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RMD-21-02: Pest risk management document for barberry (Berberis, Mahoberberis and Mahonia spp.) as a biological obstacle to the control of black stem rust (Puccinia graminis)

Effective date: June 3, 2022

Preface

As described by the International Plant Protection Convention (IPPC), pest risk analysis (PRA) includes 3 stages: initiation, pest risk assessment and pest risk management. Initiating the PRA process involves identifying pests and pathways of concern and defining the PRA area. Pest risk assessment provides the scientific basis for the overall management of risk. Pest risk management is the process of identifying and evaluating potential mitigation measures which may be applied to reduce the identified pest risk to acceptable levels and selecting appropriate measures.

This risk management document (RMD) includes a summary of the findings of a pest risk assessment and records the pest risk management process for the identified issue. It is consistent with the principles, terminology and guidelines provided in the IPPC standards for pest risk analysis.

On this page

Executive summary

Puccinia graminis Pers., black stem rust of cereals, is a regulated pest for Canada. It can cause significant damage not only to wheat, but also to barley, oat, and rye cultivars, as well as some other grasses. The fungus completes the sexual portion of its lifecycle on susceptible species of barberry (including Berberis, Mahoberberis and Mahonia spp.).

The presence of susceptible barberry plants in close proximity to fields of cereal crops can lead to localized epidemics of black stem rust. It can also lead to the development of new and more virulent races (biotypes) of the pathogen to which current cultivars of cereal crops may have little or no resistance. Therefore, barberry is regulated under the Plant Protection Act and regulations as a biological obstacle to the control of black stem rust.

In 2001, the Canadian Food Inspection Agency (CFIA) developed the Canadian Barberry Certification Program (CBCP) which describes the phytosanitary requirements relating to the import, domestic movement, sale and propagation of barberry plants in Canada. This program applies to the species and cultivars that are exempt from the prohibition of movement in Canada. Both the prohibition and the list of exemptions are currently in Schedule I of the Plant Protection Regulations. In the period since the program was implemented, new scientific literature has revealed that some of the approved barberry species or cultivars may be able to produce seed that could produce plants that are susceptible to black stem rust. In addition, new sterile barberry cultivars have been developed. The Canadian horticulture sector has requested a review of the current list of species and cultivars approved for propagation to potentially allow access to these new, less invasive cultivars.

This document presents 3 options and the CFIA's decision for managing barberry as a measure to control black stem rust in Canada. These options were proposed during consultation in April 2021, and the majority of respondents were in favour of CFIA's recommended option to remove the specific list of barberry species and cultivars exempt from the movement prohibition from the Plant Protection Regulations to facilitate changes to the list of cultivars based on science. The assessment criteria that will be used to determine which species and cultivars should be exempt from the barberry movement prohibition and the list of approved species and cultivars will be available to the public through the CFIA website. These measures are intended to protect Canada's economy by preventing the spread of barberry plants that are susceptible to black stem rust, while providing the flexibility to approve barberry species and cultivars based on the latest science.

Purpose

The purpose of this document is to communicate pest risk management considerations, and CFIA's decision for managing the risk of barberry plants serving as a biological obstacle to the control of black stem rust in Canada.

Scope

This document includes:

Information pertaining to current import requirements for specific plants or plant products may be obtained from the CFIA's Automated Import Reference System.

Definitions

Definitions of terms used in this document can be found in the International Standard for Phytosanitary Measures 5: Glossary of phytosanitary terms (PDF) or Plant health glossary of terms.

Background

Black stem rust is a serious pest of cereals (primarily wheat), that is caused by Puccinia graminis f. sp. tritici, a fungus that relies on barberry (including Berberis, Mahoberberis or Mahonia spp.) to complete the sexual portion of its lifecycle. Without this alternative host, Puccinia graminis can still infect cereals, but the pathogen population becomes less variable, and contains fewer stem rust races. This allows resistant cereal varieties to be developed, to effectively manage the disease. In addition, without this sexual lifecycle on barberry, the initial spring inoculum must arrive from distant sources, thus arriving later in the growing season and at lower levels (Bailey et al, 2003), resulting in less severe symptoms and losses.

Common barberry (Berberis vulgaris) was introduced into North America from Europe. Early settlers brought the plant for cultivation, but it readily escaped and spread to locations suitable for tree or shrub growth. For many years, barberry was known to have an adverse effect on cereals, but it was not until 1865 that the relationship between barberry and black stem rust was identified. In the early 1900s, eradication programs were initiated in Canada and the United States (U.S.), and today, although Berberis vulgaris can still be found throughout Canada, its numbers have been greatly reduced following decades of eradication – especially in the wheat producing areas of the Canadian prairies.

The U.S. Department of Agriculture's (USDA) Animal and Plant Health Inspection Service (APHIS) lists the major wheat producing states where barberry has been eradicated as protected areas and regulates interstate movement of rust-susceptible Berberis, Mahoberberis, or Mahonia into or through these protected areas. State officials within the protected areas are responsible for movement certification, and for administering an inspection program of the barberry producing facilities to ensure that they are free from rust-susceptible plants, and that the species and cultivars produced are listed as rust-resistant and remain true to type. APHIS defines rust-resistant plants as, "all plants of the genera Berberis, Mahoberberis, and Mahonia, and their progeny, that have proven resistant to black stem rust during testing by the USDA and that are listed as rust-resistant under §301.38-2 (a)(1) and (a)(2)".

In Canada, the CFIA administers the Canadian Barberry Certification Program (CBCP), which outlines the requirements for import, domestic movement, sale and propagation in Canada of barberry plants (including Berberis, Mahoberberis or Mahonia spp.). Before the program was created in 2001, the importation and inter-provincial movement in Canada of all deciduous barberry species had been prohibited since 1966. With the implementation of the CBCP, the CFIA developed a list of barberry species and cultivars that are considered resistant to black stem rust based on testing conducted by the Cereal Rust Laboratory of the USDA (University of Minnesota, St. Paul, MN) and in field plots results from the Agriculture Canada Central Experimental Farm in Ottawa. The final list of 11 cultivars was published in Schedule I of the Plant Protection Regulations as being exempt from prohibition of movement. The requirements that apply to these species and cultivars are stated in the CBCP and can be found in D-01-04: Plant protection import and domestic movement requirements for barberry (Berberis, Mahoberberis and Mahonia spp.) under the Canadian Barberry Certification Program.

Risk assessment summary

Pest biology

Black stem rust

Puccinia graminis has a complicated life cycle, composed of 5 spore stages and 2 hosts.

Urediospores (grass to grass infection): The uredial stage is often referred to as the repeating stage since it can continue to produce spores on wheat as long as the wheat plant is alive. It is through this asexual stage that an epidemic is sustained as a new generation of urediospores can be produced every 7 to 14 days. These spores can rapidly spread the infection over a wide area through wind dispersion.

Teliospores, Basidiospores and Pycniospores (grass to barberry infection): Overwintering black teliospores form on cereal when it is ripe. Without the presence of susceptible barberry, the stem rust disease cycle ends as the teliospores formed in the autumn cannot infect wheat or barley (or other host cereal crops) the following season. If exposed to extended periods of freezing temperatures, teliospores germinate in the spring to produce short-lived basidiospores which infect young tissues (2 weeks old or fewer) of susceptible barberry (Zhao et al. 2016). Once barberry is infected, the fungus produces pycnia which produce pycniospores. If fertilization occurs between pycnia of different mating types, then aeciospores can be