of crops including Citrus  species such as 
mandarins . The region also produces  strawberries, herbs, Asian vegetables, brassicas, 
chestnuts, greenhouse crops, lettuce, olives, onions, persimmons, pumpkin and silverbeet 
(HortResearch 2005; Plant and Food Research 2011). It has a moderate climate favouring 
plant  species from many clima tic zones (Esler 1988).  
• Bay of Plenty: During summer the region experiences average daily air temperatures over 
20°C. The low-lying, coastal areas experience mild winters  (NIWA 2013). T auranga produces 
feijoas, citrus, avocado s, asparagus, tamarillos and k iwifruit (HortResearch 2005; Plant and 
Food Research 2010).  
• Gisborne : Has a large number of sunshine hours and low wind. Rainfall is unevenly 
distributed, with a prominent winter maximum. There  are small areas of the region that have  
high productivity for fruits and vegetables (NIWA 2016). Prominent crop species include citrus, 
wine grapes, apples and squash ( Plant and Food Research 2019).   
 
The large number  of pests associated with Citrus species, and the fact that a number of the a ssessed 
pathogens are recently described, means  that a detailed assessment of establishment and potential 
distribution is not possible. With respect to establishment and range, climate is generally a more 
important consideration for invertebrate pests than  for pathogens. Although climate is not the primary 
indicator of a pathogen ’s ability to establish, it is a useful when  consider ing the  extent of disease 
expression , particularly if pathogen spread is dependent on a vector. The climate overlap between 
New Zealand and where a pathogen has been reported is assessed using the tool described in 
Phillips et al. (2018). This tool is based on the c limate  match index (CMI) CLIMEX -MCR of CLIMEX 
version 3.3. The tool allows the comparison of New Zealand’s climate in general with areas where a 
pest/ pathogen occurs overseas. The CMI range extends from 0 to 1; the higher the CMI, the more 
similar the climate of the region to which the CMI pertains and the New Zealand climate. A CMI of 0.7 14 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  or more between the New Zealand climate and the existing range of the pathogen indicates a more 
similar climate and therefore a higher likelihood of establishment. A CMI of less than 0.7  indicates  less 
similarity between New Zealand and the pathogen’s existing range (Phillips et al. 2018 ). 
 
For many of the pest/pathogens assessed, this tool is likely to be a sufficient indication of climatic 
suitability in New Zealand for the pest to establish. Figure 4 shows the whole -world map with CMI data 
from Phillips et al. (2018). When using the tool, the map can be enlarged  to show more detail at a 
regional level.   
 
 
Figure 4: Climate Match Index (CMI). World climate similarities with all New Zealand (Phillips et al. 2018)  
 
 
2.6 General information related to impacts of pests and diseases  
 
2.6.1  Potential impacts on non -Citrus species  
When considering impacts, MPI assesses  close family relatives to be the most likely to be  affected by 
pests and pathogens associated with Citrus spp. Citrus belongs to the family Rutaceae, a 
cosmopolitan family with around 150 genera (The Plant  List 2013). Citrus is the main economically 
important genus, although there are other genera that  provide fruit , such as Casimiroa , and species in 
other genera that pro vide flavouring, for example Galipea officinais , which is the source of angostura 
bitters , and Bergera koenigii, used in Indian and Sri Lankan cooking (Mabberley 2008). There are also 
a number of ornamental species from other Rutaceae genera grown in New Z ealand, such as Boronia, 
Choisya  and Coleonema  (Landcare Research 2020).  
 
New Zealand has three endemic species in the Rutaceae: Leionema nudum, Melicope simplex and 
M. ternate (Landcare Research 2020). The two Melicope species are found in lowland areas in both 
the North and South Islands, while L. nudum is found only in the northern half of the North Island (AVH 
2020). Neither the Leionema nor Melicope species are threatened (de Lange et al. 2018).  
 
The Rutaceae is a common family in cultivation in New Zealand , but few species have naturalised , 
and none have done so extensively (Landcare Research 2020).  
 
 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 15 2.6.2  Potential for economic impacts to the Citrus industry  
The New Zealand citrus industry comprises around 1, 660 hectares divided between approximately 
316 growers, with most commercial production taking place in the Gisborne and Northland regions, 
followed by Auckland, Bay of Plenty and Hawkes’s Bay, with much less in other regions through out 
the North Island and in parts of the South Island (Plant  and Food Research  2019).   
 
Growers were estimated to have produced 34,096 tonnes of citrus in 2018/2019 (Plant and Food 
Research  2019). Most product is grown for the  domestic market (NZIER 2016). In 2018/19, 
New Zealand domestic sales of fresh citrus fruit were worth  NZ$58.5  million (mandarins NZ$25.2  
million , oranges NZ$18.0  million , lemons $12.0  million , limes NZ$2.0 million , tangelos NZ$1.0 million , 
grapefruit NZ$0.3 million ) (Plant and Food Research  2019).  
In 2019 , export sales (free -on-board value) of fresh fruit were worth NZ $12 million (lemons $9.8  M, 
oranges NZ$1.7 million , mandarins NZ$0.4 million , tangelos NZ$0.1 million ) (Plant and Food 
Research  2019). Processing mainly involves juicing citrus and other human consumption items 
(NZIER 201 6). Domestic and export sales in relation to the processing of citrus h ave been estimated 
to be worth NZ$55.4  million, with the citrus processing value estimated as NZ$11.7  million (NZIER 
2016). In 2012/2013 (April year), the impact of citrus on the GDP was estimated to be NZ$27.1 million 
(NZIER 2016). This was calculated from tree sales, farm gate sales, domestic sales, processing 
(mainly juice) and export sales. A summary of the New Zealand citrus industry is provided in Table 3.  
 
Table 3: How big is the New Zealand citrus industry?  (NZCGI , accessed 23 Oct 2020 )  
 Growers*  Hectares  
planted  Number of  
Trees  Tonnes 
(Fruit) Domestic  
Sales ( NZ$ 
M) Export  
(NZ$ M) 
Citrus , total  320 1,663 1 million + 29,740  $58. 3 M $12 M 
Mandarins  198 556 513,871  10,920  $25 M $0.4 M 
Oranges  183 783 320,84 0 10,100  $18 M $1.7 M 
Tangelos  28 22 11,105  640 $1 M $0.1  M 
Lemons  180 260 153,73 0 7,000 $12 M $9.8 M 
Limes  50 27 8,960 710 $2 M – 
Grapefruit  18 15 4,247  370 $0.3 M – 
* Many growers produce more than one citrus variety.  
 
The average yield is 18  T/ha over all varieties. Information on the New Zealand citrus  growing season 
is provided  in Figure 5.  
 
 
 
Figure 5: When  is citrus in season in New Zealand? (NZCGI, accessed 23 Oct 2020 ) 
 
 
2.7 References for Chapter 2  
 
Allan  Herbarium (20 19) Ngā Tipu o Aotearoa – New Zealand Plant Names Database. Landcare 
Research; NZ. https://nzflora.landcareresearch.co.nz. Accessed 29 March  2019. 
AVH (2020) Australasian Virtual Herbarium . https://avh.chch.org.au/  (accessed May 2020)  
16 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Barrett, H C; Rhodes, A M (1976) A numerical taxonomic study affinity relationships in cultivated 
Citrus and its close relatives. Systematic Botany , 1(2): 105 –136.  
De Lange, P J; Rolfe, J R; Barkla, J W; Courtney, S P; Champion, P D; Pe rrie, L R; Beadel, S M; Ford, 
K A; Breitwieser, I; Schonberger, I; Hindmarsh -Walls, R; Heenan, P B; Ladley, K (2018) Conservation 
status of NZ indigenous vascular plants, 2017. New Zealand Threat Classification Series 22 . 
Department of Conservation; Wellin gton. 82 pages. https://www.doc.govt.nz/documents/science -and-
technical/nztcs22entire.pdf   
Halloy, S R P; Beck, S G; Ledezma, J C (2008) Central Andean Grasslands (Páramo, Puna) and 
High-Andean (central and southern Perú, western Bolivia, northern Chile and northwestern Argentina). 
In Peart, B (ed)  Compendium of Regional Templates on the Status of Temperate Grasslands 
Conservation and Protection . IUCN; Qu ito, Ecuador; pp 148 –159.  
Halloy, S R P; Mark , A F ( 1996 ) Comparative leaf morphology spectra of plant communities in 
New Zealand, the Andes and the European Alps. Journal of the Royal Society of New  Zealand , 26(1): 
41–78. 
IPCC_WGI (2013) Working Group I contribution to the IPCC Fifth Assessment Report Climate Change 
2013: The Physical Science Basis - Final draft (Accepted). Intergovernmental Panel on Climate 
Change.  
Kean, J M; Brockerhoff, E G; Fowler, S V; Gerard, P J; Logan, D P; Mullan, A B; Sood, A; T ompkins, 
D M; Ward, D F (2015) Effects of climate change on current and potential biosecurity pests and 
diseases in New Zealand. Ministry for Primary Industries, Wellington.  
Köppen, W (1936) Das geographische System der Klimate. In Köppen, W; Geiger, R (ed s) Handbuch 
der Klimatologie . Vol. 1, Part C. Gebrüder Borntraeger; Berlin, Germany; pp C1 –C44.   
Mabberley, D J (2008) The Plant -book: a portable dictionary of plants, their classifications and uses. 
Cambridge University Press, United Kingdom. 3rd edition.  
MfE (2018) Climate Change Projections for New Zealand. Ministry for the Environment (MfE), 
Wellington.  
MPI (2018) Import risk analysis: Actinidia  plants for planting (plants in vitro ). Ministry for Primary 
Industries, Wellington.  
MPI (2019) Post Entry Quarantine for Plants. https://www.mpi.govt.nz/dmsdocument/11368  Accessed 
18 September 2020.  
Nicolosi, E; Deng, Z N; Gentile, A; La Malfa, S; Continella, G; Tribulato, E (2000) Citrus phylogeny and 
genetic origin of important species as investigated by molecular markers. Theoretical and Applied 
Genetics , 100: 1155 –1166 . https://link.springer.com/article/10.1007/s001220051419  
NIWA (2 013) The climate and weather of Bay of Plenty, 3rd edition. 
https://niwa.co.nz/static/BOP%20ClimateWEB.pdf  
NIWA (2016) The climate and weather of the Gisborne district, 2nd edition. https://niw a.co.nz/our -
science/climate/publications/regional -climatologies/gisborne  
NIWA (2017) Climate change scenarios for New Zealand. https://niwa.co.n z/our -
science/climate/information -and-resources/clivar/scenarios#regional . 
NIWA (2020) The National Climate Database. https://cliflo.niwa.co.nz/ . 
NZIER (2016) How valuable is that plant species? Application of a method for enumerating the 
contribution of selected plant species to New Zealand’s GDP. MPI Technical Paper No: 2016/62. 
Prepared for the Ministry for Primary Industries by NZIER, New Zealand Institute of Economic 
Research. (227 p ages )  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 17 PBI (2020) Plant Biosecurity Index ( version 02.01.00) . Ministry for Primary Industries internal 
database.  
Phillips, C B; Kean, J M; Vink, C  J; Berry, J A (2018) Utility of the CLIMEX ‘match climates regional’ 
algorithm  for pest risk analysis: an evaluation w ith non -native ants in New Zealand. Biological 
Invasions , 20(3): 777 –791. Climate match tool available at: https://b3nz.shinyapps.io/CMI -maps/.  
Plant & Food Research (2019) Fresh Facts: New Zealand Horticulture . The New Zealand Institute for 
Plant and Food  Research Ltd, Auckland. https://www.freshfacts.co.nz/files/freshfacts -2019.pdf  
Rubel, F ; Kottek , M (2010 ) Observed and projected climate shifts 1901 –2100 depicted by world maps 
of the Köppen -Geiger climate classification. Meteorologische Zeitschrift , 19(2):135–141(137).  
Sutton, P J H; Bowen , M (2019 ) Ocean temperature change around New Zealand over the last 36 
years. New Zealand Journal of Marine and Freshwater Research , 53(3): 305 –326. 
The Plant List (2013) Version 1.1. http://www.theplantlist.org/ . Accessed 29 March 2019.  
The Plant List (2013) Rutaceae . Version 1.1. http://www.theplantlist.org/1.1/browse/A/Rutaceae/  
Accessed 29 March 2019.  
Wallace -Wells, D  (2019 ) The Uninhabitable Earth . Annotated Edition . Intelligencer ; New York. 
http://nymag.com/intelligencer/2017/07/climate -change -earth -too-hot-for-humans -annotated.html . 
WMO (2019 ) The State of the Global Climate in 2018. http://ane4bf -datap1.s3 -eu-west-
1.amazonaws.com/wmocms/s3fs -
public/ckeditor/files/Draft_Statement_26_11_2018_v12_approved_jk_0.pdf?VXUDp1UTysIkHog4_TT
uiHsIzZ6A9D93 . 
Wu, G A; Terol, J; Ibanez, V; López -García, A; Pérez -Román, E; Borredá, C; Domingo, C; Tadeo, F R; 
Carbonell -Caballero, J; Al onso, R; Curk, F (2018) Genomics of the origin and evolution of Citrus . 
Nature , 554(7692): 311 –316. https://doi.org/10.1038/nature25447  
Zhang, S; Liang, M; Wang, N; Qiang, X; Deng, X, Chai, L (2018) Repro duction in woody perennial 
Citrus: an update on nucellar embryony and self -incompatibility. Plant Reproduction , 31: 43 –57. 
https://doi.org/10.1007/s00497 -018-0327 -4 
  18 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  3 Hazard identification  
 
 
In order to identify hazards  that potentially meet risk evaluation criteria, hazard identification was 
conducted as a ‘gap analysis’ of the 2016 work,  focus ing on the following : 
• Pathogens , nematodes, or diseases  associated with the commodity;  and, 
• Not assessed in the 2016 draft review;  OR, 
• Measures were proposed in 2016 but the decision was not supported by risk assessment;  
• The pathogen , nematode or disease  has traits that mean that i t may not be detected or 
contained during one growing season in level 3A post -entry quarantine  such as : 
o the ability to  be latent for long periods (more than one growing season , such as fungi 
which can be endophytic );  
o the tendency to  only produce  symptoms under certain growing conditions , such as 
when the plants are stressed;  
o the ability to  rapidly produce wind -dispersed spores.  
 
The hazard identification search did not identify any nematodes or diseases that were considered 
hazards; however , a number of pathogens were identified. Therefore, in the remaining sections , only 
pathogens are cons idered.  
 
Because this import risk analysis  will be used to develop  an import health standard  for all Citrus spp. 
listed in the Plant Biosecurity Index , the hazard identification  needs to take  this into account ( identified  
pathogens may only be reported fro m a restricted number of Citrus species).  
 
Hazard identification  for this project  used a range of sources , including:  
• CABI Crop Protection Compendium (2018/ 2019/2020) 
• CAB Abstracts  
• Google Scholar  
• Google  
• EPPO Global Database  
• Existing pest lists from  the Citrus  germplasm IHS and the draft 2016 pest list  
• Farr & Rossman (2017/2018 /2020 ) (for fungi and oomycetes)  
• Ferris (2020)  (for nematodes)  
• MPI Emerging Risks System database  
• General literature searches  
A list of species identified at the hazard identif ication stage as associated with the commodity, not 
present in New Zealand, not assessed in the 2016 draft review, and therefore requiring further 
assessment (a Pest Risk Assessment) is provided in Table 4. 
 
Table 4: Results of hazard identification for citrus cuttings . 
Pest group  Species requiring pest risk assessment  (PRA)  
Fungi  Colletotrichum abscissum  
Colletotrichum  limetticola  
Diaporthe baccae, D. hongkongensis, D. novem  
Elsino e australis  
Erysiphe quercicola, Fibroidium tingitaninum  
Lasiodiplodia brasiliensis, L. citricola, L. hormozganensis, L. iranensis, L. mediterranea, L. mitidjana, 
L. pseudotheobromae, L. subglobosa  
Phyllosticta citrocarpa  
Plenodomus tracheiphilus  
Virus  Citrus leprosis viruses: Citrus leprosis virus C (CiLV -C), Citrus leprosis virus C2  (CiLV -C2), Hibiscus 
green spot virus 2, Orchid fleck dichorhavirus [citrus strain], Citrus leprosis N dichorhavirus, Citrus 
chlorotic spot dichorhavirus, Citrus chlorotic spot virus  
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 19 Groups (e.g. genera or family) or high -profile species that did not meet the criter ia for requir ing 
pest risk assessment are listed in Appendix 1, along with the rationale for excluding them at 
the hazard identification stage.  
 
 
3.1 References for Chapter 3  
 
CABI Crop Protection Compendium . Information on crop pests.  https://www.cabi.org/cpc/  
EPPO Global Database.  European and Mediterranean Plant Protection Organization (EPPO)  
database for all pest -specific information that has been produced or collected by EPPO.  
https://gd.eppo.int/  
 
Farr, D  F; Rossman, A  Y. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. 
https://nt.ars -grin.gov/fungaldatabases/  
 
Ferris, H (2020) Nemaplex.  The nematode -plant expert information system. Department of 
Entomology and Nematology, University of California, Davis. http://nemaplex.ucdavis.edu/  
 
 
  20 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  4 Risk assessment  criteria  
 
The purpose of the risk assessments in this  import risk analysis  (IRA) is to assess the level of risk that 
hazards (e.g. pests and diseases) present to New Zealand.  
4.1 Risk management questions  
Each individual pest risk assessment answers the following questions:  
1. Does the pest  or disease meet the criteria to be a quarantine pest under IPPC?26 
2. Does the pest or disease meet (or potentially meet) the criteria for additional measures?  
4.2 Criteria and traits for additional measures  
Pathogens  that meet or potentially meet the criteria for additional measures are those that:  
• Are associated with leafless Citrus budwood; and  
• Are u nlikely to be detected or contained during one growing season in Level 3A post -entry 
quarantine , for example : 
o if the pathogen can be latent for long periods witho ut showing symptoms,  
o if the pathogen rapidly produces copious quantities of wind -dispersed spores,  
o  if the pathogen is vector -transmitted , and there are vectors present in New Zealand, 
and the vectors are small and mobile enough to enter a 3A post -entry quarantine 
facility, acquire the pathogen and then escape the facility.  
 
4.3 Assessment method  
A range of different approaches can be used for risk assessment. The most important factor in 
determining the approach is the risk management question and the level of assessment needed to 
support a robust and transparent risk management decision.  
 
In the case of the Citrus  nursery stock  import risk  analysis , the risk management question is specific, 
aiming to identify pests and diseases  that meet the criteria for needing additional measures over basic 
conditions . 
 
The pest risk assessment  used is called a targeted pest risk assessment , as it is targ eted at 
answering a limited range of questions. The pest risk assessment  method used covers the following 
questions:  
• Does the pest or disease  meet the criteria to be a quarantine pest under the IPPC?  
• Is the pathogen associated with the commodity?27 
• Does th e pest or disease meet the criteria for requiring additional measures over the basic 
conditions ? 
 
The questions above require  a binary answer —either the pest s or diseases  meet the criteria,  or they 
do not. Where the uncertainty is limited or does not affec t the conclusion, the answer to the risk 
management question is given as either:  
• The pest or disease meets  the criteria for requiring additional measures.  
• The pest or disease  does not meet the criteria for requiring additional measures.  
 
In some cases, unc ertainty in the assessment means that it is unclear whether the pest or disease  
meets the criteria or not. The pest or disease  may meet some criteria but not others, or the evidence 
may be limited. In other cases, the status of the pest or disease  as a quarantine pest may be 
uncertain, or the association with the commodity  may be weak. In these cases, the pest or disease  
requires  further consideration in the risk management proposal, taking articles 2.2 and 5.7 of the 
SPS Agreement into account.  
 
Where there is some evidence for the pest or disease  meeting the criteria, but there is substantial 
uncertainty, this uncertainty is sta ted in the conclusion. For example: the overall conclusion is given 
as: 
 
26 This question is a part of hazard identification (or pest categorisation in IPPC) but is documented in more detail as a part of 
the risk assessment.  
27 These first two questions are part of hazard identif ication but are included if further risk assessment is done.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 21 • The pest or disease  may meet the criteria for requiring additional measures, but this is 
uncertain.  
 
To answer these questions, the pest risk assessment s use the CASE schema. Under the  CASE 
schema, the contention  or conclusion  (that is, the answer to the risk management question) is 
presented first, followed by the arguments  supporting this contention and the evidence  and sources  
supporting each argument.  
 
For nursery stock  IRAs, past experience has shown that the critical aspects of the risk that needs to 
be assessed are : 
 
1. Likelihood of entry : 
a. The strength or frequency of the association with the host material  
b. Likelihood of entry given the application of basic conditions  
2. Likelihood of establishment : 
a. The ability of the pest or disease  to move from imported fruit and into a suitable  
environment to allow establishment (exposure)  
b. The suitability of the New Zealand environment for the pest or disease (including 
clima te, host plants and vectors)  
3. The potential impacts  in New Zealand : 
a. Economic impacts: on Citrus  and other economic ally important  plants (symptoms  on 
individual plants , crop yield, costs of management practices, trade restrictions , etc.) 
b. Environment  impacts:  on native plants and ecologies  
c. Other impacts (e.g. human health, socio -cultural) . 
 
For each of the critical aspects listed above, the following criteria and rankings are used in this IRA to 
assess the overall risk of each pest or disease considered to be a hazard on the pathway . 
 
Entry  
 
1a. Strength or frequency of association with the commodity  
 
Strong  There is a c lear biological reason that the pathogen is in side citrus 
budwood or strongly attached to the outside of citrus  budwood.  
Moderate  There is a link between the pathogen and citrus budwood but not under all 
circumstances, for example , only when the pest or pathogen is at high 
incidence levels , or there is an other less strong or frequent relationship.  
Weak  The pathogen is o nly rarely associated with the commodity . 
Negligible  There is no association of the pathogen  with the commodity as described in 
this import risk analysis .  
 
 
For each of the following likelihood and impact scores, the following ranking scales will be used 
against the listed criteria:  
 
High Extending above the normal or average level  
Moderate/Medium  Around the normal or average level  
Low Less than average, coming below the normal level  
Very low  Close to insignificant  
Negligible  Not worth considering; insignificant  
 
 
1b. Likelihood of entry into New Zealand after the application of the minimum requirements  
 
Criteria  The effect the biology and epidemiology of the pest or disease , the 
commodity description, the trade pathway, and  the application of the basic 
conditions  affect the likelihood that the pest or disease  will be associated 
with the commodity on arrival in New Zealand . 
 
 
 
 22 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Establishment  
 
2. Suitability of the New Zealand environment  
 
Criteria  The effect  the biology and epidemiology of the pest or disease  affect the 
likelihood that it will establish and build a population and spread into the 
environment, based on factors such as climate suitabili ty and the availability 
of hosts or potential hosts.  
 
Impact s  
 
3. The economic, sociocultural, environmental,  and human health  impacts to New Zealand   
 
Criteria  The effect  the biology and epidemiology of the pest or disease  affect the 
extent to which the pest or disease will cause impacts on New Zealand 
plants and subsequently cause wider impacts on the econom y, 
environment, socio -cultural, and/or human health . 
 
 
Confidence in the evidence – weight of evidence, uncertainty  
 
Weighing the evidence is an inherent part of every scientific assessment . The analyst  review s all 
available data and  come s to conclusions based on an assessment of their overall confidence in the 
results of all reviewed studies.  EFSA (2014) is used as gui dance for weighing the evidence. In the 
pest risk assessments in this project, the uncertainty associated with a conclusion/contention is stated 
in each contention. Unless the uncertainty is rated as low , the rationale for the uncertainty rating will 
be stated in the text.  The uncertainty is ranked according to DEFRA (2011), see Table 5 .   
 
 Table 5: Rankings used for uncertainty in the pest risk assessments (DEFRA 2011) . 
 
High • Scarce or no data available; evidence provided in unreliable 
reports; or  
• Very few  personal communications /observations ; and/or  
• Authors’ or experts’ conclusions vary considerably  
Moderate  • Some or only incomplete data available; evidence provided in small 
number of references; authors’ experts’ conclusions vary; or  
• Limited evidence from field observations; or  
• Solid and complete data available from other species  that can be 
extrapolated to the species being considered.  
Low • Solid and complete data available ; strong evidence in multiple 
references with most authors coming to the same conclusions; or  
• Considerable and consistent experience from field observations  
 
4.4 References for Chapter 4  
Defra (2011) Department for Environment, Food and Rural Affairs: Guideli nes for Environmental Risk 
Assessment and Management - Green Leaves III. Prepared by Defra and the Collaborative Centre of 
Excellence in Understanding and Managing Natural and Environmental Risks, Cranfield University, 
November 2011. 
https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/694
50/pb13670 -green -leaves -iii-1111071.pdf  
 
EFSA (2014) European Food Safety Authority: Guidance on the use of the weight  of evidence 
approach in scientific assessments. EFSA Journal , 15(8): 4971 . 
 
 
   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 23 5 Pest risk assessments: Fungi  
5.1 Colletotrichum abscissum  (post-bloom fruit drop)   
 
Colletotrichum  abscissum  causes brown and necrotic lesions on the petals of blossoms and early fruit 
drop in sweet orange, lemon, lime and other citrus varieties.  
 
Taxonomy  
Scientific name:  Colletotrichum abscissum  Pinho & O.L. Pereira (2015)  
Order/ family:  Glomerellales /Glomerellaceae   
Synonyms:  Colletotrichum acutatum  J.H. Simmons [post -bloom fruit drop strain]; Colletotrichum  
gloeosporioide s [slow-growing orange  strain ] 
Common names : Post -bloom fruit drop ; PFD   
Notes:  Colletotr ichum  abscissum  was only recently named and was historically referred to as the 
post-bloom fruit drop strain of C. acutatum  (Crous et al . 2015 ) and the slow-growing orange  strain of 
C. gloeosporioide s (Brown et al. 1996). Molecular comparisons showed that C. abscissum ITS and 
GAPDH  sequences had 100% identity with sequences in Genbank from the citrus post -bloom fruit 
drop strain designated as C. acutatum by Peres et al. (2008) (Crous et al. 2015). In this pest risk 
assessme nt, information from older references relating to the post -bloom fruit drop strain of 
C. acutatum  and the slow -growing orange strain of C. gloeosporioide s (e.g. Brown et al. 1996 , Peres 
et al. 2008, Lima et al. 2011, Dewdney 2015, Timmer and Peres 2015) ha s been understood to refer 
to what is now known as C. abscissum. In addition, approximately 20% of post -bloom fruit drop in 
Brazil is caused by C. gloeosporioide s (Lima et al. 2011; Silva et al. 2017) . This strain has not been 
assessed separately.  
 
5.1.1  Summary of conclusion s 
• Colletotrichum  abscissum  meets the criteria to be a quarantine pest for New Zealand.  
• The association of C. abscissum  with leafless budwood  of Citrus spp. is considered  weak  with 
low uncertainty.  
• The likelihood of C. abscissum  entering New Zealand in association with citrus nursery stock 
is considered  negligible , with low uncertainty.  
• Given that C. abscissum  is not expected to enter New Zealand associated with leafless Citrus  
budwood, further assessment is not required.  
• Colletotrichum  abscissum  may not need  to be considered for additional measures  on Citrus  
budwood .  
 
5.1.2  Hazard identification: regulatory status  
Given the arguments and evidence below, Colletotrichum  abscissum meets the 
criteria to be a quarantine pest for New Zealand . 
Criteria for being a regulated quarantine pest, relevant to this assessment are: the pest is not present 
in the pest risk assessment area (New Zealand) and is of potential importance (able to establish and 
cause harm28). 
 
Colletotrichum abscissum  is not known to be present in New Zealand:  
• Colletotrichum abscissum  is not recorded in either NZFungi 2 (2020) or PPIN (2020) . 
• Colle totrichum abscissum is only recently named and was historically  referred to as the slow - 
growing orange strain of C. gloeospor ioides  or post -bloom fruit drop strain of C. acutatum  
(Crous et al . 2015 ). Both C. acutatum and C. gloeosporioides are recorded as present in 
New Zealand  (NZFungi 2 2020; PPIN 2020).  
• NZFungi 2 (2020) and PPIN (2020) have collection records of C. acutatum from lemon, 
mandarin, Meyer lemon and tangelo, and C. gloeosporioides from orange, lemon and 
unspec ified c itrus from several different regions.  Where there is a record of the plant part that 
 
28 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.  24 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  fungal isolates were collected from, it is usually fruit, sometimes leaf or stem but none of the 
isolates identified as C. acutatum  or C. gloeosporioides  were colle cted from citrus flowers,  
blossoms or petals in New Zealand (NZFungi 2 2020; PPIN 2020).  
• The regulatory status of C. abscissum has not yet been determined (BRAD 2020; ONZPR 
2020).  
Colletotrichum abscissum  has the potential to establish and spread in New Zealand:  
• Hosts of C. abscissum  include most citrus species, but the disease is most severe on sweet 
oranges, lemons, and limes, and less severe on grapefruit and tangerines (Peres et al. 2005) . 
• Citrus species are widely grown in New Zealand , both commercia lly (27 ha; approximately 
9,000 commercial tree s) and by home gardeners (section 2.6). Therefore, suitable host plants 
are likely to be present to support establishm ent.   
• Colletotrichum abscissum  was only recently described in São Paulo , Brazil ( Crous et al . 
2015 ), but post-bloom  fruit drop, highly likely to be caused by C. abscissum,  is reported  in the 
tropical and subtropical areas of the Americas, from Florida (US A) in North America to 
Uruguay in South America ( Timmer  and Peres 2015).  Some parts of  its distribution (e.g. much 
of Uruguay , parts of Florida, Mexico and Brazil) represent areas with similar climatic 
conditions with New Zealan d indicated by a CMI (climate match index) ≥0.7, while much of its 
current distribution has CMI <0 7 indicating that the climate is not very similar to New Zealand 
(Phillips et al. 2018).  
• If C. abscissum  was to enter the New Zealand environment , there woul d be no barrier to 
spread because  C. abscissum  produces abundant c onidia  (asexual spores), which can be 
spread by water splash or windblown rain and pollinators, such as bees (Agostini and Timmer 
1994; Peres et al. 2005 ; Timmer and Peres 2015).   
 
Colletot richum abscissum  has the potential to have economic and sociocultural impacts by causing 
yield losses in citrus:  
• Post-bloom fruit drop caused by C. abscissum  is most severe on sweet orange ( C. sinensis ), 
lemon ( C. limon ), and Tahitian lime ( C. latifolia ), and less severe on grapefruit ( C. paradisi ) 
and tangerine ( C. reticulata ) (Peres et al. 2005).  Economic impacts of C. abscissum are likely 
to be limited to the citrus industry.  
• Colletotrichum abscissum  causes orange to reddish -brown necrotic lesions on the petals of 
blossoms, and early fruit drop in sweet orange, lemon and Tahitian lime ( Crous et al . 2015 ; 
Dewdney 2015 ; Timmer and Peres 2015 ). The fruitlets detach between the calyxes and young 
fruit, and the calyxes (or buttons) remain on the plant and d o not abscise as they normally 
would if no fruit is set (Dewdney 2015; Rodrigues Marques  et al. 2020).  
• Sweet orange, lemon, Tahitian lime and other citrus crops are commercially produced in 
New Zealand. In 2019 , export sales  of fresh citrus fruit were wort h NZ$12 million, and the 
value of domestic citrus sales was NZ$58.5 million (Plant and Food Research 2019 ). 
• Post-bloom fruit drop is considered a limiting factor for citrus production  (causing yield losses 
of approximately 90%)  in region s of Central America and Brazil  with predominantly tropical 
climates ( Rodrigues Marques  et al. 2020).  
• In Florida, impacts of the disease are more sporadic,  but the disease  can cause production 
losses in  seasons when conditions favour disease development (Dewdney 2015).  
• The fungi may cause impacts to home gardeners who grow Citrus spp., as lemons and other 
citrus are commonly grown in home gardens across New Zealand.  
• Since C. abscissum is mostly reporte d as a citrus pathogen and there are no native species of 
Citrus  (Allan Herbarium  2021), the likelihood of the pathogen causing  environmental impacts 
is considered very low. 
 
5.1.3  Hazard identification: commodity association  
Given the arguments and evidence below, t he association of C. abscissum  with 
leafless budwood of Citrus spp. is considered  weak, with low uncertainty.  
Colletotrichum abscissum  does not colonise stems or shoots of citrus plants:  
• Colletotrichum abscissum  is usually reported to sur vive between flowering periods as 
appressoria on surfaces of citrus leaves and persistent calyxes (Dewdney 2015; Waculicz -
Andrade  et al. 2017) and would not be expected to be on budwood.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 25 • In the next season, s ubstances from petals stimulate germination of a ppressoria to form 
conidia on the surface. These conidia are s plash -dispersed to flowers  in the same tree and 
reinitiate the cycle  (Timmer and Peres 2015) . Colletotrichum abscissum  does not reproduce in 
the absence of flowers and does not usually colonise other plant parts (Timmer and Peres 
2015). Colletotrichum abscissum  does not colonise leaves as an endophyte (Dewdney 2015; 
Nicoletti 2019 ; Waculicz -Andrade  et al. 2017).   
• However, orange leaves from nursery plants and budwood increase blocks at four comm ercial 
citrus farms in São Paolo, Brazil were contaminated with C. abscissum conidia, suggesting 
that the fungus may also be associated epiphytically on the surface of budwood, especially in 
areas where the fungus is widespread (Vargas Mun õz 2018).  
 
5.1.4  Risk assessment: entry  
Given the arguments and evidence below, the likelihood of  C. abscissum  entering 
New Zealand associated with leafless  budwood of Citrus spp. is  considered  
negligible, with low uncertainty.  
There is only a weak association between C. abscissum and citrus budwood (see above).  
Minimum requirements reduce the likelihood of entry to negligible:  
• Plants in areas with recent C. abscissum  outbreaks are likely to have persistent calyxes 
attached, a visible symptom of post -bloom fruit drop (Dewd ney 2015; Timmer and Peres 
2015) and are, therefore, highly unlikely to be used as a source of commercial budwood.  
• Budwood will not have leaves or persistent calyxes attached.  
• Conidia are highly unlikely to remain viable on the surface of budwood and buds  through pre -
import fungicide treatments, transit, grafting procedures and a growing season in post-entry 
quarantine . 
• Of the countries where C. abscissum  is reported to occur , citrus budwood has only ever been 
imported to New Zealand from the USA, the last  time in 2005 (Quancargo 2020). As this 
pathway is inactive and other potential pathways have never had trade, material is unlikely to 
be sourced from countries where post-bloom fruit drop is known to occur. However, trade on 
these pathways cannot be ruled  out in the future.  
There is low uncertainty in this conclusion. The symptoms described in the literature suggest that 
infected plants would usually be easily detectable, and recently infected plants would not be used to 
produce budwood.  
 
5.1.5  References  
Allan  Herbarium (20 21) Ngā Tipu o Aotearoa – New Zealand Plant Names Database. Landcare 
Research; NZ. https://nzflora.landcareresearch.co.nz. Accessed 4 August  2020.  
Agostini, JP; Timmer, L W (1994) Population dynamics and survival of strains of C. gloeosporoid es on 
Citrus in Florida. Phytopathology 84: 420–425 
https://www.apsnet.org/publications/phytopathology/backissues/Documents/1994Articles /Phyto84n04_
420.PDF   
BRAD (2020) Internal MPI database. Accessed 26  June 2020 
Brown, A E ; Sreenivasaprasad, S; Timmer, L W (1996) Molecular characterization of slow -growing 
orange and key lime anthracnose strains of Colletotrichum  from citrus as C. acutatum.  Phytopathology  
86(5):  523–527 
Crous, P  W; Wingfield, M  J; Guarro, J ; Hernández -Restrep o, M; Sutton, D  A; Acharya, K ; Barber, P  A; 
Boekhout, T ; et al.  (2015) Fungal Planet description sheets: 320 –370 – Colletotrichum abscissum  
Pinho & O.L. Pereira, sp. nov. Fungal Planet 357 . Persoonia  – Molecular Phylogeny and Evolution of 
Fungi 34: 236–237. 
https://www.ingentaconnect.com/search/article?option1=tka&value1=Colletotr ichum+abscissum&page
Size=10&index=1#   
Dewdney, M (2015) Postbloom fruit drop: spring is coming. Citrus Industry November 2015: 12 –15 
https://crec.ifas.ufl.edu/ extension/trade_journals/2015/2015_November_postbloom.pdf   26 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Lima, W G; Spósito, M B; Amorim, L; Gonçalves, F P; de Filho, P (2011) Colletotrichum 
gloeosporioides , a new causal agent of citrus post -bloom fruit drop. European Journal of Plant 
Pathology  131: 157–165 
MacKenzie , S J; Peres , N A; Barquero , M P; Arauz , L F; Timmer , L W (2009) Host range and genetic 
relatedness of Colletotrichum acutatum  isolates from fruit crops and leatherleaf fern in Florida. 
Phytopathology  99: 620–631  
 
Nicoletti, R (2019 ) Endophytic fungi of citrus plants.  Agriculture , 9: 247.   
doi:10.3390/agriculture9120247    
NZFungi 2 (2020) New Zealand Fungi and Bacteria. Manaaki Whenua – Landcare Research database. 
https://nzfungi2.landcareresearch.co.nz/default.aspx?NavControl=search&selected=NameSearch  
Accessed  4 August 2020 
ONZPR (2020) Official New Zealand Pes t Register. 
https://pierpestregister.mpi.govt.nz/PestsRegister/ImportCommodity/  Accessed: 26 June 2020  
Peres, N A; Timmer, L W; Adaskaveg, J E; Correll, J C (2005) Lifestyles of Colletotrichum acutatum. 
Plant Disease , 89(8):  784–796 https://apsjournals.apsnet.org/doi/pdfplus/10.10 94/PD -89-0784   
Peres, N  A; MacKenzie, S J ; Peever, T L ; Timmer, L W (2008 ) Postbloom fruit drop of citrus and Key 
lime anthracnose are caused by  distinct phylogenetic lineages of Colletotrichum acutatum . 
Phytopathology , 98: 345–352. https://apsjournals.apsnet.org/doi/pdfplus/10.1094/PHYTO -98-3-0345   
Phillips, C B; Kean, J M; Vink, C  J; Berry, J  A (2018) Utility of the CLIMEX ‘match climates regional ’ 
algorithm for pest risk analysis: An evaluation with non -native ants in New Zealand. Biological 
Invasions , 20(3): 777‒791. https://doi.org/10.1007/s10530 -017-1574 -2  
Plant and Food Research (2019) Fresh Facts: New Zealand Horticulture . The New Zealand Institute 
for Plant and Food Research Ltd, Auckland. https://www.freshfacts.co.nz/files/freshfacts -2019.pdf  
PPIN (2020) Internal MPI database. Accessed 30  November 2020  
Rodrigues Marques , J P; Bellato Spósito , M; Amorim , L; Sgarbiero Montanha , G; Silva Junior , G J; 
Pereira de Carvalho , H W; Appezzato -da-Glória, B (2020) Persistent calyxes in postbloom fruit drop: A 
microscopy and microanalysis perspective. Pathogens , 9(4): 251. Doi: 10.3390/pathogens9040251. 
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7238034/  https://www.mdpi.com/2076 -
0817/9/4/251/htm   
Silva, A  O; Savi, D  C; Gomes, F  B; Gos, F  M W R; Silva J unior, G J; Glienke, C  (2017 ) Identificatio n of 
Colletotrichum species associated with postbloom fruit drop in Brazil through GAPDH sequencing 
analysis and multiplex PCR. European Journal Plant Pathology , 147(4):  731–748. 
Timmer , L W; Peres , N A (2015 ) Where have all the flowers gone? Postbloom fru it drop of citrus in the 
Americas. Journal of Citrus Pathology , 2(1): iocv_journalcitruspathology_28302  
Vargas Munõz, V N (2018) Detection and quantification of Colletotrichum abscissum  from leaves of 
budwood increase block and citrus nursery plants by real time PCR. Master ’s dissertation . Escola 
Superior de Agricultura Luiz de Queiroz, University of São Paulo, Piracicaba. 
doi:10.11606/D.11.2019.tde –22112018 –154045.  
Quancargo (2020) Inte rnal MPI database Accessed: 21  July 2020 
Waculicz -Andrade, C  E; Savi, D  C; Bini, A  P; Adamoski, D; Goulin, E H; Silva Jr, G J; Massola Jr, N S; 
Terasawa, L G; Kava, V; Glienke, C (2017)  Colletotrichum gloeosporioides  sensu stricto: an 
endophytic species or  citrus pathogen in Brazil? Australasian Plant Pathology , 46: 191–203. 
https://doi.org/10.1007/s13313 -017-0476 -1  
 
   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 27 5.2 Colletotrichum limetticola  (Key lime anthracnose ) 
 
Colletotrichum limetticola  is the fungus that  causes key lime anthracnose disease. Symptoms include 
necrotic lesions on leaves, fruits, twigs, flowers, premature fruit drop and blight of entire shoots of key 
lime ( Citrus aurantiifolia ). 
 
Taxonomy  
Scientific name: Colleto trichum limetticola (R.E. Clausen) Damm, P.F. Cannon & Crous (2012)  
Order/ family : Glomerales/Glomeraceae  
Synonyms:  Colletotrichum acutatum  J.H. Simmons [lime anthracnose strain or lime withertip strain]; 
Gloeosporium limetticola  R. E. Clausen 1912; Gloeosporium fructigenum f. limetticola  (R.E. Clausen) 
G.J.M. Gorter (1962)  
Common names: Key lime anthracnose; lime anthracnose; lime withertip (Damm et al. 2012)  
Notes:  In the past , C. limetticola was usually described as the key lim e anthracnose strain of 
C. acutatum or C. gloeosporioides , and sometimes classified as G. limetticola (Damm et al. 2012).  
Gloeosporium limetticola was reported as the cause of  withertip disease of C. aurantiifolia in Cuba.  
However, a recent phylogenetic st udy found that the withertip disease of C. aurantiifolia  was 
apparently identical to key lime anthracnose (KLA), a specific disease of leaves, twigs, flowers and 
fruits of key lime, and reclassified both as C. limetticola  (Damm et al. 2012).  In this pest risk 
assessment , information from references relating to the lime anthracnose strain of C. acutatum  (e.g. 
Peres et al. 2005; 2008; MacKenzie et al. 2009; Serrano et al. 2010; Ruiz et al. 2014) is understood as 
referring  to what we now call  C. limetticola.  
 
5.2.1  Summary of conclusions  
• Colletotrichum limetticola  meets the criteria to be a quarantine pest for New Zealand.  
• The association of C. limetticola  with leafless Citrus  budwood is considered  high, with low 
uncertainty.  
• The likelihood of C. limetticola  entering New Zealand in association with leafless Citrus  
budwood  is considered  negligible, with low uncertainty.  
• Given that C. limetticola  is not expected to enter New Zealand associated with leafless  Citrus  
budwood, furthe r assessment is not required.  
• Colletotrichum limetticola  may not be considered for additional measures  on citrus budwood . 
 
5.2.2  Hazard identification: regulatory status  
Given the arguments and evidence below, Colletotrichum limetticola meets the 
criteria to be a quarantine pest for New Zealand . 
Criteria for being a regulated quarantine pest, relevant to this assessment are: the pest is not present 
in the pest risk assessment area (New Zealand) and is of potenti al importance (able to establish and 
cause harm29). 
 
Colletotrichum limetticola is not known to be present in New Zealand:  
• Colletotrichum limetticola is not recorded in either NZFungi 2 (2020) or PPIN (2020)  
• In the past , C. limetticola was classified as Gloeosporium limetticola  or the lime anthracnose 
strain of C. acutatum or C. gloeosporioides. Both C. acutatum and C. gloeosporioides are 
recorded as present in NZ (NZFungi 2 2020). NZFungi 2 (2020) records G. limetticola as a 
synonym of C. acutatum .  
• NZFungi 2 (2020) and PPIN (2020) have collection records of C. acutatum from lemon, 
mandarin, Meyer lemon and tangelo, and C. gloeosporioides from orange, lemon and 
unspecified citrus from several different regions. There are n o collections of Gloeosporium 
limetticola in New Zealand  recorded in either database , and there is  no record of any  
Colletotrichum  species collected  from C. aurantiifolia .  
• The regulatory status of C. limetticola has not yet been determined (BRAD 2020; ONZ PR 
2020).  
 
 
29 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.  28 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Colletotrichum limetticola has the potential to establish and spread in New Zealand:  
• Colletotrichum limetticola is mainly reported in the Americas, including the United States 
(Florida, Texas), Brazil (São Paulo), Mexico, Belize, Costa Rica, Cuba and the Dominican 
Republic (Peres et al. 2008; Damm et al. 2012; Ruiz et al. 2014). Some areas where 
C. limetticola is found have a similar climate to the whole of New Zea land, based on a climate 
match index ≥ 0.7 (Phillips et al. 2018) . 
• Key or Mexican lime ( Citrus aurantiifolia ) is the major host of C. limetticola  (Peres et al. 2008)  
and is grown in New Zealand both commercially and occasionally by home gardeners (section 
2.6). 
• Therefore, suitable host plants in suitable environmental conditions are likely to be present to 
support establishment, at least in some parts of New Zealand.  
• Colletotrichum limetticola produces conidia (asexual spores) on susceptible tissues ( Peres et 
al. 2005). Conidia are spread by rain -splash to nearby hosts and can be dispersed by 
windblown rain over greater distances. Therefore, if the fungus enter ed the N ew Zealand 
environment , in an area where key lime plants were grown, there would be no barrier to 
spread. However, potential spread of C. limetticola is likely to be limited by host availability , 
since  key lime is not commonly grown in many parts of New Ze aland.  
Colletotrichum limetticola has the potential to have economic and sociocultural consequences by 
causing symptoms in key lime and, potentially, sweet orange and apple:  
• The reported impacts of C. limetticola are limited to C. aurantiifolia (Peres et al. 2005; 2008).  
• Limes are commercially grown in New Zealand for the domestic market, with a domestic sales 
value of NZ$2 million ( Plant and Food Research 2019 ). However, the information on sales 
value does not differentiate between key lime and Tahitian l ime ( C. latifolia ). Given that 
Tahitian lime ( C. latifolia ) is not a susceptible host, economic impacts of C. limetticola would 
be limited to an unknown proportion of the New Zealand lime crop.  
• Key limes are occasionally grown in home gardens in New Zealand.  
• Colletotrichum limetticola causes severe anthracnose symptoms on twigs, shoots, leaves and 
flowers of key lime plants and premature fruit drop ( Figure 6) (Chen  et al. 2005; Serrano et al. 
2010). It causes necrosis in key lime plants, with symptoms ranging from small lesions to 
blight of entire shoots and inflorescences (Peres et al. 2005).  
• Lesions on leaves are circular to oval brown spots, and lesions on mature  leaves may have a 
shot hole appearance (i.e. a hole in the centre of the lesion) (Serrano  et al. 2010; Ruiz et al. 
2014).  
• Twigs show severe blight, wilt, and dieback symptoms (Serrano  et al. 2010; Ruiz et al. 2014).  
• In flowers, water -soaked lesions form on the petals (Chen et al. 2005; Ruiz et al. 2014) . 
• Infection of young fruit usually results in premature fruit drop (similar to that caused by 
C. abscissum, see section 5.1), leaving persistent calyxes on the plant (Chen et al. 2005; 
Serrano et al. 2010; Ruiz et al. 2014) . Late fruit infections produce lesions that are often large 
and deep, and the fruit becomes misshapen (Serrano et al. 2010).   
 
  
Figure 6: Key lime anthracnose symptoms on fruit twigs and shoots (Serrano et al. 2010).  
 
 
 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 29 • In artificial inoculation studies, C. limetticola caused lesions on blossoms and postbloom fruit 
drop symptoms in sweet orange ( C. sinensis ) (Peres et al. 2005; 2008; MacKenzie et al. 
2009) . Consequently, sweet orange is sometimes reported as a host . However, although key 
lime anthracnose was a severe problem in key lime production in Western Me xico, post-bloom 
fruit drop was not observ ed on oranges or Tahiti an limes grown in the area  (Peres et al. 2008).  
Furthermore,  searches of the literature  using ‘ Colletotrichum ’ and ‘citrus’  (Google Scholar, 
CAB Abstracts) found no primary records of C. lime tticola  or the key lime anthracnose strain of 
C. acutatum  infecting stems or shoots of orange in natural infections.  
• Colletotrichum limetticola was one of the Colletotrichum species recently isolated from lesions 
on apple leaves and flowers in Paraná and Rio Grande do Sul, Brazil, and the isolates caused 
leaf spot symptoms in pathogenicity tests (Moreira et al. 2019). Nevertheless, C. limetticola 
was much less frequently isola ted from apples than other Colletotrichum species, and it is 
uncertain whether it contributed to disease symptoms in natural infection.  
 
5.2.3  Hazard identification: commodity association  
Given the arguments and evidence below, the association of C. limetticola  with 
leafless C. aurantiifolia  budwood is considered  strong with low uncertainty, but 
C. limetticola is highly unlikely to be associated with budwood of other citrus species . 
Colletotrichum limetticola can be present in the stems of infected key lime plan ts:  
• Symptoms of key lime anthracnose include necrotic lesions on leaves, fruits, twigs  and 
flowers, and blight of entire shoots (Peres et al. 2008).  
• All young tissues of key lime are susceptible and severely attacked by C. limetticola (as 
C. acutatum ) (Peres et al. 2005).  
5.2.4  Risk assessment: entry  
Given the arguments and evidence below, the likelihood of C. limetticola entering 
New Zealand associated with leafless C. aurantiifolia budwood is considered 
negligible, with low uncertainty.  
Colletotri chum limetticola has a strong association with leafless C. aurantiifolia budwood.  
• The fungus infects all young key lime tissues, including twigs and shoots (see above).  
However, C. aurantiifolia plants infected with C. limetticola  are unlikely to be impo rted into New 
Zealand  
• Key lime  plants with visible necrosis caused by C. limetticola  are highly unlikely to be used to 
produce budwood for export to New Zealand.  
• Of the countries where the disease is reported to occur, citrus budwood has only ever been 
imported to New Zealand from the USA, the last time in 2005 (Quancargo 2020). As this 
pathway is inactive and other potential pathways have never had trade, material is unlikely to 
be sourced from countries where lime anthracnose is known to occur. However, t rade on 
these pathways cannot be ruled out in the future.   
Minimum requirements reduce the likelihood of entry to negligible.  
• Colletotrichum limetticola will produce visibly detectable symptoms within one growing 
season. Symptoms of C. limetticola  develop rapidly on young key lime tissues (Peres et 
al. 2008). In pathogenicity tests, all shoots of key lime seedlings or rooted cuttings 
sprayed with conidial suspensions of C. limetticola developed necrotic lesions within 3 –6 
days (e.g. Agos tini et al. 1992; Brown et al. 1996; Peres et al. 2008)  
• Therefore, plants infected with C. limetticola  are highly unlikely to be used as a source of 
commercial budwood , because disease symptoms are likely to be obvious , and the 
fungus will be detected by visual inspection.  
• Any dried conidia  (spores)  would be highly unlikely to remain viable on the surface of 
budwood and buds through pre -import fungicide treatments and grafting procedures. If 
conidia did survive, symptoms would develop rapidly in post-entry quarantine , once  the 
conidia were wetted and dispersed to young actively growing host tissues.  30 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  There is low uncertainty in this conclusion. The symptoms described in the literature suggest that 
heavily infected material would be easily detectable and would not be used to produce budwood, 
or that symptoms of C. limetticola would develop rapidly and b e noticed at the border or in post-
entry quarantine . 
  
Furthermore, if C. limetticola  were to produce symptoms in post -entry quarantine, any spores would 
be contained in level 3 A:  
• Colletotrichum limetticola is spread via splash -dispersed conidia (Peres et al. 2008) , and there 
is no evidence for spread by airborne ascospores (Peres et al. 2005).Therefore, it is highly 
likely that C. limetticola would be contained in level 3 post-entry quarantine , because there are 
measures in place to contain water borne pathogens (MPI 2019).  
• Other measures in place within level 3 A glasshouses (including protective clothing and hand 
washing) (MPI 2019) would reduce the likelihood of viable conidia leaving a glasshouse and 
then transferring to a suitable host to a ver y low level.   
Given that C.  limetticola  is not expected to enter New Zealand associated with leafless citrus 
budwood, further assessment is not required.  
 
5.2.5  References  
Agostini, J P; Timmer, L W; Mitchell, D J (1992) Morphological and pathological characte ristics of 
Colletotrichum gloeosporoides  from Citrus. Phytopathology  82: 1377 –1382 
https://www.apsnet.org/publications/phytopathology/backissues/Documents/1992Articles/Phyto82n11_
1377.PDF   
ONZPR (2020) Official New Zealand Pest Register. 
https://pierpestr egister.mpi.govt.nz/PestsRegister/ImportCommodity/  Accessed: 26 June 2020  
BRAD (2020) Internal MPI database. Accessed 26  June 2020. 
Brown, A E; Sreenivasaprasad, S; Timmer, L W (1996) Molecular characterization of slow -growing 
orange and key lime anthracno se strains of Colletotrichum  from citrus as C. acutatum.  
Phytopathology , 86(5):  523–527. 
Chen, H‐Q; Cao, L Dekkers, K L; Rollins, J A; Ko, N J; Timmer, L W; Chung, K ‐R (2005) A gene with 
domains related to transcription regu lation is required for pathogeni city in Colletotrichum acutatum  
causing key lime anthracnose. Molecular Plant Pathology , 6: 513–525. https://doi.org/10.1111/j.1364 -
3703.2005.00300.x   
Damm, U; Cannon, P F; Woudenberg, J H C; Crous, P W (2012) The Colletotrichum acutatum  species 
complex. Studies in Mycology , 73: 37–113. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3458 416/  
MacKenzie, S J; Peres, N A; Barquero, M P; Arauz, L F; Timmer, L W (2009). Host range and genetic 
relatedness of Colletotrichum acutatum  isolates from fruit crops and leatherleaf fern in Florida. 
Phytopathology , 99: 620–631. https://apsjournals.apsnet.org/doi/pdfplus/10.1094/PHYTO -99-5-0620    
Moreira, R R; Peres, N A; May De Mio, L L (2019) Colletotrichum acutatum and C. gloeosporoides  
species complexes associated with apple in Brazil. Plant Disease , 103: 268–275. 
https://apsjournals.apsnet.org/doi/pdf/10.1094/PDIS -07-18-1187 -RE  
MPI (2019) Ministry for Pr imary Industries Standard PEQ.STD Facility Standard: Post Entry 
Quarantine for Plants . https://www.mpi.govt.nz/dmsdocument/11368 -Post-Entry -Quara ntine -for-
Plants -Facilities -Standard  Accessed August 2020.  
 
NZFungi 2 (2020) New Zealand Fungi and Bacteria. Manaaki Whenua -Landcare Research database. 
https://nzfungi2.landcareresearch.co.nz/  Accessed 4  August 20 20. 
Peres, N A; Timmer, L W; Adaskaveg, J E; Correll, J C (2005) Lifestyles of Colletotrichum acutatum. 
Plant Disease , 89(8):  784–796 https://apsjournals.apsne t.org/doi/pdfplus/10.1094/PD -89-0784    
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 31 Peres, N A; MacKenzie, S J; Peever, T L; Timmer, L W (2008) Postbloom fruit drop of citrus and key 
lime anthracnose are caused by distinct phylogenetic lineages of Colletotrichum acutatum . 
Phytopathology , 98: 345–352. https://apsjournals.apsnet.org/doi/pdfplus/10.1094/PHYTO -98-3-0345   
Phillips, C B; Kean, J M; Vink, C  J; Berry, J (2018) Utility of the CLIMEX ‘match climates regional ’ 
algorithm for pest risk analysis: An evaluation with non -native ants in New Zealand. Biological 
Invasions , 20(3): 777‒791. https://doi.org/10.1007/s10530 -017-1574 -2  
Plant & Food Research (2019) Fresh Facts: New Zealand Horticulture . The New Zealand Institute for 
Plant and Food Research Ltd, Auckland.  https ://www.freshfacts.co.nz/files/freshfacts -2019.pdf   
PPIN (2020) Internal MPI database. Accessed 26  June 2020. 
Quancargo (2020) Internal MPI database . Accessed 21  July 2020. 
Ruiz, A; Parra C C, da Graça, J V; Salas, B; Malik, N S A; Kunta, M (2014) Molecular characterization 
and pathogenicity assays of Colletotrichum acutatum , causal agent for lime anthracnose in Texas. 
Revista Mexicana de Fitopatología , 32: 52–61. 
Serrano, D ; Serrano, E ; Dewdney, M ; Southwick, C (2010) Citrus Diseases. USDA/APHIS/PPQ 
Center for Plant Health Science and Technology. Accessed August 2020 
 
  32 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  5.3 Diaporthe  spp. associated with citrus: Diaporthe baccae , 
D. hongkongensis  and D. novem   
 
Diaporthe baccae, D. hongkongensis  and D. novem are fungal pathogens that are reported to cause 
stem -end rot of fruit, lesions on leaves, twig and branch cankers, and dieback in citrus, grapevine or 
other plants. Diaporthe (Phomopsis ) species  often have broad host r anges and  broad geographical 
distributions and are frequently reported as pathogens, endophytes or saprobes  in plants . They can be 
opportunistic pathogens that remain latent in plants for long periods but cause disease in older plants, 
during periods of en vironmental stress or when plants are injured or weakened by other pathogens.  
 
Taxonomy  
Scientific name: Diaporthe baccae  L. Lombard, Polizzi & Crous (2014)  
Synonyms:  None in Mycobank, Species Fungorum or Farr and Rossman (2020)  
Order/ family: Diaporthales /Diaporthaceae  
Notes: Diaporthe baccae is closely related to D. foeniculina  (which is present in New Zealand) , and 
some authors consider them to be the same species . Hyde et al. (201 7) suggest that D. baccae  
should be synonymised with D. rhusic ola (or D. rhoicola ). Farr and Rossman list D. rhusicola  as a 
synonym of D. foeniculina . Species Fungorum  (2020) and Mycobank (2020) record D. rhoicola  Crous 
(2011)  as the current name of D. rhusicola  but do not record it as a synonym of D. foeniculina . 
NZFungi2 (2020) and PPIN (2020) record D. foeniculina  as present in  New Zealand  but ha ve no 
record of these other species. Farr and Rossman do not record D. baccae  and D. foeniculina  as 
synonyms.  For the purposes of this assessment, D. baccae is considered a separate species.  
 
Scientific name: Diaporthe hongkongensis  R. R. Gomes, C. Glienke & Crous (2013)  
Synonyms:  Diaporthe lithocarpus  Y. H. Gao, W. Sun & L. Cai 2014  
Order/Family: Diaporthales /Diaporthaceae  
 
Scientific name: Diaporthe novem  J. M. Santos, Vrandečić & A.  J. L. Phillips (2011)  
Synonyms: Diaporthe pseudolongicolla  Petrović (2012);  Diaporthe pseudolongicolla  K. Petrović, L. 
Riccioni & M. Vidić  (2018)  
Order/ family: Diaporthales /Diaporthaceae  
 
Genera l information about Diaporthe  spp. 
Diaporthe is a genus of fungi  that often have broad host ranges and  geographical distributions and 
can be associated with plants  as pathogens, endophytes or saprobes  (Gomes et al. 2013). Some 
plant associated Diaporthe species are also reported as  pathogens of humans and other mammals  
(Gomes et al. 2013).  Diaporthe  spp. are known to cause root and fruit rots, dieback, cankers, leaf 
spots, blights, decay and wilt  in plant hosts (Gomes et al. 2013). Historically, new Diaporthe  species 
were identified based on host association (e.g. D. citri  on Citrus , D. ampelina on grapes), which led to 
numerous species names ( Dissanayake  et al. 2017). This means that Diaporthe pathogen s of Citrus  
are frequent ly identified as D. citri  or its asexual state Phomopsis citri in taxonomic and plant 
pathological studies and regional checklists  (Udayanga et al. 2014). Other Diaporthe  or Phomopsis  
species described from citrus such as D. citrincol a, P. californica , P. caribaea , P. cytosporella and 
D. medusaea  were also considered synonyms of D. citri  by some authors. Canker, gummosis and 
melanose symptoms in citrus from Japan and China were sometim es attributed to D. meduseae  
(current name D. rudis ) and P. cytosporella  (Huang et al. 2013; Yamoto 1976; Zhang et al. 2008 ). 
Recent phylogenetic studies are identifying an increasing number of Diaporthe species from citrus 
plants as endophytes or isolated  from disease lesions (e.g. Guarnaccia and Crous 2017 ; Huang et al. 
2013  and 2015). Many of these species are not host -specific and can cause disease in other plants. A 
single species can be found on more than one host , and conversely , several Diapo rthe species can be 
found on a single host ( Dissanayake  et al. 2017).  
The biology and epidemiology of cankers on trunks, branches and twigs, melanose  and fruit rots on 
Citrus  have been described (although attributed to D. citri or D. medusaea ). Searches  (Goog le 
Scholar, CAB Abstracts, August 2020)  with the species names and ‘citrus’ as search terms found very 
little specific information about the biology of the recent ly described citrus -associated species 
D. baccae , D. hongkongensis and D. novem , so older info rmation about D. citri, D. medusaea  and 
other Diaporthe species has been used as a surrogate .  
 
 
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 33 5.3.1  Summary of conclusion s 
• The association of Diaporthe spp. with Citrus spp. budwood is considered strong with low 
uncertainty.  
• The likelihood of D. hongkongensis entering associated with citrus nursery stock is  considered 
high, with moderate uncertainty.  
• The likelihood of D. baccae or D. novem entering associated with citrus nursery stock is 
considered very low  to moderate  with moderate  uncertainty.  
• The likelihood of D. baccae, D. hongkongensis or D. novem  establishing is considered  high, 
with low uncertainty.  
• The introduction of  D. baccae, D. hongkongensis or D. novem  is considered likely to cause 
moderate economic impacts for New Zealand , with moderate  uncertainty.  
• The introduction of any one of any of these  Diaporthe spp. associated with  citrus  is considered 
likely  to cause  low socio -cultural impacts in New Zealand , with moderate uncertainty.  
• The introduction of any one of th ese Diaporthe spp. associated with  Citrus is considered  likely 
to cause  very low to moderate  environmental impacts in New Zealand , with moderate  
uncertainty.  
• The introduction of any one of these Diaporthe spp. associated with  Citrus is considered likely 
to cause  very low human health impacts in New Zealand , with moderate uncertainty.  
• Diaporthe baccae, D. hongkongensis and D. novem may be considered for additional 
measures on citrus budwood.  
 
The moderate uncertainty in many of these conclusions is because D. baccae, D. hongkongensis and 
D. novem  are emerging pathogens, each with only a few published reports.  
• In the past , Diaporthe  species affecting each host were often grouped together, with a species 
and disease name related to that host (e.g. D. citri ). However, many of the Diaporthe  species 
recently found in citrus, even those that have only been reported as symptomless endophytes 
in citrus, apparently cause disease symptoms in a range of o ther hosts.  
• In pathogenicity tests, D. baccae, D. hongkongensis and D. novem  can cause disease 
symptoms in many of their known hosts. However, such tests often involve inoculating the 
plant with high concentrations of spores or mycelium. It is uncertain to  what extent these 
Diaporthe species cause disease under natural infection conditions.   
• Disease symptoms attributed to Diaporthe  are more frequent and severe in older plants, 
suggesting that they may be opportunistic rather than primary pathogens.  Diaport he species 
can have long latent periods as asymptomatic endophytes, but they can sporadically cause 
severe outbreaks of disease, particularly when plants are injured or stressed by environmental 
conditions or other pathogens.  
• Diaporthe baccae, D. hongkong ensis and D. novem have been isolated from disease lesions 
in natural infections of plant hosts. However, Diaporthe  species have been reported in 
coinfection with each other and other plant pathogens (e.g. Pintos et al. 2018). Therefore, i t is 
not always c lear how often each of these was the only fungal species isolated from a 
particular lesion and whether D. baccae, D. hongkongensis or D. novem caused the disease 
symptoms. It is possible that these Diaporthe species were secondary invaders of the disease 
lesions or were present in the plant as endophytes with no role in disease.  
• New hosts of D. baccae, D. hongkongensis and D. novem  are likely to be reported in the 
future, given there have been several recent reports of new host associations and 
economically  significant diseases caused by these species.  
 
5.3.2  Hazard identification: regulatory status  
Diaporthe baccae , D. hongkongensis and D. novem  meet the criteria to be 
quarantine pests for New Zealand . 
Criteria for being a regulated quarantine pest, relevant to this assessment are: the pest is not present 
in the pest risk assessment area (New Zealand) and is of potential importance (able to establish and 
cause harm30). 
 
30 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.  34 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand   
These  Diaporthe species  are not known to be present in New Zealand:  
• Diaporthe bacc ae, D. hongkongensis and D. novem31 are not known to occur in New Zealand. 
Diaporthe hongkongensis is recorded as absent and D. baccae, and D. novem  are not 
recorded in NZFungi 2 (2020). None of these species are  recorded in PPIN (2020).  
• Diaporthe baccae, D. hongkongensis and D. novem do not have a quarantine status recorded 
in BRAD or ONZPR . 
Diaporthe baccae, D. hongkongensis and D. novem  have the potential to establish and spread in New 
Zealand:  
• These Diaporthe species have been reported from areas that have a very similar climate to 
the whole of New Zealand ( climate match index with New Zealand of 0.7‒0.9) including Italy, 
France, Spain, California and parts of China, eastern Australia and Turkey (Phillips et al. 
2018). Diaporthe baccae is reported from Croatia, France, Italy and Spain (Lombard et al. 
2014 ; Guarnaccia and Crous 2017 ; Guarnaccia et al. 2018),  D. hongkongensis is reported 
from China and Turkey (Huang et al. 2015 ; Erper et al. 2017), and  D. novem is reported from 
Italy, Iran, e astern Australia, USA (northern California), South Africa, France and Spain (Alavi 
and Faraki 2016; Guarnaccia and Crous 2017; Lawrence et al. 2015, Lesuthu et al. 2019; 
Pintos et al. 2018; Thompson et al. 2018).  
• Suitable hosts are widespread in New Zealan d. For example, all these Diaporthe species have 
been reported from citrus and grapevines ( Vitis vinifera ) (Dissanayake et al. 2015; Guarnaccia 
and Crous 2017; Guarnaccia et al. 2018; Huang et al. 2015; Pintos et al. 2018; Udayanga et 
al. 2014 ). Citrus and  grapes are commonly grown in domestic gardens and are grown 
commercially in New Zealand.  
Diaporthe baccae, D. hongkongensis and D. novem  have the potential to have economic and 
sociocultural impacts by causing disease symptoms on citrus and other plants:  
• Diaporthe baccae and D. novem  have been described as causing disease symptoms in citrus 
plants, such as leaf scabs, branch cankers and twig dieback (Guarnaccia and Crous 2017). 
Citrus is an important commercial crop for New Zealand and is commonly grown by  home 
gardeners (section 2.6.2 ).  
• Diaporthe baccae, D. hongkongensis  and D. novem  have been isolated from grapevines ( Vitis 
vinifera ) with cankers and dieback symptoms (Dissanayake et al. 2015; Guarnaccia et al. 
2018; Lesuthu et al. 2019; Lawrence et al. 2 015). Wine represents New Zealand’s second 
largest horticultural export, with a value of NZ$1.8 billion ( Plant and Food Research 2019 ). 
• Diaporthe hongkongensis has been reported to cause rot in kiwifruit, both pre -harvest  and 
post-harvest (Li et al. 2016; Erper et al. 2017). In 2019, kiwifruit exports from New Zealand 
earned more than NZ$2.3 billion ( Plant and Food Research  2019).  
• Diaporthe hongkongensis and D. novem have been described as causing disease symptoms 
such as leaf spots and dieback in a broad r ange of hosts, including ornamental and amenity 
species such as camellia (Gao et al. 2016), sunflower and hydrangea (Thompson et al. 2018). 
These species have the potential for socio -cultural impacts on home gardeners and on public 
parks and amenity plantings.  
5.3.3  Hazard identification: commodity association  
Given the arguments and evidence below, t he association of D. baccae, 
D. hongkongensis  and D. novem  with leafless  Citrus budwood is considered strong , 
with low uncertainty . 
These Diaporthe species have all been reported from twigs and branches of citrus plants:  
• Diaporthe hongkongensis  has been i solated from asymptomatic twigs of Citrus reticulata, C. 
unshiu, C. grandis and C. sinensis , as well as from citrus scab o n leaves of C. reticulata  and C 
unshiu  (Huang et al.  2015) .  
 
31 Although Udayanga et al. (2015) inc luded a D. novem sample  from carrot in New Zealand in their taxonomy, there is no 
record of Diaporthe  or Phomopsis on carrots in NZFungi 2 or PPIN. There are no collection details for the fungal sample used in 
the study. Currently, the status of D. novem in New Zealand is absent (Wellcome Ho, Plant Health and Environment Laboratory, 
MPI, pers. comm., 10  August 2020).  
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 35 • Diaporthe  baccae and D. novem  were i solated from symptomatic twigs, branches and trunks 
of citrus (Guarnaccia and Crous 2017).  
• There are only a few reports of D. baccae, D. hongkongensis and D. novem associated with 
citrus plants , and only D. hongkongensis  has been described from citrus plants without 
disease symptoms. Literature searches in CAB abstracts and Google Scholar (Augus t 2020) 
using the species name and ‘citrus’ as search terms found only the records cited in Table  6 and 
references to these studies in taxonomic studies but no specific evidence for asymptomatic  
infections of citrus with D. baccae or D. novem . However,  D. novem has been isolated from 
healthy grapevines ( Pintos et al. 2018) , so it can infect plants asymptomatically, at least in 
some hosts . 
 
5.3.4  Risk assessment: entry  
Diaporthe baccae, D. hongkongensis and D. novem have  a strong association with Citrus budwood, 
as they have been isolated from citrus twigs and branches (see Hazard identification: commodity 
association).  
Diaporthe species are more likely to show symptoms in old, poorly managed or stressed plants  (Gao 
2006;  Zhang et al. 2008 ; Aguilera -Cogley and Vicent 2019) , but such plants are extremely unlikely to 
be used to produce budwood material for export to New Zealand . Trees harbouring endophytic 
Diaporthe fungi may show no symptoms at all . Therefore, there is the potential for infect ed 
asymptomatic material to be used for propagation.   
 
Given the arguments and evidence below, t he likelihood of D. hongkongensis  
entering New Zealand associated with citrus budwood is high, with moderate 
unce rtainty . 
• In a study of endophytic Diaporthe in citrus in China, D. hongkongensis  was i solated from 
asymptomatic twigs of Citrus reticulata and C. sinensis in Jiangxi , C unshiu in Zhejiang  and 
C. grandis in Fujian , as well as two isolates from citrus scab o n leaves of C. reticulata and 
C. unshiu in Fujian  (Huang et al . 2015) . This study isolated 44 endophytic Diaporthe strains in 
twigs and branches of citrus and Fortunella plants, of which five isolates from asymptomatic 
twigs (1 –2 years old) were identified as D. hong kongensis.   
• Diaporth e hongkongensis  has only been reported from China and Turkey , and there is no 
record of Citrus nursery stock being imported from these coun tries (Quancargo 2020) , 
although trade on these pathways cannot be ruled out in future.  
• There is moderate uncertainty in this conclusion, since the evidence for an asymptomatic 
association is based on a single study and comparison with other species in the  genus. 
Nevertheless, this study sampled healthy twigs from only 30 citrus trees (five trees randomly 
selected from each of six study sites). Diaporthe  hongkongensis  was isolated from four twig 
samples, suggesting that asymptomatic D. hongkongensis  infecti on of citrus in China is not 
uncommon. Furthermore, the low likelihood of entry is based on the current recorded 
distribution of D. hongkongensis, and, given the possibility of latent infections, the pathogen 
may be more widespread than is currently report ed.  
Given the arguments and evidence below, t he likelihood of D. baccae  or D. novem  
entering New Zealand associated with citrus budwood is very low to moderate , with 
moderate uncertainty . 
• There is no specific information about whether D. baccae and D. novem  can be latent and 
asymptomatic in citrus plants, because they have only been reported in studies of plants  with 
disease symptoms  (Alavi and Faraki 2016; Guarnaccia and Crous 2017) .  
• Diaporthe baccae  was isolated in a survey of orange, lemon, grapefruit and mandarin plants 
with twig dieback and branch and trunk cankers  and was one of the more frequent Diaporthe 
species found in Italy ( Guarnaccia and Crous 2017 ).  
• Diaporthe novem  was isolat ed from twigs of C. japonica and C. aurantiifolia  with dieback 
symptoms in Italy in the same survey (Guarnaccia and Crous 2017) and from citrange 
rootstock (cross between C. sinensis  and P. trifoliata ) in Iraq,  with symptoms including rot, 
discoloration of  wood, yellowing and decline  (Alavi and Faraki 2016).  36 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • The very low likelihood estimates for D. baccae and D. novem entering  New Zealand  
associated with citrus budwood  is based on the assumption that systemic symptomless 
infections with these fungi can occur in citrus but are rare, especially  in young healthy plants . 
Diaporthe  species have been reported as latent pathogens in other species, sometimes at 
high rates and in coinfection wit h other fungal pathogens. In a survey of 150 young grapevine 
plants from two commercial  nurseries in Spain and one in Franc e, 93% of the plants were 
infected by at least one grapevine trunk pathogen  (Pintos et al. 2018 ). Most vines were 
infect ed with more than one pathogen  per plant (40% were infected by two, 31% by three and 
9% by four grapevine trunk pathogens)  (Pintos et al. 2018 ). Although these plants appeared to 
be in good condition, Diaporthe including D. novem , as well as other latent pathogens (e.g . 
Botryosphaeriaceae, Nectriaceae , petri disease fungi) , were present ( Pintos et al. 2018 ). The 
Diaporthe  species  were usually  associated with the rootstock or graft union , but a small 
number were isolated from the scion  (Pintos et al. 2018 ), although infe ction of the scion may 
have occurred after grafting . 
• However, t here is moderate uncertainty around th is conclusion , because the frequency of 
association of these Diaporthe species with citrus is unknown, and there are no reports of 
D. baccae and D. novem  from citrus twigs or branches without visible disease lesions . As 
previously mentioned, these Diaporthe species were only recently described , and the literature  
about them  is currently limited  to a small number of studies. Furthermore, m ost research has 
focused on diseased plants . Nevertheless, some recent surveys have focussed on fungal 
endophytes  in citrus or other species (e.g. Huang et al. 2015; Gao et al. 2016; Pintos et  al. 
2018). These studies demonstrate that Diaporthe  spp. can be  associated with plants that 
appear healthy , but do not provide specific evidence relating to latent asymptomatic 
association of D. baccae  or D. novem with citrus.  
The minimum requirements do  not significantly reduce the likelihood of entry because  Diaporthe  spp. 
have been reported from asymptomatic plants and may not develop visible symptoms within one 
growing season:   
• Visual inspection of budwood and the mother plants is likely to detect sym ptomatic material, 
but not asymptomatic infection.   
• Symptoms of Diaporthe  disease are unlikely to be expressed during  post-entry quarantine , as 
plants would be young, well maintained and grown under conditions that enhance growth . 
Such plants  are unlikely to encounter the stresses that promote  disease (such as drought , 
flooding and extreme cold/heat ).  
Note.  If D. baccae, D. hongkongensis or D. novem  were to produce symptoms in post-entry 
quarantin e, symptoms are likely to be detected well bef ore spores are produced, so this risk is likely to 
be managed in level 3 A: 
• These Diaporthe  species are reported from lesions on twigs , leaves,  branches and/or trunks , 
but conidia (asexual spores) and ascospores (sexual spores) of Diaporthe  species are usua lly 
only produced on dead twigs or dead wood  (Mondal et al.  2004, 2007; Punithalingam  and 
Holliday  1973; Zhang et al. 2008 ; Yamoto 1976) (see below) .  
• It is highly unlikely that dead citrus would be left in post-entry quarantine  for long enough for 
spores to be produced .  
• Waste treatment measures in place within level 3 A glasshouses (MPI 2019), would prevent 
any material from infected plants that died in post-entry quarantine  from being discarded into 
the environment.  
5.3.5  Risk assessment: l ikelihood of establis hment and spread  
These Diaporthe species are reported from citrus and other hosts that are commonly grown in 
New Zealand commercially and in domestic gardens, as well as from some wild plants and weeds. 
Climate is unlikely to limit the establishment of these species, since most reports of these species are 
from geographical areas with climate match indices of ≥ 0.7 w ith the whole of New Zealand, indicating 
that these areas have very similar climates to New Zealand (Phillips et al. 2018) (see Table 6 and more 
detailed information fo r each species below). As D. baccae,  D. hongkongensis and D. novem  are only 
recently described, they are likely to have even broader geographical distributions and host ranges 
than those recorded here.  
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 37 Table 6: Records of hosts and geographic location of D. baccae , D. hongkongensis  and D . novem  with climate 
match indices  of location to New Zealand  
Diaporthe 
Species  Host plants  Region and 
country  CMI 
range 
(Philips 
et al. 
2018).  Reference  
D. baccae  Blueberry  Italy 
 0.8–0.9 
with 
small 
areas of 
0.7 Lombard et al. 
2014  
Citrus  Italy 0.8–0.9 
with 
small 
areas of 
0.7 Guarnaccia and 
Crous 2017  
Grapevine  Croatia; France , 
Spain  0.8–0.9 
with 
small 
areas of 
0.7 Guarnaccia et 
al. 2018  
D. hongkongensis  Citrus (mandarin, unshiu, pomelo 
and orange)  China  (Fujian, 
Jiangxi, Zhejiang ) 0.6–0.7 Huang et al . 
2015  
Camellia sinensis  and numerous 
other species , including species or 
families that are grown in  New 
Zealand, e.g. Miscanthus sinensis 
[Gramineae]; Castanopsis  eyrie, 
Castanopsis carlesii , Quercus 
glauca (as synonym 
Cyclobalanopsis glauca ) and Herba 
Patriniae [Fagaceae] ; Ilex latifolia 
[Aquifoliaceae]  China ( Guangxi, 
Jiangxi, Nanchang, 
Ganzhou, Zhejiang)  0.6–0.7 
 Gao et al. 2015  
Kiwifruit  Sichuan , China; 
Turkey  0.7–0.8 Li et al. 2016; 
Erper et al. 
2017  
Grapevines  Hunan, China  0.7 Dissanayake et 
al. 2015  
D. novem  Citrange (cross between 
C. sinensis and P. trifoliata )  
Citrus  (C. japonica and 
C. aurantiifolia ) Mazandaran, Iran ; 
Italy 0.7–0.9 
(with 
small 
areas of 
0.5) Alavi and Faraki 
2016 ; 
Guarnaccia and 
Crous 2017   
Commercial sunflower ( Helianthus 
annuus ), other crop species 
including Cicer arietinum  
(chickpea), Glycine max  (soybean), 
Lupinus alba  (lupin), Sorghum 
bicolor  (sorghum) Vicia faba  (faba 
bean) and Vigna radiata  
(mungbean), and with the weed 
species Datura stramonium  
(common thornapple), Malva 
parviflora  (small flowered mallow), 
Rapistrum rugosum  (turnip weed), 
Sambucus gaudichaudiana  (wild 
elderberry), Sisymbriu m orientale  
(Indian hedge mustard), Sonchus 
oleraceus  (sowthistle),  Verbena  
sp., Vicia sativa  (common vetch), 
and Xanthium strumarium  
(Noogoora burr)  Eastern Australia, 
from sites in 
Victoria, 
Queensland and 
New South Wales  0.7–0.9 Thompson et al. 
2018  38 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Diaporthe 
Species  Host plants  Region and 
country  CMI 
range 
(Philips 
et al. 
2018).  Reference  
Grapevines  and Vitis sp. rootstock  Western cape, 
South Africa; 
northern California 
from Merced, Napa, 
San Benito, Solano 
counties; France, 
Spain  Mostly 
0.7–0.9, 
with 
some 
areas of 
0.6 Lesuthu et al. 
2019; Lawrence 
et al. 2015; 
Pintos et al. 
2018  
Willows ( Salix  sp.) and almond 
(Prunus dulcis ) California from 
Merced, Napa, San 
Benito, Solano 
counties  0.7–0.9 Lawrence et al. 
2015  
Kiwifruit  Chile  Mostly 
0.7–0.9, 
with 
some 
areas of 
0.6 Diaz et al. 
2014, 2017  
Asclepias syriaca , Aspalathus 
linearis  (rooibos), soybean, 
Hydrangea macrophylla  
(hydrangea), sunflower  Croatia, Italy , 
Portugal and South 
Africa  Mostly 
0.7–0.9, 
with 
some 
areas of 
0.5–0.6 Santos et al. 
2011  
 
Notes on  life cycle and  spread of Diaporthe  species   
Diaporthe species are generally spread  by rain splash of conidia (asexual) spores, and to a lesser 
extent by  windblown  ascospores (se xual spores) . These fungi can also be graft -transmitted . For 
example:  
• Diaporthe  citri survives as quiescent infections in twigs and only colonises twigs and branches 
after they die (Gopal 2014).  
• The main form of inoculum for D. citri  is conidia , which are  produced in pycnidia on dead twigs 
and branches and spread by rain splash (Punithalin gam and Holliday  1973; Mondal et al.  
2004, 2007 ).  
• Ascospores of D. citri are produced in perithecia on decaying wood in the soil or dead 
branches remaining in the tree and are dispersed by wind (Mondal et al. 2007; Gopal 2014).  
• Although ascospores are no t considered a major source of inoculum for local spread of D. citri 
within an orchard , they play a significant role in long -distance dispersal (Gopal 2014).  
• Diaporthe medusaea  produces conidia  on dead branches and invades wounded tissue  
(Zhang et al. 2008 ; Yamoto 1976 ). Annual pruning wounds provide many infection sites for 
Diaporthe pathogens each growing season ( Pintos et al. 2018).  
• In a survey that identified D. baccae, D. novem  and several other new Diaporthe species from 
citrus  in Europe , formation of pycnidia (asexual reproductive structures which produce conidia) 
was observed on dead twig tissue  (Guarnaccia and Crous 2017) .  
• Literature searches in CAB Abstracts and Google Scholar (August 2020) using the species 
name as a search term found no records that specifically reported ascospore production  in 
D. baccae,  D. hongkongensis or D. novem . 
• In other woody species , Diaporthe species are reported as graft -transmitted, e.g. in grapes, 
young vines may become infected with D. ampelina due to the use of infected mother vines  or 
through cross -contamination during the grafting process  (Pintos et al. 2018). The pathogen 
can therefore spread to new areas by movement of infected propagation material.  
• It is assumed  that D. baccae, D. hongkongensis and D. novem  spread in the same way  as 
other, better studied, Diaporthe species and therefore that they have the po tential to spread in 
New Zealand.  
• Diaporthe pathogens frequently have an extended latent asymptomatic phase or are 
asymptomatic endophytes in some hosts (Gao et al. 2016; Huang et al. 2015; Pintos et al. 
2018), so there is the possibility that they may sp read and establish undetected. Such 
infections would be very difficult to control by the time disease symptoms emerge.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 39  
Given the arguments and evidence below, t he likelihood of D. baccae establishing in 
New Zealand is considered high , with low uncertainty .  
• Diaporthe baccae  has been  reported from citrus and blueberries in Italy and from grapevines 
in Croatia, France,  and Spain (Lombard et al. 2014; Guarnaccia and Crous 2017, Guarnaccia 
et al. 2018). These countries have climate match indices with the whole of New Zealand in the 
range 0.7 –0.9, so environmental conditions are unlikely to limit the establishment or sprea d of 
D. baccae .  
• Host availability would not be limiting for D. baccae since  its hosts are extremely widespread 
in New Zealand. For example, i n 2019 , 1,660 ha were planted with commercial citrus,  640 ha 
with blueberries  and more than 38 ,000 ha with grapevi nes for wine production ( Plant and 
Food Research 2019 ).  
• It is assumed that D. baccae would be able to spread to nearby hosts in New Zealand via 
water  splash of conidia  and over longer distances by wind dispersal of ascospores or through 
human movement of latently infected propagation material (see above) . 
 
Given the arguments and evidence below, t he likelihood for D. hongkongensis 
establishing in New Zealand is consider ed high , with low uncertainty.  
• Diaporthe hongkongensis  has mainly been reported in China, but has also been reported in 
Artvin, Turkey (Dissanayake et al. 2015; Erper et al. 2017; Gao et al. 2015; Huang et al. 2015; 
Li et al. 2016; Manawasinghe et al. 201 9). Some areas in China where D. hongkongensis has 
been reported have climate match indice s of 0.7, and Artvin has a climate match index of 0.8 
with the whole of New Zealand. Based on this, environmental conditions in New Zealand are 
unlikely to limit the establishment or spread of D. hongkongensis.  
• Diaporthe hongkongensis  has been isolated from citrus, grapevines, Camellia sinensis  and 
kiwifruit (Huang et al. 2015 ; Dissanayake et al. 2015; Manawasinghe et al. 2019 ; Gao et al. 
2015 ; Li et al. 2016). Gao et al. (2015) also identified D. hongkongensis  in numerous wild 
hosts in Gutianshan nature reserve (China), including the common New Zealand weed 
Miscanthus and species in the Fagaceae, a plant family common in New Zealand. Diaporthe 
hongkongensis  was also re ported from kiwifruit in Artvin, Turkey (Erper et al. 2017 ; Li et al. 
2016).  
• Host availability would not be limiting for  D. hongkongensis . Citrus and grapevines are widely 
grown commercially and in home gardens (see above). In New Zealand, more than 12,000 
hectares are planted with commercial kiwifruit (Plant and Food Research 2019 ). Camellias are 
widespread throughout New Zealand in home g ardens and as amenity plantings , and 
Miscanthus is a common weed. These widespread plants could provide a reservoir of 
inoculum to spread the fungus.  
• It is assumed that D. hongkongensis would be able to spread to nearby hosts in New Zealand 
via water  splash of conidia  and over longer distances by wind dispersal of ascospores or 
through human movement of latently infected propagation material (see above) . 
 
Given the arguments and evidence below, t he likelihood of  D. novem establishing in 
New Zealand is  considered high , with low uncertainty.  
• Diaporthe novem  has been identified in a wide range of commercial crops and weeds, many 
of which are widespread in New Zealand. Diaporthe novem is reported from citrus in Italy 
(Guarnaccia and Crous 2017 ) and Iran  (Alavi and Faraki 2016 ), grapevines in Northern 
California  (Lawrence et al. 2015) , South Africa ( Lesuthu et al. 2019 ), France and Spain (Pintos 
et al. 2018) and from kiwifruit in Chile ( Díaz et al. 2014 , 2017) . A recent survey reported that 
D. novem was widespread in eastern Australia in numerous agricultural, horticultural and wild 
hosts, including sorghum, sunflowers, lupins, verbena and vetch ( Thompson et al. 2018 ). It 
has also been reported from willow in Ca lifornia (Lombard et al. 2015) and hydrangea in 
Portugal (Santos et al. 2011).  Most reports of D. novem  are from geographical areas with 
climate match indices  in the range 0.7 –0.9 with the whole of New Zealand. This indicates that 
areas where D. novem are found have very similar climates to New Zealand and that 
environmental conditions are unlikely to limit its establishment or spread.  40 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • Host availability would not be limiting for D. novem  since its hosts are extremely widespread in 
New Zealand. C itrus,  grapes and kiwifruit are grown commercially and in home gardens. 
Hydrangeas, lupins, sunflowers are widespread throughout New Zealand in home gardens 
and as amenity plantings. Lupins and sorghum are grown as forage. In addition, NZFlora 
(Allan Herbarium 2020) records many reported hosts of D. novem  species as “Wild, Exotic 
(Fully naturalised) ”, including willow, lupins, verbena, c ommon thornapple , sowthistle, s mall-
flowered mallow , turnip weed, Noogoora bur r, vetch and a number of Sambucus (elder)  
species (alth ough not S. gaudichaudiana ). These widespread weeds could provide a reservoir 
of fungal inoculum to spread the disease.  
• It is assumed that D. novem would be able to spread to nearby hosts in New Zealand via 
water  splash of conidia  and over longer distances by wind dispersal of ascospores or through 
human movement of latently infected propagation material (see above) . 
There is very low uncertainty in these conclusions , since existing reports of D. baccae, 
D. hongkongensis  and D. nov em are predominantly from regions with very similar climates to 
New Zealand and include commercial hosts that are widely produced in New Zealand. In addition, 
hosts of D. hongkongensis  and D. novem  include amenity plants, weeds and wild plants that are lik ely 
to be present in gardens and near production areas in New Zealand.  
 
5.3.6  Risk assessment: impacts to New Zealand  
Notes on dieback diseases caused by Diaporthe  
• Impacts of new Diaporthe  species are likely to become more severe as plants age (i.e. the 
impacts may be delayed for some years) and are likely to be sporadic and more severe in 
times of environmental stress such as extreme heat, cold, drought or heavy rainfall. High 
temperatures , cold injury, drought, rain in spring and early summer, and poor orchard 
management practices are reported to promote outbreaks of D. medusaea in citrus in China 
(Gao 2006; Zhang et al. 2008).  
• Likewise, disease of citrus caused by D. citri becomes more s evere as the tree ages. In a 
survey in Panama, melanose symptoms were observed mainly in sweet orange and grapefruit 
orchards older than 10 years, usually with poor management (Aguilera -Cogley and Vicent 
2019).   
• A 2011 outbreak of D. novem  causing severe s tem lesions and premature aging in a 
commercial sunflower crop in Queensland, Australia was triggered by sustained warm 
temperatures , above -average rainfall and subsequent flooding (Thompson et al. 2018).  
• Impacts may be mitigated by good management practic es (e.g. prompt removal of damaged 
and dead branches) .   
 
Given the arguments and evidence below , the introduction of D. baccae is 
considered likely to cause  moderate economic impacts for New Zealand, with 
moderate uncertainty . 
Diaporthe baccae has been re ported to cause disease in mandarin, grapevines and blueberry plants 
in countries with climates similar to New Zealand:  
• Diaporthe baccae was isolated from orange, lemon, grapefruit and mandarin plants with twig 
dieback and branch and trunk cankers in a su rvey in Italy (Guarnaccia and Crous 2017). In 
pathogenicity tests, however, D. baccae  only caused symptoms in mandarin. Melanose and 
stem -end rot of fruit were not observed in any of the citrus plants surveyed. Yield losses 
caused by D. baccae  were not des cribed . However , worldwide , trunk canker (caused by all 
pathogens) is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999).  
Therefore, it is assumed that canker s caused by D. baccae  have the potential to result in 
losses.  
• Diaporthe baccae  was isolated from grapev ines in Croatia, France and Spain during a survey 
of grapevine -associated  Diaporthe  in Europe and Israel (Guarnaccia et al. 2018). Disease 
symptoms associated with Diaporthe  included  cane and leaf spot, cane bleaching and 
additionally vascular browning and  sectorial necrosis in grapevine wood . Diaporthe baccae  
caused stem lesions in grapevines in pathogenicity tests ( Guarnaccia et al. 2018 ). However,  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 41 since samples  for the study were collected from asymptomatic and symptomatic grapevines , it 
is not certain w hether D. baccae was associated with disease symptoms in natural infection . 
• Wine is the second most valuable horticultural export for New Zealand (value NZ$1.8 billion) 
(Plant and Food Research 2019 ). Therefore, crop losses and loss of productive grapevine s 
have the potential to cause significant economic consequences for New Zealand.   
• Diaporthe baccae  was collected in a 2012 survey in Sicily, Italy (CMI=0.7 –0.8) from blueberry 
plants with cankers at their bases and brown lesions developing on the green stems and 
twigs, which led to twig blight (Lombard et al. 2014). Cankers in the crowns of plants led to 
plant death. In pathogenicity tests on blueberry plants, D. baccae  replicated these symptoms.  
• In 2019, blueberries were New Zealand’s most valuable berry crop, with a domestic sales 
value of NZ$23 million  and exports earning $ 38.9 million. Losses in this crop and damage or 
death of plants at commercial production sites have the potential to cause significant 
economic consequences for New Zealand.  
 
 
Given the arguments and evidence below , the introduction of D. hongkongensis is 
cons idered likely to cause  moderate economic impacts for New Zealand, with  
moderate uncertainty . 
• Diaporthe hongkongensis is reported as a grapevine pathogen , isolated in  Hunan, China, a 
region with a climate similar to the whole of New Zealand ( climate match i ndex = 0.7) , from 
grapevine wood from vines showing poor growth, bark and discolouration of the pedicels in 
grape bunches ( Dissanayake et al. 2015) . Diaporthe hongkongensis caused stem lesions in 
pathogenicity tests ( Dissanayake et al. 2015 ). 
• Wine is the s econd most valuable horticultural export for New Zealand (value NZ$1.8 billion) 
(Plant and Food Research 2019 ). Therefore, crop losses and loss of productive grapevines  
have the potential to cause significant economic consequences for New Zealand.   
• In Artv in, Turkey (CMI = 0.8), D. hongkongensis  caused necrotic and collapsed lesions at the 
stem ends of ripening kiwifruit on vines, reducing fruit production in three commercial orchards 
(Erper et al. 2017). In this study, D. hongkongensis was the only pathogen reported , and it 
caused symptoms in pa thogenicity testing. Diaporthe hongkongensis  (as D. lithocarpus ) was 
also reported as one of the Diaporthe  species c ausing post -harvest rot of kiwifruit in Sichuan 
(Li et al. 2015).  
• In 2019, kiwifruit exports earned more than NZ$2.3 billion ( Plant and Food Research 2019 ), so 
crop losses through pre -harvest  and post -harvest rots are likely to cause economic impacts.  
 
Given the arguments and evidence below , the introduction of D. novem  is considered 
likely to cause  moderate  economic impacts for New Zealand , with moderate 
uncertainty . 
• Diaporthe novem  was isolated from lime and kumquat plants with twig dieback in a survey  in 
Italy (although it occurred less frequently than D. foeniculina and D. baccae ) (Guarnaccia and 
Crous 2017). In pathogenicity tests, lime, lemon, and mandarin plants were susceptible to 
D. novem , although it was only weakly aggressive compared with the other citrus -associated 
Diaporthe tested. In east Mazandaran  (Iran), an area which generally has a similar climate to 
the whole of New Zealand ( climate match index = 0.6 –0.8), D. novem  was reported as the 
cause of gummosis , with symptoms including rot, wood discolouration and decline in c itrange 
(C. sinensis × P. trifoliata ) rootstock  (Alavi and Faraki 2016 ). 
• Yield losses caused by D. novem  were not described . However , it is assumed that trunk 
disease and  damage to rootstocks  caused by D. novem  has the potential to cause economic 
impacts through yield losses  or loss of productive plants.  
• Diaporthe novem  was isolated from dormant  Vitis sp. rootstock canes , rootstock and Vitis 
champinii  in the Western Cape province of South Africa (CMI = 0.6 –0.9) (Lesuthu et al. 2019) 
and from wood cankers on grapevines in Cali fornia (Lawrence et al. 2015). Diaporthe novem  
caused stem lesions in pathogenicity tests (Lawrence et al. 2015; Lesuthu et al. 2019).  
• New Zealand wine exports are very significant ( NZ$1.8 billion), and therefore , yield losses or 
damage to grapevines would  have economic consequences.  42 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • Diaporthe  novem was reported as one of the Diaporthe species  causing post -harvest rot of 
kiwifruit in Chile ( Díaz et al. 2014 , 2017). In 2019, kiwifruit exports earned more than NZ$2.3 
billion ( Plant and Food Research 2019 ), so losses through post -harvest rot are likely to result 
in economic impacts.  
• Diaporthe novem also causes disease symptoms (e.g. stem lesions)  in a range of forage 
crops, legumes and ornamental plants (e.g. lupin, sorghum, sunflower,  chickpea,  soybean, 
faba bean, mung bean) (Thompson et al.  2018). It has potential for impacts on the pastoral 
sector, cut flower production and horticulture.   
There is moderate  uncertainty around the potential for D. baccae, D.  hongkongensis and D. novem  to 
have ec onomic impacts in New Zealand for the following reasons.  
• Diaporthe baccae, D. hongkongensis and D. novem have been isolated from disease lesions 
in natural infections of plant hosts. However, it is not always clear how often they were the 
only fungal spec ies isolated and whether they caused the disease symptoms observed in the 
host. It is possible that these Diaporthe  species were secondary invaders of the disease 
lesions or were present in the plant as endophytes with no role in disease.   
• Several other economically significant Diaporthe species including  D. ampelina,  D. citri sensu 
stricto , D. eres, D. foeniculina, D. rudis  and D. sojae are present in New Zealand, often closely 
related and  with overlapping host ranges (including citrus, gra pe, kiwifruit, etc). For example, 
taxonomic studies suggest that D. baccae is very closely related to  D. foeniculin a (Hyde et al. 
2017), which is reported as a shoot blight, leaf spot, and opportunistic fruit rot, with hosts 
including citrus, grapevines, b lueberries, camellias, kiwifruit and many others (Farr and 
Rossman 2020) . Therefore, it is highly uncertain whether D. baccae, D. honkongensis  and D. 
novem will have greater or different impacts beyond the impacts of the Diaporthe species  
already established here.  
• Diaporthe  species often occur in coinfection with each other and/or other latent pathogen 
species (e.g. Botryosphaeriaceae ). However, pathogens may  compete , leading to no change 
or even reduction in disease severity. For example, the presence of Neofusicoccum  
mediterraneum spores significantly reduced  germination of D. rhusicola  spores in in vitro  
experiments ( Agustí -Brisach  et al. 2019). Inoculating  walnut shoots and hulls  with D. rhusicola 
four days before introducing N. mediterraneum  caused a delay in lesion development in 
shoots and hulls compared with the other two interaction treatments  (simultaneous or the 
other way around) ( Agustí -Brisach  et al. 2019).  
• Diaporthe baccae, D. hongkongensis and D. novem can cause disease symptoms in many of 
their known hosts in pathogenicity tests. However, such tests often involve inoculating the 
plant with high concentrations of spores or mycelium. It is uncertai n to what extent these 
Diaporthe species cause disease under natural infection conditions.   
• Disease symptoms attributed to Diaporthe  are more frequent and severe in older plants, 
suggesting they may be opportunistic rather than primary pathogens. Diaporth e pathogens 
can have long latent periods as asymptomatic endophytes but cause occasional  severe 
outbreaks of disease, particularly when plants are injured or stressed by environmental 
conditions or other pathogens. This means that impacts from D. baccae, D . hongkongensis 
and D. novem  may be delayed, sporadic and difficult to separate from impacts from other 
pathogens and adverse environmental events.  
• Given that  D. baccae, D. hongkongensis  and D. novem  were only recently described and can 
cause disease symptoms in a range of species from different families, they may affect other 
hosts that are economically important in New Zealand.  
 
Given the arguments and evidence below , the introduction of D. baccae,  
D. hongkongensis or D. novem  is considered likely to cause  low sociocultural 
impacts in New Zealand , with moderate uncertainty . 
The fungi may cause impacts to home gardeners, public parks and amenity plantings:  
• As mentioned above, Diaporthe baccae,  D. hong kongensis and D. novem cause s disease 
symptoms such as leaf scabs, branch cankers, twig dieback and fruit rots in plants such as 
blueberry, citrus, grapevines and kiwifruit which are often grown in New Zealand gardens. 
These species have the potential to r educe the productivity and yield of fruit crops for home  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 43 gardeners, since these Diaporthe  spp. have been reported to cause significant cankers that 
lead to loss of branches, or plant death in some hosts.   
• Other hosts of D. hongkongensis and D. novem includ e amenity species such as camellia , 
hydrangea , sunflower and lupin (see Table 6). For example, D. novem  caused stem lesions 
and lodging in patches of a commercial crop of sunflower in Australia (Thompson et al. 
2018). In contrast, D. hongkongensis in camellia was sometime s associated with leaf lesions, 
and sometimes asymptomatic (Gao et al. 2016), but it is not clear whether D. hongkongensis  
seriously damaged the plants.  
• The extent of impacts in home and civic gardens is uncertain. Impacts would most likely be 
sporadic, mo re common in older plantings, and linked to environmental conditions, stress, 
injury or infection with other pathogens. The uncertainty in the conclusion is moderate 
because of this , and the reasons outlined above.  
 
Given the arguments and evidence below , the introduction of D. baccae,  
D. hongkongensis or D. novem  is considered likely to cause very low to moderate  
environmental impacts in New Zealand , with moderate uncertainty . 
• Literature searches in CAB Abstracts and Google Scholar (August 2020) using the species 
name as a search term  found no reports of D. baccae, D. hongkongensis or D. novem 
infecting any plants that are native to New Zealand. However, D. hongkongensis and 
D. novem in particular have been isolated from a diverse  range of wild hosts in many different 
families (Gao et al. 2015; Thompson et al. 2018 ). Therefore, it is possible  that the fung i could 
cause disease in  native species present in New Zealand.  
• The uncertainty with this conclusion is high because the fungi are recently described and not 
described from New Zealand. Although no records were found of disease caused by these 
Diaporthe species in New Zealand native plants, the fungi may not have had the opportunity to 
infect such hosts if they are not common in the areas where these fu ngi are found.  
 
Given the arguments and evidence below , the introduction of  D. baccae, 
D. hongkongensis or D. novem is considered likely to cause very low  human health 
impacts in New Zealand , with moderate uncertainty.  
Some Diaporthe species are harmful to human or animal health:  
• Diaporthe  (Phomopsis) species (e.g. Diaporthe phaseolorum , Diaporthe raonikayaporum , 
Diaporthe sojae ) have occasionally been reported to cause eye, skin and soft tissue 
infections, particularly in immunocompr omised patients (Guégan et al. 2016; Howard et al. 
2019; Mattei et al. 2017).  
• Diaporthe  species have occasionally been reported to produce harmful mycotoxins in animal 
or human food. For example, Diaporthe toxica  produces Phomopsin A (PHO -A), a mycotoxin 
known to be responsible for fatal liver disease of lupin -fed sheep (Schloß et al. 2017).  
• Literature searches in CAB abstracts and Google Scholar (August 2020) using the species 
name as a search term found no specific reports of D. baccae, D. hongkongensis  and D. 
novem  causing human or animal disease, either directly or through mycotoxins in fo od. 
However, there is moderate uncertainty in the conclusion because these species are recently 
described and human or animal health impacts cannot yet be ruled out.  
 
5.3.7  References  
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Zhou, Y; Hyde, K D; Brooks , S; Yan, J (2019) High genetic diversity and species complexity of 
Diaporthe  associated with grapevine dieback in China. Frontiers in Microbiology , 10: 1936. 
https://www.frontiersin.org/article/10.3389/fmicb.2019.01936  
Mattei, A S; Severo, C B; Guazzelli, L S; Oliviera, F M; Gené, J; Guarro, J; Cano, J, Carlos Severo, L 
(2013) Cutaneous infection by Diaporthe p haseolorum  in Brazil. Medical Mycology Case Reports  2: 
85–87. doi:10.1016/j.mmcr.2013.03.001  
Mondal, S N; Agostini, J P; Zhang, L; Timmer, L W (2004) Factors affecting pycnidium production of 
Diaporthe citri  on detached citrus twigs. Plant Disease , 88: 37 9–382. 
Mondal, S N; Vicent, A; Reis R F; Timmer, L W (2007) Saprophytic colonisation of citrus twigs by 
Diaporthe citri  and factors affecting pycnidia production and conidial survival. Plant Disease , 91: 387 –
392. 
Mycobank (2020 ) Mycobank Fungal Databases, Nomenclature & Species Banks. 
https://www.mycobank.org/quicksearch.aspx . Accessed August –September 2020 . 46 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Myo, Z; Seint, S A; Matsumoto, M (2020) Colletotrichum  and Diapo rthe species associated with 
soybean stem diseases in Myanmar. Journal of General Plant Pathology , 86: 114 –123. 
https://doi.org/10.1007/s10327 -019-00902 -5.  
NZFungi2 (2020) New Zealand Fungi and Ba cteria. Manaaki Whenua  ‒ Landcare Research  database . 
https://nzfungi2.landcareresearch.co.nz/   
ONZPR (2020) Official New Zealand Pest Register. 
https://pierpestregister.mpi.govt.nz/PestsRegister/ImportCommodity/  Accessed August 2020  
Phillips, C B; Kean, J M; Vink, C  J; Berry, J (2018) Utility of the CLIMEX ‘match climates regional ’ 
algorithm for pest risk analysis: An evaluation with non -native ants in New Zealand. Biological 
Invasions , 20(3): 777‒791. https://doi.org/10.1007/s10530 -017-1574 -2  
Pintos, C; Redondo, V; Costas, D; Ag uín, O; Mansilla, P (2018) Fungi associated with grapevine trunk 
diseases in nursery produced Vitis vinifera  plants. Phytopathologia Mediterranea , 57(3): 407 –424. 
doi:http://dx.doi.org/10.14601/Phytopathol_Mediterr -22964  
PPIN (2020) Internal MPI database. Accessed August 2020 . 
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Descriptions of Fungi and Bacteria 1973 No. 40 pp. Sheet 396 ref.4  
Santos, J M; Vrandečić, K; Cosić, J; Duvnjak, T; Phillips, A J (2011) R esolving the Diaporthe  species 
occurring on soybean in Croatia. Persoonia , 27: 9 –19. doi:10.3767/003158511X603719. 
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Schlo ss, S; Hackl, T; Herz, C; Lamy, E; Koch, M; Rohn, S; Maul, R (2017) Detection of a toxic 
methylated derivative  of Phomopsin A produced  by the legume -infesting fungus  Diaporthe toxica. 
Journal of Na tural Products , 80(6): 1930 –1934. doi:10.1021/acs.jnatprod.6b00662  
Species Fungorum (2020) Accessed August –September 2020 . 
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Diaporthe novem  isolated from sunflow er (Helianthus annuus ) and other crop and weed hosts in 
Australia. European Journal of Plant Pathology , 152, 823 –831. https://doi.org/10.1007/s10658 -018-
1515 -7  
Timmer, L W; Garnsey, S M; Graham, J H (1999) Compendium of Citrus Diseases , second edition . 
APS Press; St Paul, USA.  
Udayanga, D; Castlebury, L A; Rossman, A Y; Hyde, K D (2014) Species limits in Diaporthe : 
molecular re -assessment of D. citri, D. cytosporella, D. foeniculina  and D. rudis.  Persoonia , 32: 83 –
101. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4150081/   
Xu, G; Qui, F; Li, X; Zheng, F Q; Zheng, L; Miao, W G; Xie, C P (2020) Diaporthe limonicola  causing 
leaf spot disease on Areca catechu  in China. Plant Disease , 104(6): 1869 . 
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Yamoto , H (1976) A species of Diaporthe  pathogenic to citrus. Annals of the Phytopathological Society 
of Japan , 42: 56 –59. https ://doi.org/10.3186/jjphytopath.42.56   
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with dieback diseases in China, with twelve new species described. MycoKeys , 39: 97 –149. 
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its integrated control. South China Fruits , 2008(2): 16 –17. Abstract only . 
   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 47  
5.4 Elsinoe australis  (sweet orange scab)  
 
Elsinoe  australis  (sweet orange scab)  is a fungus that causes premature fruit drop and unsightly corky 
blemishes (scabs) on citrus fruit and occasionally leaves and twigs, particularly in sweet orange and 
mandarin. This disease causes yield losses and reduces the market value of fresh citrus fruit .  
 
Taxonomy  
Scientific name: Elsinoe  australis Bitancourt and Jenkins  (1936 )  
Order/ family: Myriangiales (previously Dothideales)/ Elsinoaceae  
Other names: Sphaceloma australis  Bitanc ourt & Jenkins  (1936) , sweet orange scab, SOS (CABI 
2020)  
Notes : There are several pathotypes of E. australis , and they differ in their ability to cause disease in 
citrus. 
• The sweet orange scab (SOS) pathotype of E. australis was first reported in Paraguay in 1882 
and mainly occurs in South America (Argentina, Bolivia, Paraguay, Uruguay and Brazil) 
(Bitancourt and Jenkins 1937; Sivanesan  and Critchett  1974). It affects a range of citrus hosts, 
but sweet orange ( Citrus sinensis ) is the major host (EFSA 2017).  
• Hyun et al. (2007, 2009) reported a new pathotype of E. australis  from fruit of natsudaidai 
(C. × natsudaidai ) in Korea. This pathotype has also been detected in Honshu, Japan32 and is 
recently invasive in the USA, where it causes lesions on a much wider range of citrus hosts, 
including sweet orange, lemon (C. limon ), tangerine ( C. reticulata ) and grapefruit ( C. paradisi ) 
(Kunta et al. 2013).  
• Two pathotypes of E. australis  are reported from Australia, from finger lime ( Citrus australica ) 
fruit (Miles et al. 2015) and from jojoba ( Simmondsia chinensis ) (Ash et al. 2012).  
• Elsinoe australis  (natsudaidai pathotype) was recently reported from poplar ( Populus 
tomentosa and P. de ltoides)  in China (Zhou et al. 2020).  
 
5.4.1  Summary of conclusions  
• The association of  E. australis  with leafless  Citrus  budwood is considered  weak  with low 
uncertainty.  
• The likelihood of E. australis entering associated with leafless  Citrus  budwood is consider ed to 
be negligible , with low uncertainty.   
• Elsinoe australis  may not be considered for additional measures.  
• Given that E. australis  is not expected to enter New Zealand associated with leafless Citrus  
budwood, further assessment is not required.  
5.4.2  Hazard  identification: regulatory status  
Elsinoe  australis meets the criteria to be a quarantine pest for New Zealand .  
Criteria for being a regulated quarantine pest , relevant to this assessment are: the pest is not present 
in the pest risk assessment area (New Zealand) and is of potential importance (able to establish and 
cause harm33). 
 
Elsinoe  australis is recorded as absent from New Zealan d:  
• It is recorded as absent in NZ Fungi 2 (2020) and NZOR  (2020) . 
• It is not recorded in PPIN (2020).  
• It is listed as ‘Regulated’ in B RAD and ONZ PR (2020) . 
 
Elsinoe  australis has the potential to establish and spread in New Zealand:  
• Elsinoe  australis is commonly  reported from areas with a very similar climate to New Zealand , 
indicated by a climate match index  (CMI) of ≥0.7 (Phillips et al.  2018) . The sweet orange 
pathotype is reported in South America, including Argentina, Uruguay and Rio Gr ande do Sul 
in Brazil (EPPO 2020).  The natsudaidai pathotype  has been reported from Jeju Island, Korea , 
 
32 IPPC pest report 2014. Accessed September 2020 from 
https://www.ippc.int/static/media/files/pestreport/2014/05/28/detection_of_elsinoe_australis_in_japan.pdf . 
33 Refer to ISPM 5  for the definition of a quarantine pest  under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.  48 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  and Honshu, Japan  (Hyun et al. 2007; EPPO 2020). A closely related pathotype  is recently 
invasive in some US states (Louisiana, Florida, Mississippi, Texas, Arizona and parts of 
California (Kunta et al. 2013).  
• Elsinoe  australis is most often reported from Citrus and Fortunella  species (CABI 2020; EPPO 
2020) . Citrus is  commercially  grown in New Zealand and commonly grown in  gardens . 
 
Elsinoe  australis has the potential to cause  impacts to New Zealand : 
• Elsinoe  australis has the potential to harm citrus , which is of economic importance to New 
Zealand.  
• Elsinoe  australis has the potenti al to have socio -cultural impacts: citrus is commonly planted in 
home gardens.  
 
5.4.3  Hazard identification: commodity association  
Given the arguments and evidence below, t he association of E. australis with Citrus 
spp. is considered  strong . However , the association with leafless budwood is 
considered  weak with low uncertainty . 
• The major host of E. australis is sweet orange (C. sinensis ), and it has also been reported 
from many other citrus species ( Table 7).  
 
Table 7: Species of Citrus  and related genera susceptible to sweet orange scab caused by E. australis (Kunta et 
al. 2013; Farr and Rossman 2020; CDFA 2020)  
Scientific name  Common name  
C. sinensis  Sweet orange  
C. aurantiifolia  Mexican lime  
C. aurantium   Bitter orange  
C. australis   Finger lime  
C. limon  Lemon  
C. nobilis   Tangor  
C. × paradisi   Grapefruit  
C. reticulata   Mandarin/tangerine  
C. unshiu   Satsuma mandarin  
C. grandis/C.maxima  Pomelo (detected in a survey in Japan34)  
C. latifolia  Tahiti lime  
 
 
Elsinoe australis is only occasionally associated with stems , shoots or twigs  of citrus plant s. 
• Elsinoe australis mainly causes symptoms on fruit, and l esions caused by E. australis on twigs 
of citrus plants are rare (Bitancourt and Jenkins 1937).  
• Most later authors do not mention symptoms of E. australis on twigs, stems or shoots (e.g. 
Timmer et al. 1996;  Timmer 2000;  Hyun et al. 2007;  Chung 201 1; Kunta et al. 2013 ). 
• CDFA (2020) describe warty lesions and corky eruptions caus ed by E. australis on young 
twigs, shoots and stems of nursery plants , but evidence from other sources  suggests that this 
is also a rare symptom in the USA (Schultz  et al. 2013; UF/IFAS Citrus extension 2020;  LSU 
AgCentre (accessed 29  November 2020) and other articles on the LSU AgCentre website; 
USDA -APHIS 2020).  
5.4.4  Risk assessment: entry  
Given the arguments and evidence below, t he likelihood of E. australis  entering 
associated with citrus budwood is  considered negligible , with low uncertainty . 
Elsinoe  australis  can be associated with citrus budwood (see above) but the likelihood is low.  
• It is rare for E. australis  to be associated with stems, shoots or twigs of citrus plants (see 
above).  
• Although Chung (201 1) states that E. australis  probably survives solely in fruit, Bitancourt and 
Jenkins (1937) believ ed that infected twigs were almost certainly a source of inoculum for 
infections in the next season.  Sivanesan and Critchett (1974) also believed old lesions on 
 
34 IPPC pest report 2014. Accessed September 2020 from 
https://www.ippc.int/static/media/files/pestreport/2014/05/28/detection_of_elsinoe_australis_in_japan.pdf .  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 49 twigs to be a probable source of infection at the start of each season (in addition to fruit and 
leaf lesions).  
• Plants from areas with high levels of E. australis are extremely unlikely to be used for 
comme rcial budwood production.  
• Since stem infections are rare and cause obvious , visible symptoms ( warty lesions and corky 
eruptions ), it is not likely  that contaminated material will be used for propagative material .   
 
 
The minimum requirements reduce the likelihood of entry  to a negligible level because the latent 
period for symptoms of E. australis  is short  and symptoms are likely to be detected prior to export or 
within one growing season in post -entry quarantine . 
• Bitancourt and Jenkins  (1937 ) describe t he twig lesions as comparatively rare and 
inconspicuous. However, the examples they photographed were clearly visible without 
magnification. Since imported budwood will not include leaves, any lesions are likely to be 
exposed and therefore easily detected by visual inspection.  
• Although no studies were found that determined the rate of symptom development on twigs or 
shoots, evidence from leaf and fruit infections suggests that symptoms will develop within 10 
days . 
o Scab symptoms developed 5–7 days after inoc ulation  of grapefruit, sweet orange, 
lemon and tangerine with E. australis (the natsudaidai pathotype from the USA)  in 
detached leaf assays  (Kunta et al. 2013 ). 
o Fruit of grapefruit, tangerine, and sweet orange inoculated with E. australis  isolates 
develope d scab symptoms 8 –10 days after inoculation  (Bitancourt and Jenkins 1937 ; 
Kunta et al. 2013; EFSA 2017 ). 
 
There is low uncertainty associated with this conclusion. Searches of CAB Abstracts, CABI and 
Google Scholar using the search terms ‘Elsinoe australis’ and ‘latent’ or ‘endophyte’ or ‘systemic’ 
returned no evidence to suggest that E. australis can remain latent in citrus budwood for long periods.  
 
Given that E. australis is not e xpected to enter New Zealand associated with leafless Citrus  budwood, 
further assessment is not required.  
 
5.4.5  References  
Ash, G J; Stodart, B; Hyun, J -W (2012) Black scab of Jojoba ( Simmondsia chinensis ) in Australia 
caused  by a putative new pathotype  of Elsinoe australis . Plant Disease , 96: 629 –634. 
https://apsjournals.apsnet.org/doi/pdfplus/10.1094/PDIS -06-11-0465   
 
Bitancourt, A A; Jenkins, A E (1936) Perfect stage of the sw eet orange fruit scab fungus. Mycologia , 
28: 489 –492.  
 
Bitancourt, A A; Jenkins, A E (1937) Sweet Orange scab caused by Elsinoe australis. Journal of 
Agricultural Research , 54(1): 1 –18. 
 
BRAD (2020) Biosecurity Risk Analysis Database. Ministry for Primary Industries internal database. 
Accessed August 2020.  
 
CDFA (2020) California pest rating proposal for Elsinoe australis  Bitanc. & Jenkins 1936 Sweet 
orange scab. California Department of Food and Agriculture.  
https://blogs.cdfa.ca.gov/Section3162/wp -content/uploads/2020/05/Elsinoe_australis_PRP -ADA.pdf   
 
Chung, K -R (2011) Elsinoe fawcettii  and Elsinoe australis : the fungal pathogens causing citrus scab. 
Molecular Plant Pathology , 12(2): 123 –135. 
https://bsppjournals.onlinelibrary.wiley.com/doi/full/10.1111/j.13 64-3703.2010.00663.x   
 
CABI (2020) Elsinoe australis ( sweet orange scab ). In Invasive Species Compendium . CAB 
International ; Wallingford, UK. www.cabi.org/isc Accessed September 2020.  
 
EFSA (2017) Pest categorisation of Elsinoe fawcettii  and E. australis . EFSA Journal , 15(12): e05100. 
https://doi.org/10.2903/j.efsa.2017.5100   
 50 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  EPPO (2020) EPPO Global Database. https://gd.eppo.int/ . Accessed August 2020.   
 
Farr, D  F; Rossman A Y (2020) Fungal Databases, U.S. National Fungus Collections, ARS, USDA. 
https://nt.ars -grin.gov/fungaldatabases/   
 
Hyun, J W; Peres, N A; Yi, S -Y; Timmer, L W; Kim, K S; Kwon, H M; Lim, H -C (2007). Development of 
PCR assays for the identification of species and pathotypes of  Elsinoe  causing scab on citrus. Plant 
Disease , 91: 865 –870. https://doi.org/10.1094/PDIS -91-7-0865  
 
Hyun, J W; Yi, S H; MacKenzie, S J; Timmer, L W; Kim, K S; Kwon, H M; Lim, H -C (2009). Pathotypes 
and geneti c relationship of worldwide collections of Elsinoe  spp. causing scab diseases of citrus.  
Phytopathology , 99: 721 –728. https://doi.org/10.1094/PHYTO -99-6-0721  
 
Kunta, M; Rascoe, J; de Sa, P B; Timmer, L W; Palm, M E; da Graça, J V; Mangan, R L; Malik, N S A; 
Salas, B; Satpute, A; SétamouI, M; Skaria, M (2013). Sweet orange scab with a new scab disease 
“syndrome ” of citrus in the USA associated with Elsinoe  australis. Tropical Plant Pathology , 38: 203 –
212. https://doi.org/10.1590/S1982 -56762013005000003  
 
LSU AgCentre . Louisiana plant pathology disease identification and management series 3169. Citrus 
scab and Sweet orange scab. https://www.l suagcenter.com/NR/rdonlyres/E9FEE4CD -CED2 -4807 -
98D3 -1F8FF8F0AF5F/74234/pub3169CitrusScabsHIGHRES.pdf  Accessed 29  November 2020 . 
 
Miles, A K; Tan Y P; Shivas, R G;Drenth, A (2015). Novel pathotypes of Elsinoe australis  associated 
with Citrus australasica and Simmondsia chinensis  in Australia. Tropical Plant Pathology , 40: 26 –34. 
https://doi.org/10.1007/s40858 -015-0005 -0 
 
NZFungi2 (2020) New Zealand Fungi and Bacteria. Manaaki Whenua – Landcare Researc h database . 
https://nzfungi2.landcareresearch.co.nz/   
 
NZOR (2020) New Zealand Organisms Register. http://www.nzor.org.nz/  Accessed September 2020 . 
 
ONZPR (2020) Official New Zealand Pest Register. 
https://pierpestregister.mpi.govt.nz/PestsRegister/ImportCommodity/  Accessed August 2020 . 
 
Phillips , C B ; Kean , J M ; Vink , C J; Berry , J A (2018) Utility of the CLIMEX ‘match climates regional ’ 
algorithm for pest risk analysis: An evaluation with non -native ants in New Zealand.  Biological 
Invasions , 20(3): 777 –791. 
 
Plant Health Australia (2020) Sweet orange scab fact sheet. 
https://www.planthealthaustralia.com.au/wp -content/uploads/2013/01/Citrus -sweet -orange -scab -
FS.pdf . Accessed 12  October 2020 . 
 
PPIN (2020) Plant Pest Information Network, version 5.03.01. Ministry for Primary Industries internal 
databa se. Accessed August 2020 .  
 
Schultz, D; Rybak, M; French, R D (2013) Citrus scab and sweet orange scab. Texas A&M Agrilife 
extension PLPA -Cit013 -02. http://agrilife.org/amarillo/files/2010/11/CitrusScab20 13-1.pdf  Accessed 29  
November 2020 . 
 
Sivanesan, A; Critchett, C (1974) Elsinoe australis. CMI Descriptions of pathogenic fungi  
and bacteria No. 440. CAB International ; Wallingford, UK.  
 
Timmer, L W (2000) Scab diseases. In Timmer, L W;  Garnsey, S M; Graha m, J H (eds) (2000) 
Compendium of Citrus Diseases . Seco nd edition . APS Press; St Paul, USA . 
 
Timmer, L W; Priest, M; Broadbent, P; Tan, M -K (1996) Morphological and pathological 
characterisation of species of  Elsinoe  causing diseases of Citrus. Phytopathol ogy, 86: 1032 –1038. 
https://www.apsnet.org/publications/phytopathology/backissues/Documents/1996Articles/Phyto86n10_
1032.PDF   
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 51 UF/IFAS citrus extension (2020) Sweet Orange Scab. University of Florida.  
https://crec.ifas.ufl.edu/extension/plant_pathology/sweet_orange_scab.shtml  Accessed 30  November 
2020 . 
 
USDA -APHIS (2020) Sweet Orange Scab. Last modified 2  June 2020. 
https://www.aphis.usda.gov/ap his/ourfocus/planthealth/plant -pest-and-disease -programs/pests -and-
diseases/citrus/sweet -orange -scab  Accessed 29  November 2020 . 
 
Zhou, L; Xiao, H; Ma, X; Cheng, Q (2020) Elsinoe australis causing spot anthracnose on poplar in 
China. Plant Disease , 104(8): 2202 –2209. https://apsjournals.apsnet.org/doi/10.1094/PDIS -11-19-
2349 -RE  
 
 52 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  5.5 Erysiphe quercicola  and Fibroidium tingitaninum  (powdery 
mildew of citrus)  
 
The asexual forms of Erysiphe quercicola  and Fibroidium tingitaninum  are the causative agents of 
fungal powdery mildew disease on Citrus spp. The disease is typified by the appearance of white 
‘powdery’ growth on the surfaces of leaves, shoots and young fr uits. 
 
Taxonomy  
Scientific name: Fibroidium tingitaninum  (Carter) Braun and Cook  (2012)  
Order/ family : Erysiphales/Erysiphaceae  
Synonyms: Oidium tingitaninum , Acrosporium tingitaninum   
Common names: Powdery mildew of citrus  
Notes: This fungus was originally recorded on leaves of Citrus nobilis (tangor), as O. tingitaninum, in 
California (Index Fungorum  2020 ).  
 
Scientific name:  Erysiphe quercicola  Takam and Braun (2007)  
Order/ family : Erysiphales/Erysiphaceae  
Synonyms:  Oidium citri, O. anacardi i, Acrosporium anacardii, Pseudoidium anacardii,  O. heveae, 
O. mangiferae . 
Notes: Erysiphe quercicola was first described by Takamatsu et al. (2007) from leaves of Quercus 
phillyreoides (black ridge oak) in Japan . Based on phylogenetic analysis powdery mildew occurring on 
several hosts , it was identified as asexual E. quercicola (Takamatsu et al. 2007). The asexual names 
O. anacardia , O. citri, O. heveae and O. mangiferae are considered synonyms.  
The literature fo und concerning this species causing citrus powdery mildew refers to both O. citri and 
E. quercicola . Recent literature of the fungus on Citrus spp. and other hosts refers to E. quercicola 
(Tam et al. 2016; Baiswar et al. 2015; Siahaan et al. 2016; Fonseca et al. 2019). In keeping with the 
move away from the use of the Oidium spp. names, E. quercicola is used in this assessment.  
 
Powdery mildew lifecycle  
Fungi in the order Erysiphales are commonly referred to as powdery mildews (Glawe 2008). The 
complete li fe cycle of powdery mildews may involve an asexual stage as well as a sexual stage  
(Glawe 2008 ). During asexual reproduction , conidia are produced on the host. The  conidia  have a 
white, powdery appearance , and the conidia production stage is the  state that is referred to as 
‘powdery mildew’. Conidia are produced in large amounts, within a short space of time (3 –7 days post 
infection under disease -promoting conditions) and therefore can cause rapid spread of the disease . 
Powdery mildews can overwi nter as dormant asexual mycelia in b uds of host plants or as sexual 
ascospores independent of a host ( Glawe 2008 ).  
 
The main disease symptoms of powdery mildew and spread of the disease are due to the asexual 
stage of the fungi. The literature o n F. tingitaninum and E. quercicola  on citrus (as well as other hosts) 
does not mention the sexual stages. Therefore, the asexual forms of citrus powdery mildews  are of 
most concern.   
 
Uncertainty  
Identification and ecological studies of citrus powdery mildew have been hampered , as the disease is 
caused by the asexual form , and the sexual form often does  not occur (particularly in the tropics where 
the di sease  is most prevalent), which is needed for species identification (Limkaisang et al. 2006). 
Formerly, the asex ual form s (Oidium spp.) were described based on host plants and morphological 
characteristics, but this was not always sufficient to clearly differentiate the forms  (Limkaisang et al. 
2006). Recently, molecular methods have been successful in identifying the anamorphic forms of 
powdery mildews (Baiswar et al. 2015; Takamatsu et al. 2007), which has led to some previously 
identified records being reassigned (Holford e t al. 2010).  
Furthermore, the literature that refers to the causative agents of citrus powdery mildew disease does 
not always differentiate between the two species (as mentioned above). This is due to either the use 
of the disease name, the use of names t hat have since become synonyms, or records where the 
causative agent is given as O. tingitaninum but it is not clear what method was used in the 
identification (Whiteside et al. 1988; Gupta and Gupta 1992; Reddy 2010). Where possible, the two 
species have been assessed separately. However, where information either  was not available for the 
individual species or did not differ between the species , they were assessed together.  
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 53 5.5.1 Summary of conclusion s 
• The likelihood of F. tingitaninum and E. quercicola enterin g associated with leafless of Citrus 
budwood  is considered  low, with moderate uncertainty . 
• The likelihood for E. quercicola establishing in New Zealand is considered high , with low 
uncertainty.  
• The likelihood of F. tingitaninum establishing  in New Zealand  is considered  moderate, with low 
uncertainty . 
• The introduction of  E. quercicola is considered  to cause  moderate  economic impacts in New 
Zealand , with low uncertainty.  
• The introduction of  F. tingitaninum is likely  to cause  low economic impacts in New Zealand , 
with low uncertainty.  
• The introduction of  E. quercicola or F. tingitaninum is likely to cause low sociocultural impacts 
in New Zealand , with low uncertainty.  
• The introduction of  E. quercicola or F. tingitaninum is likely to cause very low environmental 
impacts in New Zealand , with low uncertainty.  
• The introduction of  E. quercicola or F. tingitaninum is likely  to cause negligible  human health 
impacts , with low uncertainty.  
• Fibroidium  tingitaninum and E. quercicola may be considered for additional measures  on 
citrus budwood .  
 
5.5.2  Hazard identification: quarantine pest status  
 
Given the arguments and evidence below , F. tingitaninum and E. quercicola meet the 
criteria to be quarantine pests for New Zealand  
Criteria for being a regulated quarantine pest relevant to this assessment are: the pest is not present 
in the pest risk assessment area (New Zealand) , and the pest is of potential importance (able to 
establish and cause ha rm35). 
 
Oidium tingitaninum and O. citri are not known to be present in New Zealand . 
• Fibroidium  tingitanium is not known to occur in New Zealand. It is not recorded in PPIN (2020) 
or NZFungi (2020). The quarantine status of the fungus in New Zealand is ‘ regulated’ in 
ONZPR and BRAD  (2020), under the synonym O. tingitanium .  
• Erysiphe quercicola is not known to occur in New Zealand. It is not recorded in PPIN (2020) 
and is listed as absent in NZFungi 2 (2020). Erysiphe quercicola is not recorded in ONZPR 
(2021).  Oidium citri is recorded in BRAD , but no regulatory status is assigned.  
Fibroidium tingitaninum and E. quercicola  have the potential to establish and spread in New Zealand:  
• The fungi are reported to cause disease in countries with similar climates to New Zealand.  
• High humidity is favour able for  citrus powdery mildew expression (Whiteside et al. 1988). In 
New Zealand , most commercial citrus orchards are in the north of the North Island ( Plant and 
Food Research 2019), which has a warm, humid, sub -tropical climate (section 2.6). 
• Citrus species are also widely grown in New Zealand both commercially and by home 
gardeners throughout the country (section 2.6).  
• Therefore, suitable host plants in suitable environmental conditions are likely to be present to 
support establishment.   
 
Oidium tingitaninum and E. quercicola  have the pot ential to have economic and sociocultural 
consequences by causing disease of  citrus and oak . 
• On citrus,  powdery mildews cause symptoms on leaves, shoots and young fruits. Infection 
reduces the photosynthetic power of the tree and severely infected trees dr op fruit early. 
Severe infection can have significant effects on fruit yield and marketability (Biosecurity 
Queensland 2011).   
• All known citrus cultivars are affected , and there are no known resistant cultivars (Whiteside et 
al. 1988; Biosecurity Queensla nd 2011).  
 
35 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for fa ctors to consider 
when defining “harm”.  54 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • Citrus is an important commercial crop for New Zealand and is commonly grown by home 
gardeners ( section  2.6).  
• Erysiphe quercicola also causes powdery mildew of oak (Takamatsu et al. 2007), which is 
grown for timber, as a forage crop and as an amenity plant in New Zealand (Halliwell 1979; 
Horizons R egional Council 2017).   
 
5.5.3  Hazard identification: commodity association  
Given the arguments and evidence below , the association of  Fibroidium tingitaninum 
and E. quercicola  with leafless Citrus budwood  is considered strong, with low 
uncertainty .  
Mycelia of powdery mildews can be present in the buds of infected plants:  
• These fungi affect all aerial parts of citrus plants (Reddy 2010). Powdery mildews are not 
internal pathogens , but rather , form myceliu m that grow s on the outside of (generally) new, 
green growth (Agrois 1978).  
• The powdery mildew fungi overwinter in buds of infected plants, as dormant mycelia . 
(Whiteside et al. 1988; Reddy 2010; Brazee 2019). Therefore, mycelium may be present on 
leafless  budwood produced from an infected mother plant.  
5.5.4  Risk assessment : likelihood of entry   
Given the arguments and evidence below, the likelihood of F. tingitaninum and 
E. quercicola  entering New Zealand associated with leafless  Citrus budwood  is 
considered  low, with low uncertainty . 
Fibroidium  tingitaninum and E. quercicola  have a strong association with leafless citrus  budwood, as 
powdery mildews overwinter in buds:  
• Citrus powdery mildews overwinter in buds of infected plants as dormant mycelia, which are 
the source of new infection come spring, when conidia are produced and easily spread 
(Whiteside et al. 1988; Reddy 2010; Brazee 2019).  
• In apple, the dormant shoots of plants heavily infected with powdery mildew the previous year 
are covered in dense, white fungal mycelium , and the terminal bud is pinched (Agriculture 
Victoria, undated). Therefore, such material is unlikely to be used to produce budwood. 
However, shoo ts may also appear normal but harbour overwintering mycelia in healthy -
looking leaf buds (Agriculture Victoria undated). Such material may be unknowingly used for 
producing budwood.  
• Citrus powdery mildew has a tropical/subtropical distribution and is repor ted from Asia, the 
Caribbean, Central and South America, Uganda and the USA (Florida and occasionally 
California on tangerines) (Whiteside et al. 1988; Thaung 2007; Chung 2011). Of the countries 
where the disease is reported to occur on Citrus spp., only the USA has  ever exported citrus 
budwood  to New Zealand, the last time in 2005 (QuanCargo 2020 ). As this pathway is inactive 
and other potential pathways have never had trade, material is unlikely to be sourced from 
countries where citrus powdery mildew is known to occur. However, trade on these pathways 
cannot be ruled out in the future.  
• There is a low likelihood that severely infected plants would be used to produce budwood 
material. However, trees that were only mildly infected can appear healthy but harb our 
mycelium in dormant buds. Therefore, during times of mild disease infection, there is the 
potential for some contaminated material to be used for leafless budwood.  
There is some uncertainty around the frequency by which plant material may be harbouring  dormant 
powdery mildew mycelium, but otherwise appear healthy. The symptoms described in the literature 
suggest that heavily infected material would be easily detectable and would not be used to produce 
budwood or symptoms would be noticed at the border.  
 
Minimum requirements reduce the likelihood of entry to low, as t he fungi  are likely to cause visibly 
detectable symptoms within one growing season:   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 55 • Fibroidium tingitaninum and E. quercicola  overwinter in buds of infected plants as dormant 
mycelia, which a re the source of new infection come spring (Whiteside et al. 1988; Reddy 
2010; Brazee 2019). If the material is derived from heavily infected trees,  disease symptoms 
would be visibly detectable. However, the material may also be infected and appear healthy  
early in the season.  
• Following overwintering, when conditions become favourable in spring, the fungi resume 
growing and invade newly developing shoots and leaves (Brazee 2019).  
• No evidence was found of F. tingitaninum or E. quercicola  (syn. O. citri ) causing asymptomatic 
infection of Citrus spp. Google Scholar and CAB Abstracts were searched using the terms: 
citrus powdery mildew  or Oidium tingitaninum/Fibroidium tingitaninum or Erysiphe  
quercicola/Oidium citri  + asymptomatic/dormant/latent.  
• Sastra -Hiday at (1992) showed that the disease caused by F. tingitaninum has a four -day 
infection cycle, when conditions were conducive to disease. The optimal conditions for conidial 
germination were found to be 20 –25°C and 70 –80% relative humidity. Epidemic levels 
occurred when rainfall was low. Young leaves (up to three weeks following emergence) were 
most vulnerable to infection.   
 
However, if F. tingitaninum and E. quercicola  were to produce symptoms in post -entry quarantin e, the 
conidia produced during the growing season may not be contained in level 3 A:  
• If leafless budwood infected with overwintering mycelia of F. tingitaninum and E. quercicola, 
any conidia produced while in post-entry quarantine  may escape from the glasshouse 
between inspections of the plants. For level 3 A facilities , there are no requirements for 
measures to contain airborne, fungal spores (MPI 2019) .  
• Exposure of the pathogens to the New Zealand environment may then occur if sui table hosts 
are present near the post-entry quarantine  glasshouse, for example , if the facility is located 
near oak trees or a citrus orchard. However, the amount of inoculum likely to escape is small , 
and the conidia would have to land on a suitable host under suitable conditions to germinate 
and cause disease. The likelihood of this occurring is rated very low.  
• Other measures in place within level 3 A glasshouses (including protective clothing  and hand 
washing) (MPI 2019)  would reduce the likelihood of any spores/conidia leaving the glasshouse 
due to human activity, and then potentially transferring to a suitable hosts , to a very low level.  
5.5.5  Risk assessment: l ikelihood of establishment and spread  
 
The current distribution of F. tingitaninum and E. quercicol a causing disease on Citrus spp. is difficult 
to determine . 
• Much of this difficulty is d ue to the large number of synonyms for the powdery mildew 
pathogens, as well as the confusion in the literature between E. quercicola  and F. tingitaninum 
(DROPSA undate d). Furthermore, many records did not list the species in question and either 
referred to generic ‘powdery mildew’ or Oidium spp. 
• Table 8 gives  the distribution information for citrus powdery mildew found during the review of 
the literature. Many sources did not give the specific fungal species causing the disease or the 
host it  was found on.  
• Literature where the specific fungal species causing powdery mildew of citrus was described 
is used for the assessment of establishment potential (Table 9). The reports of O. tingitaninum 
are restricted to a report from California, whereas E. quercicola is more widespread in both 
Asia and North America.  
• After examining many specimens of powdery mildew fungi , Boesewinkel (1981) suggested 
that disease caused by asexual F. tingitaninum only occurred in California and that all other 
specimens of citrus powdery mildew represented asexual E. quercicola  (Boesewinkel 1981, 
cited in de Jesús Yáñez -Morales  et al. 2009). This hypothesis is supported by Holford et al. 
(2010) , who identified the causative agent of citrus powdery mildew in Bhutan to be 
E. quercicola , rather than F. tingitaninum as previously reported. It is also representative of the 
recent lit erature, where the causative agent of citrus powdery mildew has been identified as 
E. quercicola  (Table 9).  56 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • The move towards more accurate diagnoses, based on molecular rather than morphological 
methods ( Limkaisang  et al. 2006), may mean that reports of F. tingitaninum in other countries 
are reclassified to E. quercicola.  
  
Table 8: Distribution of citrus powdery mildew, as described in the literature. Specific species and host information 
was not necessarily available. Sources: CABI (2020), DROPSA (undated), Thaung (2007), Holford et al. (2010), Ray 
(2017), Tam et al. (2016), Chung ( 2011), Reddy (2010), de Jesús Yáñez -Morales  et al. (2009)  
Continent/Region  Countries  
Asia Myanmar,  India, Taiwan, Viet  Nam, Bhutan, Cambodia, 
China, Hong Kong, Israel, Indonesia (Java, Sumatra), 
Malaysia, Nepal, Philippines, Sri Lanka, Timor -Leste  
Africa  Uganda  
North America  USA (California, Florida), Mexico  
Central America  Costa Rica, Guatemala, Panam a, Honduras  
South America  Brazil  
Caribbean  Antigua, Cuba  
Countries  in bold are countries  we have imported citrus nursery stock from (Quancargo 2020) . 
 
 
Table 9: Distribution of Fibroi dium tingitaninum and Oidium  citri (syn. Erysiphe quercicola ) on Citrus spp. based on 
records where the fungal species responsible was de scribed.   
Species  Continent  Country  Host  Reference  
Fibroidium 
tingitaninum (syn. 
O. tingitaninum ) North America  USA 
(California)  Citrus sp. (tangerine)  Boesewinkel 1981 
cited in de Jesús 
Yáñez -Morales  et al. 
(2009)  
Erysiphe quercicola 
(syn. O. citri ) Asia India  Citrus reticulata (Khasi mandarin)  Baiswar et al. (2015)  
Viet Nam C. reticulata (mandarin)  Tam et al. (2016)  
Bhutan  C. reticulata (mandarin), Citrus × 
insitorum  (Carrizo citrange), Citrus 
× limon  (Rangpur lime), Citrus × 
aurantium (Tsunokaori tangor)  Holford et al. (2010)  
Nepal  Citrus sp.  Pandey and Adhikari 
(2005 ) 
Myanmar  Citrus spp.  Thaung (2007 ) 
Malaysia  C. sinensis (orange)  Braun and Cook 2012 
cited in Tam et al. 
(2016 ) 
North America  Mexico  Citrus  × limon  (Rangpur lime)  de Jesús Yáñez -
Morales  et al. (2009 ) 
 
 
Both E. quercicola and F. tingitaninum are wind -transmitted  and mechanically transmitted:  
• No evidence was found of the fungi requiring a vector for transmission.  
• The fungal conidia that typify powdery mildew disease  are wind -dispersed  (Whiteside et al.  
1988 ). Movement of infected plant material  will spread the fun gi and spread can also occur 
within orchards via human activity ( conidia on clothing, equipment and vehicles) (B usiness  
Queensland 2019).  
• Therefore, if the fungi were to enter the New Zealand environment , there would be no barrier 
to spread , and they are likely to spread to other suitable hosts.  
 
Given the arguments and evidence below, the likelihood of E. quercicola  establishing 
in New Zealand is considered high, with low uncertainty.  
The fung us is described  causing powdery mildew of Citrus spp. in some regions with climatic similarity 
to New Zealand :  
• Of the countries/regions where E. quercicola is reported causing citrus powdery mildew ( Table 
8), four  have areas with a similar climate with the whole of New Zealand: Nepal (composite  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 57 match index (CMI) 0.4 ‒0.8), Bhutan (0.4 ‒0.7), India (0.4 -0.8) and Mexico (0.4 ‒0.8) (0.6 ‒0.8) 
(Phillips et al. 2018). The other countries (Myanmar, Indonesia, Viet  Nam and Malaysia) do 
not have a similar climate to New Zealand (CMI <0.7).  
• This suggests that there are regions of New Zealand where the fungi have the potential to 
establish, most likely warmer regions such as the north of the North Island (where most of the 
commercial citrus is grown) ( Plant & Food Research  2019).  
• High humidity favours the expression of powdery mildew disease (Agrois 1978).  
• Sastra -Hidayat (1992) found that the optimal condition s for conidial germination are 20 –25°C 
temperatures and 70 –80% relative humidity. Epidemic levels of citrus powdery mildew occur 
during periods of high relative humidity (Whiteside et al.  1988; Sastra -Hidayat 1992;  Timmer 
et al. 2003).  
• In Bhutan , powdery mildew caused by E. quercicola is found on C. reticulata in all growing 
regions and is a significant disease. It is most severe in the south of the country, where the 
climate is humid and sub -tropical. The disease is especially common in plant nur series, as 
well as overcrowded, shady and poorly vented plantations on valley floors (Holford et al. 
2010).  
• In Viet  Nam, citrus powdery mildew is most common in valley orchards in the north of the 
country between February and May (Tam et al. 2016); the tim e of year with the highest 
humidity, low rainfall and warm temperatures.  
• In New Zealand , citrus in mainly grown in areas with high humidity and warm summers 
(Chappell 2013a, b; Chappell 2016). The high humidity is likely to be suitable for E. quercicola 
to establish and for citrus powdery mildew disease development.  
 
The records of E. quercicola causing powdery mildew disease on Citrus spp. include countries with 
areas of climate similarity with New Zealand citrus -growing regions. Most commercial citrus o rchards 
are found in the north of the North island, with a warm and humid climate, which is likely to be suitable 
for establishment and disease expression. The presence of suitable host plants in a suitable 
environment means that the likelihood of establis hment is rated as high.  
 
Erysiphe quercicola has been reported from hosts other than Citrus spp. in countries with a similar 
climate to N ew Zealand : 
• Erysiphe quercicola  has been found causing oak powdery mildew all over France and 
successfully overwinters there. It is noted that milder win ters are favourable for the survival of 
the fungus ( Marçais  et al. 2017). Many Quercus spp. (oaks) are fully naturalised in 
New Zealand ( Allan Herbarium  2020) , and there is a high climate similarity between Fra nce 
and the generalised climate  of New Zealand (CMI 0.9) (Phillips et al. 2018). Th e fungus has 
the potential to establish and overwinter in the New Zealand , as suitable host plants are widely 
available and the climate is suitable.  
• The fungus was identifi ed as one of the causative agents of powdery mildew of Mangifera 
indica (mango) in the Malaga region of Spain (Desprez -Loustau et al. 2017). Erysiphe 
quercicola was isolated from 97% of the 140 samples tested, from six different orchards. 
Although mango is  not commonly grown in New Zealand, this report further suggests that the 
climate in New Zealand is suitable for establishment of E. quercicola , as the Malaga region 
has a high climate similarity with New Zealand (CMI 0.8)  (Phillips et al. 2018) .  
Based on  the reports of E. quercicola causing disease in a range of countries with climatic 
similarity to New Zealand (particularly France and Spain , which are highly similar) , as well as the 
reports of the fungus affecting multiple hosts, citrus and oak being rel evant for New Zealand, the 
likelihood of E. quercicola establishing in New Zealand is rated as high.  
 
Given the arguments and evidence below, the likelihood of F. tingitaninum 
establishing in New Zealand is considered  moderate, with low uncertainty.  
The host range of F. tingitaninum is restricted to Citrus spp. and may only be present in California . 
• It has been suggested that F. tingitaninum is restricted to California ( Boesewinkel 1981, cited 
in de Jesús Yáñez -Morales  et al. 2009) . This is supported in recent literature, where asexual 
E. quercicola has been identified as the causative agent of citrus powdery mildew in many 
countries ( Table 8), including where the causative agent has previously been identified as 
asexual F. tingitaninum (Holford et al. 2010).  58 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • California has a similar climate to New Zealand (CMI 0.6 –0.8), which suggest s that at least 
some regions of New Zealand would h ave a climate suitable for establishment, most likely in 
the warmer regions such as the north of the North Island (where most of the commercial citrus 
is grown) ( Plant and Food Research  2019).  
• The species may also occur in Florida (Chung 2011) (CMI 0.5 –0.7). 
• Although present in California, citrus powdery mildew disease caused by the asexual form of 
F. tingitaninum only occurs occasionally (Whiteside et al. 1988).  
• As described above, some of the citrus -growing regions of New Zealand experience high 
humidit y, which favours powdery mildew disease.  
• No records of F. tingitaninum on hosts other than Citrus spp. were found in the literature.  
Fibroidium  tingitaninum is reported from California, which has climatic similarity with New Zealand. 
However, d ue to the restricted host and geographical range, the likelihood of establishment is rated 
moderate.  
 
  
5.5.6  Risk assessment: impacts to New Zealand  
 
Given the arguments and evidence below , the introduction of  E. quercicola is 
considered likely  to cause modera te economic impacts for New Zealand , with low 
uncertainty . 
Erysiphe quercicola has been reported causing significant yield losses in Citrus spp. 
• Erysiphe quercicola has been reported from a range of Citrus spp. ( Table 8). Citrus reticulata 
(mandarin) and C. sinensis (sweet orange) are commonly grown commercial species in 
New Zealand (section 2.6). Therefore, impacts to these species have the potential to cause 
consequences of economic significance.  
• Mycelia growth of asexual E. quercicola is described as dense , “covering leaves with a  thick, 
white coating ” (Petch 1945 cited in Holford et al. 2010). Growth occurs on both the upper and 
lower leaf surface and can cause dieback and defoliation (Holford et al. 2010). Such 
symptoms reduce the productivity, yield and fruit quality (Holford et  al. 2010).  
• In Viet  Nam, the mycelium of E. quercicola was found covering  young leaves and fruit of 
Citrus reticulata (Tam et al. 2016). The affected young fruit dropped prematurely and resulted 
in up to 80% yield loss (Gupta and Gupta 1992; Tam et al. 20 16). 
• Severe powdery mildew infection can be debilitating for the relevant trees (Timmer et al. 
2003).  
• Such yield losses would have significant economic consequences to the affected growers. 
Furthermore, the rapid expression and spread of the disease (see l ife cycle section) would 
mean that during seasons of suitable conditions , losses are likely to occur in whole orchards.  
Disease expression is likely to be limited to regions of New Zealand where citrus is grown and 
which experience periods of high humidity  and moderate temperatures. Therefore, economic 
impacts to individual affected growers and the wider community in such areas may be significant. 
The impact for the citrus industry, at least in years with weather conditions that facilitate disease, 
may be s ignificant. Therefore, the likelihood of the fungus causing economic impacts is rated 
moderate.   
 
 
Given the arguments and evidence below , the introduction of F. tingitaninum is 
considered likely  to cause  low economic impacts for New Zealand , with low 
uncertainty . 
The fungus appears to be restricted to causing occasional disease on citrus in California:  
• Boesewinkel (1981) proposed that E. quercicola, rather than F. tingitaninum , is the major 
cause of citrus po wdery mildew worldwide ( Boesewinkel 1981, cited in de Jesús Yáñez -
Morales  et al. 2009; Holford et al. 2010).  
• Although present in California, citrus powdery mildew disease caused by the asexual form of 
F. tingitaninum only occurs occasionally (Whiteside et  al. 1988).   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 59 • The mycelium of the of F. tingitaninum are described as initially being sparse and then 
becoming denser but never felt -like in appearance. Mycelial growth arises on the upper 
surface of young leaves, causing leaf deformation but little other d amage (Carter 1915 , cited 
in Holford et al. 2010).  
• Yield or crop loss specifically attributed to F. tingitaninum was not found in the literature.  
• Based on the literature , the host range of the fungus is restricted to Citrus spp.  
It has been suggested tha t F. tingitaninum is limited to California, where it causes occasional disease. 
The restricted host range, distribution and the limited accounts of disease caused by the fungus mean 
that the likelihood of F. tingitaninum causing economic impacts in New Zea land is rated low.  
 
 
Given the arguments and evidence below , the introduction of F. tingitaninum or 
E. quercicola  is considered likely  to cause low sociocultural impacts in New Zealand , 
with low uncertainty . 
The fungi may cause impacts for home gardeners who grow Citrus spp. in areas of the country where 
environmental conditions are suitable . 
• As mentioned in the section above, citrus powdery mildew causes symptoms that would 
reduce the productivity and yield o f citrus trees for home gardeners.  
• However, such impacts would be restricted to gardeners in the limited regions of the country 
with suitable environmental conditions.   
   
Quercus spp. are hosts of Erysiphe quercicola . However , the level of impact is lik ely to be negligible:  
• Oaks are grown in New Zealand for timber and as an amenity or forage crop (Halliwell 1979; 
Horizons Regional Council 2017 ; NZWood undated ). 
• The host range of E. quercicola is not restricted to a narrow group of plant taxa and is reported 
from a range of woody trees, including Quercus spp. (oaks) (Takamatsu et al. 2007; Gautam 
2015; Meeboon and Takamatsu 2020).  
• Erysiphe quercicola causes foliar symptoms, indistinguishable to those caused by another oak 
powdery mildew E. alphitoides (Marçais  et al. 2017). Erysiphe alphitoides is present in 
New Zealand on Quercus spp. (NZFungi 2020).  
• Although E. alphitoides is described as causing significant impact to plants at a foliar level, it is 
not usually considered a problem beyond the individual plant level ( Marçais  and Desprez -
Loustau 2014). Therefore, it can be assumed that although E. quercicola may cause unsightly 
symptoms on the leaves, it is unlikely to have significant consequences f or the trees. 
Furthermore, the impacts are unlikely to be above those already caused on Quercus spp. in 
New Zealand by E. alphitoides.  
• No evidence was found in the literature of F. tingitaninum affecting hosts other than Citrus 
spp. Therefore, the fungus appears to have a restricted host range , and it does not appear 
that this species would have any consequences on other hosts.  
There are reports of the powdery mildew fungi causing foliar and fruit symptoms, as well as significant 
yield losses. However, the se are likely to be restricted to certain areas of New Zealand and may only 
occur sporadically during years of suitable climatic conditions and are therefore rated low.  
 
Given the arguments and evidence below , the introduction  F. tingitaninum or 
E. quercic ola is considered  likely to cause very low  environmental impacts in 
New Zealand , with low uncertainty . 
• The asexual form of Erysiphe quercicola  has been isolated from a range of tree hosts , in 
multiple plant families  (Siahaan et al. 2016; Meeboon and Takamatsu 2020). As the fungus 
has a broad host range,  it may be that it could infect environmental species, including native 
species present in New Zealand.  
• However, such reports are from tropical regions, where citrus powdery disease is most 
prevalent, and the fungi are therefore unlikely to occur in the New Zealand environment, 
except in some restricted areas with sufficiently warm temperatures and high humidity.   
• Fibroidium tingitaninum appears to have a restricted h ost range , as no evidence was found of 
the species affecting hosts other than Citrus spp. As there are no native Citrus spp. in 60 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  New Zealand  (Allan Herbarium  2020), the likelihood of F. tingitaninum having environmental 
consequences in New Zealand is  very low.  
 
Given the arguments and evidence below , the introduction of  F. tingitaninum or 
E. quercicola  is considered likely  to cause negligible  human health impacts in 
New Zealand , with low uncertainty . 
Powdery mildews are not known to pose risks to human health:  
• No evidence was found of these fungi, or other powdery mildew fungi, causing human health 
issues.  
 
5.5.7  References  
Agriculture Victoria (undated) Powdery mildew of apples. http://agriculture.vic.gov.au/agriculture/pests -
diseases -and-weeds/plant -diseases/fruit -and-nuts/pome -fruit-diseases/powdery -mildew -of-apples  
Accessed 8  July 20 20. ISSN: 13298062  
Agrios, G N (1978) Plant Pathology . Second  edition. Academic Press.  
Allan Herbarium (20 21) Ngā Tipu o Aotearoa – New Zealand Plant Names Database. Landcare 
Research; NZ. https://nzflora.landcareresearch.co.nz . Accessed 4  August 2020.  
Baiswar, P; Ngachan, S V; Rymbai, H; Chandra, S (2015) Erysiphe quercicola , a powdery mildew 
fungus on Khasi mandarin in North East India.  Australasian Plant Disease Notes , 10(1): 30.  
Biosecurity Queensland (2011) Citrus powdery mildew. 
https://www.daf.qld.gov.au/__data/assets/pdf_file/0006/65166/Citrus -Citrus -powdery -mildew.pdf  
Accessed 26 June 20 20. 
Boesewinkel, H J (1981) The identity of powdery mildew of Citrus . Nova Hedwigia , 34: 731 –741. 
BRAD (2020) Internal MPI database. Accessed 26  June 2020 . 
Brazee N J (2019) Powdery Mildew. University of Massachusetts Amherst. 
https://ag.umass.edu/landscape/fact -sheets/powdery -mildew  Accessed 26  June 2020  
Braun, U; Cook, R T A (2012) Taxonomic Manual  of the Erysiphales ( Powdery Mildews ). CBS 
Biodiversity Ser ies, No. 11. CBS; Utrecht, Netherlands.  
Business Queensland (2019) Citrus Powdery mildew. 
https://www.bu siness.qld.gov.au/industries/farms -fishing -forestry/agriculture/crop -growing/priority -
pest-disease/citrus -powdery -mildew  Accessed 26  June 2020 . 
CABI (2020) https://www.cabi.org/cpc  Accessed 23  July 2020 . 
Carter, C N  (1915) A powdery mildew on citrus. Phytopathology, 5: 193–196.  
Chappell, P R (2013a) The climate and weather of Northland. NIWA Science and Technology Series 
59. 
Chappell, P R (2013b) The climate and weather of Auckland. NIWA Science and Technology Series  
60. 
Chappell, P R (2016) The climate and weather of Gisborne. NIWA Science and Technology Series 70. 
Chung, K R (2011) Citrus diseases exotic to Florida: Powdery mildew. University of Florida IFAS 
extension. https://ufdcimages.uflib.ufl.edu/IR/00/00/49/95/00001/PP28800.pdf  (26/6/20)   
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Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 63 5.6 Lasiodiplodia  species associated with disease of Citrus trees  
 
Members of the fungal genus Lasiodiplodia  are opportunistic pathogens and are reported causing 
stem -end rot, fruit rot, tree canker, root and collar rot of a range of hosts plants  including Citrus spp. 
 
Taxonomy  
Scientific name: Lasiodiplodia brasiliensis  Netto et al. (2014)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found   
Notes: Phylogenetically , L. brasiliensis is closely related to L. viticola but is differentiated by unique 
fixed alleles at one locus as well as by the conidia of L. brasiliensis being longer and wider (Netto et al. 
2014). The fungus was first reported from Carica papaya  (papaya) with stem -end rot in Brazil 
(collected in 2007) and later  from Mangifera indica (mango) collected in 2010 (Netto et al. 2014). 
Since the first report, the fungus has been isolated from a wide range of countries and multiple hosts 
including Citrus latifolia (Persian lime) in Mexico ( Bautista -Cruz et al. 2019).    
 
Scientific name: Lasiodiplodia citricola  Abdollahzadeh et al. (2010)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found   
Notes: Phylogenetically , L. citricola is closely related to L. parva, although the former produces longer 
and wider conidia ( Abdollahzadeh et al. 2010) . The fungus was first reported from Citrus sp. in Iran 
(Abdollahzadeh et al. 2010) and has since been reported from a broad range of hosts and locations , 
including Juglans regia (European walnut) and Prunus persica  (peach) in California (Chen et al. 
2013a; Chen et al. 2013b), Citrus latifolia (Persian lime) in Mexico ( Bautista -Cruz et al. 2019) and Vitis 
vinife ra (grapevine) in Australia (Burgess et al. 2019).  
 
Scientific name:  Lasiodiplodia hormozganensis  Abdollahzadeh et al. (2010)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found   
Notes: Phylogenetically , L. hormozganensis is closely related to L. citricola and L. parva  but can be 
distinguished based on the dimensions of conidia and paraphyses (Abdollahzadeh et al. 2010) . The 
fungus was first reported from diseased mango and Olea  sp. (olive) in Iran ( Abdollahzadeh et al. 
2010 ) and has since been reported from multiple hosts and countries , including  Citrus spp. in Oman 
(Al-Sadi et al. 2013 ).  
 
Scientific name: Lasiodiplodia  iraniensis  Abdollahzadeh et al. (2010)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found   
Notes: This species is clearly distinct from the other Lasiodiplodia species but is  most closely related 
to L. theobromae (Abdollanhzadeh et al. 2010) . The fungus was first described from mango, Citrus 
sp., Eucalyptus  sp., Salvadora persica  (kharijal), Terminali a catap pa (country almond)  and Juglans sp. 
(walnut) in Iran ( Abdollahzadeh et al. 2010) . It has also been reported from  Citrus spp. in Oman  (Al-
Sadi et al. 2013) .  
  
Scientific name: Lasiodiplodia  mediterranea  Linaldeddu et al. (2015)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found  
Notes: Lasiodiplodia  mediterranea  is phylogenetically closely related to L. pseudotheobromae but 
differentiated by the shape and size of the conidia  and the paraphyses ( Linaldeddu et al. 2015 ). The 
fungus has been reported from Citrus sinensis (orange)  in Algeria a s well as grapevine and Quercus 
ilex (holm oak)  in Italy (Sardinia ) (Linaldeddu et al. 2015)  and Vaccinium corymbosum  (blueberry)  in 
the USA (Wiseman et al. 2017).  
 
Scientific name: Lasiodiplodia mitidjana Berraf -Tebbal et al. (2020 )  
Order/Family: Botryosphaeriales/Botryosphaeriaceae  64 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Synonyms: None found   
Notes: The species is phylogenetically very closely related to L. citricola, being distinguished based 
on the s ize of the conidia  (Berraf -Tebbal et al. 2020).  The fungus has been reported from diseased  
orange trees in Algeria ( Berraf -Tebbal et al. 2020).  
 
Scientific name: Lasiodiplodia pseudotheobromae  Alves et al. (2008)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms: None found   
Notes: This fungus w as identified as a cryptic species36 of L. theobromae based on ITS and EFI -α 
sequence analysis  and was first described from samples previously identified as L. theobromae , 
including one from Citrus aurantium (bitter orange) in Suriname (Alves et al. 2008). The fungus has 
now been isolated from numerous hosts and countries including grapevine and bl ueberry  in Australia 
(Burgess et al. 2019)  and causing post -harvest fruit rot of Citrus limon (lemon) in Turkey (Awan et al. 
2016).  
 
Scientific name: Lasiodiplodia subglobosa Machado et al. (2014)  
Order/Family: Botryosphaeriales /Botryosphaeriaceae  
Synonyms : None found   
Notes: Described following phylogenetic analysis (ITS and EFI -α sequences) of fungal isolates from 
Jatropha carcas  trees with collar and root rot disease  in Brazil.  Compared to the other species , there 
were not many reports beyond the first identification. The fungus has been reported from diseased 
Citrus latifolia (Persian lime)  in Mexico (Bautista -Cruz et al. 2019 ).  
 
The species of Lasiodiplodia  identified as associated with disease of Citrus trees are  considered 
together for the commodity association and entry sections, as , based on the literature , there is little 
difference between the species for these sections. In the establishment and economic impacts 
sections , they are assessed separately. Many of these species are newly described , and there is very 
limited literature available, resulting in high uncertainty associated with several of the conclusions.  
 
5.6.1  Summary of conclusion s 
 
Summary t able 2: Summary of conclu sions for the identified Lasiodiplodia spp.  
Species   Criteria  
Entry  Establishment  Economic 
impacts  Socio -
cultural 
impacts  Environmental 
impacts  Human 
health 
impacts  
Lasiodiplodia brasiliensis  Rating  low low moderate  low low very low  
Uncertainty  high low high low high low 
Lasiodiplodia citricola  Rating  low high low low low very low  
Uncertainty  high low high low High  low 
Lasiodiplodia hormozganensis  Rating  low low moderate  low low very low  
Uncertainty  high low high low high low 
Lasiodiplodia iranensis  Rating  low moderate  low low low very low  
Uncertainty  high high high low high low 
Lasiodiplodia mediterranea  Rating  low high moderate  low low very low  
Uncertainty  high high low low high low 
Lasiodiplodia mitidjana  Rating  low moderate  low low low very low  
Uncertainty  high high high low high low 
Lasiodiplodia pseudotheobromae  Rating  low moderate  high low low very low  
Uncertainty  high moderate  moderate  low high low 
Lasiodiplodia subglobosa  Rating  low moderate  low low low very low  
Uncertainty  high low high low high low 
 
The identified Lasiodiplodia spp. may be considered for additional measures.  
 
 
36 ‘Cryptic species’ refers to a species that cannot easily be distinguished from another based entirely on morphology. However,  
molecular marker analysis shows that the species forms a distinct phylogenetic lineage.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 65 5.6.2  Hazard identification: quarantine pest  status  
Given the arguments and evidence below, t he identified Lasiodiplodia species meet 
the criteria to be quarantine pests for New Zealand . 
Criteria for being a regulated quarantine pest relevant to this assessment are: the pest is not present 
in the pest risk assessment  area (New Zealand) and is of p otential importance (able to establish and 
cause harm37). 
 
The identified Lasiodiplodia spp. are not known to be present in New Zealand . 
• Lasiodiplodia pseudotheobromae is listed as absent (NZFungi 2 2020) and is not recorded in 
PPIN (2020). There is no reco rd for the species in ONZPR (2020) or BRAD (2020).  
• Lasiodiplodia brasiliensis, L. citricola, L. hormozganensis, L. iraniensis, L. mediterranea, 
L. mitidjana and L. subglobosa are not listed in NZFungi 2 (2020), PPIN (2020), BORIC (2020) 
or BRAD (2020).  
 
The identified Lasiodiplodia spp. have the potential to establish in New Zealand . 
• The assessed Lasiodiplodia species have been reported from countries with a similar climate 
to, or regions with, a similar climate to New Zealand (including Australia, Italy, Algeria and 
Mexico) ( Table 10).  
• The species have been isolated from hosts commonly grown in New Zealand, both 
commercially and by home gardeners (inc luding Citrus spp., Rosa sp., Solanum melongena 
(eggplant), Malus spp. (apples), Vitis vinifera (grapevine), Prunus persica (peach), Eucalyptus 
sp. and Vaccinium corymbosum (blueberry) . See Table 10.  
• Therefore, suitable host plants in suitable environmental conditions are likely to be present to 
support establishment.  
 
The identified Lasiodiplodia spp. have the potential to cause economic and sociocultural 
consequences b y causing disease on citrus and other hosts:  
• The assessed Lasiodiplodia spp. have all been described as associated with disease of Citrus 
spp. ( Bautista -Cruz et al. 2019; Al -Sadi et al. 2013; Berraf -Tebbal et al. 2020 ). Disease 
symptoms associated with the se fungi on Citrus spp. are described as gummosis, stem/trunk 
canker and branch dieback ( Table 10). 
• Citrus is an important commercial crop for New Zealand and is commonly grown by home 
gardeners (section 2.6). Therefore, symptoms reducing the longevity or production  of the plant 
has the potential to cause both economic and social consequences.  
• Lasiodiplodia brasiliensis, L. citricola, L. hormozganensis  and L. pseudotheobromae have 
been associated with diseased grapevines (Carlucci et al. 2015;  Dissanayake et al. 2015 ; 
Correia et al. 2016 ). Wine represents New Zealand’s second largest horticultural export, with a 
value of $1 .8 billion ( Plant and Food Research  2019).  
 
5.6.3  Hazard identification: commodity association  
Given the arguments and evidence below, the association of  the identified 
Lasiodiplodia spp. with leafless Citrus budwood  is considered strong, with low 
uncertainty . 
 
All the assessed Lasiodiplodia spp. have been isolated from aboveground plant parts of Citrus spp. 
• All the assessed Lasiodiplodia spp. infect aboveground plant parts including the trunk, 
branches and fruit (Abdollahzadeh et al. 2010; Bautista -Cruz et al. 2019; Berraf -Tebbal et al. 
2020).  
• The fungi are opportunistic and enter hosts via wounds and natural openings such as 
lenticels and stomata ( Slippers and Wingfield 2007 ). Therefore, there are no barriers as to 
which tissues the fungi may infect.  
• The related species L. theobromae causes fruit stem -end rot in multiple crop species , 
including avocado, mango and citrus, by growing into the fruit ste m from the branches 
 
37 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for fact ors to consider 
when defining “harm”.  66 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  (Queensland Dept. of Agriculture and Fisheries 2018). Al -Sadi et al. (2013) also reported 
dieback and gummosis of acid lime ( C. aurantifolia ) in Oman (and sweet lime , location 
unspecified).  
• It is considered that all members of the Botryosphaeriaceae  have an endophytic phase 
(Slippers and Wingfield 2007 ). Therefore, the fungi may be associated with material used for 
budwood without causing symptoms.  
• The Botryosphaeriaceae overwinter as pycnidia in diseased woody plant parts and in woody  
plant debris ( Úrbez -Torres  2013 ). Other endophytic fungi overwinter within their host plant 
(Dutta et al. 2014).  
• There are reports of the fungi causing disease of Citrus in nine countries around the world 
(Table 10).  
 
5.6.4  Risk assessment : likelihood of entry  
 
Given the arguments and evidence below, the  likelihood of any one of the assessed 
Lasiodiplodia spp. entering New Zealand associated with  leafless Citrus budwood  is 
considered  low, with high uncertainty . 
 
Individually , the Lasiodiplodia  spp. have a moderate association with Citrus budwood:  
• All the assessed Lasiodiplodia spp. have been isolated from above ground plant parts of 
Citrus spp. ( Table 10). They are opportunistic pathogens and can infect any part of the plant 
through wounds or natural openings (Slipper and Whiteside 2017).  
• Botryosphaeriacea e cause asymptomatic infections of hosts (Slipper and Whiteside 2017). In 
mango , the related species L. theobromae has been found to occur endophytically in stem 
tissue (Johnson et al. 1992). Although there are no published papers confirming that the 
assessed Lasiodiplodia spp. have an asymptomatic phase, the re has not been any work 
testing asymptomatic tissue. Therefore, there is the potential for infected material to 
unknowingly be used for budwood production.   
• There are no records of citrus nursery stock being imported to New Zealand from the 
countries where the identified Lasiodiplodia spp. have been reported on Citrus spp.38 (Table 10) 
(Quan Cargo 2020). Therefore, current tr ade patterns suggest that material is unlikely to be 
sourced from countries where the fungi occur on citrus. However, trade from further countries 
cannot be ruled out in the future.  
• Some of the Lasiodiplodia spp. (L. brasiliensis, L. citricola, L. hormozganensis, L. iranensis, 
L. mediterranea and L. pseudotheobromae)  have been reported from countries where citrus 
nursery stock has been imported (USA ) (Wiseman et al. 2017) , but from hosts other than 
Citrus  spp.  
• Lasiodiplodia pseudotheobromae has been most frequently reported from citrus hosts (Table 
6.5) and  has the strongest association with leafless citrus budwood of the assessed species.   
The minimum requirements reduce the likelihood of entry as Lasiodiplodia spp. to a moderate degree, 
with high uncertainty:  
• Visual inspection of budwood and the mother plants is likely to detect symptomatic material.  
• Symptoms that develop within post -entry quarantine would also be determined.  
• The environmental conditions require d for disease expression of the Lasiodiplodia species are 
not currently reported in the literature.  
• The time between host plant infection and disease expression of naturally infected host s in the 
field was not reported in the literature. In the pathogenici ty tests described below, the 
symptoms developed in less than one growing season.   
• The fungi have successfully induced symptoms on citrus in pathogenicity tests:  
o Bautista -Cruz et al. (2019) tested the pathogenicity of L. subglobosa, L. iraniensis, 
L. pseu dotheobromae, L. theobromae, L. brasiliensis and L. citricola on C. latifolia 
(Persian lime). The assays were conducted on 18 -month -old plants that were wound -
inoculated with a mycelial plug. The plants were covered with plastic to maintain 
 
38 Mexico, Iran, Oman, Algeria, Suriname, Turkey, Bangladesh, Pakistan, Puerto Rico   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 67 humidity for th ree days following inoculation and maintained in a glasshouse under 
natural light conditions. The temperature was maintained at 30 ±5°C. After 30 days 
under these conditions, all species tested produced gum exudation and lesions.  
o Ahmed et al. (2020) used ar tificial inoculations to fulfil Koch’s postulates of 
L. pseudotheobromae on C. reticulata (mandarin) . One-year-old plants were 
wounded, inoculated with a mycelial plug and sealed with parafilm. The plants were 
incubated at 25 ±2°C under greenhouse conditions. After five weeks , symptoms of 
gum exudation and bark cankers were observed.  
o Plants in post-entry quarantine are held at temperatures between 18 –25°C (MPI 
Standard 155.02.06). Therefore, conditions within the post-entry quarantine  
glasshouses ma y be suitable for disease expression . However , this is not certain.  
• Other members of the Botryosphaeriacea e cause asymptomatic infections of hosts and only 
induce disease under stress conditions (Slipper and Whiteside 2017). In mango , the related 
species L. theobromae has been found to occur endophytically in stem tissue (Johnson et al. 
1992). Due to a wide range of such examples, it is believed  that all the Botryosphaeriaceae  
experience an endophytic phase (Slippers and Wingfield 2007). No records were fo und in the 
literature of the assessed Lasiodiplodia spp. being associated with asymptomatic infection . 
However , the studies found all look ed at symptomatic material.  
• The minimal requirements have the potential to reduce the likelihood of entry if the fungi 
produce visible symptoms, but not for endophytic fungi.  
 
There is high uncertainty associated with this conclusion, and the likelihood of entry may in fact be 
highe r. As these are emerging pathogens, the literature is currently limited , and many of the reports of 
the fungi from citrus have been made in recent years. Furthermore, there is the potential for these 
fungi to infect hosts endophytically, as is the case for  other B otryosphaeriacea e, including 
L. theobromae  (Johnson et al. 1992) . However , there are no reports of the assessed species occurring 
as endophytes. If evidence become s available, the risk w ill need to be reassessed.   
 
5.6.5  Risk assessment: l ikelihood of establishment and spread  
 
Given the arguments and evidence below, t he likelihood of L. brasiliensis 
establishing in New Zealand is considered  low, with low uncertainty . 
• Of the 10 records of L. brasiliensis found in the literature, eight are fr om regions with poor 
climate similarity to New Zealand (CMI  <0.7), with the other two from regions with low 
similarity (CMI 0.5 –0.8) (Table 10).  
• Burgess et al. (2019) d ivided Australia into climate zones based on temperature and humidity 
and matched the locations where Lasiodiplodia spp. have been isolated in Australia to these 
climate zones. A comparison  of these climate zones with the New Zealand climate (Phillips et 
al. 2018)  suggests that the New Zealand climate is unlikely to be suitable for the 
establishment of L. brasiliensis . 
• The reported host range of the fungus includes tropical plants not grown in New Zealand 
(such as Dimocarpus longan (longan), papaya and mango ). 
• There are three records of the fungus from plants commonly grown commercially or by home 
gardeners (grapevine, a pple, Persian lime) ( Table 10). New Zealand has 8,615 ha of a pple 
trees  and 33,981 ha of grape vines  (Plant and Food Research  2019). Apple trees and 
grapevines can both  support establishment . However , they are unlikely to be present in a 
suitable climate.   
• Due to the poor climate similarity between New Zealand and where the species has been 
reported as well as the mostly tropical host range , the likelihood of establishment is 
considered low.   
 
Given the arguments and evidence below, t he likelihood of L. citricola establishing in 
New Zealand is considered  high, with low uncertainty . 
• All records of L. citricola found in the literature are from  countries with some climate overlap 
with New Zealand (CMI  >0.7), including some regions with high similarity (Italy CMI 0.8 –0.9; 68 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Australia CM I 0.7–0.9) ( Table 10). This  suggests that regions of New Zealand would have a 
climate suitable for establishment.  
• Burgess et al. (2019) divided Australia into climate zones based on temperature and humidity 
and matched the locations where Lasiodiplodia spp. have been isolated in Australia to these 
climate zones. The Australian climate zones where the fungus is present  have a strong 
similarity to all of New Zealand (Phillips et al. 2018), which  suggests that there are regions  of 
New Zealand suitable for e stablishment of L. citricola . 
• The current ly reported host range of L. citricola represent s plants that are all grown in 
New Zealand, including the commercial crops grape, peach and citrus ( Table 10). Grapes in 
particular have a large commercially planted area of 33,981  ha (Plant and Food Research  
2019). Such plants are also commonly  grown by home gardeners.  
• Lasiodiplodia citricola has also been reported from Juglans reg ia (European walnut) Chen et 
al. (2013a) , which is fully naturalised in New Zealand ( Allan Herbarium 2020).  
• Due to the high climate overlap between the reported geographic range of the species and 
New Zealand, as well as the abundance of suitable host s in New Zealand , the likelihood of 
establishment is considered  high.   
 
Given the arguments and evidence below, t he likelihood of L. hormozganensis 
establishing in New Zealand is considered low, with low uncertainty   
• The geographic distribution of L. hormozganensis does not represent countries with a similar 
climate to New Zealand (CMI  <0.7), with most records from Asia and the Caribbean ( Table 10).    
• Burgess et al. (2019) divided Australia into climate zones based on temperature and humidity 
and matched the locations where Lasiodiplodia spp. have been isolated in Australia to these 
climate zones. A comparison of  these climate zones  with the New Zealand  climate  (Phillips et 
al. 2018) suggests that the New Zealand climate is unlikely to be suitable establishment of 
L. hormozganensis . 
• The host range of the species is largely tropical p lants that are  not present in New Zealand, 
including crop plants such as Phoenix dactylifera (date palm), Mangifera indica (mango), 
Dimocarpus longan (longan) and Carica papaya  (papaya) as well as environmental species 
Adansonia spp. (see Table 10). However, the host range does include Vitis vinifera (grapevine) , 
Solanum melongena (eggplant)  and C. sinensis (sweet orange), which are common crop 
species in  New Zealand.  
• The tropical distribution and tropical plant host range suggests that the likelihood of 
L. hormozganensis establishing in New Zealand is low.  
 
Given the arguments and evidence below,  the likelihood of L. iranensis establishing 
in New Zealand is considered  moderate, with high uncertainty . 
• The reports of L. iranensis found in the literature include reports from regions with climate 
overlap with New Zealand (CMI  ≥0.7) as well as from areas with poor climate similarity (CMI  
<0.7) ( Table 10). 
• This suggests that although there may be regions in New Zealand that have a suitable climate 
for establishment, these are likely to be limited and  most likely restricted to the warmer areas 
of New Zealand, such as the northern regions of the North Island.  
• Burgess et al. (2019) divided Australia into climate zones based on temperature and humidity 
and matched the locations where Lasiodiplodia spp. h ave been isolated in Australia to these 
climate zones. A compari son of  these climate zones with the New Zealand climate  (Phillips et 
al. 2018) suggests that the New Zealand climate is unlikely to be suitable establishment of 
L. iranensis . 
• The current reported host range of L. iranensis includes many tropical species that are not 
grown in New Zealand ( Table 10). However, it does include plants commonly gro wn both 
commercially and by home gardeners, including Eucalyptus sp., grapevine, olive, Citrus sp. 
(see table). Grapes in particular have a large area planted for commercial production (33,981 
ha) as well as olives (921 ha) ( Plant and Food Research  2019).    
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 69 • Based on the reports of the species from areas with climate overlap and from hosts commonly 
grown in New Zealand , the likelihood of establishment is rated as moderate. Establishment 
would be restricted to warmer regions of New Zealand.  
• However, there is high uncertainty associated with this conclusion. The related species 
L. theobromae is present in New Zealand but has not thrived (NZFungi 2 2020). Furthermore, 
the most frequently reported hosts of the species are tropical plant s, and it is not clear how 
important species such as grapevine and olive are for L. iranensis.  
 
Given the arguments and evidence below, t he likelihood of L. mediterranea 
establishing in New Zealand is considered  high, with low uncertainty . 
• This species has been reported in three locations, all of which have climatic similarity to 
New Zealand: Italy (CMI 0.8 –0.9), Oregon , USA  (CMI 0.7 –0.8), north of Algeria (Oued El 
Alleug and Boufarik) (CMI of 0.7 ) (Table 10).   
• This suggests the New Zealand climate is suitable for the  establishment of the species.  
• As well as C. sinensis, L. mediterranea  has been reported from grapevine and blueberry , 
which are commercially grown in New Zealand ( Plant and Food Research  2019). Grapes in 
particular have a large commercially planted area (33,981 ha in 2017) ( Plant and Food 
Research  2019). It has also been isolated from holm oak ( Linaldeddu et al. 2015) , which is 
fully naturalised in New Zealand ( Allan Herbarium 2020). Therefore, suitable hosts are likely to 
be present in suitable conditions to support establishment.  
 
Given the arguments and evidence below, t he likelihood of L. mitidjana establishing 
in New Zealand is  considered moderate, with high uncertainty .   
• As this fungus has only recently been described, there is only one record of this fungus in the 
literature —from C. sinensis in Algeria ( Berraf -Tebbal et al. 2020) . The fungus was reported 
from the north of the  country (Oued El Alleug and Boufarik), which has a CMI of 0.7 with 
New Zealand ( Table 10). This suggests that although  there are likely to be regions of 
New Zealand suitable for establishment, these are likely to be limited and are most likely the 
warmer regions of New Zealand (su ch as the north of the North Island).  
• Citrus crops are mostly grown in the warmer regions of New Zealand (section 2.6) and 
therefore suitable hosts may be present in suitable conditions for establishment.  
• Based on the current information, the likelihood of establishment is rated as moderate, as 
although the climate suggests some regions of New Zealand may be suitable, the host range 
is limited to C. sinensis . There is high uncertainty due to the lack of literature. As this is a 
recently reported pathogen , new information (such as through the emerging risk  system) may 
mean that the risk needs to be reassessed.  
 
Given the arguments and evidence below, t he likelihood of L. pseudotheobromae 
establishing in New Zealand is considered moderate, with moderate uncertainty . 
• The reports of L. pseudotheobromae found in the literature include reports from regions with 
climate overlap with New Zealand (CMI  ≥0.7) as well as from areas with poor climate similarity 
(CMI  <0.7) ( Table 10). There is a record on Rosa sp. from the Netherlands but based on the 
knowledge of how these plants are grown in the Netherlands (Alves et al. 2008), this may be 
from a glasshouse.  
• This suggests that although there may be regions in New Zealand that have a suitable climate 
for establishment, these are likely to be limited and most likely restricted to t he warmer areas 
of New Zealand, such as the northern regions of the North Island.  
• This is supported by Burgess et al. (2019) who divided Australia into climate zones based on 
temperature and humidity and matched the locations where Lasiodiplodia spp. have been 
isolated in Australia to these climate zones. By comparing these climate zones to the New 
Zealand climate (Phillips et al. 2018), it suggests that some regions of New Zealand may be 
suitable for L. pseudotheobromae to establish.  70 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • Correia et al. (2016) noted that although the optimal mycelial growth temperatures of 
L. pseudotheobromae on agar is 30.1 °C, it was able to grow at 10 °C.  
• The fungus has been isolated from a Rosa sp. (Burgess et al. 2019; Alves et al, 208), Citrus 
spp. ( Abdollahzadeh  et al. 2010 ; Awan et al. 2016 ; Ahmed et al. 2020) , blueberry  (Burgess et 
al. 2019) and grapevine  (Dissanayake et al. 2015 ; Burgess et al. 2019 ). Such plants are 
commonly grown in New Zealand as both commercial crops ( Plant and Food Research  2019) 
and by h ome gardeners. Grapes in particular have a large commercially planted area (33,981 
ha in 2017) ( Plant and Food Research  2019). Therefore, suitable hosts are likely to be present 
to support establishment, especially citrus and grapes , as commercial orchards  are mostly in 
the warmer regions of the North Island ( Plant and Food Research  2019).  
• The closely related species L. theobromae is present in New Zealand (NZFungi 2020). 
Although this has been reported from hosts commonly grown in New Zealand (EPPO 2020)  
and from countries with a similar climate (CABI 2020), the collections in New Zealand are 
limited to one from Begonia × hiemalis (Hiemalis begonia) and two from Ipomoea batatas 
(kūmara) in Auckland (NZFungi 2 2020).  This suggests that the conditions in New Zealand are 
not conducive for establishment of the fungus outside this limited area.  
The climatic conditions from where the fungus has been isolated suggest that only limited regions of 
New Zealand would be suitabl e for the fungus  (restricted to warmer regions such as the north of the 
North Island) . However, the wide reported host range, including hosts  that are grown in these warmer 
regions are likely to be present to support establishment. Therefore, the likelihoo d of establishment is 
rated moderate. There is uncertainty associated with this conclusion , as although the closely related 
species L. theobromae is present in New Zealand, it is not widespread.  
 
Given the arguments and evidence below, t he likelihood of L. subglobosa 
establishing in New Zealand considere d to be  moderate, with high uncertainty .   
• All records of L. subglobosa are from regions with some climate similarity with New Zealand 
(CMI  ≥0.7) ( Table 10).   
• The current described host list of L. subglobosa is limited to Persian lime ( Bautista -Cruz et al. 
2019) , Jatropha carcas (Machado et al. 2014 ) and Annona muricata (soursop) ( Machado et al. 
2019). Of these species, only Persian lime  is grown in New Zealand ( Allan Herbarium 2020).  
• The likelihood of establishment is rated moderate based on the suitability of the New Zealand 
climate, even though the host range is currently limite d. This is because there are recent 
reports of new hosts of the fungus , and if these represented plants are grown in New Zealand , 
there is a good likelihood that the fungus could  establish.  
• There is high uncertainty associated with this conclusion due to t he lack of available literature. 
Further information received (i.e. via the emerging risk system ) may warrant the risk being 
reassessed.  
 
If the fungi were to enter, they would be able to spread between suitable hosts:  
• The Botryosphaeriaceae  produce asexu al spores  (conidia)  that are spread to other hosts by 
watersplash  (e.g. from overhead irrigation) , rainfall events and wind (Úrbez -Torres et al. 
2010).  
• Therefore, there are pathways of  spread  for the fungi between  suitable  hosts if the  fungi  enter 
New Zeal and.  
• As Lasiodiplodia spp. are predicted to have an asymptomatic phase (Slippers and Wingfield 
2007) , there is the possibility that they may spread via the movement of infected plant material 
before the infection  is detected.  
   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 71 Table 10: Hosts and distributions of the Lasiodiplodia spp. reported from Citrus spp. 
Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia 
brasiliensis  Asia Malaysia  Kelantan, Pahang, 
Perak, Sabah, 
Sarawak, Selangor  Sansevieria 
trifasciata (snake 
plant)  Leaf blight  0.4–0.5 Yee et al. (2019)  
Caribbean  Puerto Rico  Country -wide Dimocarpus longan 
(longan)  Inflores  0.5–0.6 Serrato -Diaz et al. (2019)  
Country -wide Mangifera indica 
(mango)  Inflores  0.5–0.6 Serrato -Diaz et al. (2019)  
South 
America  Brazil  Minas Gerais State  Manihot esculenta 
(cassava)  Black root rot, stem cutting 
dry rot  0.5–0.7 Brito et al. (2020)  
Brazil  São Francisco 
Valley  Vitis vinifera 
(grapevine)  Dieback  0.5 Correia et al. (2016)  
Brazil  Bahia, Para íba, Rio 
Grande do Norte  Carica papaya  
(papaya)  Stem end rot  0.4–0.6 Netto et al. 2014  
Brazil  Bahia, Para íba, Rio 
Grande do Norte  Mangifera indica 
(mango)  Unknown  0.4–0.6 Netto et al. (2014)  
Brazil  Paraipaba county  Malus sp. (apple)  Stem canker, branch 
dieback  0.4–0.5 Martins et al. (2018)  
North America  Mexico  Puebla and 
Veracruz  Citrus latifolia 
(Persian lime)  Gummosis, stem canker, 
branch dieback  0.5–0.8 Bautista -Cruz et al. (2019)  
Oceania  Australia  
 Emerald (Q LD) Gossypium 
hirsutum (upland 
cotton)  Unknown  0.6 Burgess et al. (2019)  
Lasiodiplodia citricola  
 
 
 
 
 
 
 
 
 
 
 Asia  Iran  Chaboksar, Sari  Citrus sp.  Twig dieback  0.5–0.8 Abdollahzadeh et al. (2010)  
North America  Mexico  Puebla and 
Veracruz  Citrus latifolia 
(Persian lime)  Gummosis, stem canker, 
branch dieback  0.5–0.8 Bautista -Cruz et al. (2019)  
USA  Kings, Yuba and 
Fresno counties, 
California  Prunus persica 
(peach)  Stem canker  0.6–0.8 Chen et al. (2013b)  
Tulare County, 
California  Juglans regia 
(European walnut)  Graft union death  0.6–0.8 Chen et al. (2013a)  
Madera, California  Pistacia vera  
(pistachio)  Panicle and shoot blight  0.6–0.7 Chen et al. (2014)  
Europe  Italy Southern  Vitis vinifera 
(grapevine)  Unknown  0.8–0.9 Raimondo et al. (2014)  72 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia citricola  Oceania  Australia  Waikerie (SA), 
Canowindra (NSW), 
Irymple (V IC) Vitis vinifera 
(grapevine)  Unknown  0.7–0.9 Burgess et al. (2019)  
Lasiodiplodia 
hormozganensis  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 Asia  Iran Hormozgan  Mangifera indica 
(mango)  Twig dieback  0.4–0.5 Abdollahzadeh et al. (2010)  
Oman  
 Unknown  Citrus limetta 
(sweet lime)  Dieback and gummosis  0.4–0.5 Al-Sadi et al. (2013)  
Unknown  Citrus latifolia (acid 
lime)  Dieback and gummosis  0.4–0.5 Al-Sadi et al. (2013)  
Unknown  Citrus sinensis 
(sweet orange)  Dieback and gummosis  0.4–0.5 Al-Sadi et al. (2013)  
Seeb, Barka and 
Musanaa  Mangifera indica 
(mango)  Dieback and gummosis  0.3–0.4 Al-Sadi et al. (2013)  
Unknown  Phoenix dactylifera 
(date palm)  Necrotic roots  0.4-0.5 Al-Sadi et al. (2013)  
UAE Unknown  Phoenix dactylifera 
(date palm)  Unknown  0.3–0.4 Al-Sadi et al. (2013)  
Malaysia  Kelantan, Pahang, 
Perak, Sabah, 
Sarawak, Selangor  Sansevieria 
trifasciata (snake 
plant)  Leaf blight  0.4–0.5 Yee et al. (2019)  
Caribbean  Puerto Rico  Country -wide Dimocarpus longan 
(longan)  Fruit rot  0.5–0.6 Serrato -Diaz et al. (2019)  
Haiti Montrouis  Solanum 
melongena 
(eggplant)  Fruit rot  0.5 Fayette et al. (2019)  
Oceania  Australia  Broome (WA), 
Darwin (NT)  Adansonia gregorii 
(baobab)  Unknown  0.4 Burgess et al. (2019)  
Australia  Darwin (NT)  Adansonia za  Unknown  0.4 Burgess et al. (2019)  
Australia  Darwin (NT)  Adansonia digitata 
(African baobab)  Unknown  0.4 Burgess et al. (2019)  
South 
America  Brazil  Minas Gerais  Manihot esculenta 
(cassava)  Black root rot, stem cutting 
dry rot  0.5–0.7 Brito et al. (2020)  
Brazil  Minas Gerais, Bahia  Annona squamosa 
(sugar apple)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Bahia, Para íba Ricinus communis  
(castorbean)  Basal stem rot  0.5–0.6 Custódio  et al. (2018)   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 73 Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia 
hormozganensis  Brazil  São Francisco 
Valley  Vitis vinifera 
(grapevine)  Dieback  0.5 Correia et al. (2016)  
Brazil  Bahia, Para íba, Rio 
Grande do Norte  Carica papaya  
(papaya)  Stem -end rot  0.4–0.6 Netto et al. (2014)  
Lasiodiplodia iranensis  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 Africa  Mozambique  Unknown  Adansonia digitata  
(African baobab)  Unknown  0.5–0.6 Bautista -Cruz et al. (2019)  
North America  Mexico  Puebla and 
Veracruz  Citrus latifolia 
(Persian lime)  Gummosis, stem canker, 
branch dieback  0.5–0.8 Bautista -Cruz et al. (2019)  
South 
America  Brazil  Minas Gerais  Manihot esculenta 
(cassava)  Black root rot, stem cutting 
dry rot  0.5–0.7 Brito et al. (2020)  
Brazil  Minas Gerais, Bahia  Annona muricata 
(soursop)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Minas Gerais, Bahia  Annona squamosa 
(sugar apple)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Minas Gerais, Bahia  Annona atemoya 
(atemoya)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Unknown  Jatropha carcas  Unknown  - Bautista -Cruz et al. (2019)  
Brazil  São Francisco 
Valley  Vitis vinifera 
(grapevine)  Dieback  0.5 Correia et al. (2016)  
Peru  Piura district  Mangifera indica 
(mango)  Dieback  0.4–0.7 Rodríguez -Gálvez et al. 
(2016)  
Asia Iran  Unknown  Citrus sp.  Twig dieback  - Abdollahzadeh et al. (2010)  
Iran  Unknown  Mangifera indica 
(mango)  Twig dieback  - Abdollahzadeh et al. (2010)  
Iran  Unknown  Eucalyptus sp.  Twig dieback  - Abdollahzadeh et al. (2010)  
Iran  Unknown  Olea sp.  Twig dieback  - Abdollahzadeh et al. (2010)  
Iran  Golestan Province  Juglans sp. (walnut)  Twig dieback  0.6–0.7 Abdollahzadeh et al. (2010)  
Iran  Hormozgan 
Province  Salvadora persica  
(kharijal)  Twig dieback  0.4–0.5 Abdollahzadeh et al. (2010)  
Iran  Unknown  Terminalia catap pa 
(country almond)  Twig dieback  - Abdollahzadeh et al. (2010)  
Malaysia  Kelantan, Pahang, 
Perak, Sabah, 
Sarawak, Selangor  Sansevieria 
trifasciata (snake 
plant)  Leaf blight  0.4–0.5 Yee et al. (2019)  74 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia iranensis  Caribbean  USA Puerto Rico  Nephelium 
lappaceum  
(rambutan)  Branch dieback and leaf 
blight  0.5–0.6 Serrato -Diaz et al. (2019)  
Puerto Rico  Dimocarpus longan 
(longan)  Inflor escences  and fruit rot  0.5–0.6 Serrato -Diaz et al. (2019)  
Puerto Rico  Mangifera indica 
(mango)  Inflores cences  0.5–0.6 Serrato -Diaz et al. (2019)  
Oceania  Australia  Colignan (Vic)  Dodonaea viscosa 
(hopbush)  Unknown  0.7 Burgess et al. (2019)  
Australia  Broome (WA)  Adansonia gregorii 
(boab) Unknown  0.4 Burgess et al. (2019)  
Australia  Kimberley (WA)  Eucalyptus sp. Unknown  0.4–0.5 Burgess et al. (2019)  
Australia  Kununurra (WA)  Mangifera indica 
(mango)  Unknown  0.4 Burgess et al. (2019)  
Lasiodiplodia 
mediterranea  Africa  Algeria  Oued El Alleug, 
Boufarik  Citrus sinensis 
(sweet orange)  Trunk canker  0.7 Berraf -Tebbal et al. (2020)  
North America  USA  Oregon  Vaccinium 
corymbosum 
(blueberry  Cane dieback  0.7–0.8 Wiseman et al. (2017)  
Europe  Italy  Sardinia  Vitis vinifera 
(grapevine)  Dieback  0.8–0.9 Linaldeddu et al. (2015)  
Sardinia  Quercus ilex (holm 
oak) Branch canker  0.8–0.9 Linaldeddu et al. (2015)  
Lasiodiplodia mitidjana  Africa  Algeria  Oued El Alleug, 
Boufarik  Citrus sinensis 
(sweet orange)  Trunk canker  0.7 Berraf -Tebbal et al. (2020)  
Lasiodiplodia 
pseudotheobromae  
 
 
 
 
 
 
 
 North America  Mexico  Puebla and 
Veracruz)  Citrus latifolia 
(Persian lime)  Gummosis, stem canker, 
branch dieback  0.5–0.8 Bautista -Cruz et al. (2019)  
South 
America  
 
 
 
 
 
 Suriname  Unknown  Citrus aurantium 
(bitter orange)  Unknown  0.4–0.5 Alves et al. (2008)  
Brazil  Minas Gerais State  Manihot esculenta 
(cassava)  Black root rot, stem cutting 
dry rot  0.5–0.7 Brito et al. (2020)  
Brazil  São Francisco 
Valley  Vitis vinifera 
(grapevine)  Dieback  0.5 Correia et al. (2016)  
Brazil  Piracicaba  Diospyros kaki 
(persimmon)  Post-harvest fruit rot  0.6 Nogueira et al. (2017)   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 75 Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia 
pseudotheobromae  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 South 
America  Peru  Piura  Mangifera indica 
(mango)  Dieback  0.4–0.7 Rodríguez -Gálvez et al. 
(2016)  
Brazil  Bahia, Paraiba, Rio 
Grande do Norte  Carica papaya  
(papaya)  Stem -end rot  0.4–0.6 Netto et al. (2014)  
Brazil  Minas Gerais, Bahia  Annona crassiflora 
(marolo)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Minas Gerais, Bahia  Annona muricata 
(soursop)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Minas Gerais, Bahia  Annona squamosa 
(sugar apple)  Dieback  0.5–0.7 Machado et al. (2019)  
Brazil  Minas Gerais, Bahia  Annona atemoya 
(atemoya)  Dieback  0.5–0.7 Machado et al. (2019)  
Asia Turkey  Çukurova  Citrus limon (sweet 
lemon)  Post-harvest fruit rot  0.7–0.8 Awan et al. (2016)  
Bangladesh  Rajshahi  Citrus sp.   Stem -end rot  0.4 Sultana et al. (2018)  
Pakistan  Sargodha, Bhulwal, 
Kot Momin, 
Faisalabad, Toba 
Tek Singh  Citrus reticulata 
(mandarin)  Trunk cankers  0.4–0.6 Ahmed et al. (2020)  
Iran Unknown  Citrus sp.  Twigs  - Abdollahzadeh et al. (2010)  
Malaysia  Kelantan, Pahang, 
Perak, Sabah, 
Sarawak, Selangor  Sansevieria 
trifasciata (snake 
plant)  Leaf blight  0.4–0.5 Yee et al. (2019)  
China  Hubei, Jiangsu  Vitis vinifera 
(grapevine)  Pedicel and penduncle 
discolouration  0.7 Dissanayake et al. (2015)  
China  Yantai, Shandong  Malus pumila (syn. 
Malus × domestica ) 
(apple)  Canker and shoot dieback  0.7 Xue et al. (2019)  
China  Jiangsu  Celtis sinensis 
(hackberry)  Stem canker  0.7 Liang et al. (2019)  
Africa  Zaire  Unknown  Coffea sp. Unknown  0.5–0.6 Abdollahzadeh et al. (2010)  
Central 
America  Costa Rica  Unknown  Gmelina arborea 
(Candahar tree)  Unknown  0.4–0.6 Abdollahzadeh et al. (2010)  
Caribbean  
 USA 
 Puerto Rico  Citrus sp. 
(tangerine)  Branch dieback  0.5–0.6 Serrato -Diaz et al. (2019)  76 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Species  Continent  Country  State/Region  Host  Symptoms  / plant parts  
affected  CMI (Phillips 
et al. 2018)  Reference  
Lasiodiplodia 
pseudotheobromae  Caribbean  USA Puerto Rico  Nephelium 
lappaceum 
(rambutan)  Branch dieback and fruit rot  0.5–0.6 Serrato -Diaz et al. (2019)  
Puerto Rico  Dimocarpus longan 
(longan)  Inflores cences  0.5–0.6 Serrato -Diaz et al. (2019)  
Unknown  Acacia mangium 
(mangium ) Unknown  0.5–0.6 Alves et al. (2008)  
Europe  Netherlands  Unknown  Rosa sp.  Unknown  0.9 Alves et al. (2008)  
Oceania  Australia  Broome (WA), 
Gumlu (Q LD) Mangifera indica 
(mango)  Unknown  0.4–0.5 Burgess et al. (2019)  
Australia  Canarvon (Q LD), 
Swan District (WA)  Vitis vinifera 
(grapevine)  Unknown  0.5–0.7 Burgess et al. (2019)  
Australia  Tolga (Q LD) Rosa sp. Unknown  0.4 Burgess et al. (2019)  
Australia  Tolga (Q LD) Macadamia sp.  Unknown  0.4 Burgess et al. (2019)  
Australia  Kuranda (Q LD) Eucalyptus pellita 
(large fruited red 
mahogany)  Unknown  0.5 Burgess et al. (2019)  
Australia  Mareeba (Q LD) Dimocarpus longan 
(longan)  Unknown  0.5 Burgess et al. (2019)  
Australia  Tully (Q LD) Annona muricata 
(soupsop)  Unknown  0.5 Burgess et al. (2019)  
Australia  Corindi (NSW)  Vaccinium 
corymbosum 
(blueberry)   Unknown  0.7 Burgess et al. (2019)  
Australia  Kununurra (WA)  Santalum album 
(Indian sandalwood)  Unknown  0.4 Burgess et al. (2019)  
Lasiodiplodia 
subglobosa  North America  Mexico  Puebla , Veracruz  Citrus latifolia 
(Persian lime)  Gummosis, stem canker, 
branch dieback  0.5–0.8 Bautista -Cruz et al. (2019)  
South 
America  Brazil  Minas Gerais, 
Espírito Santo, 
Piauí, São Paulo  Jatropha carcas  collar and root rot  0.5-0.7 Machado et al. (2014)  
Brazil  Minas Gerais, Bahia  Annona muricata 
(soursop)  Dieback  0.5–0.7 Machado et al. (2019)  
Countries in bold represent  countries where Citrus nursery stock has been exported to New Zealand (Quancargo 2020)    
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 77  
 
5.6.6  Risk assessment: impacts  to New Zealand  
 
Given the arguments and evidence below , the introduction of L. brasiliensis is likely 
to cause moderate economic impacts for New Zealand, with high uncertainty . 
The species has been reported from diseased C. latifolia trees .  
• Lasiodiplodia brasiliensis has been isolated from C. latifolia trees with symptoms of gummosis, 
stem canker and branch dieback in Mexico ( Bauti sta-Cruz et al. 2019) . 
• This species was the third most frequently isolated (12.5% of all isolates) ( Bautista -Cruz et al. 
2019 ). It was found in the both populations in Puebla state ( six orchards), but not from the 
Veracruz populations. In artificial inocul ation assays of one -year old Persian limes , L. 
brasiliensis induced necrotic lesions and gum exudation but was found to be less virulent than 
L. subglobosa, L. pseudotheobromae and L. iranensis (Bautista -Cruz et al. 2019 ).  
• Yield losses caused by the patho gen were not described, however worldwide trunk canker 
disease is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999). 
Therefore, it is assumed that trunk canker caused by L. brasiliensis has the potential to result 
in similar losses.   
• In 2019 , limes had a domestic value of NZ$2 million ( Plant and Food Research  2019).  
 
There are reports of L. brasiliensis being associated with disease of other economically significant 
hosts . 
• In Brazil , L. brasiliensis has been identified as a causative agent of canker and branch dieback 
of apple (Martins et al. 2018).  The fungus was isolated from symptomatic tissue and 
pathogenicity was confirmed via artificial inoculation assays (Martins et al. 2018).  The level of 
yield loss associated with infection with L. brasiliensis was not described.  
• Apples are the third most significant horticulture export for New Zealand, worth NZ$828.8 
million in 2019 ( Plant and Food Research  2019). Therefore, losses for this industry have the 
potential to cause significant consequences for the New Zealand economy.   
• Correia et al. (2016) isolated L. brasiliensis during a survey of Lasiodiplodia spp. associated 
with Botryosphaeria dieback of grapes in eastern Brazil; the species represented 15% of the 
isolates. In pathogenicity tests on detached shoots, L. brasiliensis induced the longest lesions 
of all the species tested (Correia et al. 2016). In Brazil, grapevine dieback caused by members 
of the Botryosphaeriaceae is becoming increasingly signi ficant, reducing the longevity and 
production of plants (Correia et al. 2016).  
• Wine is the second most valuable horticultural export for New Zealand (value NZ$1.8 billion) 
(Plant and Food Research  2019). Therefore, losses in grape  crops have the potential  to cause 
significant economic consequences for New Zealand.  
• Other reported hosts are tropical species that are not important crops for New Zealand (Table 
10).   
 
Due to the potential to cause impacts to grape and apple crops, as well as limes, the economic impact 
of L. brasiliensis is rated as moderate. There is high uncertainty associated with th e conclusion, which 
is further discussed below.  
 
Given the arguments and evidence below , the introduction of L. citricola is 
considered likely to cause low economic impacts for New Zealand, with high 
uncertainty . 
The species has been reported from disease d C. latifolia trees:  
• It has also been isolated from C. latifolia trees with symptoms of gummosis, stem canker and 
branch dieback in Mexico ( Bautista -Cruz et al. 2019) . 
• This species was the least frequently isolated by Bautista -Cruz et al. (2019 ) (3% of a ll 
isolates). It was only found in one orchard in Puebla state. In artificial inoculation assays of 
one-year-old Persian limes , L. citricola induced necrotic lesions and gum exudation but was 
found to be less virulent than L. subglobosa, L. pseudotheobromae and L. iranensis (Bautista -
Cruz et al. 2019 ).  78 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • Yield losses caused by the pathogen were not described . However , worldwide , trunk canker 
disease is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999). 
Therefore, it is assumed that trunk canker caused by L. citricola has the potential to result in 
similar losses.   
• In 2019 , limes had a domestic value of NZ$2 million ( Plant and Food Research  2019).  
• This species was also reported from Citrus sp. in Iran during a survey of Botryosphaeriaceae 
in diseased orchards ( Abdollahzadeh et al. 2010 ). How frequently the species was isolated 
was not reported , and Koch’s postulates were no t fulfilled. Furthermore, as the species was 
not identified, there is currently no evidence of the species infecting other members of the 
Citrus genus.   
This species has been reported from other significant hosts for New Zealand:  
• Lasiodiplodia citricola  was identified causing stem canker in Prunus persica (peach) in 
California (Chen et al. 2013b). The disease was found on young trees and caused the death 
of 30 trees in  the Fresno and Yuba counties and a further six in Kings County (Chen et al. 
2013b).  
• In 2019 , peaches had a domestic value of NZ$9 million and an export value of NZ$0.4 million 
(Plant and Food Research  2019).  
• There is no evidence of the  fungal  species infecting other species of Prunus . However, the 
broad reported host range reported suggests that there is the potential  for the  fungus  to do so .  
• The fungus has also been isolated from grapevine in Australia and Italy, although it is not 
known if these plants displayed symptoms ( Raimondo et al. 2014; Burgess et al. 2019) . 
However, the sy mptoms caused by this species on this host are not described.  
Based on the current evidence of the host range, the potential economic impacts associated with the 
species is rated as low. There is high uncertainty associated with this conclusion. For examp le, it is 
not known if it is able to infect other members of Citrus or Prunus, however if it does there is the 
potential for further impacts. The uncertainty is further discussed below.  
 
Given the arguments and evidence below , the introduction of L. hormozganensis is 
considered likely to cause moderate economic impacts for New Zealand, with high 
uncertainty . 
The species is reported causing disease on multiple citrus species:  
• This species  has been reported associated with C. lime tta (sweet lime) , C. latifolia (sour lime) 
and C. sinensis (orange) in Oman ( Al-Sadi et al. 201 3). The trees showed symptoms of 
dieback and gummosis.  
• The species represented 45% of isolated Lasiodiplodia spp. and in pathogenicity assays 
caused wilting in 30–73% of inoculated seedlings ( Al-Sadi et al. 201 3). 
• Losses associated with this species were not described, however it is assumed that the 
symptoms would cause a decrease in the productivity and/or longevity of the plant.  
• In 2019 limes has a domestic value of NZ$2 million and oranges had a domestic value of 
NZ$18 million and an export value of NZ$1.7 million ( Plant and Food Research  2019).  
 
There are reports of L. hormozganensis  associated with disease of other economically  significant 
hosts:  
• The other economically significant host s reported for the fungus are eggplant and grape ( Table 
10) 
• Correia et al. (2016) isolated L. hormozganensis during a survey of Lasiodiplodia spp. 
associated with Botryosphaeria dieback of grapes in eastern Brazil; the species represented 
7% of the isolates. In pathogenicity tests on detached shoots, L. hormozganensis induced 
visible lesions and was assessed to h ave intermediate aggressiveness compared to the other 
species tested (Correia et al. 2016). In Brazil, grapevine dieback caused by members of the 
Botryosphaeriaceae is becoming increasingly significant, reducing the longevity and 
production of plants (Corr eia et al. 2016).  
• Wine is the second most valuable horticultural export for New Zealand (value NZ$1.8 billion) 
(Plant and Food Research  2019). Therefore, losses in th is crop have the potential to cause 
significant economic consequences for New Zealand.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 79 • In Haiti , the species was identified causing fruit rot of eggplant, with a disease incidence of 
approx. 20% ( Fayette et al. 2019) . Eggplants are grown in New Zealand for the domestic 
market, with a value of NZ$8.5 million ( Plant and Food Research  2019).  
Due to the potential to cause losses to citrus, grape and eggplant crops the potential for economic 
impacts is rated as moderate. There is high uncertainty associated with  this conclusion, which is 
further discussed below.   
 
Given the arguments and evidence below , the introduction of L. iraniensis is 
considered likely to cause low economic impacts for New Zealand, with high 
uncertainty . 
The species is reported causing dise ase on multiple citrus species:  
• This species has been isolated from C. latifolia (Persian lime) trees with gummosis, stem 
canker and branch dieback in Mexico (Bautista -Cruz et al. 2019). Lasiodiplodia iranensis  was 
the least frequently isolated by Bautista -Cruz et al. (2019) (3% of all isolates). It was only 
found in one population from Veracruz state (three orchards). In artificial inoculation assays of 
one-year old Persian limes , L. iranensis induced necrotic lesions and gum exudation but was 
found to be more virulent than L. brasiliensis, L. theobromae and L. citricola (Bautista -Cruz et 
al. 2019).  
• Yield losses caused by the pathogen were not described . However , worldwide , trunk canker 
(caused by all pathogens) is responsible for 10 –30% of losses in citrus orchards (Timmer et 
al. 1999). Therefore, it is assumed that trunk canker caused by L. iranensis has the potential 
to result in similar losses.  
• This species  has also been  isolated from C. reticulata (mandarin)  in Oman, during a survey of 
trees with dieback and gummy exudate symptoms ( Al-Sadi et al. 201 3). The species 
represented 10% of isolated Lasiodiplodia spp. and in pathogenicity assays caused wilting in 
17–77% of inoc ulated seedlings (Al -Sadi et al. 2013).  
• In 2019 limes and mandarins had a domestic value of NZ$2 million and NZ$25 million 
respectively, with mandarins also having an export value of NZ$0.4 million.   
• The species was also isolated from Citrus sp. with twig  dieback in Iran ( Abdollahzadeh et al. 
2010) . How frequently the species was isolated was not reported , and Koch’s postulates were 
not fulfilled.  
The species has been isolated from other significant hosts with disease symptoms . However , its role 
as the causative agent is not confirmed . 
• The fungus has been isolated from Eucalyptus sp. with twig dieback in Iran  (Abdollahzadeh et 
al. 2010 ) and from Eucalyptus sp. in Australia (Burgess et al. 2019), although symptoms are 
not described. In the study by Abdollahzadeh et al. (2010 ), Koch’s postulates were not fulfilled.  
• Eucalyptus is grown as a timber species in both the North Island and South Island , with a total 
planted area of 22,307  ha, which contribute d NZ$41 million to the New Zealand GDP in 2018 
(FOA 2018) . Therefore, losses for this industry could have significant impacts for the 
New Zealand economy. However, further evidence is needed before this species can be 
considered the  causal agent of disease on this host. If this was the case, the potential for 
economic impacts would be higher.  
Based on the current evidence of the species causing disease symptoms on citrus, the potential 
economic impacts are rated lo w. There is high uncertainty associated with this conclusion, which is 
discussed further below.  
 
Given the arguments and evidence below , the introduction of L. mediterranea is 
considered likely to cause moderate economic impacts for New Zealand, with high 
uncertainty . 
The species has been reported from diseased C. sinensis  trees:  
• The only record of L. mediterranea on citrus is from Algeria, where it was isolated from 
C. sinensis (orange) trees with trunk canker ( Berraf -Tebbal et al. 2020) .  
• Ten orange  orchards in northern Algeria were surveyed for the causal agents of canker and 
dieback. Lasiodiplodia mitidjana, L. mediterranea, Diplodia spp. plus a Dothiorella sp. were 
isolated. In all the orchards , at least two species were found , and the Lasio diplodia spp. were 80 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  most frequently detected ( Berraf -Tebbal et al. 2020) . In pathogenicity tests on orange  shoots, 
L. mediterranea induced internal necrotic lesions.  
• Yield losses caused by the pathogen were not described . However , worldwide , trunk canker 
disease is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999). 
Therefore, it is assumed that trunk canker caused by L. brasiliensis has the potential to result 
in similar losses.   
• There is no evidence of the species infecting other sp ecies of Citrus. However, given the 
reports from other host species , there is the potential for L. mediterranea to infect other Citrus 
spp.  
• Oranges had a domestic value of NZ$18 million and an export value of NZ$1.7 million in 2019 
(Plant and Food Researc h 2019).  
 
The species has been reported from diseased grapevine . 
• Lasiodiplodia mediterranea  has also been reported from two grapevine samples in Sardinia, 
Italy, displaying dieback symptoms (Linaldeddu et al. 2015). The species was isolated from 
declining grapevines from a single site in Sardinia. In pathogenicity studies . the species 
caused discolouration of the bark and vascular tissue (Linaldeddu et al. 2015). The losses 
associated with this species were not described.  
• Wine is the second most valuable horticultural export for New Zealand (value NZ$1.8 billion) 
(Plant and Food Research  2019). Therefore, losses in th is crop have the potential to cause 
significant  economic consequences for New Zealand.  
Due to the potential to cause losses to citrus and grape , the economic impacts are rated  moderate. 
There is high uncertainty associated with this conclusion, which is further discussed below.  
 
Given the arguments an d evidence below , the introduction of L. mitidjana is 
considered likely to cause low economic impacts for New Zealand, with high 
uncertainty . 
The species has been reported from diseased C. sinensis trees . 
• Lasiodiplodia mitidjana is recently described , and there is only one report of the species in the 
literature , from C. sinensis (orange) in Algeria with trunk canker symptoms ( Berraf -Tebbal et 
al. 2020) .   
• Ten orange orchards in northern Algeria were surveyed for the causal agents of canker a nd 
dieback. Lasiodiplodia mitidjana, L. mediterranea, Diplodia spp. and a Dothiorella sp. were 
isolated. In all the orchards , at least two species were found , and the Lasiodiplodia spp. were 
most frequently detected ( Berraf -Tebbal et al. 2020) . In pathogen icity tests on orange shoots, 
L. mitidjana induced internal necrotic lesions.  
• Yield losses caused by the pathogen were not described . However , worldwide , trunk canker 
disease is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999). 
Therefore, it is assumed that trunk canker caused by L. mitidjana has the potential to result in 
similar losses.  
• In 2019 , oranges had a domestic value of NZ$18 million and an export value of NZ$1.7 
million.  
Based on the current, restricted host range of the species the potential economic impacts are rated as 
low. There is high uncertainty associated with this conclusion, which is further discussed below.   
 
Given the arguments and evidence below , the introduction of L. subglobosa is 
considered likely to cause  low economic impacts for  New Zealand , with high 
uncertainty . 
The species has been reported from diseased C. latifolia  trees . 
• This species has been reported from C. latifolia (Persian lime) in Mexico with gummosis, stem 
canker and branch dieback ( Bautista -Cruz et al. 2019) .  
• In Mexico , this species was the least frequently isolated by Bautista -Cruz et al. (2019 ) (3% of 
all isolates). It was only found in one population from Veracruz state (n=three orchards). In 
artificial inoculation assays of one -year-old Persian limes , L. iranensis induced necrotic lesions  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 81 and gum exudation but was found to be more virulent than L. brasiliensis, L. theobromae and 
L. citricola (Bautista -Cruz et al. 2019 ). 
• Yield losses caused by the pathogen were not described, howe ver worldwide trunk canker 
disease is responsible for 10 –30% of losses in citrus orchards (Timmer et al. 1999). 
Therefore, it is assumed that trunk canker caused by L. subglobosa has the potential to result 
in similar losses.  
• In 2019 , limes had a domestic value of NZ$2 million ( Plant and Food Research  2019).  
• There is no evidence of the species infecting other species of Citrus. However, given the 
reports from other host species there is the potential for L. subglobosa to infect other Citrus 
spp.  
 
This spe cies has not been reported from any other host that has economic significance for  
New Zealand (Table 10).  
 
Based on the current available evidence for this species, the potential economic impacts associated 
with the species are rated low. There is high uncertainty associated with this conclusio n, which is 
further discussed below.   
 
 
Uncertainty  
There is high uncertainty associated with the impact conclusions . 
• These are emerging pathogens , and currently , there are limited data available in some areas, 
such as the frequency of disease and level of impact for each species and full host range. 
Because these are emerging pathogens and there is recent new information, new evidence 
may become available that would require the risk to be reassessed. Such information would 
be captured by the emerging ris k system.  
• There are several reports of the Lasiodiplodia spp. occurring in hosts as mixed infections 
(Chen et al. 2013a ; Bautista -Cruz et al. 2019;  Yee et al. 2019 ). Furthermore, Botryosphaeria 
dieback of grape is reported to be caused by a complex of fungi (Correia et al. 2016). It may 
be that individually the assessed species have the potential to only cause low economic 
consequences, but the introduction of multip le species may have a cumulative effect 
increasing disease severity and economic impact.  
• For the Lasiodiplodia species reported from only one citrus (or Prunus ) species ( Table 10) it is 
not clear whether they can infect other species within the genus. If this was found to be the 
case, the risk would need to be reassessed.  
• The different species have largely been separa ted based on phylogenetic analysis (Alves et 
al. 2008; Abdollahzadeh et al. 2010 ) and the fully biological differences associated with these 
new species are not investigated.  
• As shown in Table 10, it appears that different species have different host ranges and climatic 
requirements. However, as a number of these species are newly described, there is 
uncertainty as to whether this is the fully elucidated host and geograp hic range.   
• The conditions required to induce disease symptoms are not described.  
• Although the type species of the genus Lasiodiplodia theobromae is present in New Zealand,  
the records are limited to one from Begonia × hiemalis (Hiemalis begonia) and two  from 
Ipomoea batatas (kumara) in Auckland (NZFungi 2 2020).  No evidence was found of this 
species causing serious disease in New Zealand (Google scholar ‘lasiodiplodia theobromae 
disease New Zealand’). Furthermore, although it is a known pathogen of grapev ines overseas 
(Burruano et al. 2008; Rodriguez -Gálvez et al. 2015) it is not found in New Zealand vineyards 
(Baskarathevan et al. 2012; Billones -Baaijens and Savocchia 2018). Therefore, there is the 
potential that this may be the case for L. pseudotheobrom ae. There is less uncertainty 
associated with this species, as there are reports from multiple countries of this species being 
the sole causative agent of disease , and there is more literature available.  
 
 
 82 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Given the arguments and evidence below , introduction of L. pseudotheobromae is 
considered likely to cause high economic impacts for  New Zealand, with moderate 
uncertainty . 
The species is reported causing disease on multiple citrus species . 
• There are multiple records of L. pseudotheobromae associ ated with Citrus spp. in several 
countries (Table 10). 
• This species has been isolated from trees with gummosis, stem/trunk canker and branch 
dieback (Sultana et al. 2018 ; Bautista -Cruz et al. 2019; Serrato -Diaz et al. 2019; Ahmed et al. 
2020) as well as from fruit with post -harvest (Awan et al. 2016) and stem -end rot (Sultana et 
al. 2018).  
• Lasiodiplodia pseudotheobromae was the most frequently isolated species from disea sed 
Persian limes in Mexico, accounting for 47% of all isolates (Bautista -Cruz et al. 2019). In 
pathogenicity studies on one -year old Persian limes, necrotic lesions and gum exudates were 
induced. This species was more virulent than L. brasiliensis, L. the obromae and L. citricola  
(Bautista -Cruz et al. 2019).  
• In Pakistan, Ahmed et al. (2020) reported tree  canker caused, by L. pseudotheobromae, in 
orchards of C. reticulata reached disease incidence  of 40%. Yield losses were not reported, 
however worldwide trunk canker disease is responsible for 10 –30% of losses in citrus 
orchards (Timmer et al. 1999).  
• Lasiodiplodia pseudotheobromae has also been described as a causative agent of post-
harvest  rot of  lemon (Awan et al. 2016). In pathogenicity studie s, the fungus was found to be 
highly pathogenic, damaging 40 –50% of the fruit surface after five days (Awan et al. 2016).  
Such symptoms would reduce yields post -harvest and the marketability of infected fruits.    
• In 2019  limes, lemons and mandarins had a domestic value of NZ$2million, NZ$12 million and 
NZ$25 million respectively, with lemons and mandarins having export values of NZ$9.8 million 
and NZ$0.4 million respectively  (Plant and Food Research 2019) .   
 
There are reports of L. pseudotheobromae causin g disease on other economically important hosts:  
• The fungus has also been isolated from grapevines  showing dieback symptoms ( Correia et al. 
2016) , as well as pedicel and pend uncle  discolouration ( Dissanayake et al. 2015) .  
• Correia et al. (2016) isolated L. pseudotheobromae during a survey of Lasiodiplodia spp. 
associated with Botryosphaeria dieback of grapes in eastern Brazil. The species was the least 
frequently isolated species, representing 3% of the isolates. In pathogen icity tests on 
detached shoots, L. pseudotheobromae induced visible lesions and was assessed to have 
intermediate aggressiveness compared to the other species tested (Correia et al. 2016). In 
Brazil, grapevine dieback caused by members of the Botryosphaeri aceae is becoming 
increasingly significant, reducing the longevity and production of plants (Correia et al. 2016).  
• Wine is the second most valuable horticultural export for New Zealand (value $1 .8 billion) 
(Plant and Food Research  2019). Therefore, losses  in this crop have the potential to cause 
significant economic consequences for New Zealand.  
• Lasiodiplodia pseudotheobromae was found to be a causative agent of post -harvest 
persimmon rot in Brazil ( Nogueira et al. 2017) . The disease incidence in the samp led fruit was 
estimated at 10%  (Nogueira et al. 2017) . Persimmons are grown in New Zealand for the 
domestic and export market, worth NZ$1.5 and NZ$10 million respectively ( Plant and Food 
Research  2019).  
• The species has also been found causing shoot and sid e branch die back and cankers of 
apple trees in China (Xue et al. 2019). D isease symptoms were different to other canker 
diseases described on apples (Xue et al. 2019). The fungus was isolated from diseased tissue 
and pathogenicity was confirmed by inocula tion assays of detached twigs (Xue et al. 2019). 
The level of yield loss associated with this disease is not reported, however such symptoms 
can be assumed to reduce the productivity of infected trees and would reduce the yield.  
• Apples are the third most s ignificant horticulture export for New Zealand, worth NZ$828.8 
million in 2019 ( Plant and Food Research  2019). Therefore, losses for this industry have the 
potential to cause significant consequences for the New Zealand economy.   
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 83 The records of the L. pseudotheobromae as the causative agent of post -harvest rot of economically 
important species, as well as  associated with dieback and canker of trees means that the potential 
economic impacts are rated as high. There is moderate uncertainty associated with this conclusion  
 
 
Given the arguments and evidence below , the introduction of any one of the  
identified  Lasiodiplodia spp. is considered likely to cause low socio -cultural impacts in 
New Zealand, with high uncertainty . 
The identified Lasiodiplodia spp. have been reported causing disease of socially important plants to 
New Zealand:  
• Apples, citrus and grapes  are hosts of some of the Lasiodiplodia  spp. and are socially 
important plants grown by home gardeners.  
• The species L. hormozganensis, L. pseudotheobromae and L. brasiliensis and L. iraniensis, 
along with L. theobromae have been found causing leaf blight symptoms in Sansevieria 
trifasciata  (syn. Dracaena trifasciata ) (snake plant), a popular ornamental plant (Yee et al. 
2019). Lasiodiplodia theobromae is present in New Zealand but has not been reported from 
this host (NZFungi 2 2020). There is the potential  that if further Lasiodiplodia spp. were 
introduced disease of S. trifasciata may occur, but the risk is rated as low.    
There is high uncertainty associated with this conclusion, as outlined in the economic impacts section.  
 
Given the arguments and evidence below, t he introduction of any one of the 
identified  Lasiodiplodia spp. is considered likely to cause low environment al impacts 
in New Zealand , with high uncertainty  
Lasiodiplodia spp. have not been reported causing disease in environmental plants present in New 
Zealand:  
• Diseases caused by Lasiodiplodia spp. are mostly reported affecting crop species. However, 
the fungi  have been isolated from environmental Adansonia spp. in Australia ( Burgess et al. 
2019 ).  
• Burgess et al. (2019) also state that there is evidence that crop plants acquire 
Botryosphaeriaceae from environmental species in the local area. Suggesting that 
environmental plants can be infected and act as an inoculum source for infection of other 
plants.    
• Based on the lack of reports of the fungi causing impacts in environmental hosts, and the 
highly sporadic nature of disease associated with Lasiodiplodia spp. the likelihood of 
environmental impacts associated with these fungi is rated as low .   
 
There is high uncertainty associated with this conclusion, as outlined in the economic impacts section.  
 
Given the arguments and evidence below, t he introduction of any one of the  
identified Lasiodiplodia spp. is considered likely to cause very low human health 
impacts in New Zealand , with low uncertainty . 
Only one report of the assessed Lasiodiplodia spp. causing human infection was found :  
• In India L. pseudotheobromae was identified as the causative agent of fungal keratitis 
(inflammation of the cornea) in a farmer following injury by a mango tree branch (Vanam et al. 
2019).   
• All other reports found of human infection caused by Lasiodiplodia spp. (Google Scholar 
search  terms ‘Lasiodiplodia human infection’)  were identified as L. theobromae.   
• Lasiodiplodia theobromae is present in New Zealand (NZFungi 2 2020). No reports of this 
fungus causing human infection in New Zealand were found (Google Scholar search terms 
‘Lasiod iplodia theobromae human infection New Zealand’).  
• Based on the available literature no evidence was found to suggest that L. 
pseudotheobromae, or any of the other species,  would cause any further human health 84 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  consequences beyond those potentially associat ed with L. theobromae (which is present in 
New Zealand).  
    
5.6.7  References  
 
Abdollahzadeh, J; Javadi, A; Goltapeh, E M; Zare, R; Phillips, A J L (2010) Phylogeny and morphology 
of four new species of Lasiodiplodia  from Iran.  Persoonia: Molecular Phylogeny an d Evolution of 
Fungi , 25: 1. 
Ahmed, M Z; Shafique, M S; Anwaar, H M A; Sarfraz, S; Tufail, M R; Fayyaz, A; Muntaha, S; Haque, 
K; Ghuffar, S; Amrao, L (2020) First Report of Lasiodiplodia pseudotheobromae  causing trunk cankers 
in Citrus reticulata  Blanco (Kinnow) in Pakistan.  Plant Dis ease , 104(9): 2522 . 
https://doi.org/10.1094/PDIS -12-19-2683 -PDN   
Al-Sadi, A M; Al -Wehaibi, A N; Al -Shariqi, R M; Al -Hammadi, M S; Al -Hosni, I A; Al -Mahmooli, I H; Al -
Ghaithi, A G (2013) Population  genetic analysis reveals diversity in Lasiodiplodia  species infecting 
date palm, Citrus , and mango in Oman and the UAE.  Plant Disease , 97(10): 1363 –1369.  
Alves, A; Crous, P W; Correia, A; Phillips, A J L (2008) Morphological and molecular data reveal 
cryptic speciation in Lasiodiplodia theobromae . Fungal Diversity , 28: 1–13. 
Awan, Q N; Akgül, D S; Unal, G (2016) First report of Lasiodiplodia pseudotheobroma e causing 
postharvest fruit rot of lemon in Turkey.  Plant Disease , 100(11): 2327 –2327.  
Baskarathevan, J; Jaspers, M V; Jones, E E; Ridgway, H J (2012) Incidence and distribution of 
botryosphaeriaceous species in New Zealand vineyards.  European Journal of Plant Pathology , 132(4): 
549–560. 
Bautista -Cruz, M A; Almaguer -Vargas, G; Leyva -Mir, S G; Colinas -León, M T; Correia, K C; Camacho -
Tapia, M; Robles -Yerena, L; Michereff, S J; Tovar -Pedraza, J M (2019) Phylogeny, distribution, and 
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  88 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand   
5.7 Phyllosticta citricarpa  (citrus black spot)  
 
Phyllosticta citricarpa (citrus black spot) causes severe spots and lesions affecting the rinds of fruit 
and sometimes leaves. Although the juice quality is unaffected, the blemished fruit is unappealing and 
unsuitable for marketing as fresh fruit. Most commercial citrus species are affected, and severe losses 
have been reported in lemons, sweet oranges and grapefruit.  
 
Scientific name: Phyllosticta citricarpa (McAlpine) Aa (1973)  
Order/Family: Botryosphaeriales/Botryosphaeriaceae   
Other names include: Guignardia citricarpa Kiely  (1949),  Phoma citricarpa McAlpine (1899)  
 
Taxonomic notes: Citrus is host to several other Phyllosticta and Guignardia species , and historically 
these species were sometimes misidentified as P. citricarpa (Glienke et al. 2011; Wang et al. 2012) , 
which can lead to uncertainty in distribution records. For example, P. capitalensis  and G. mangiferae 
are widespread geographically, have broader host ranges than P. citricarpa , are present in 
New Zealand (NZFungi 2 2020) and non -regulated ( ONZPR  2020).  
 
 
5.7.1  Summary of conclusions  
• Phyllosticta citricarpa meets the criteria to be a quarantine pest for New Zealand.  
• The association of P. citricarpa  with leafless Citrus budwood  is considered  moderate , with low 
uncertainty.  
• The likelihood of P. citricarpa  entering New Zealand associat ed with leafless Citrus  budwood  
is considered  to be  low, with high uncertainty.  
• The likelihood of P. citricarpa establishing in New Zealand is  considered  to be  high, with low 
uncertainty.  
• The introduction of P. citri carpa is considered likely to cause moderate economic impacts for  
New Zealand overall, but high for the citrus industry, with low uncertainty.  
• The introduction of  P. citricarpa is considered likely to cause low sociocultural impacts for in 
New Zealand,  with low uncertainty.  
• The introduction of  P. citricarpa is considered likely to cause very low environmental impacts 
in New Zealand,  with low uncertainty.  
• The introduction of  P. citricarpa is considered likely to cause very low human health impact s 
for in New Zealand,  with low uncertainty.  
• Phyllosticta citrocarpa may be considered for additional measures  on citrus budwood .  
 
The high uncertainty around the likelihood of entry results from limited information about frequency of 
association of P. cit ricarpa with young, healthy shoots and branches of citrus plants.   
5.7.2  Hazard identification: regulatory status  
 
Given the arguments and evidence below, Phyllosticta citricarpa meets the criteria to 
be a quarantine pest for New Zealand . 
Criteria for being a regulated quarantine pest relevant to this assessment are: the pest is not present 
in the pest risk assessment  area (New Zealand), and  the pest is  of potential importance (able to 
establish and cause harm39). 
 
Phyllosticta citricarpa is not known to be present in New Zealand:  
• Phyllosticta citricarpa  is recorded as ‘recorded in error’ in NZFungi 2 (2020) and NZOR (2020) . 
It is listed as ‘ regulated’ in ONZPR  (2020).  
 
Phyllosticta citricarpa has the potential to establish and spread in New  Zealand . 
 
39 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 89 • Phyllosticta citricarpa is reported from many areas with very similar climate s to the whole of 
New Zealand, indicated by a climate match index (CMI) of ≥0.7 (Phillips et al.  2018) , including 
parts of Argentina, Australia (New South Wales and some parts of Queensland), Uruguay and 
South Africa ( EFSA 2014;  EPPO 2020a)  
• The host range is citrus  and species in related genera in the Rutaceae such as Poncirus and 
Fortunella  (Baayen et al. 2002; EFSA 2014;  Farr and Rossman 2020).  
• Citrus trees are commercially grown in New Zealand and are commonly grown in home 
gardens ( section  2.6).  
 
Phyllosticta citricarpa has the potential to cause economic, soci ocultural  and environmental impacts to 
New Zealand . 
• Phyllosticta citricarpa has the potential to harm citrus , which  is of economic importance to 
New Zealand.  
• Phyllosticta citricarpa has the potential to have soci ocultural impacts , because  citrus is 
commonly planted in home gardens.  
• Given that the reported hosts of P. citricarpa are Citrus, Poncirus or Fortunella  species and 
that there are no native species in  New Zealand in  these genera ( NZFlora 2020 ), impacts on 
native plants are likely to be low.  
• However, it is highly likely that increased applications of fungicides would be required to 
manage the pa thogen in commercial production areas, and this has the potential to cause  
environmental impacts.  
 
5.7.3  Hazard identification: commodity association  
 
Given the arguments and evidence below , the association of P. citricarpa with 
leafless Citrus budwood  is consid ered moderate , with low uncertainty . 
Phyllosticta citricarpa  is reported from most commercially grown citrus species.  
• Hosts of P. citricarpa include lemon, sweet orange, mandarins and grapefruit  (EFSA 2014, 
see Table 11). Fortunella  spp. (kumquat ) and Poncirus  trifoliata  (trifoliate orange ) are also 
susceptible to P. citricarpa  (EFSA 2014) .  
• Although  Tahitian lime ( C. latifolia ) fruit does not show symptoms i n natural infection, even in 
areas with high levels of inoculum , P. citricarpa was isolated from asymptomatic fruit and 
cause d lesions on Tahitian lime leaves  (Baldassari et al. 2008; Wang et al. 2016).  
• Likewise, sour orange ( C. aurantium ) and its hybrids  are often reported as not susceptible to 
the pathogen ( Kotzé 1981 ; Baldassari et al. 2008; EFSA 2014 ), but the fungus has been 
isolated from lesions on fruit of this species ( Baayen et al. 2002 ; Baldassari et al. 2008;  
Wulandari et al. 2009 ; Glienke et al. 2011).  
• There is moderate uncertainty about the host status of pomelo ( C. maxima /C. grandis ). 
Wulandari et al. (2009) classified all the Phyllosticta isolates in their study that came from 
pomelo (as C. maxima ) as Phyllosticta  citriasiana , although most had previously been 
classified as P. citricarpa . These isolates came from China, Thailand and Viet  Nam. In a later 
study, several Phyllosticta isolates from pomelo in Guangdong, Guangxi and Fujian were 
identified as P. citriasiana (Wang et al . 2012) . Phyllosticta citriasiana was not identified from 
other citrus species , and P. citricarpa was not identified in pomelo in these studies.  However, 
Glienke et al. (2011) identified an isolate from C. maxima  in Brazil as P. citricarpa.  
 
Table 11: Citrus and related species that can be infected by P. citricarpa (EFSA 2014)  
Scientific name (EFSA 2014)  Common name (EFSA 20 14) 
C. limon   Lemon  
C. sinensis   Sweet orange  
C.reticulata   Mandarin  
C. unshiu    Satsuma mandarin  
C.paradisi   Grapefruit  
C. medica   Citron  
C.aurantiifolia   Key lime  
C. limettioides   Sweet lime  
C.hystrix   Kaffir lime  
C. latifolia   Tahitian lime (does not produce symptoms on fruit)  
C. aurantium  Sour orange (does not usually produce symptoms)  90 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Scientific name (EFSA 2014)  Common name (EFSA 20 14) 
Fortunella  spp.  Kumquat  
Poncirus trifoliata   Trifoliate orange  
 
 
Phyllosticta citricarpa is reported from  twigs of citrus plants.  
• Small (0.5 –2 mm in diameter), round, slightly sunken lesions with a brown to black margin and 
a grey to light brown centre may occur on small twigs of citrus plants, most often in lemon 
(C. limon ) (IPPC 2014). Pycnidia may occasion ally be present in the centre of the lesions 
(IPPC 2014).  
 
 
5.7.4  Risk assessment: likelihood of entry  
 
Given the arguments and evidence below , the likelihood of P. citricarpa  entering 
New Zealand with  leafless Citrus budwood  is con sidered  low, with high uncerta inty. 
 
The association of P. citricarpa with leafless budwood of Citrus spp. is rated moderate (see above).  
 
There is some evidence that P. citricarpa  can colonise twigs and branches as an asymptomatic 
endophyte , although such infections are rarely detected, and it is uncertain whether they occur in 
young healthy tissues:  
 
• Citrus budwood with visible lesions is highly unlikely to be selected for export to New Zealand.  
o Phyllosticta citricarpa  can cause s mall (0.5 –2 mm in  diameter)  lesions on small twigs , 
most often in lemon plants ( C. limon ) (IPPC 2014) .  
o Twig lesions are  round  and slightly sunken  with a brown to black margin and a grey to 
light brown centre  (IPPC 2014) . Pycnidia may occasionally be present in the  centre of 
the lesions  (IPPC 2014) . The lesions are confined to discrete spots on twigs (Tran et 
al. 2017).  
o Such lesions are likely to be visible, particularly once leaves are removed from the 
budwood.  
• Phyllosticta citricarpa  has been detected in and cultured from citrus  twigs and branches 
without visible symptoms:  
o A recent study investigated the prevalence of P. citricarpa in young C. sinensis shoots 
and C. sinensis branches of different ages (d e Oliveira Silva  et al. 2017). Phyllosticta  
citricarpa was isolated  at a very low frequency (0.8%) from older branches but not 
from young shoots or young branches . The study authors concluded that fungi had 
not yet had an opportunity to colonise these younger tissues, as neither P. citricarpa, 
nor other fungal species were recovered  (de Oliveira Silva et al. 2017) . Dead 
branches also yielded no P. citricarpa , but in this case , it is likely that  the fungus was 
outgrown by other faster -growing fungi such as Colletotrichum  and Penicillium  species  
(de Oliveira Silva et al. 2017) . 
o In inoculation experiments, young branches were coloni sed by P. citrocarpa , and the 
pathogen could be recovered 45 days after inoculation with  no visibly detectable 
lesions or  fruiting bod y formation on  the inoculated tissue ( de Oliveira Silva  et al. 
2017). However, at 90 and 135 days, the pathogen was not recovered from the 
inoculated branches , and lesions or reproductive structures were not observed at any 
stage.  
o In this study, P. citricarpa DNA was not detected by c ulture independent PCR  of DNA 
extracts from  shoots or branches of any age , which de Oliveira Silva  et al. (2017) 
surmised was due to a low concentration of the pathogen in samples.  
o Phyllosticta citricarpa  has been is olated/detected by PCR -based techniques from 
citrus twigs (Meyer et al. 2012). However, the age of the twigs in this study was not 
given. In addition, a positive PCR test result does not necessarily prove that there are 
viable  fungal spores , hyphae or myce lium present .  
• EFSA (2014) notes that citrus plants for planting have been assumed to be a very important 
potential pathway for the entry of P. citricarpa  into new areas , because aerial parts of 
budwood, scions, rootstocks and nursery plants of citrus spec ies may be infected with  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 91 P. citricarpa  without , or with very few , symptoms and citrus plants are normally propagated 
vegetatively by grafting onto rootstocks.  
• EFSA (2014) considered it likely that there will be a high prevalence of P. citricarpa  in citrus 
planting material for propagation purposes if citrus nurseries are located near citrus orchards 
infected by the pathogen.  
• However, EFSA (2014) found no data on the prevalence of P. citricarpa  in citrus nurseries in 
countries where the pathogen is currently distributed and no authenticated records of P. 
citricarpa  introductions into new areas through plants for planting.  
• EFSA (2014) considered that P. citricarpa  is most likely to be associated with plants for 
planting as mycelium in latently inf ected leaves.  
• Therefore, along with visual inspection to remove budwood with visible P. citricarpa lesions, 
removal of the leaves to meet the commodity description reduces the likelihood of P. citricarpa 
entering New Zealand associated with citrus budwood  to low. However, there is high 
uncertainty in this conclusion , because the frequency of asymptomatic P. citricarpa  infections 
of shoots and branches  in natural infection is not well defined . 
 
 
The minimum requirements are unlikely to further reduce the li kelihood of entry , assuming that  
P. citricarpa can (rarely) colonise budwood  in latent infections without causing visible symptoms within 
one growing season . 
• Visual inspection of budwood and the mother plants is likely to detect symptomatic material, 
but n ot asymptomatic infection.  
• Apart from lemons, lesions of P. citricarpa on leaves are rare especially in young healthy 
plants (Kotzé 1981; EFSA 2014). Citrus plants will produce leaves in post entry quarantine but 
will not fruit, which reduces the likelihoo d of P. citricarpa infections being detected.  
• EFSA (2014) considered that it is highly likely that infected citrus plant propagation material 
will be asymptomatic, since citrus black spot symptoms do not generally appear on trees until 
they are over 10 years old, and P. citricarpa has been known to re main latent for even longer 
periods.  
• If P. citricarpa was latent in citrus budwood at the time of entry, s ymptoms may not develop 
during one growing season in post entry quarantine , as plants would be young, well 
maintained and grown under conditions that  enhance growth .  
Given that asymptomatic P. citricarpa  infections of shoots and branches may be extremely rare or may 
not occur in natural infection , there is high uncertainty around the likelihood of P. citricarpa  entering 
New Zealand associated with lea fless Citrus  budwood. At present, there is insufficient evidence to be 
certain whether asymptomatic P. citricarpa  infections of twigs and branches are very rare or if fungal 
mycelium in early infections is present in very low amounts. The fungus is seldom detected by culture -
based or PCR -based techniques. Nevertheless, it is highly likely that if budwood containing latent 
P. citricarpa  mycelium is imported , the infections will escape detection during phytosanitary inspection 
and one growing season in post -entry quarantine.  
 
 
5.7.5  Risk assessment: l ikelihood of establishment  and spread  
 
Given the arguments and evidence below , the likelihood of P. citricarpa establishing 
in New Zealand is  considered  high, with low uncertainty.  
The suitability of the New Zealand environment for P. citricarpa to establish is considered  high. 
Phyllosticta citricarpa  is commonly reported from subtropical citrus -growing areas with summer rainfall. 
Many of these areas have  very similar climate conditions to the whole of New Zealand, indicated by a 
climate match index (CMI) of ≥0.7 modelled by Phillips et al. (2018).  
 
• The current global distribution of P. citricarpa is shown in Figure 7 and the CMI for each 
country/state is given in Table 12. Climate is highly unlikely to limit the establishment of 
P. citrocarpa , because it is reported from many areas with very similar climates to 
New Zealand including Uruguay, regions of Brazil ( e.g. Rio Grande do Sul and Santa 92 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Catarina) , Australia ( e.g. New South Wales and Victoria), and the eastern provinces of South 
Africa  (e.g. Eastern Cape, Kwa Zulu Natal and Mpumalang a).  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Figure 7: Distribution of P. citricarpa  (orange shaded areas and yellow dots indicate countries where P. citricarpa 
has been reported)  (EPPO 2020)    
 
Table 12: Distribution of P. citricarpa  (EPPO 2020a)  
CMI values of ≥0.7 have very similar climate conditions to the whole of New Zealand (Phillips et al.  2018)  
Region  Country  State/Province (if recorded)  CMI range (Philips et 
al. 2018).  
Africa  Angola (restricted distribution)   0.5–0.7 
Ghana (restricted distribution)   ≤0.6 
Kenya   0.4–0.8 
Mozambique   ≤0.6 
Namibia (few occurrences),   0.5–0.7 
South Africa (restricted 
distribution. Not present in 
Western Cape, Northern Cape, 
Free State)  Eastern Cape  0.7–0.9 
Gauteng  0.6–0.8 
KwaZulu -Natal  0.7–0.8 
Limpopo  0.6–0.7 
Mpumalanga  0.7–0.8 
North West Province  0.6–0.7 
Tunisia (restricted distribution)   0.5–0.8 
Uganda   0.5–0.8 
Zambia   ≤0.6 
Zimbabwe   0.5–0.7 
Asia Bhutan   0.4–0.7 
China (restricted distribution)  Fujian  0.6–0.7 
Guangdong  0.4–0.7 
Guangxi  0.5–0.7 
Jiangsu  0.7 
Sichuan  0.6–0.8 
Yunnan  0.6–0.8 
Zhejiang  0.7 
India (restricted distribution)  Maharashtra  ≤0.6 
Indonesia   ≤0.6 
Philippines   ≤0.6 
Taiwan   0.4–0.8 
North America  USA Florida ( Lee, Charlotte, Collier, 
Hendry and Polk counties)  0.5–0.6 
 Cuba   ≤0.6 
South America  Argentina   0.6–0.9 
 Brazil  Amazonas  ≤0.6 
 Espírito Santo  ≤0.6 
 Minas Gerais  ≤0.6 
 Paraná  0.6–0.8 
 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 93 Region  Country  State/Province (if recorded)  CMI range (Philips et 
al. 2018).  
 Rio de Janeiro  0.5–0.7 
 Rio Grande do Sul  0.7–0.9 
 Santa Catarina  0.7–0.9 
 São Paulo  0.5–0.7 
 Uruguay   0.7–0.9 
Oceania  Australia  New South Wales  0.6–0.9 
Queensland  0.4–0.8 
Victoria  0.7 –1 
 
Host availability is unlikely to be a limiting factor for P. citricarpa  to establish in New Zealand  
• Most commercial citrus cultivars are susceptible to P. citricarpa  to some degree ( Table 13) 
especially lemons and sweet oranges (Kotz é 1981)   
• In New Zealand, 783 hectares  are planted in commercial oranges, 556 ha in mandarins, 25 ha 
in lemons and 15 ha in grapefruit ( Plant and Food Research  2019). Citrus is commercially 
produced in both the North Island and the South Island , with most commercial production 
taking place in the North Island (Section 2.4.1 ). Citrus trees are commonly grown in domestic 
gardens.  
 
Phyllosticta citricarpa  is spread by rain splash and wind , and it is likely to spread easily in New 
Zealand once it in fects a susceptible host:  
 
• In Australia, South Africa and South America (Argentina, Brazil) ascospores (sexual spores) 
formed in pseudothecia in leaf litter from citrus trees are the major source of inoculum to 
spread the pathogen  (Reis et al. 2006; Tran e t al. 2017).  
o Release of ascospores from leaf litter requires moisture from rainfall, irrigation or 
possibly heavy dew (EFSA 2014; Reis et al. 2006). Even a small amount of rain can 
trigger ascospore release (Reis et al. 2006).  
o Once released, ascospores ar e spread by wind currents to leaves, twigs and young 
fruit of citrus (Kotz é 1981).   
o Ascospore release in Argentina and South Africa peaks in December –January . In 
Brazil , the peak is January –February (Reis et al. 2006). Ascospores are infectious at 
temperatures between 15 °C and 29.5°C and require 15 –38 hours of wetness (Reis et 
al. 2006; EPPO 2020b).  
o Most citrus plants in New Zealand set fruit in November (late spring/ear ly summer) 
(Brown 20 01), although some citrus trees in New Zealand produce fruit through the 
year.  
o Fruit are susceptible to infection by P. citricarpa  for at least 4 –5 months after petal fall 
(Reis et al. 2006) , and leaves are susceptible for 10 months po st formation (EFSA 
2014). Therefore, susceptible fruit and leaves will almost certainly be present at times 
when ascospores are released.  
• Ascospores require two mating types to be present. However, in Brazil, Zimbabwe and 
Queensland, Australia, conidia (a sexual spores) are now recognised as a significant source of 
inoculum for spreading the pathogen even though ascospores are present (Spósito et al. 
2011; Wang and Dewdney, 2019).  
o Conidia of P. citricarpa are produced in pycnidia in lesions on infected fruit , leaves 
and branches and can be spread by watersplash and windblown rain (Kotz é 1981 ; 
EFSA 2014; Tran et al. 2017) . 
o Phyllosticta citricarpa  is recently invasive in Florida where the disease originated from 
a single clonal lineage. Only one m ating type is present and P. citricarpa  reproduces 
asexually so only conidia (asexual spores) are produced (Wang et al. 2016; Hendricks 
et al. 2020 ). Evidence from Florida suggests that P. citricarpa can establish and 
spread in an area via dispersal of conidia even if only one mating type is present, as 
has apparently happened in Florida  (Tran et al. 2017, 2020; Hendricks et al. 2020 ). 
However, the situation in Florida (with no sexual stage) is currently unique.  
• As most commercial citrus fruit sets in Novem ber (Brown 20 01), young susceptible fruit will be 
most abundant in December and early January when temperatures are likely to be warm 
enough for the fungus to release spores and infect fruit. For example, in Kerikeri, a citrus -
growing region, summers are w arm and humid , and daytime maximum air temperatures 94 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  usually range from 22 °C to 26 °C (Section  2.4.1 ). These conditions are likely to favour infection 
of young fruit with P. citricarpa ascospores  or conidia . 
• Phyllosticta citricarpa  has established and spread  to new area s in other parts of the world.  
o In Nabeul,  Tunisia (an area with a CMI of 0.7 with the whole of New Zealand ), 
symptoms were first observed on lemon and orange fruit in March and April 2019 
(Boughalleb -M’Hamdi et al. 2020) . Following this d iscovery, plants with symptomatic 
fruit were observed in 69 out of 339  lemon and orange orchards  surveyed  from June 
to September 2019  (Boughalleb -M’Hamdi et al. 2020).  
o Phyllosticta citricarpa  was first reported  on sweet orange trees in a grove  in Florida, 
USA in 2010 (Schubert et al. 2012), and by July 2019 , the quarantine zone 
encompass ed 1160.32 km ² in the Lee, Charlotte, Collier, Hendry and Polk counties 
(Hendricks et al. 2020) . 
o In South Africa , disease symptoms were observed for 30 years before the disease 
reached epidemic levels and fungicidal control became necessary (Kotz é 1981).  
 
 
5.7.6  Risk assessment: impacts to New Zealand  
Given  the arguments and evidence below, t he introduction of P. citricar pa is 
considered likely to cause moderate economic impacts for New Zealand , but high  
economic impacts  for the citrus industry, with low uncertainty.  
Damage and symptoms caused by P. citricarpa  can reduce fruit quality.  
• Phyllosticta citricarpa  causes black  spot lesions on citrus fruit ( Figure 8).  
o The most common symptom is shallow lesions  known as hard spots, which are  3–
10 mm in diameter, with a grey to tan centre and a dark brown to black margin (IPPC, 
2014). Pycnidia commonly form in the centre of hard spots (Miles et al. 2019).  
o Lesions range in size from small freckle spots and false melanoses  to virulent spots 
(sunken i rregular red to brown or colourless lesions that form late in the season on 
heavily affected mature fruit)  (IPPC  2014 ). Virulent spots grow rapidly, can cover two 
thirds of the fruit within 4 –5 days and can cause premature fruit drop ( IPPC  2014 ); 
o In Brazil  and Florida, interaction between the fungus and spider mites can result in 
crack s in the skin  (Miles et al. 2019).  
• Infections near the pedicel (stem) of the developing fruit may lead to premature fruit drop 
(Baayen et al. 2002). Yield losses due to prema ture fruit drop have been reported in Brazil 
(Reis et al. 2006). Hendricks et al. (2020) discuss use of fungicides to reduce crop losses due 
to premature fruit drop, suggesting that such losses are also a concern in Florida.  
• Except for C. aurantium  and its  hybrids and  C. latifolia , all commercially grown citrus species 
are susceptible to black spot disease caused by P. citricarpa  (Kotz é 1981). In particular, heavy 
losses of lemon, sweet orange and grapefruit crops are reported.  
• Although the lesions do not usually affect the internal fruit or juice quality, i nfected fruit are 
unmarketable as fresh fruit ( Kotzé 1981; Zavala et al. 2014).  
 
  
Figure 8: Lesions on citrus fruit caused by P. citricarpa.  From left to right: Citrus black spot lesions  (Florida Division 
of Plant Industry Archive 2008) ; hard spot on orange, with pycnidia visible in the middle of the lesions  (Cesar 
Calderon 2006) ; cracked spot lesions on Valencia orange  (P. Barkley 2004). 
 
 
 
 
 
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 95 Phyllosticta  citricarpa has been reported to cause severe damage and production loss of citrus in 
areas with  a similar climate to New Zealand . 
• In 1895 in New South Wales, P citricarpa  caused serious losses to late Valencia oranges from 
blemished fruit from infections in the field and from latent infections which developed on fruit in 
transit (Sutton and Waterston 196 6).  
• In 1945, more than 90% of fruit from unprotected trees in some ar eas of East and North 
Transvaal (now Limpopo and Mpumalanga)  was unfit for export (Sutton and Waterston 196 6).  
• In China , Phyllosticta citricarpa has also been reported to cause crop losses of lemons in 
Sichuan, Valencia oranges in Chongqing and some mandarin varieties in Zhejiang and Jiangxi 
(Wang et al. 2012).  
• Damage from P. citricarpa is most severe when mean maximum temperatures are between 2 –
25°C while the fruit is maturing or when the temperature is 30°C when the fruit is mature 
(Sutton and Water ston 196 6). Therefore, at the times when fruit is maturing in commercial 
citrus -growing areas,  climate  conditions are likely to favour severe damage from the disease. 
However, in New Zealand , average temperatures at harvest are likely to be  lower than 30 °C. 
• Depending on the suitability of the climate and the susceptibility of hosts it can take 5 –30 
years from the time citrus black spot symptoms  are first noticed in an area for the disease to 
reach epidemic proportions (Kotz é 1981). However, if P. citricarpa  established, New Zealand 
is likely to be at the shorter end of that timeframe , given that the New Zealand climate is likely 
to favour spread of the fungus and given that susceptible citrus varieties such as sweet 
oranges and lemons are commonly grown . 
 
If P. citricarpa  becomes established, there are likely to be increased costs to citrus producers from in -
field fungicide applications during fruit development to prevent high levels of infection and damage to 
the crop.  
• For example, in an experimental citrus  plot in São Paulo , Brazil,  that was not treated with 
fungicide during the susceptible period of fruit development, the mature fruit showed 100% 
incidence of citrus black spot  (Baldassari  et al. 2006).  
• In Queensland, São Paulo and Florida, regular applications of fungicide throughout the period 
when fruit are susceptible are necessary to prevent fruit from being infected ( Lanza et al. 
2018 ; Hendricks et al. 2020; Tran et al. 2020).  
• Furthermore,  because of the long latent period,  it is not possible to know if the fungicide 
applications have been successful until the end of the season  when the visible citrus black 
spot symptoms  develop on the fruit ( Tran et al. 2020 ).  
• It is likely that there would be addi tional costs and delay in implementing effective fungicide 
treatments , because research would be required to adapt spray regimes for New Zealand 
conditions. In Brazil, field trials were required because spray regimes from South Africa were 
not as effective  at controlling P. citricarpa in São Paulo (Lanza et al. 2018). Field trials to 
evaluate fungicide  regimes  were also carried out in Florida (Hendricks et al. 2020).  
• Managing the disease with fungicides is costly , and it can be difficult to control the dise ase 
sufficiently to produce fresh fruit that is acceptable to consumers (Tran et al. 2017). Citrus 
black spot disease, caused by the fungus P. citricarpa , is estimated to cost Australian citrus 
growers approximately NZ$80 million  per year through export re strictions, fungicide 
applications and fruit damage (Hort Innovation 2018).  
 
Citrus is economically important in New Zealand (Table 3,  Section 2.6.2 ).  
• Phyllosticta citricarpa would be like ly to affect yields and marketability of most commercial 
citrus crops in New Zealand, including oranges, lemons, mandarins, grapefruit and some 
limes.  
• In 2019 , export sales  of fresh citrus fruit were worth NZ$12 million, and the value of domestic 
citrus sales was NZ$58.5 million (Plant and Food Research  2019).  
 
 
Establishment of P. citricarpa  is likely to increase phytosanitary measures required for export to 
countries where the pest is absent or regulated.  
• Phyllos ticta citricarpa is an A1 pest for the European Union (EPPO 2020a).  It is still regulated 
by the USA and under eradication in parts of Florida (USDA -APHIS 2020). Parts of Australia 96 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  are maintained as pest-free areas for P. citricarpa40. Infected citrus fruit could not be export ed 
to these areas.  
• An incursion of P. citricarpa in New Zealand could cause impacts from removal of productive 
plants, costs of surveillance and loss of income from sales of fresh citrus in domestic and 
export markets. For example, Florida has maintained its quarantine zones for P. citricarpa 
since 2010 , and fresh citrus fruit cannot be transported outside of these areas (USDA -APHIS 
2020).  
 
There is low uncertainty in t his conclusion , because e conomically significant disease has been 
recorded in areas with similar climate to New Zealand, so the impact of P. citricarpa  on the 
New Zealand citrus industry is likely to be high. Evidence from other countries suggests that there will 
be ongoing costs to manage the disease. However, there is some uncertainty about how long it would 
take for impacts to become seve re. Impacts are likely to increase over time as inoculum levels 
increase and the disease spreads to new areas of New Zealand.  
 
 
Given the arguments and evidence below, t he introduction of  P. citricarpa is 
considered likely to cause low sociocultural impacts in New Zealand,  with low 
uncertainty.  
• Phyllosticta citricarpa can sometimes cause premature fruit  drop, which would affect the 
productivity of citrus trees in home gardens.  
• Damage to fruit from home gardens may make such fruit unattractive; although the damage is 
limited to the peel and is not known to affect the quality or taste of the fruit itself.  
 
 
Given the arguments and evidence below, t he introduction of  P. citricarpa is 
considered likely to ca use very low environmental impacts in New Zealand is likely , 
with low uncertainty.  However , there may be some indirect impacts  in citrus 
producing areas due to increased use of fungicides to control the disease.  
• Developing fruit are susceptible to P. citri carpa for several months, and regular spraying with 
fungicide is current practice in areas with the disease . 
•  For example, in Florida, the recommended fungicide regime for control of P. citricarpa  is to 
apply fungicides on a 21 - to 28-day cycle from early May (late spring) to mid -September (early 
autumn) (Hendricks et al. 2020). Recent research suggests that fungicide applications over an 
even longer period of 180 or 220 days would more effectively protect the fruit. In São Paulo  
fungicide applications  at intervals through the production period  are used  to prevent infection 
of fruit with P. citricarpa (Lanza et al. 2018) . 
• Since P. citricarpa is mostly reported as a citrus pathogen , and there are no native species of 
Citrus  (or Poncirus  or Fortunella ) (Allan  Herbarium 2020 ), it seems likely that environmental  
impacts would be low.  
• There is low uncertainty in this conclusion. Although there are historic reports of a non -
pathogenic form of P. citricarpa from other plant families (Anacardiaceae, Aquifoliaceae, 
Bignoniaceae, Burseraceae, Cunoniaceae, Dioscoreaceae, Gramineae, Lauraceae, 
Leguminosae, Liliaceae, Lythraceae, Magnoliaceae, Myrtaceae, Orchidaceae, Passifloraceae, 
Proteaceae, Rosaceae, Rutaceae, Solanaceae, Sterculiaceae, Theaceae) (Sutton and 
Waterston  1966) , records on hosts outside the Rutaceae  family  are doubtful and presumably 
refer to Phyllosticta  capitalensis  or Guignardia  mangiferae  (Glienke et al. 2011 ; Farr and 
Rossman 2020 ). 
 
Given the arguments and evidence below, the introduction of P. citricarpa is 
considered likely to cause very  low human health impacts in New Zealand,  with low 
uncertainty.  
• Phyllosticta citricarpa is a plant pathogen , and no evidence was found of effects on  human or 
animal health.  
 
40 MICoR (Australian Government Depart ment of Agriculture, water and the Environment Manual of Importing Country 
Requirements; Lemons; European Union): The European Union formally recognises the states of South Australia, and Western 
Australia as free from black spot (Phyllosticta citricarpa ). 
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 97 • However, there is potential for  indirect impacts on human health due to  increased use of 
fungicides for pathogen control.  
 
 
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Wang, N -Y; Rascoe, J; Picton, D (2012) First report of Guignardia citricarpa  associated with citrus 
black spot on sweet orange ( Citrus sinensis ) in North America . Plant Disease , 96(8): 1225 . 
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Sutton, B C; Waterston, J M (1966) Guignardia citricarpa.  [Descriptions of Fu ngi and Bacteria]. IMI 
Descriptions of Fungi and Bacteria . No. 9 : 85 ref.8.  
 
Tran, N T; Miles, A K; Dietzgen, R G; Dewdney, M M; Zhang, K; Rollins, J A; Drenth, A (2017) Sexual 
reproduction in the citrus black spot pathogen Phyllosticta citricarpa. Phytopathology , 107: 732 –739. 
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Tran, N T; Miles, A; Dietzgen, R G; Shuey, T A; Mudge, S R; Papacek, D; Chandra, K A; Drenth, A 
(2020) Inoculum dynamics and infection of citrus fruit by  Phyllo sticta citricarpa . Phytopathology , 110 
(10): 1680 –1692 . https://apsjournals.apsnet.org/doi/abs/10.1094/PHYTO -02-20-0047 -R  
 
USDA -APHIS (2020) Plant Pests and Diseases Program s: Citrus black spot. 
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56762014000200002   
  100 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  5.8 Plenodomus tracheiphilus  (mal secco disease of citrus)  
 
Plenodomus tracheiphilus  is a mitosporic (asexual) fungal pathogen that causes  mal secco , a highly 
destructive vascular disease of Citrus  (especially lemon) and related genera. The disease lowers fruit 
yield, resulting f rom a reduction in canopy volume  due to twig death, and eventually kills affected trees 
(Migheli et al. 2009).  
 
Taxonomy  
Scientific name:  Plenodomus tracheiphilus (Petri) Gr uyter, Aveskamp & Verkley  
Order/ family: Pleosporales/Leptosphaericeae  
Other scientific names: Phoma tracheiphila ; Bakerophoma tracheiphila ; Deuterophoma tracheiphila  
Common name: mal secco, mal secco of citrus, c itrus mal secco, citrus wilt, mal secco disease of 
citrus, dieback of citrus, wilt of citrus (E FSA 2014 ; EPPO 2020)  
 
General information on the  biology  of P. tracheiphilus  
Plenodomus tracheiphilus only reproduces asexually , and no sexual stage  (teleomorph)  of this fungus 
has been identified (Perrotta and Graniti 1988; Migheli et al. 2009; EFSA 2014). The asexual fruiting 
bodies (pycnidia) usually develop on withered twigs as raised black spots within lead -grey or ash -grey 
areas and produce infective conidia  (pycnoconidia). Phialides on ‘free’ mycelial hyphae growing in the 
xylem, on wounded plant tissues and exposed wood surfaces of t he tree or in debris also produce 
conidia (phialoconidia) (Perr otta and Graniti 1988). Dispersal of conidia from pycnidia and exposed 
phialides to other parts of the same plant or to a new host occurs mainly by rain (especially windblown 
rain), but conidia  can also be dispersed by overhead irrigation,  wind, birds, ins ects and farm tools, etc. 
(Migheli et al. 2009; Nigro et al. 2011). The conidia infect host tissue (leaves, twigs, branches, roots) 
via wounds/injuries caused by cultivation practices, hail and frost, insect/bird feeding and other means, 
and eventually rea ch the xylem vessels. Infection of the host and disease development is favoured by 
warm, humid conditions (14 –28°C and 65 –90% relative humidity), with 20 –25°C being the optimum 
temperature range for mycelial growth of the fungus and symptom expression, and  30°C stopping 
fungal growth inside the host (Perrotta and Graniti 1988).  
 
5.8.1  Summary of conclusions  
• Plenodomus tracheiphilus  meet s the criteria  to be a quarantine pest for New Zealand . 
• The association of Plenodomus tracheiphilus  with leafless citrus  budwood  (especially lemon, 
Citrus limon ) is considered strong, with low uncertainty . 
• The likelihood of Plenodomus tracheiphilus  entering New Zealand associated with leafless 
Citrus budwood  is considered low, with low uncertainty.  
• The likelihood of Plenodomus tracheiphilus  establishing in New Zealand is considered  high, 
with low uncertainty.  
• The introduction of  Plenodomus tracheiphilus  is considered likely to cause low economic 
impacts for New Zealand (but impacts in citrus, specif ically lemon production is likely high), 
with moderate uncertainty.  
• The introduction of Plenodomus tracheiphilus  is considered likely to cause moderate 
sociocultural impacts in New Zealand , with low uncertainty.  
• The introduction of Plenodomus tracheiphilus  is considered likely to cause negligible 
environmental impacts in New Zealand, with low uncertainty.  
• The introduction of Plenodomus tracheiphilus  is considered likely to cause negligible human 
health impacts in New Zealand, with low uncertainty.  
• Plenodomu s tracheiphilus  may be considered for additional measures  on citrus budwood .  
 
 
 
 
 
 
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 101 5.8.2  Hazard identification: regulatory status  
Given the arguments and evidence below , Plenodomus tracheiphilus meets the 
criteria to be a quarantine pest for New Zealand . 
Criteria for being a regulated quarantine pest relevant to this assessment are: the pest is not present 
in the pest risk assessment  area (New Zealand), and  the pest is  of potential importance (able to 
establish and cause harm41). 
 
Plenodomus tracheiphilus  is not known to be present in New Zealand . 
• Plenodomus tracheiphilus  is not listed in NZFungi 2 (2020) or PPIN (2 020). 
• Plenodomus tracheiphilus  (listed as Phoma tracheiphila , synonyms: Bakerophoma 
tracheiphila , Deuterophoma tracheiphila ) is a regulated pest for New Zealand  (ONZPR  2020; 
BRAD  2020). 
Plenodomus tracheiphilus  has the potential to establish in New Zealand:  
• Plenodomus tracheiphilus  is present in Africa: Algeria, Egypt, Libya, Tunisia ; Asia: Armenia , 
Iraq, Israel, Lebanon, Republic of Georgia, Syria, Turkey, Yemen ; Europe: Albania, Cyprus, 
France, Greece, Italy, Spain, Russia  (CPC 2019; EPPO 2020).  
• Based on a climate match index (CMI) developed by Phillips et al . (2018 ), some of the above 
countries (or regions within) have high climate  similarity (CMI ≥0.7) to New Zealand , including 
areas where citrus is grown : Albania (0.8 –0.9); Algeria ( 0.3–0.8); Armenia (0.7 –0.8); France 
(0.8–0.9); Georgia (0.7 –0.9); Greece (0.7 –0.9), Italy (0.8 –0.9); Lebanon (0.7 –0.8); Turkey 
(0.7–0.9); Spain (0.8 –0.9).  
• Lemon ( C. limon ), which is the most susceptible host of P. tracheiphilus , is commercially 
grown across 257 ha in the warmer northern parts of New Zealand ( Plant and Food Research 
2019), as well as in home gardens across the country.  
• Following establis hment, l ong-distance spread of the pathogen between orchards and regions 
is likely to occur  mainly through  the distribution of infected material (budwood or whole plants)  
for planting  (Nigro et al. 2011; CPC 2019; EPPO 2020).  
Plenodomus tracheiphilus  has the potential to cause economic and sociocultural consequences . 
• Plenodomus  tracheiphilus  is the most destructive fungal pathogen of lemons ( C. limon ) in the 
Mediterranean region and ca n affect 100% of trees in an orchard of a susceptible lemon 
cultivar (Perrotta and Graniti 1988, cited in  Migheli et al. 2009; Nigro et al. 2011; EFSA 2014 ). 
• The pathogen reduces the quantity and quality of lemon production and kills infected plants, 
thus limiting the use of susceptible species and cultivars, some of which produce better quality 
fruit than less susceptible cultivars (Migheli et al. 2009; Nigro et al. 2011; EPPO 2020).  
• Lemons have cultural value in New Zealand, as fruit from home gardens is commonly shared 
with family, friends and colleagues . 
 
5.8.3  Hazard identification: commodity association  
Given the arguments and evidence below , the association of Plenodomus 
tracheiphilus  with leafless Citrus budwood  (especially C. limon ) is rated as strong, 
with low uncertainty . 
 
Plenodomus tracheiphilus is reported from citrus, especially lemons . 
• Almost all citrus species are susceptible to P. tracheiphilus by inoculation, but l emon ( Citrus 
limon ) is the main  host, and the only species in which economic damage has been widely 
reported (Raimondo et al. 2007; Migheli et al. 2009; Nigro et al. 2011; EFSA 2014; Ben -Hamo 
et al. 2020).  
• Other Citrus  species and related genera in the Rutaceae family are listed as either m inor or 
incidental hosts , although CPC (2019) includes citron ( C. medica ) and bergamot 
(C. bergamia ) as main hosts (Table 14). 
 
41 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for fa ctors to consider 
when defining “harm”.  102 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Table 14: List of P. tracheiphilus  hosts (from EPPO 2020 and CPC 2019)  
Scientific name  Common name  Host Status  (EPPO 2020)  Host status (CPC 2019)  
C. limon  Lemon  Major  Main  
C. aurantiifolia  Mexican/ key lime  Minor  Other  
C. aurantium  Sour orange  Minor  Other  
C. bergamia  Bergamot  Minor  Main  
C. jambhiri  Rough lemon  Minor  Other  
C. medica  Citron  Minor  Main  
C. deliciosa  Tangerine  Incidental  Not listed  
C. paradisi  Grapefruit  Incidental  Other  
C. reticulata  Mandarin  Incidental  Other  
C. sinensis  Sweet orange  Incidental  Other  
C. unshiu  Satsuma mandarin  Not listed  Other  
C. latifolia  Tahiti lime  Not listed  Other  
C. nobilis  Tangor  Not listed  Other  
C. limonia  Mandarin lime  Not listed  Other  
C. macrophylla  Alemow  Not listed  Other  
C. volkameriana  Volkamer lemon  Incidental  Not listed  
C. myrtifolia  Myrtle-leaved orange  Minor  Not listed  
Citroncirus   Minor  Not listed  
Fortunella  Kumquat  Minor  Other  
Poncirus trifoliata  Trifoliate orange  Minor  Other  
× Citrofortunella 
microcarpa  Calamansi/Philippine 
lemon  Minor  Other  
 
Plenodomus tracheip hilus is a systemic pathogen , and conidia and mycelia are likely to be present in 
young twigs and stems of infected plants:  
• The pathogen infects host tissues (leaves, branches, twigs and roots) through 
wounds/injuries , and invades  the lumen of the xylem  where it  spreads systemically ; being 
transported in the xylem sap (Perrott a and Graniti 1988).  
• Systemic infection due to the presence  of conidia and mycelia i n the xylem means that most 
parts of the tree are able to carry the fungus  (Perrott a and Graniti 1988 ). 
 
5.8.4  Risk assessment: likelihood of entry 
Given the arguments and evidence below, t he likelihood of Plenodomus tracheiphilus  
entering New Zealand associated with leafless Citrus budwood is low, with low 
uncertainty . 
• Plenodomus tracheiphilus  has a strong association with budwood of Citrus : Although almost 
all citrus species are susceptible when artificially inoculated , field observations show that 
lemon ( C. limon ) is the most susc eptible citrus species (Migheli et al. 2009; Nigro et al. 2011; 
EFSA 2014; CPC 2019; EPPO 2020).  
• CPC (2019) considers citron ( Citrus medica ) and bergamot ( C. bergamia ) susceptible 
varieties, but there is little supporting field evidence.  
• The pathogen is systemic. However, mycelial growth is inhibited inside the host during hot 
periods ( >30°C)  (Perrotta and Graniti 1988), and trees that are only recently infected in these 
conditions may appear healthy while harbouring conidia and mycelia systemically (Migh eli et 
al. 1981).  
• Plenodomus  tracheip hilus has been detected  by PCR  in twigs collected from naturally infected 
asymptomatic p lants (Balmas et al. 2005) .  
• Based on the last two points above, there is the potential for some contaminated material to 
be colle cted as budwood.  
However:  
• It is unlikely that p lants from areas with high levels of mal secco disease or severely infected 
plants with obvious symptoms will be used to produce commercial budwood material.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 103 • Material infected with P. tracheiphilus is unlikely to be included if budwood is collected in 
spring when symptoms are clearly visible . The disease first appears  as shoot and interveinal 
leaf chlorosis , followed by dieback of twigs and branches  (Migheli et al. 2009; Nigro et al.  
2011; EFSA 2014; CPC 2019).  
• In addition, w hen the wood of infected twigs, branches or trunks is cut or stripped of bark, a 
characteristic salmon -pink or orange -red discolouration of the wood may be seen; this internal 
symptom is associated with gum produc tion within the xylem vessels (Perrotta and Graniti 
1988).   
Minimum requirements reduce the likelihood of entry by a high degree, with low uncertainty . Although 
symptoms may not always be obvious prior to export, they are likely to be detected during one 
growing season in post-entry quarantine . 
• Warm moist conditions are conducive to infection of the host and disease development ; 
conidia germinat e at temperatures between 5°C and 30°C , with 20–25°C being the range for 
optimum  growth of mycelium within the hos t (Perrott a and Graniti 1988 ; Migheli et al. 2009; 
Nigro et al. 2011).  
• Although temperature regulation is not a general requirement in Level 3A post-entry 
quarantine  facilities, temperature and other conditions (e.g. humidity) must be adequate for 
the plan ts to grow through a full growing season. This will likely include temperatures within 
the range (14–28°C) suitable for the fungus to grow and express symptoms. Average summer 
temperature s across most of New Zealand’s North Island, for example, range from 18–21°C  
(NIWA 2020).  
• Disease symptoms first appear on new growth as shoot and interveinal leaf chlorosis , followed 
by dieback of twigs and branches , with leaves falling off while their petioles remain attached to 
the twigs/branches (Migheli et al. 2009; Nigro et al. 2011). The growth of sprouts from the 
base of the affected branches and  growth of  suckers from the rootstock are also very common 
respon ses of host plants to infection (Migheli et al. 2009; Nigro et al. 2011) . 
• In a laboratory experiment in which seedlings of sour orange ( C. aurantium ) were  inoculated 
with P. tracheiphilus  and incubated at 25 °C, leaf chlorosis was evident 5 –7 days post 
inoculation , and by day 25,  the chlorosis covered ∼30% of leaf surface area (Raimondo et al. 
2007). The leaf blade was shed between 45 and 55 days after inoculation , and the petiole was 
shed some days later. At leaf blade shedding, ∼45% of the leaf surface are a was still green 
with no visible symptoms of damage. Also, the expanded ‘wings’ of the petiole were green and 
visually healthy (Raimondo et al. 2007).  
• Perrotta and Graniti (1988) also reported that on sour orange seedlings  artificially infected with 
P. tracheiphilus , pycnidia (which appear as black spots within lead -grey or ash -grey areas on 
affected twigs) were more abundant at a mean temperature of 10.5 °C (range 3 –19°C) than at 
20–22°C, and optimum differentiation and development of pycnidia in vitro  occurs between 
10°C and 15°C . 
• Based on the above evidence, it is very likely that plants grafted with P. tracheiphilus -infected 
budwoo d and grown in a Level 3A post-entry quarantine  facility will show visible symptoms.  
 
If P. tracheiphilus produces symptoms in Level 3A  post-entry quarantine , the conidia produced during 
the growing season are likely to be contained . 
• The conidia of P. tracheiphilus are non -motile and rely mainly on passive dispersal by 
watersplash, windblown rain, insects, birds, etc . to infect new host plant tissues (Perrotta and 
Graniti  1988) .  
• Isolation of P. tracheiphila from air samples in Italy  (Balmas et al. 2005 ) suggests that conidia 
may be airborne, but airborne conidia may have limited mobility; the fungus  spread only a 
short  distance  (15–20 m) from an inoculum  source, although distance of spread may be 
increased by the prevailing wind direction  (Laviola and Scarito 1989, cited in Nigro et al. 
2011) . 
• On the other hand, Tuttobene (1994 ) (cited in Nigro et al. (2011)) explains that the  short 
distance travelled by P. tracheiphila  pycnoconidia indicates that these conidia do not behave 
as other airborne disseminated conidia , which tallies with the notion that they are immersed in 
mucilage  and are , therefore, mainly dissem inated by rain -splash or irrigation.   104 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  • It is unlikely there will be strong winds in a Level 3A post-entry quarantine  facility , and, as 
such, the likelihood that airborne spores of P. tracheiphila will escape is very low , even though 
these facilities do not have measures to contain airborne fungal spores (MPI 2019) .  
• If P. tracheiphilus spores escape  from the facility via wind action, they are not likely to land on 
a suitable host, unless a citrus orchard is located close to the post-entry quarantine  facility , 
which is very unlikely .  
• Other measures in place within Level 3A glasshouses (including protective clothing, 
handwashing) (MPI 2019)  further reduce the likelihood of any conidia leaving the glasshouse 
due to human activity and, potentially, transferring to a suitable host.  
Uncertainty:  
Uncertainty, with respect to entry, is mainly due to the slight possibility that spores produced in post-
entry quarantine  may become airborne and escape into the environment , although this, and 
subsequent exposure to host p lants, is unlikely.  
 
5.8.5  Risk assessment: l ikelihood of establishment and spread  
Given the arguments and evidence below, t he likelihood of Plenodomus tracheiphilus  
establishing in New Zealand is considered  high, with low uncertainty . 
 
Environmental conditions (climate and host availability) in New Zealand, and the biology of the 
pathogen make establishment likely . 
• Plenodomus tracheiphilus  occurs in Africa : Algeria, Egypt, Libya, Tunisia ; Asia: Armenia , Iraq, 
Israel, Lebanon, Republic of  Georgia, Syria, Turkey, Yemen ; and Europe : Albania, Cyprus, 
France, Greece, Italy, Spain, Russia  (CPC 2019; EPPO 2020).  
• Based on a climate match index (CMI) developed by Phillips et al . (2018 ), some of the above 
countries (or regions within) have  a suffic iently similar climate  (CMI ≥0.7) to New Zealand , 
including to areas in New Zealand where citrus is grown : Albania (0.8 –0.9); Algeria (some 
parts have 0.7 –0.8); Armenia (0.7 –0.8); France: Corsica (0.8 –0.9); France (0.9); Georgia (0.7 –
0.9); Greece (0.7 –0.9); Lebanon (0.7 –0.8); Turkey (0.7 –0.9); Italy: Sardinia (0.8 –0.9), Sicily 
(0.7–0.8); Spain (0.8 –0.9).  
• Average summer temperatures of 18–21°C , and average annual temperatures of 10 –16°C in 
New Zealand’s citrus -growing areas  (NIWA 2020)  are adequate for survival of the fungus , 
because  the conidia (spores) germinate at temperatures between 5°C and 30°C, with 
optimum mycelial growth within the host occurring between 20 –25°C (Migheli et al. 2009; 
Nigro et al. 2011).  
• Lemon ( C. limon ), which is the most susceptible host of P. tracheiphilus , is commercially 
grown on about 260 hectares in the warmer northern parts of New Zealand’s North Island 
(Plant and Food Research  2019) and is the most common citrus variety in home gardens 
across the country . 
 
Once established, the pathogen is likely to spread . 
• Short -range (within orchard) spread of P. tracheiphilus  is very likely to occur via conidia, 
dispersed mainly by water (rain splash, windblown rain, overhead irrigation). Conidia may also 
be carried by birds and insects or on contaminated tools such as pruning shears ( Migheli et al. 
2009; Nigro et al. 2011 ). 
• The primary source s of inoculum  are conidia  from pycnidia  that develop  mainl y on young 
shoots of diseased plants  at relatively low temperatures in late autumn and winter  (Nigro et al. 
2011). Phialoconidia, which are produced quickly and abundantly by hyphae on wounded 
infected shoots , are responsible for the epidemic explosion of infections after hailstorms 
and/or heavy rain with strong wind during late summer  to early autumn, when there are no 
pycnoconidia able to germinate (Perrotta and Graniti 1988;  Migheli et al. 2009; Nigro et al. 
2011).  
• Infected twigs and branches can remain infectious for several weeks , and fungal propagules 
can survive within plant debris in orchard soil for up to a year (De Cicco et al. 1987 cited in 
Migheli et al. 2009). The fungus can survive long term in the vascular tissues of citrus plants , 
because  citrus is a perennial host (Nigro et al. 2011).   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 105 • Long -distance spread of the pathogen between orchards and regions is likely to occur mainly 
through the distribution of infected budwood or whole plants for planting (Nigro et al. 2011; 
CPC 2019; EPPO 2020).  
 
5.8.6  Risk assessment: i mpacts  to New Zealand  
Given the arguments and evidence below , the introduction of  Plenodomus 
tracheiphilus  is likely to cause low economic impacts for New Zea land (but its impact 
on commercial lemon production and export is likely to be high), with moderate 
uncertainty.  
• In the Mediterranean region, P. tracheiphilus  is the most destructive fungal pathogen of 
lemons ( C. limon ) and can affect 100% of trees in an orchard of a susceptible lemon cultivar 
(Perrotta and Graniti 1988; Nigro et al. 2011; CPC 2019 ). 
• Further, P. tracheiphil us is likely to affect exports of New Zealand lemons due to phytosanitary 
measures that will be re quired, given that the pathogen is a quarantine p est for several 
regional plant protection services  that cover many countries, i.e. the European and 
Mediterranean Plant Protection Organization (EPPO), the Asia and Pacific Plant  Protection 
Commission (APPPC ), the Caribbean Plant Protection Commission (CPPC), the Comité de 
Sanidad Vegetal del Cono Sur (COSAVE), the Inter-African Phytosanitary Council (IAPSC), 
the North American Plant Protection Organization (NAPPO)  and the  Pacific Plant Protection  
Organi sation (PPPO) , and national plant protection organisations (Nigro et al. 2011; EPPO 
2020).  
• By attacking the vascular system, which leads to dieback and eventual death of affected 
plants, mal secco disease reduces the quantity and quality of lemon production and  limits the 
use of susceptible cultivars that produce better quality lemons than less susceptible cultivars 
(Migheli et al. 2009; Nigro et al. 2011; EFSA 2014; CPC 2019; EPPO 2020).  
• A rapidly fatal form of the disease, described as “mal fulminante”, is app arently due to root or 
stem infections that quickly invade the functional xylem, causing a rapid wilting of branches or 
the whole tree (Perotta and Graniti 1988; Migheli et al. 2009; Nigro et al 2011; EFSA 2014).  
• Given its high susceptibility to the pathog en, lemon is citrus crop most likely to be  affected if 
mal secco establishe s in New Zealand . Lemons had a domestic sales value of NZ$12 million  
in 2018/ 2019 and an export (f ree-on-board) sales value of NZ$9.8 million  in 2019 ( Plant and 
Food Research  2019).  
• The o ptimum temperature range for disease development is 20 –25°C . Hence, in the 
Mediterranean region, mal secco disease progresses rapidly in the spring and autumn and 
slows down in the summer when high temperature s (≥30°C) inhibit  the growth of the fungus 
and invasion of the hosts’ vascular system (Perrotta and Graniti 1988; Migheli et al. 2009; 
Nigro et al. 2011 ; Ben -Hamo et al. 2020) . 
• In contrast to the Mediterranean region, disease severity could remain moderate -to-high 
throughout summer in New Zealand’s main citrus production areas where the average 
summer temperature range is 18–21°C  (NIWA 2020) , and not high enough (i.e. less than 
30°C) to inhibit the pathogen’s growth and its invasion of the host vascular system (Perrotta 
and Gr aniti 1988; Migheli et al. 2009; Nigro et al. 2011 ; Ben -Hamo et al. 2020) . 
• Additional production costs will be incurred for control measures, which mainly comprise of 
cultural practices such as pruning and burning of infected branches or whole plants (Migh eli et 
al. 2009; EFSA 2014; CPC 2019; EPPO 2020).  
• Economic i mpact may be mitigated by the fact that trifoliate orange ( Poncirus trifoliata ), the 
most widely used rootstock in New Zealand commercial citrus  (Currie and Harty 2001 ), is 
reported to be resistant /tolerant  to P. tracheiphilus  (Perrotta and Graniti 1988 ; CPC 2019 ). 
However,  the extent to which trifoliate rootstock would reduce severity of the disease on  
commercial lemon cultivars  in New Zealand  (e.g. Yen Ben)  is uncertain , because there are no 
data on the s usceptibility of New Zealand scion cultivars to the pathogen . 
• Plenodomus tracheiphilus has not been reported as causing economic damage in other citrus 
varieties (CPC 2019; EPPO 2020).  106 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Given the arguments and evidence b elow, the introduction of  Plenodomus 
tracheiphilus  is considered likely to cause moderate sociocultural impacts in 
New Zealand, with low uncertainty . 
• Lemon trees are widely grown in home gardens across New Zealand, and lemon s are  
commonly shared with frien ds, families and colleagues. The spread of mal secco disease to 
home gardens is, therefore, likely to cause sociocultural impact s. 
• Other citrus varieties grown in home gardens, e.g. oranges and mandarins, are not likely to be 
affected . The pathogen has only been reported causing damage/losses in lemons (CPC 2019; 
EPPO 2020).  
 
Given the arguments and evidence below , the introduction of  Plenodomus 
tracheiphilus is likely to cause negligible  to very low environmental impact s in 
New Zealand , with low uncertainty . 
• Plenodomus tracheiphilus is mainly reported as a pathogen of Citrus , with occasional reports 
from Poncirus  and Fortunella , but there are no native species of these genera in New Zealand  
that could be affected.  
 
Given the arguments and evidence  below , the introduction of Plenodomus 
tracheiphilus is likely to cause negligible human health impacts  in New Zealand , with 
low uncertainty . 
• Plenodomus tracheiphilus is not known to cause any disease or health conditions in humans.  
 
 
5.8.7  References  
Ben-Hamo, M ; Ezra, D ; Krasnov, H ; Blank, L (2020) Spatial and temporal dynamics of mal secco 
disease spread in lemon orchards in Israel.  Phytopathology , 110(4) : 863–872. 
BRAD (2020) Biosecurity Risk Analysis Database. Ministry for Primary Industries intern al database. 
Accessed 10 November 2020 . 
Currie, A; Harty, A (2001) Lemons and limes . Rootstocks . In Mooney , P (ed)  Growing Citrus  in New 
Zealand : A practical guide. HortResearch and New Zealand Citrus Growers Inc. ; Wellington, New 
Zealand.  Pp 17 –25. https://www.zeafruit.co.nz/wp -content/uploads/2019/01/NZCGI -Growing -Citrus -in-
NZ-A-Practical -Guide.pdf  Accessed 17 November 2020 . 
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Accessed 18 November 2020.  
EFSA (2014) EFSA Panel on Plant Health. Scientific Opinion on the pest categorisation of 
Plenodomus tracheiphilus  (Petri) Gruyter, Aveskamp & Verkley [syn. Phoma tracheiphila  (Petri) L.A. 
Kantschaveli & Gikashvili] . EFSA Journal , 12(7): 3775 –3808.  
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2020 . 
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agent of mal secco disease of citrus, in Israel. European Journal of Plant Pathology , 118(2) : 183–191. 
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disease caused by Phoma tracheiphila : a potential threat to lemon production worldwide. Plant 
Disease , 93(9): 852 –867.  
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Quarantine for Plants . https://www.mpi.govt.nz/dmsdocument/11368 -Post-Entry -Quarantine -for-
Plants -Facilities -Standard  Accessed 13 November 2020.  
 
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research. Journal of Plant Pathology , 93(3): 523 –560. 
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Database . https://nzfungi2.landcareresearch.co.nz/  Accessed 10 November 2020.  
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Perrotta , G; Graniti , A (1988 ) Phoma tracheiphila  (Petri). Kantschaveli et Gikashvili. In Smith , I M; 
Dunez , J; Lelliot , R A; Phillips , D H; Archer , S A (eds) European Handbook of Plant Diseases . 
Blackwell Scientific Publications ; Oxford, UK . Pp 396–398. 
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Biology , 34(8): 720 –729. 
  108 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  6 Pest risk assessment: Viruses  
 
6.1 Citrus leprosis viruses  
Citrus leprosis is a non -systemic disease caused by several viruses that are spread by species of 
Brevipalpus  mites. Local necrotic lesions form on the surf ace of citrus leaves, stems and fruit at the 
feeding sites of mites  that carry the viruses . Severe disease can result in extensive crop loss and tree 
debilitation .  
 
Taxonomy  
Notes: Although the  viruses that cause citrus leprosis are  from two taxonomic orders, they have some 
important features in common: the production of non -systemic lesions on citrus and transmission by 
tenuipalpid false spider mites in the genus Brevipalpus  (EFSA 2017 ). 
There are two forms of citrus leprosis : the c ytoplasmic form (CL -C) where the virus particles replicate 
in the cytoplasm of infected host cells, and the nuclear form (CL -N) where they replicate in the nucleus 
(Cook et al. 2019 ). 
CL-C is caused by three viruses from two genera, Cilevirus  and Higreviru s, in the family Kitaviridae : 
Citrus leprosis virus C  (CiLV -C), Citrus leprosis virus C2  (CiLV -C2) and Hibiscus green spot virus 2  
(HGSV -2). 
CL-N is caused by three viruses from the one genus, Dichorhav irus, but in a different family 
(Rhabdo viridae ) and or der (Mononegarivales ) from the CL -C viruses: Orchid fleck dichorhavirus  
(OFV), Citrus leprosis N dichorhavirus  (CiLV -N) and Citrus chlorotic spot dichorhavirus  (CiCSV).  
 
Scientific name:  Citrus leprosis virus C  
Order/ family/genus : Martellivirales /Kitaviridae /Cilevirus  
Other scientific names: Citrus leprosis virus  
Abbreviation: CiLV -C 
Notes:  CiLV -C is the most widespread and best studied of the viruses associated with citrus leprosis  
disease (Bastianel et al. 2010). Its geographic ra nge appears to be confined to the Americas. Sweet 
orange ( Citrus sinensis ) is the most susceptible host while other citrus species are affected to varying 
degrees with many more recently considered resistant or asymptomatic to leprosis (Chagas 2000; 
Bastia nel et al. 2010 ). 
 
Scientific name : Citrus leprosis virus C2  
Order/ family/genus : Martellivirales /Kitaviridae /Cilevirus  
Abbreviation: CiLV -C2 
Notes:  CiLV -C2 has been identified in s weet orange ( C. sinensis ) in several citrus -growing areas in 
Colombia. It was recognised as a distinct virus from CiLV -C after tests for the latter failed on 
symptomatic material ( Roy et al. 2013a ). 
 
Scientific name:  Hibiscus green spot virus 2   
Order/ family/genus : Martellivirales /Kitaviridae /Higrev irus 
Abbreviation:  HGSV -2 
Notes:  HGSV -2 was first found in Hawaii in association with mild citrus leprosis -like symptoms in 
Volkamerian lemon ( Citrus volkameriana ) and nearby symptomatic Hibiscus arnottianus  plants 
(Melzer et al. 2012 ). Surveys have shown that its host range includes mandarin  (C. reticulata ), navel 
orange (C. sinensis ) and Hibiscus tiliaceus  (Roy et al. 2015a ). 
 
Scientific name:  Orchid fleck dichorhavirus [citrus  strain]  
Order/ family/genus : Mononegarivales /Rhabdoviridae /Dichorhavirus  
Other scientific names:  Orchid fleck virus  (OFV), citrus strain of Orchid fleck virus , Citrus necrotic 
spot virus , Citrus leprosis virus N  
Abbreviation s: OFV, CiNSV  
Notes: OFV has been identified in citrus in association with citrus leprosis  (Roy et al. 2020 ). The 
associated isolates were earlier known as Citrus leprosis virus N  (reported from Brazil, Colombia, 
Mexico and Panama) (Roy et al. 2013b; Roy et al. 2015a ) and Citrus necrotic spot virus  (reported from 
Mexico) (Cruz -Jaramillo et al. 2014 ) but hav e since been reclassified as variants of OFV ( Afonso et al. 
2016 ). OFV naturally infects several Citrus  spp. (Table 2).  
Symptoms typical for citrus leprosis have been observed on Valencia and navel oranges ( C. sinensis ) 
in South Africa ( Cook et al. 2019 ). Phylogenetic analyses show that the associated virus is a variant of  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 109 OFV that is more closely related to orchid isolates than to isolates from citrus. This is the first 
confirmed report of CL -N outside the Americas ( Cook et al. 2019 ). 
 
Scientific name:  Citrus leprosis N dichorhavirus  
Order/ family/genus : Mononegarivales/Rhabdoviridae/Dichorhavirus  
Other scientific names:  Citrus leprosis virus N, Citrus leprosis virus N sensu novo  
Abbreviation:  CiLV -N, CiLV -N sensu novo  
Notes: CiLV -N is a dichorhavirus recorded from sweet orange ( Citrus × sinensis ) in Brazil ( Ramos -
Gonzalez et al. 2017 ). This species was referred to as Citrus leprosis virus N  sensu novo  (CiLV -N 
sensu novo) by EFSA (2017)  to avoid confusion with dichorhavirus isolates found in citrus in Mexico 
and Colombia, which are now considered citrus strains of OFV.  
 
Scientific name : Citrus chlorotic spot dichorhavirus  
Order/ family/genus : Mononegarivales /Rhabdoviridae /Dichorhavirus  
Other scientific names:  Citrus chlorotic spot virus  
Abbreviation:  CiCSV  
Notes:  Observation of local chlorotic spots resembling early lesions of citrus leprosis  in leaves of 
sweet orange ( Citrus sinensis ) in Teresina, State of Piaui, northeastern Brazil in 2017 led to the 
identification of CiCSV (Chabi -Jesus  et al. 2018 ). The virus has also been detected in chlorotic lesions 
of beach hibiscus ( Hibiscus  tileaceus ). 
 
This assessment addresses the six viruses known to cause CL. The current import health standard 
(IHS) for citrus nursery stock requires specific t ests for CiLV -C on imported budwood in post -entry 
quarantine (PEQ). However, CiLV -C is assessed here so that the risk can be considered for a lower 
level of PEQ than stipulated in the IHS. In addition, CiLV -C is the best known and most widespread of 
the ci trus leprosis viruses , and there is more information available about this virus  than the re is about 
the other viruses , which are assumed to have similar biology.  
Given that s ome of these viruses have only recently been discovered and described, there is so me 
uncertainty about whether  there are other viruses not yet discovered that may have similar biology and 
cause citrus leprosis symptoms in citrus.  
 
6.1.1  Summary of conclusions  
• The citrus leprosis viruses meet the criteria  to be quarantine pests for New Zealand . 
• The association of the six citrus leprosis viruses  with leafless Citrus  spp. budwood is 
considered high, with low uncertainty.  
• The likelihood of any one of the six citrus leprosis viruses entering New Zealand associ ated 
with leafless Citrus  spp. budwood is considered very low, with moderate uncertainty.  
• The likelihood of any one of the citrus leprosis viruses establishing in New Zealand is 
considered moderate, with high uncertainty.  
• The introduction of any one of the  citrus leprosis viruses is considered likely to cause low to 
moderate economic impacts for New Zealand (but may be high for citrus growers), with high 
uncertainty.  
• The introduction of any one of the citrus leprosis viruses is considered likely to cause lo w 
social impacts in New Zealand, with high uncertainty.  
• The introduction of any one of the citrus leprosis viruses is considered likely to cause very low 
environmental impacts in New Zealand, with high uncertainty.  
• The introduction of any one of the citrus  leprosis viruses is considered likely to cause 
negligible human health impacts, with low uncertainty.  
• Citrus leprosis virus C, Citrus leprosis virus C2, Hibiscus green spot virus 2, Orchid fleck 
dichorhavirus [citrus strain], Citrus leprosis N dichorhavir us and Citrus chlorotic spot 
dichorhavirus may be considered for additional measures on citrus budwood.  
 
 
 
 110 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  6.1.2  Hazard identification: regulatory status  
Given the arguments and evidence below, Citrus leprosis virus C , Citrus leprosis 
virus C2 , Hibiscus green spot virus 2 , Orchid fleck dichorhavirus  [citrus strain], Citrus 
leprosis N dichorhavirus  and Citrus chlorotic spot dichorhavirus  meet the criteria to 
be quarantine pests for New Zealand . 
Criteria for being a regulated quarantine pest relevant to this asse ssment are: the pest is not present 
in the pest risk assessment  area (New Zealand), and  the pest is  of potential importance (able to 
establish and cause harm42). 
 
The six citrus leprosis viruses  are not known to be present in New Zealand . 
• Citrus leprosis virus C  is not known to occur in New Zealand. It is not recorded in Veerakone 
et al. (2015)  or PPIN (2020 ). The quarantine status of Citrus leprosis virus C  in New Zealand 
is ‘regulated’ , and it is listed in ONZPR (202 0) as Citrus leprosis virus (sy n. citrus leprosis, 
citrus leprosis disease, citrus leprosis rhabdovius, leprosis rhabdovirus).  
• Citrus leprosis virus C2  is not known to occur in New Zealand. It is not recorded in Veerakone 
et al. (2015 ), or PPIN (2020).  The quarantine status of Citrus leprosis virus C2  in New Zealand 
is currently unassessed , and it is not listed in BRAD or ONZPR . 
• Hibiscus green spot virus 2  is not known to occur in New Zealand. It is not recorded in 
Veerakone et al. (2015 ) or PPIN (2020 ). The quarantine status of Hibiscus green spot virus 2  
in New Zealand is currently unassessed , and it is not listed in BRAD or ONZPR . 
• Orchid fleck dichorhavirus  [citrus strain]  is not known to occur in New Zealand. It is not 
recorded in Veerakone et al. (2015 ), or PPIN (2020).  The quarantine status of Orchid fleck 
dichorovirus  in New Zealand is currently unassessed . It is not listed in ONZPR , but it is listed 
in BRAD (as  Orchid fleck virus) . 
• Citrus leprosis N dichorhavirus  is not known to occur in New Zealand. It is not recorded in 
Veerakone et al. (2015 ), or PPIN (2020) . The quarantine status of Citrus leprosis N 
dichorhavirus  in New Zealand is currently unassessed , and it is not listed in BRAD or ONZPR . 
• Citrus chlorotic spot d ichorhavirus  is not known to occur in New Zealand. It is not recorded in 
Veerakone et al. (2015 ), or PPIN (2020 ). The quarantine status of Citrus chlorot ic spot 
dichorhavirus  in New Zealand is currently unassessed , and it is not listed in BRAD or ONZPR . 
 
The six citrus leprosis viruses have the potential to establish and spread in New Zealand . 
• The known geographic distribution of the citrus leprosis viruse s include regions that have 
areas with similar climates to New Zealand (for example, parts of Mexico and Brazil) , although 
there is some uncertainty around the geographic distribution of the more recently discovered 
viruses.  
• There are no ecoclimatic constr aints known for the five leprosis -associated viruses that were 
evaluated by EFSA (2017) , except for those affecting their host plants and mite vectors. EFSA 
(2017)  believed the viruses would establish where their Citrus  hosts and mite vectors are able 
to develop.  
• Citrus  species, including sweet orange ( C. sinensis ), which is the most susceptible species 
(Chagas 2000 ), are grown both commercially and domestically in New Zealand, particularly in 
warmer northern regions of the country ( see sections 2.4 and 2.5 ). 
• The citrus leprosis viruses are naturally transmitted by mites of the genus Brevipalpus  
(Bastianel et al. 2010 ; Roy et al. 2015a ). Brevipalpus phoenicis  sensu lato,  B. californicus  and 
B. obovatus  are recorded as present in New Zealand ( NZOR 2020 ). 
• Therefore, suitable host plants and vectors may be present in suitable environmental 
conditions to support establishment and spread.  
 
 
 
 
 
 
42 Refer to ISPM 5  for the definition of a quarantine pest under the IPPC, and the Biosecurity Act 1993 , for factors to consider 
when defining “harm”.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 111 The six citrus leprosis viruses have the potential to  have impact s of economic and sociocultural value 
by causing symptoms on citrus in New Zealand . 
• Citrus leprosis disease caused by the expression of citrus leprosis viruses has been recorded 
in regions that have areas with similar climates to New Zealand (for example, parts of Mexico 
and Brazil).  
• Citrus leprosis induces symptoms of localised lesions on foliage, stems and fruit and severe 
disease can result in extensive crop loss and tree debilitation ( Chagas 2000 ).  
• Sweet orange ( C. sinensis ) is the primary species affe cted, while other citrus species and 
cultivars show varying levels of susceptibility or resistance ( Chagas 2000 ; EFSA 2017), 
depending on the citrus leprosis virus species.  
• Citrus, including C. sinensis , is an important commercial crop for New Zealand and is 
commonly grown by home gardeners (sections 2.4 and 2.5 ). 
 
6.1.3  Hazard identification: commodity association  
Given the arguments and evidence below, the association of the six citrus leprosis 
viruses with leafless Citrus  spp. budwood  is considered to be high, with low 
uncertainty . 
Citrus leprosis viruses can be present in young twigs and stems of infected plants . 
• Citrus leprosis is characterised by the presence of local lesions on plant parts including twigs 
and stems ( Bastianel et al. 20 10). 
• Generally, virus particles of citrus leprosis occur mostly in parenchyma cells of the lesion area 
in affected orange leaves, fruits, or stems ( Rodrigues et al. 2003a ). 
6.1.4  Risk assessment: likelihood of entry  
Given the arguments and evidence below, the likelihood of any one of the six citrus 
leprosis viruses entering New Zealand associated with leafless Citrus  spp. budwood  
is considered to be very low, with moderate uncertainty.  
The citrus leprosis viruses have  a strong association with leafless Citrus  budwood , because these 
viruses cause lesions on twigs and stems . 
• Particles of the citrus leprosis viruses occur in the parenchyma cells of the lesion area in 
affected plant tissues and do not become systemic  (see the above section 6.1.3 H azard 
identification: commodity association) . EFSA (2017 ) makes the following points:  
o Contrary to the vast majority of plant ‐infecting viruses, citrus leprosis viruses are 
unable to systemically invade their citrus host plants  (Bastianel et al. 2010 ; Roy et al. 
2015a ). These viruses are only able to move locally, from an infected cell to 
immediately neighbouring cells . 
o One of the consequences of this peculiar infection biology is that plant tissues away 
from an infection site are considered free of infection and propagation using this 
material should result in virus ‐free progeny plants . 
• CiLV -C has been recorded as causing  natural infection from many Citrus  spp. ( Table 15). The 
most s usceptible  host is sweet orange ( Citrus sine nsis), which is severely damaged; other 
citrus species and varieties, such as mandarins ( C. reticulata ) and their hybrids , are 
susceptible to varying degrees with s ome showing high levels of resistance (Chagas 2000; 
Bastianel et al. 2006 a, b; Bastianel et al. 2008; EFSA 2017 ). According to Bastianel et al. 
(2006a), lemons [ Citrus limon  (L.) Osbeck], limes [ C. aurantifolia  (Christmann) Swingle], 
grapefruit [ C. paradi si (McFad.) Hooker] and some tangors (hybrids between sweet oranges 
and mandarins) exhibit variable levels of resistance to the virus, with lemons and limes being 
considered immune to leprosis. Fewer citrus hosts are known for the other citrus leprosis 
viruses, the most  having been recorded for the citrus strain of OFV, which includes  lemons 
(C. × limon ), limes ( C. aurantiifolia ) and grapefruit ( C. × paradisi ), among others (Table 15). 
Host range s for the viruses will be determined to some extent by the host range s of their mite 
vectors.  
 112 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Table 15: Host range (natural infections only) for five viruses causing leprosis, taken from Table 5 in EFSA (2017).  
 Viruses causing citrus leprosis disease  Reference  
CiLV -C CiLV -C2 HGSV -2 OFV – 
citrus 
strains  CiLV -N 
Rutaceous host plants  
Citrus sinensis  X X  X X Ramos -Gonzalez  et al. 
(2017)  
Citrus aurantium  X   X  Roy et al. (2015a,  b) 
Citrus jambhiri  X     Roy et al. (2015a,  b) 
Citrus medica  X     Roy et al. (2015a,  b) 
Citrus reshni  X   X  Roy et al. (2015a, b)  
Citrus reticulata  × 
C. sinensis  X   X  Roy et al. (2015a,  b) 
Citrus sinensis  × Poncirus 
trifoliata  X     Roy et al. (2015a,  b) 
Citrus  × paradisi     X  Roy et al. (2015a,  b) 
C. × limon     X  Roy et al. (2015a,  b) 
C. aurantifolia     X  Roy et al. (2015a,  b) 
C. limetta     X  Roy et al. (2015a,  b) 
C. × latifolia     X  Roy et al. (2015a,  b) 
Citrus  volkameriana  X  X   Roy et al. (2015a, b); 
Melzer et al. (2012)  
C. reticulata  X     Bastianel et al. (2008)  
C. deliciosa  X     Bastianel et al. (2008)  
C. suhuiensis  X     Bastianel et al. (2008)  
C. clementina  × 
C. reticulata  X     Bastianel et al. (2008)  
C. clementina  × 
(C. reticulata  × 
C. paradisi ) X     Bastianel et al. (2008)  
C. sinensis  × C. reticulata  X     Bastianel et al. (2008)  
C. latifolia  X     Lovisolo et al. (2000)  
C. limon  X     Lovisolo et al. (2000)  
C. sinensis  × Poncirus 
trifoliata  X     Lovisolo et al. (2000)  
Swinglea glutinosa  X X  X  Leon et al. (2008)  
Non-rutaceous host plants  
Commelina  benghalensis  X     Leon et al. (2008)  
Dieffenbachia sp.  X  X  Roy et al. (2015b)  
Hibiscus arnottianus    X   Melzer et al. (201 2) 
 
 
• The likelihood of material being taken from citrus plants with lesions  is low , as there would be 
a preference for healthy looking material for export as budwood. However, lesions can be 
found in crevices of plants so could be overlooked on imported budwood.  
• Symptoms of infection have been recorded taking from 17 to 60 days to develo p after mite 
transmission with most symptoms appearing between 21 and 30 days (Chiavegato and Salibe 
1984) , so there is potential for material to be selected and imported into post-entry quarantine  
before symptoms develop.  
• The citrus leprosis viruses are t ransmitted by Brevipalpus  spp. mites (this has not yet been 
confirmed for HGSV -2 but seems likely) ( Childers et al. 2003 ; Rodrigues and Childers 2013 ; 
Roy et al. 2015a; EFSA 2017 ). Mites can be found in crevices in branches, shoots, buds . 
However , this association with the commodity is weaker than for lesions  caused by citrus 
leprosis viruses . 
• Citrus leprosis disease and the known citrus leprosis viruses have been reported almost 
entirely from North, Central and South America ( Table 16). CiLV -C is the most widely 
distributed of the citrus leprosis viruses and occurs in many countries from Mexico to 
Argentina, including many of the provinces in Brazil ( Table 16). The m ore recently discovered  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 113 virus species have been reported in locations within this range , but records are not near ly as 
widespread as for CiLV -C. A recent report of  an orchid strain of OFV causing citrus leprosis 
symptoms on Citrus sinensis  in South Africa ( Cook et al. 2019 ) is the first confirmed record of 
a citrus leprosis virus outside the Americas. Therefore, the restricted geographic distribution 
means material is unlikely to be sourced from infected regions for these species.  
 
Table 16: Geographic distribution of Citrus leprosis virus  sensu lato. Citrus leprosis is associated with at least five 
distinct virus species . The distribution below shows countries where disease symptoms have been observed (EPPO 
(2020) https://gd.eppo.int/taxon/CILV00 )  
Region  Country (State/Province)  
Africa  South Africa  
North America  Mexico, USA (Hawaii)  
Central America  Belize, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, Panama  
South America  Argentina, Bolivia, Brazil (Acre, Amazonas, Bahia, Ceara, Distriti Federal, Esp írito Santo, Goi ás, 
Mato Grosso, Mato Grosso do Sul, Minas Gerais, Par á, Paran á, Piau í, Rio de Janeiro, Rio 
Grande do S ul, Rond ônia, Roraima, Santa Cat arina, S ão Paulo, Sergipe, Tocantins), Colombia, 
Paraguay, Uruguay, Venezuela  
 
• However, there is  potential for discovery of more viruses that can cause citrus leprosis  or for 
the distribution to be wider than reported (as shown by the recent South Africa finding).   
• There is a low likelihood that symptomatic infected plants would be used to produce budwood 
material. The symptoms  show as non -systemic lesions on the plant surface so are likely to be 
detected visually. However, a very  small lesion  at an early stage of development (or recently 
following mite transmission) might go undetected  on some parts of the budwood . Therefore, 
there is the potential for some contaminated material to be used for budwood for export.  
 
The minimum requirements reduce the likelihood of entry to very low with low uncertainty , because  the 
viruses cause visibly detectable surface lesions and imported budwood would be treated with 
acaricides . 
• It is assumed that healthy looking budwood without obvious signs of disease would be 
selected for export.  
• Visual inspections are likely to detect b oth disease lesions and Brevipalpus  mites.  
• Imported citrus budwood would be treated with acaricides either prior or upon entry to post-
entry quarantine (IHS 155.02.06 ), which would be expected to kill any associated mites (for 
cuttings from non -approved fa cilities in any country).  
• Because  symptoms of infection have been recorded taking from 17 to 60 days to develop after 
mite transmission , with most symptoms appearing between 21 and 30 days (Chiavegato and 
Salibe 1984 ), there is potential for infected mater ial to initially appear healthy and then 
develop symptoms during the post-entry quarantine  period.  
• The virus would not spread from lesions in the absence of the vector mites , because the virus 
particles are found in and immediately around lesions, only mov e locally from infected to 
neighbouring cells and are unable to systemically invade Citrus  (Bastianel et al. 2010; Roy et 
al. 2015a) . Virus lesions are associated with Brevipalpus  mites’ feeding sites. Mites acquire 
the virus by feeding on the infected tis sues and are thought to remain infective for their lifetime 
(Bastianel et al. 2010; Tassi et al. 2017 ). There is no evidence the virus can be passed on 
from parent to offspring  (Tassi et al. 2017 ). 
• Therefore, the viruses are not likely spread around plant material in post-entry quarantine  
undetected , because  both lesions and mites are likely to be detected during regular 
inspections and handling of material.  
 
However, if citrus leprosis viruses produ ced surface lesions on citrus nursery stock in post-entry 
quarantine , there is a very low likelihood the virus would not be contained in level 3A . 
• Citrus leprosis viruses are transmitted by or associated with mites in the genus Brevipalpus : B. 
phoenicis  sensu lato (s.l.)  (Geijskes), B. californicus  s.l. Banks, and B. obovatus  Donnadieu 
(Childers et al. 2003 ; Rodrigues and Childers 2013 ; Roy et al. 20 15a). The following 
Brevipalpus  species have been recorded in New Zealand ( B. phoenicis  s.l., B. californicus  and 114 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  B. obovatus ) (NZOR 2020 ; Berry and Fan 2012 ; Collyer 1973 ; Manson 1967 ). It is also likely 
that B. phoenicis  sensu stricto (s.s.) is present i n New Zealand ( Beard et al. 2015 ). 
• The mites would be marginally capable of passing though ventilation mesh at Level 3 A 
(stainless steel insect -proof mesh with a maximum aperture of 0.2  mm; MPI 2019 ), given their 
body width of less than 0.2  mm ( CABI 2020 ), and would be capable of passing through 
ventilation mesh at L2 (insect -proof mesh with a maximum aperture of 0.6  mm; MPI 2019 ). 
Brevipalpus  spp. are considered to have poor natural dispersal ability  but can be moved 
longer distances passively by str ong wind (Alves et al. 2005 ) and other ‘passive’ mechanisms . 
Mites of other species have been reported at L3 A (pers . comm., R Lardner , 2020 ) but not 
necessarily entering through ventilation mesh.  
• If local New Zealand Brevipalpus  mites entered post-entry qu arantine  by passing through 
ventilation mesh , they could become infected by feeding on lesions on citrus plants . They or 
their virus -carrying offspring could also escape the post-entry quarantine  facility through the 
same ventilation mesh. Exposure of the virus pathogen to the New Zealand environment may 
then occur if suitable hosts are present near the post-entry quarantine  facility. The three 
Brevipalpus  spp. recorded in New Zealand are highly polyphagous. Childers et al. (2003)  
noted that 928 plant speci es in 513 genera within 139 families are recorded hosts of one or 
more of B. californicus  (316 species), B. phoenicis  (486 species) and B. obovatus  (451 
species). Many of the reported hosts of Brevipalpus  spp. worldwide are present in New 
Zealand. H ost records  for B. phoenicis  s.l. in New Zealand include Citrus limon  × reticulata , 
Citrus  sp., Ipomea  sp., orchids, slipper orchid and grass  (Berry and Fan 2012 ). However, the 
likelihood of  this sequence of eve nts, that is,  New Zealand mites entering post-entry 
quarantine  through ventilation mesh, picking up the virus from undetected lesions on the 
plants within, escaping the facility via the ventilation mesh and then reaching and feeding on a 
suitable host plan t for citrus leprosis viru ses, i s considered very low  at level 3 A but cannot be 
ruled out . The likelihood would be higher at level 2 post-entry quarantine , given the greater 
mesh size and construction of less sturdy material than stainless steel.  
• The facil ity construction and operational procedures implemented in level 3A glasshouses 
(including regular inspections for pests and diseases, protective clothing and handwashing) 
(MPI 2019 ), would reduce the likelihood of infected New Zealand -sourced Brevipalpus  mites 
escaping the facility to a very low level.  
 
Several factors contribute to the moderate uncertainty associated with the rating for entry to New 
Zealand. The distribution and prevalence of the different species of citrus leprosis viruses is unclear, 
especially as some of the viruses have been discovered very recentl y. There is also potential for 
further viruses to be discovered that are non -systemic, transmitted by Brevipalpus  mites and cause 
citrus leprosis disease , including in new geographic locatio ns. Citrus leprosis complex has been 
described as an emerging disease in the Americas (Roy et al. 2015a). There is uncertainty around 
which Brevipalpu s spp. are present in New Zealand, given recent changes in taxonomy in the genus 
(e.g., Beard et al. 2015 ). There is also uncertainty around their geographic distribution, range of host 
plants and abundance in New Zealand. Little published research was found in literature searches , and 
nothing  was found  to indicate any research effort on managing these species  in crops in New Zealand.  
 
6.1.5  Risk assessment: likelihood of establishment and spread  
Given the arguments and evidence below, the likelihood of any one of the citrus 
leprosis viruses establishing in New Zealand is considered to be moderate , with high 
uncertai nty. 
• Establishment of any of the citrus leprosis viruses would depend on a combination of several 
factors: The presence of suitable host plants, the presence of vectors and the suitability of the 
environment . 
• For CiLV -C, a wide range of citrus species have  been recorded with natural infections of the 
virus (see Table 16), with sweet orange ( Citrus sinensis ) being the most significant. In 
addition, a small number of other plant species, both Rutaceae and non -Rutaceae, have been 
recorded with natural infectio ns, along with many species of experimentally infected hosts  
(EFSA 2017) . Some species that are known to grow in or around citrus orchards in other 
countries (e.g. Hibiscus rosa -sinensis  and H. tiliaceus ) could support establishment by playing  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 115 in a role in the epidemiology of the diseases as a source of virus inoculum and by harbouring 
populations of mite vectors ( EFSA 2017 ) if present in similar circumstances in New Zealand.  
• Citrus is grown both commerc ially and domestically in New Zealand, especially in the warmer 
northern regions of the country. Sweet orange and m any of the other recorded hosts of CILV -
C, both natural and experimental, are present in New Zealand ( Allan Herbarium  2020 ). 
Therefore, hosts  are present but restricted in distribution rather than widely available 
throughout the country . 
• CiLV -C causes non -systemic lesions on the plant surface at the feeding sites of its mite 
vector. The virus is spread around the plant and to other plants by th e feeding activity of the 
mite. Brevipalpus phoenicis  s.l., the vector for CiLV -C, has been recorded in New Zealand, 
including from Citrus  spp. ( Berry and Fan 2012 ). Recent taxonomic revision has shown that 
B. phoenicis  is a complex of cryptic species  (Beard et al. 2015 ). As a result, one of the species 
in the complex,  B. yothersi , is now considered the main vector for CiLV -C (Tassi et al. 2017 ). 
However, it is difficult to know which of the revised species older records are referring to , and 
it is not clear if B. yothersi  is present in New Zealand. In addition, there is little recorded 
information on the distribution and abundance of Brevipalpus  spp. mites in New Zealand.  
• The mites are unlikely to move actively very far without assistance  as they move slowly and 
prefer to shelter in openings and wounds ( EFSA 2017 ). Passive mechanisms such as cultural 
practices and the movement of tools, machinery and people are likely to play a role in their 
dispersal ( EFSA 2017 ). Mites can also be spread passively by wind currents ( Alves et al. 
2005 ). 
• Some of the countries where CiLV -C occurs have areas with climatic similarity to parts of 
New Zealand , according to climate match indices (CMI) based on Phillips et al. (2018 ). For 
example, cytoplasmic lepros is (assumed to be CiLV -C) is reported widely from Brazil , 
including the southern and southeastern states  (Roy et al. 2015a ), which have areas with 0.7 –
0.9 CMI [for example, Rio Grande do Sul  (0.7–0.9 CMI) , Santa Catarina  (0.7–0.9 CMI), 
Paran á (0.7–0.8 CMI)  and S ão Paulo (parts with 0.7 –0.8 CM)], and is also reported from 
Uruguay (0.8 –0.9 CMI)  (Roy et al. 2015a ). However, EFSA (2017 ) concluded that there are no 
ecoclimatic constraints known for the five leprosis -associated viruses that were evaluated by 
EFSA  except for those affecting their host plants and mite vectors.  
• For the other citrus leprosis viruses, there is much less information than for CiLV -C. They  are 
assumed to have a similar or lower likelihood of establishment in New Zealand than CiLV -C, 
based on the availability of their known hosts and the presence of known vector sp ecies . 
There are much fewer recorded natural hosts for these viruses ( Table 14) than for CiLV -C, 
although the citrus strain of OFV has been recorded from several citrus species that C iLV-C 
has not, as well as C. sinensis . The known vectors B. phoenicis  s.l. and B. californicus  have 
been recorded in New Zealand, and B. phoenicis  s.s. is likely to be pres ent, but it is unknown 
whether B. yothersi  is present. The ho st range of any of the viruses will be  determined to 
some extent by host range of its mite vectors.  
• According to EFSA (2017) , known or likely vectors for these less common citrus leprosis 
viruses  include:  
o CiLV -C2: reported to be transmitted by B. yothersi  (used as a synonym of 
B. phoenicis  s.l.; Roy et al, 2013 a, 2015a ); 
o HGSV -2: mite transmission suspected but not confirmed ; no tentative vector species 
yet identified ( Melzer et al. 2012 ; Roy et al. 2015a) ; 
o CiLV -N: transmitted by B. phoenicis  s.s. ( Ramos -Gonzalez et al. 2017 ); 
o OFV [citrus strain]: believed to be transmitted by B. californicus , based on the mite’s  
association in the field  
• For CiCSV, B. yothersi , and possibly another species of Brevipalpus  [temporarily designated 
B. aff. yothersi ] are likely vectors b ased on association with infected plants  (Chabi -Jesus et al. 
2018 ). 
 
The main factors contribut ing to the high  uncertainty associated with the rating for e stablishment in  
New Zealand  are in relation to the Brevipalpus  mite vectors . There is uncertainty around which 
Brevipalpus  spp. are present in New Zealand, in part as a result of  recent changes in taxonomy in th e 
genus (e.g., Beard et al. 2015 ). There is also uncertainty around their geographic distribution, range of 
host plants and abundance in New Zealand. Little published research  or records were found in 116 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  literature searches , and there was nothing to indicate any research effort on managing these species 
in crops in New Zealand.  
 
6.1.6  Risk assessment: impacts to New Zealand  
Given the arguments and evidence below, the introduction  of any one of the citrus 
leprosis viruses  is considered likely to caus e low to moderate  economic impacts for 
New Zealand  (but may be high for citrus growers), with high uncertainty . 
• Citrus leprosis disease induces localised lesions on the leaves, stems and fruit ( Chagas 2000; 
Roy et al. 2015b ). When infestations of viruliferous mites are hig h, lesions in the petiole cause 
severe defoliation, lesions in the peduncle result in intense fruit drop, coalesced necrotic 
lesions induce twig death , and plants may die within 3 to 5 years ( Roy et al. 2015b ). 
• Citrus leprosis lesions, typically circular n ecrotic or chlorotic lesions on leaves, fruits and 
stems, can affect both fruit quality and production levels. The disease can cause a decrease in 
production through reduction in tree canopy development, premature fruit and leaf drop, and 
dieback ( Bastiane l et al. 2010 ). Lesions on the fruit surface reduce the aesthetic appeal of fruit 
grown for fresh consumption  (EFSA 2017 ). 
• The disease can cause up to 100% yield losses, depending upon the susceptibility of the 
citrus cultivar and level of control of the m ite vector (Rodrigues et al. 2003a ). According to 
Rodrigues et al. (2003a), Fawcett (1907 ) estimated a loss of 35 –75% from prematurely 
dropped fruit during 1905 and 1906 in Florida with this amount being similar to figures 
recorded in Brazil for different cultivars ( Rodrigues et al. 2003b ).  
• Citrus leprosis is one of the most economically important diseases of the Brazilian citrus 
industry. In 2010, Bastianel et al . reported that control of the vector mite costs Brazilian 
growers around US$800 mil lion every year.  
• Sweet orange ( C. sinensis ) is the most affected citrus species with others, such as mandarins 
(C. reticulata ) and their hybrids, being susceptible  or resistant to varying degrees. CiLV -C has 
the most extensive list of citrus hosts in compa rison with the other viruses. However, with the 
exception of HGSV -2, they have all been reported from sweet orange  (C. sinensis ), and the 
citrus strains of OFV have been recorded from some of the citrus considered more resistant to 
CiLV -C, such as lemon, l ime and grapefruit . 
• Citrus  trees , including oranges, mandarins, lemons, tangelos, limes, and grapefruit, are 
commonly grown commercial plants  in New Zealand (section 2.5.2). Therefore, impacts to 
these species have the potential to cause consequences of ec onomic significance. Oranges 
are likely to be most affected , while some other commercially grown species and varieties, 
such as lemons, may be affected to a much lesser degree or not at all, depending on the virus 
species.  
• The discovery of the presenc e of any of the citrus leprosis viruses in New Zealand , especially 
CiLV -C, is likely to have an immediate impact on exports of citrus , because the disease is not 
known to occur in any of the countries that are export destinations for New Zealand citrus . 
Response activities, if undertaken, could cost millions of dollars.  
• If the citrus leprosis viruses established longer term, then a greater and longer -term effect on 
the citrus industry could be expected through lowered production, increased management 
activities, reduced access to or increased requirements for overseas markets where the 
viruses are absent  and increased surveillance activities.  
• However, impacts on production (quality and quantity) will depend on where the mite vectors 
are present, whether t he climatic conditions are suitable for the mites to thrive in citrus 
orchards, and whether mites are already controlled in orchards by acaricides and other 
activities. Disease flourishes where the mite vectors flourish , as lesions only occur at the 
feedin g sites of viru s-carrying  mites . Therefore, citrus leprosis would have more impact in 
orchards where Brevipalpus  mite vectors are abundant and not managed. If mites are 
controlled or occur at low levels , then citrus leprosis may not have much impact on production 
except  for the situation of increased requirements for export . Some regions of New Zealand 
may be more affected than others, depending on the geographic distribution and local 
abundance of the individual Brevipalpus  species.  
• Acaricides are used in commercial citrus production in New Zealand to control citrus red mite 
(Panonychus citri ) (Mooney  2001; Jamieson and Stevens 2009 ). These are used as required  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 117 rather than routinely , as P. citri  is only a significant pest when the broad -spectrum activity of  
insecticides targeting other key pests disrupts the activity of its natural enemies . These 
treatments may offer some level of control of the Brevipalpus  spp. that can vector citrus 
leprosis viruses.  
 
The main factors contributing to the high uncertainty associated with the rating for economic impacts 
in New Zealand are in relation to the Brevipalpus  mite vectors  (as discussed earlier for establishment).  
There is uncertainty around which Brevipalpus  spp. are present in New Zealand, in part as a result of 
recent changes in taxonomy in the genus (e.g., Beard et al. 2015 ). There is also uncertainty around 
their geographic distribution, range of host plants and abundance in New Zealand. Little published 
research or records w ere found in literature searches , and there was nothing to indicate any research 
effort on managing these species in crops in New Zealand.  
 
Given the arguments and evidence below, the introduction of any one of the citrus 
leprosis viruses is considered likely to cause low soci ocultural  impacts in 
New Zealand, with high uncertainty.  
• The viruses may cause impacts to home gardeners who grow Citrus  spp. in areas of the 
country where environmental conditions are suitable for the Brevipalpus  mite vectors.  
• Symptoms of citrus leprosis  include non -systemic lesions on fruit, leaves and stems, and 
potentially the death of branches or trees , depending on the level of feeding activity of virus-
carrying  mites.  
 
Given the arguments and evidence below, the  introduction of any one of the citrus 
leprosis viruses is considered likely to cause very low environmental impacts in 
New Zealand, with high uncertainty.  
• The recorded natural hosts of the six citrus leprosis viruses are largely Citrus  species . 
However , there are no Citrus  species native to New Zealand. There are two genera within the 
Rutaceae that are endemic to New Zealand: Leionema  and Melicope . Neither the Leionema  
nor Melicope  species are considered threatened ( NZPCN 2020 ). 
• There are very few  recorded natural infections of plants outside the Rutaceae . For example,  
CiLV -C has been recorded from Commelina benghalensis  (Commelinaceae),  CiLV -C2 and 
OFV citrus strains from Dieffenbachia  sp. (Araceae), HGSV -2 from Hibiscus arnottiana  and 
CiCSV  from Hibiscus tiliaceus  (Malvaceae).  There are two native (but not endemic) Hibiscus  
species in New Zealand, both of which are considered “threatened, nationally critical” 
(H. richardsonii  and H. diversifolius  subsp. Diversifolius ) (NZPCN 2020 ). 
• There is uncertainty around the natural host ranges of any of these viruses. However, these 
would be expected to fall within the host ranges of the Brevipalpus  mite vectors.  
• Impacts on plants would be from non-systemic lesions that develop where virus-carrying  mites 
feed on leaves, stems and fruit. Therefore , the impact would be dependent on the feeding 
activity and the abundance o f virus-carrying  mites.  
• Three species of  Brevipalpus  mites known to be vectors of viruses that cause citrus leprosis 
have been reported from New Zealand. However, given the few records of the mites from 
New Zealand and the complexity of relating current taxonomy to older records, the lack of 
knowledge of population levels of the mites, especially in the natural environment, and th e 
uncertainty around the natural host range for any of the citrus leprosis viruses, it is difficult to 
estimate the likely impact of these viruses in New Zealand’s natural environment.  
 
 
Given the arguments and evidence below, the introduction of any one o f the citrus 
leprosis viruses is considered likely to cause negligible human health impacts, with 
low uncertainty.  
Citrus leprosis viruses are not known to pose risks to human health . 
• No evidence was found of any citrus leprosis viruses causing human health issues.  
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species in Mexico. Phytopathology , 105(4) : 564–575. https://doi.org/10.1094/phyto -09-14-0245 -r. 
Tassi, A D ; Garita -Salazar, L C; Amorim, L; Novelli, V M; Freitas -Astua, J; Childers, C C; Kitajima, E W 
(2017) Virus -vector relationship in the Citrus leprosis pathosystem. Experimental and Applied 
Acarology , 71: 227 –241. 
Veerakone, S; Tang, J Z; Ward, L I; Liefting, L W; Perez -Egusquiza, Z; Lebas, B S M; Delmiglio, C; 
Fletcher, J D; Guy, P L (2015) A review of the plant virus, viroid, liberibacter and phytoplasma records 
for New Zealand. Australasian  Plant Pathology  44: 46 3–514. 
 
 
 
  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 121 Appendix 1: Summary of taxa excluded at hazard identification  
 
Pest taxon  Rationale for exclusion  
Acari  (mites)  Due to the conditions in the nursery stock import health standard  (MPI Standard 155.02.06) , which require whole plants and cuttings  to undergo 
miticide treatment, it is considered that the pathway is managed as well as possible . Furthermore, the post-entry quarantine  period and 
requirements  (MPI 2019 ) (e.g. inspections and insect proof mesh) ar e likely to detect and contain any mites that survive treatment.  Therefore , MPI 
believes  that the minimum requirements manage the risk associated with mites.  
Insecta  Due to the conditions in the nursery stock import health standard  (MPI Standard 155.02.06 ), which require whole plants and cuttings to undergo 
insecticide treatment, it is considered that the pathway is managed as well as possible. Furthermore, the post-entry quarantine  period and 
requirements (MPI 2019 ) (e.g. inspections and insect proof mesh ) are likely to detect and contain any insects that survive treatment.  Therefore , 
MPI believes that the minimum requirements manage the risk associated with insects.  
Fungi (Aspergillaceae)  Aspergillus flavus, A. niger, Penicillium digitatum and P. italicum  are reported from citrus fruit but are present in New Zealand (NZ Fungi2 2020; 
PPIN 2020). Penicillium ulaiense  was considered in more depth , because it is recorded as absent from New Zeala nd (NZ Fungi2 2020). However, it 
is not generally reported as a pathogen that affects citrus plants, although it can cause rot of citrus fruit in storage. For  example, P. ulaiense  was 
commonly isolated from  packhouses in the USA but could not be detected at  production sites (Holmes et al. 1994). MPI believes  that the m inimum 
requirements manage the risks of P. ulaiense entering New Zealand associated with citrus budwood , because the imported material must be free 
from soil and other debris.  
Fungi 
(Botryosph aeriaceae)  Phyllosticta citricarpa (Guignardia citricarpa ) required a full pest risk assessment . Several other Phyllosticta spp. were excluded at the hazard 
identification stage because they are not known to be associated with branches, shoots, stems or twigs of citrus or do not meet the criteria for 
additional measures. For example:  
Phyllosticta citribraziliensis  and P. paracapitalensis have only been reported as endophytes from healthy citrus leaves ( Glienke et al. 2011; EFSA 
2014; Guarnaccia et al. 201 7a), and there is no evidence that they are associated with budwood.  
Phyllosticta citrimaxima was isolated from tan spots on the fruit surface of  pomelo fruit in Thailand (Wikee et al. 2013) . 
Phyllosticta paracitricarpa  was isolated from leaf litter of C. limon  in Greece and fruit spots on  C. limon  and C. sinensis  in China (Guarnaccia  et al. 
2017a, 2019).  
Phyllosticta citriasiana  causes citrus tan spot on C. maxima  fruit and leaves. It is only reported from tropical areas such as Thailand and Viet  Nam 
and several tropical provinces of China (Wulandari et al. 2009; Wang et al. 2012) , which have very different climate conditions to the whole of 
New Zealand, indicated by a climate match index (CMI) of ≤ 0.6 (Phillips et al. 2018). Pomelo ( C. grandis/C. maxima ) is the only recorded host of 
P. citriasiana  (Wulandari et al. 2009; Wang et al. 2012) and is not widely grown in New Zealand. Therefore, both likelihood of establ ishment and 
potential for this fungus to have impacts in New Zealand were considered extremely low.  
Phyllosticta citrichinaensis was isolated from fruit of mandarins ( C. reticulata ), pomelos ( C. maxima ), oranges ( C. sinensis ) and lemons ( C. limon ) 
(Wang et al. 2012) . No significant losses resulted from this pathogen (Wang et al. 2012).   
Fungi 
(Ceratobasidiaceae)  Rhizoctonia noxia  (synonyms Corticium koleroga ; Ceratobasidium noxium; Koleroga noxia Pellicularia koleroga ), the fungus that causes thread  
blight , has previously been assessed on fresh citrus fruit from Samoa as C. koleroga  (MAF 2008).  Rhizoctonia noxia  did not meet the criteria for 
further assessment , because MPI believes  that the  minimal requirements are likely to manage the risk of the fu ngus , because infestations of thread 
blight are highly unlikely to go undetected and infected citrus plants are highly unlikely to be used to produce budwood.  
• Rhizoctonia noxia  attacks twigs, fruit and leaves of Citrus  trees. Rhizomorphs form and cover the tissue , which may die if heavily invaded.  
Small black sclerotia often form on the rhizomorphs , and basidiospores may form on the wefts of mycelium on host tissue (Timmer 2000) . 122 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Pest taxon  Rationale for exclusion  
Fungi 
(Ceratocystidaceae)  Ceratocystis fimbriata already has additional requirements for all known host species, including citrus, in the Nursery Stock import health standard . 
Therefore, r isk assessment for this species was excluded from the scope of this import risk analysis . 
Ceratocystis radi cicola has been reported from citrus fruit (Mirzaee et al. 2008), but searches1 found no evidence of an association with branches, 
stems or twigs. In pathogenicity tests, the fungus could only enter damaged fruit through wounds or cracks (Mirzaee et al. 20 08), suggesting it is an 
opportunistic fruit rot.  
Fungi (Dermateaceae)  Cryptos poriopsis citricarpa  (synonym Pseudofabraea citricarpa ) was considered in the hazard identification , because it was recently reported as a 
destructive leaf spot which was first reported China in 2010 (Zhu et al . 2012). However, it does not meet the criteri a for further assessment , 
because there is no evidence for an association with Citrus budwood. The same species or a species with the same name was rec orded on older 
leaves of several Citrus species in the Cook Islands, Fiji, Niue, Tonga, Vanuatu and Weste rn Samoa (Johnston and Fullerton 1988). 
Cryptosporiopsis citricarpa  was not reported from stems or branches in either case. Searches43 found only these reports and taxonomic studies 
referring to Zhu et al. (2012).  
Paracercosporidium microsorum  (synonyms Cercospora microsora, Mycosphaerella microsora, Mycosphaerella millegrana, Passalora microsora ) 
was added to the initial hazard list , requiring further analysis,  because it was historically listed in the citrus nursery stock pest list. However, it did 
not me et the criteria for further assessment , because literature searches (CAB Abstracts, Farr and Rossman, Google Scholar, June 2020) using 
‘Paracercosporidium microsorum ’ or the synonyms above and ‘citrus’ as search terms found no references suggesting that th is fungus is 
associated with citrus.  
Fungi (Diaporthaceae)  In addition to D. baccae, D. hongkongensis and D. novem , which were assessed in a grouped pest risk assessment , several other Diaporthe  
species have recently been isolated from citrus plants. Diaporthe  arecae, D. biconispora, D. biguttulata, D. citriasiana, D. citrichinensis, 
D. discoidispora, D. endophytica, D. limonicola, D. melitensis, D. multigutullata, D. ovalispora, D. ovoicicola, D . subclavata, D. unshiuensis  were 
noted as potential hazards in the hazard identification for this import risk analysis  because:  
• These species are not recorded from New Zealand : NZFungi2 (2020) either records these species as absent or does not have a record of 
them. They are not recorded in PPIN.  
• They have the potential to be associated with citrus nursery stock. There is a single recent primary report of each of these species from twigs , 
branches or stems of citrus, either as endophytes or associated with disease symptoms.  
• Some of these species have the potential for impacts , because they are reported to cause disease symptoms in citrus or other economically 
important hosts.  
• However, li ke D. baccae, D. hongkongensis and D. novem, citrus disease associated with  these species has only been recently differentiated 
from disease symptoms caused by D. citri , and there are only a few reports of them in the literature.  
• Searches of Google Schola r and CAB Abstracts and Farr and Rossman (August 2020) on the species name and ‘citrus’ found only a single 
report from citrus and, in some cases, molecular taxonomy studies with no further hosts or geographical records.  
There is insufficient information about Diaporthe arecae, D. biconispora, D. biguttulata, D. citriasiana, D. citrichinensis, D. discoidispora, 
D. endophytica, D. limonicola, D. melitensis, D. multigutullata, D. ovalispora, D. ovoicicola, D. subclavata and D. unshiuensis  to assess them in 
more depth at this time, but they may be reconsidered in future if more information becomes available (e.g. from the emerging  risks system).  
Fungi 
(Glomerellaceae)  Colletotrichum  abscissum  and C. limetticola  met the criter ia for pest risk assessment (see section s 6.1 and 6.2) 
A number of other Colletotrichum  species were considered in more depth at the hazard identification stage.  
For example:  
Colletotrichum queenslandicum  has been reported from leaves of Persian lime (C. latifolia) with anthracnose symptoms on a tree at a residential 
property in Texas, USA (Kunta et al. 2018). Another recently described species, C. citri -maximae,  is reported as a symptomless endophyte in t he 
 
43 Searches of CAB abstracts, CPC and Google Scholar in June and October 2020 using the species name and “citrus” as search term s.  
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 123 Pest taxon  Rationale for exclusion  
C. gigasporum complex reported from a study of Colletotrichum species on C. maxima fruit imported from China (Douanla -Meli and Unger 2017). 
Searches on the species name in Google Scholar and CAB Abstracts found no reports of this species from other plan t parts and no reports of it 
causing disease. There is no evidence for an association of C. queenslandicum or C. citri -maximae with citrus budwood with the leaves removed.  
A number of Colletotrichum  species ( Colletotrichum catinaense, C. helleniense, C. hy stricis and C. limonicola ) were  recently reported from surveys 
as associated with citrus , but there was insufficient information to assess t hem further:  
• Colletotrichum catinaense  was isolated from C. sinensis  fruit with anthracnose (tear stain) symptoms in Portugal and  from C. reticulata leaf 
lesions and  C. aurantiifolia  twigs with wither tip symptoms in Italy (Guarnaccia et al. 2017b).   
• Colletotrichum helleniense  was isolated from twigs of Poncirus trifoliata  with wither tip, as well as lesions on fruit , in Arta, Greece (Guarnaccia 
et al. 2017b).  
• Colletotrichum hystricis  was isolated from leaf lesions on C. hystrix  in Italy (Guarnaccia et al. 2017b).  
• Colletotrich um limonicola  was isolated from leaf lesions of C. limon  in Malta (Guarnaccia et al. 2017b).  
Searches using the species name and citrus as search terms  in Google Scholar, CAB Abstracts, CABI  and Farr and Rossman (August 2020) found 
no information about the  association of these species with citrus beyond the initial report. These species may need to be assessed in future if more 
information becomes available  (e.g. from the emerging risks system).  
Fungi (Meliolaceae  – 
sooty blotches)  Meliola citricola was as sessed on citrus fruit from Samoa (MAF 2008)  and so was considered as part of the hazard identification. However, there is 
no evidence for an association with citrus budwood:  
• Meliola citricola causes unsightly black fungal growth on fruit and leaves of citrus (MAF 2008).  
Searches on the species name and ‘citrus’ as search terms in CAB Abstracts and Google Scholar (November 2020) and literature records in Farr 
and Rossman (2020) found some recor ds of M. citricola,  and the related species M. camelliae, in historic country indexes and lists of fungal 
species , but no evidence was found for an association with branches, twigs, shoots or stems of citrus.   
Fungi 
(Mycosphaerelleaceae)  A number of Myco sphaerella  and Zasmidium  leaf and fruit spot species were considered during the hazard identification process, including:  
• Mycosphaerella citri  (synonym Zasmidium citri ) does not meet the criteria for further assessment because there is no pathway for 
estab lishment from leafless citrus  budwood (based on information in MAF 2008). Mycosphaerella citri  causes greasy spot of citrus leaves 
and greasy spot rind blotch of citrus (MAF 2008).  
• The CABI datasheet (2020) says it is not transmitted  via budwood . 
• Since Mycosphaerella citri  overwinters in the soil and sporulates on fallen leaves (MAF 2008), removing the leaves and importing clean , 
rootless budwood prevents entry and establishment of th e pathogen via this pathway.  
• Mycosphaerella horii is also reported to sporulate on decomposing leaves (Ieki 1986).  
Several other Mycosphaerella  and Zasmidium species are reported to cause leaf and/or fruit spots in citrus but do not meet the criteria for further 
assessment (e.g. M. citrigena , M. loefgrenii, Z. fr ucticola , Z. fructigenum  and Z. indonesianum ).  
• Searches on the species name (Google Scholar, CABI, CAB Abstracts, Farr and Rossman, June 2020) found no detail on life cycle and 
no evidence for an association with citrus budwood with no leaves.  
• Since these species are closely related to M. citri , the life cycle is likely to be similar. Assuming these other Mycosphaerella  and 
Zasmidium species overwinter in the soil and sporulate on fallen leaves, removing the leaves and importing clean rootless b udwood 
prevents these pathogens from entering New Zealand and establishing from citrus nursery stock.  
Pseudocercospora angolensis (synonyms:  Cercospora angolensis; Phaeoramularia angolensis ; Pseudophaeoramularia angolensis ) was 
considered in some depth du ring the hazard identification process because this fungus is reported to cause spots and lesions on leaves, fruit and 124 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Pest taxon  Rationale for exclusion  
sometimes stems of all citrus species, including grapefruit, lemon, orange, lime and tangerine (Seif and Hillocks 1993 , 1998).  However, MPI 
believes  that the biosecurity risks associated with P. angolensis are managed by minimum measures. Pseudocercospora angolensis is highly 
unlikely to be associated with healthy citrus budwood, because the fungus only causes stem lesions in severely disea sed plants with visible lesions 
on the leaves:   
• Pseudocercospora angolensis causes spots on leaves which can coalesce, particularly on young leaves , and cause yellowing and early leaf 
loss.  
• Stem lesions are not frequent and mostly occur as an extension of  lesions on the petiole  (Seif and Hillocks 1993).   
• Occurrence of several such lesions at the stem tip results in dieback; those on other parts of the stem coalesce, become cork y, and crack. At 
the base of the dead stem , there is usually a profuse growth of  secondary shoots.   
In addition, P. angloensis is only found in sub -Saharan Africa (not reported from South Africa) and Yemen (EFSA 2017). There are no records of 
imports of Citrus nursery stock from countries where P. angolensis  is reported, although trade on these pathways cannot be ruled out in future.  
Fungi (Nectriaceae)  Several species in the Nectriaceae were con sidered during the initial hazard identification stage.  
Several Fusarium species have recently been isolated from citrus plants but do not meet the criteria for additional measures:  
• Fusarium citricola, F. ensiforme, F. salinense, F. sarcochroum, F. siculi  were noted as potential hazards in the hazard identification for this 
import risk analysis  because:  
o These species are not recorded from New Zealand – NZFungi2 (2020) either records these species as absent or does not have a 
record of them.  
o They have the potential to be associated with citrus nursery stock. There is a single recent primary report of each of these species 
from twigs, branches or stems of citrus,  either as endophytes or associated with disease.  
o Some of these species have the potential for impacts because they are reported to cause disease symptoms in citrus or other 
economically important hosts.  
o Searches of Google Scholar , CAB Abstracts and Farr and Rossman (August 2020) on the species name and ‘citrus’ found only a 
single report from citrus and, in some cases, molecular taxonomy studies with no further hosts or geographical records.  
o There is insufficient information  about the association of F. citricola, F. ensiforme, F. salinense, F. sarcochroum or F. siculi with citrus  
to assess them in more depth at this time, but they may be reconsidered in future if more information becomes available (e.g.  from 
the emerging risks system).  
o Fusarium solani  and F. oxysporum are reported as citrus root pathogen s and are now considered to be a species complexes, 
however F. solani sensu stricto (as its synonym Nectria haematococca ) and F. oxysporum sensu stricto have both been recorded 
from citrus plants in New Zea land (NZFungi 2 2020).  
Cylindrocarpon lichenicola  (synonyms include Fusarium lichenicola and Neocosmospora lichenicola ) was reported as a cause of severe post -
harvest fruit rot of pomelo in Viet  Nam (Amby et al . 2015) , but there is no evidence that it is as sociated with citrus budwood. However, although 
other citrus species developed rot symptoms in pathogenicity tests (Amby et al. 2015) searches using the search terms ‘ Cylindrocarpon lichenicola’ 
or its synonyms and ‘citrus’ found no other reports of C. lichenicola from citrus. Cylindrocarpon lichenicola  is also reported as a cause of 
opportunistic infections in humans in tropical areas (e.g. Summerbell and Schroers 2002), and it is likely that it is a commo n environmental fungus 
in tropical areas.   
Neocosmospora euwallaceae (synonym Fusarium euwallaceae ) does not meet the criteria for additional measures , because it is a wood rot fungus 
that colonises beetle galleries and is spread by beetle vectors (Paap et al . 2018). It is therefore highly unlikely to be associated with citrus 
budwood.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 125 Pest taxon  Rationale for exclusion  
Fungi (Pleosporaceae)  A number of Alternaria species were considered in more depth at the hazard identification stage but do not meet the criteria for additional 
measures:  
• A number of Alternaria  species are described  from Citrus  but are now considered synonyms of species that are present in N ew Zealand  and 
have been recorded from Citrus here (e.g.  A. pellucida  is a synonym of A. alternata ; A. scorzonerae  is a synonym of A. linicola ). 
• Alternaria limicola,  the cause of the citrus leaf spot disease mancha foliar de los citros, attacks young twigs and leaves, producing small 
chlorotic spots with raised centres (Timmer et al. 2000). Affected leaves often abscise and twigs may die back (Timmer et al.  2000)  
• It is uncertain wh ether A. limicola  can spread from infected twigs. It produces airborne conidia in leaf lesions (Palm and Civerolo 1994), 
however, no records were found that reported whether conidia were produced in lesions on twigs.  
• The risk of A. limicola  entering New Z ealand is likely to be managed by minimum measures because:  
o Disease symptoms develop rapidly, so it is very unlikely that budwood will be sourced from plants infected with A. limicola.  Palm and 
Civerolo (1994) describe leaves with both mature and newly  formed lesions 5 days after inoculation. Timmer et al. (2000) r eport that 
conidia of A. limicola germinate within 4 hours and penetrate the tissue within 12 hours, and that A. limicola  sporulates about 8 days 
after symptoms develop.  
Alternaria limicola  has a very limited geographical distribution. Palm and Civerolo ( 1994) report the disease from the pacific coast of Mexico, but not 
elsewhere in Mexico. No reports were found of A. limicola  from anywhere else in the world.  
Fungi (Capnodiaceae 
and Chaetothyriaceae -
sooty moulds)  Capnodium citri  is a sooty mould fungus associated with honeydew -excreting insects such as mealybugs, aphids or soft scales (MAF 2008). It is 
not pathogenic to plants, although it can cause production losses by impairing photosynthesis (MAF 2008).  
The following sooty mo ulds have been reported from citrus , but fungal symptoms (and the underlying insect infestations) are visually detectable in 
a phytosanitary inspection, and therefore , the biosecurity risks associated with these species are managed by minimum requirements:  Antennella 
citrina, Capnodium citri, Capnodium tanakae, Capnophaeum fuliginoides, Chaetothyrium citri, Chaetothyrium javanicum, Chaetoth yrium 
spinigerum, Hypocapnodium japonicum.  
Fungi (Wood, root, butt 
or rot fungi e.g. 
Agaricales, 
Hymenochaetales, 
Polyporales, many 
Xylariales)  Fungi that cause root and butt rots of citrus plants and are only reported to be associated with roots and butts were not assessed further. Likewise, 
wood rots that are only reported from mature woody tissues of citrus plants were  not assessed. The risk of these pathogens entering New Zealand 
is managed by the commodity description,  because it is highly unlikely that such fungi will be associated with shoots and new growth from which 
budwood cuttings are taken. For example:  
• Armilla ria luteobubalina  and A. mellea were assessed in the Prunus import risk analysis . Armillaria species are associated with roots and 
crowns and are sometimes saprophytic but are unlikely to be associated with healthy dormant cuttings with roots removed.  
• Another root rot, Pyrrhoderma noxium  (Corner) L.W. Zhou & Y.C. Dai (2018) , is on the pest list of the existing import health standard  as 
Phellinus noxius. This pathogen was previously assessed by MPI , and the likelihood of it entering New Zealand associated w ith rootless 
budwood was assessed as negligible (MPI 2016) . 
• Ganoderma lucidum  causes white discolouration and white stringy wood rot in the roots and bases of trunks of host plants (CPC 2021).  
• Fomitiporia mediterranea infects citrus trees via pruning wounds, causing white rot decay in trunks and large branches (Elena et al 2006) . 
* Searches of Google Scholar and CAB Abstracts with the species name and ‘Citrus’ as search terms. In situations where there were hundreds  of search results , the firs t 10 pages of 
Google Scholar records were scanned for relevant records.  
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 128 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Appendix 2: Glossary and Abbreviations  
 
Term or abbreviation  Definition  
BORIC  Biosecurity Organisms Register for Imported Commodities , a retired MPI database  now replaced by ONZPR  
BRAD  Biosecurity Risk Analysis Database (MPI database)  
CASE  Contention , Argument , Source , Evidence. Under the CASE schema, the contention or conclusion is presented 
first, followed by the arguments supporting this contentio n and the evidence and sources supporting each 
argument.  
CMI Climate (or composite) match index , a value that indicates the similarities between a location overseas and 
New Zealand (Phillips et al. 2018)  
Commercial production  A process/system where activities, such as in -field monitoring, in -field pest control activities, harvesting, 
cleaning, sorting and gradin g have been undertaken to produce a commodity that is free of defects such as 
broken skin, rot and damage. Depending on the systems in place, these activities can be undertaken at any 
stage from the point of planting to the point of export.  
Commodity desc ription  The commodity description defines the form of the commodity that is covered by the IRA, e.g. the commodity 
species and the countries under consideration. The commodity description may also include commercial 
production and/or grading requirements o r other commodity quality specifications.  
CPC  Crop Protection Compendium (CABI database)  
Disease  A disorder of structure or function in a plant, especially one that affects a specific location and is not simply a 
direct result of physical injury  
Endemic  An animal, plant, pest, or disease that is native to and is not naturally found outside a defined g eographical 
area 
Establishment  Perpetuation, for the foreseeable future, of an organism or disease within an area after entry  
ERS Emerging Risk System (MPI workflow)  
Exposure  The process of the hazard organism moving from the commodity it arrived on to another host (also called 
“transfer”)  
Exotic  This word has different meanings in different fields, but in this document it is defined as an animal, plant, pest 
or disease that is not indigenous to New  Zealand.   
Biosecurity New Zealand   Citrus budwood for propagation IRA, April 2021  • 129 Term or abbreviation  Definition  
Hazard  A hazard is a pest (including arth ropods and pathogens) or disease that is not present in the PRA area, e.g. 
New Zealand (or is present but still represents a biosecurity risk, e.g. is capable of vectoring pathogens not 
present in the PRA area), has the ability to establish and cause harm in the PRA area and is associated with 
the entry pathway (commodity/country of origin) under consideration.  
Indigenous  Native; organism originating or occurring naturally in a specified area  
Inspection  Official visual examination of plants, plant product s or other regulated articles to determine if pests are present 
and/or to determine compliance with phytosanitary regulations (FAO 2012)  
Introduced  Not indigenous, not native to the area in which it now occurs, having been brought into this area directly or 
indirectly by human activity  
IPPC  International Plant Protection Convention, a 1951 multilateral treaty overseen by the Food and Agriculture 
Organization that aims to secure coordinated, effective action to prevent and to control the introduction and 
spread of pests of plants and plant products  
ISPM  International Standards for Phytosanitary Measures : international standard s adopted by the Conference of the 
Food and Agriculture Organization, the Interim Commission on phytosanitary meas ures or the Commission on 
phytosanitary measures, established under the IPCC  
IHS Import health standard  
IRA Import risk analysis , an administrative process through which quarantine policy is developed or reviewed, 
incorporating risk assessment, risk management and risk communication  
MPI Ministry for Primary Industries, New  Zealand  
NPPO  National plant protection organisation, official service established by a government to discharge the functions 
specified by the IPPC.  
NZOR  New Zeal and Organisms Register  
ONZPR  Official New Zealand Pest Register (MPI database) , replacement of BORIC  
PEQ  Post-entry quarantine  
Pest  Any species, strain or biotype of plant, animal, or pathogenic agent injurious to plants or plant products  
PFA Pest-free area  
PFPP  Pest-free place of production  
PPIN  Plant Pest Information Network database (MPI) : a record of organisms collected in New Zealand and identified 
by MPI’s Plant Health and Environment Laboratory  
PRA  Pest risk assessment or pest risk analysis  130 • Citrus budwood for propagation IRA, April 2021  Biosecurity New Zealand  Term or abbreviation  Definition  
QuanCargo  New Zealand border transaction database, detailing commercial consignments and interceptions of pests made 
by quarantine inspection (MPI)  
Quarantine pest  A quarantine pest is an organism that is not present in a PRA area, e.g. New Zealand (or is present but still 
represents a biosecurity risk, e.g. is capable of vectoring pathogens not present in the PRA area) and is 
capable of establishing and causing harm in the PRA area.  
Risk management question/s  Specific question/s that the risk manager needs answered in order to make a decision. They are based on the 
commodity description and basic measures for that commodity type.  
Vector  An organism or object that transfers a pest, parasite, pathogen or disease from one area or host to a nother.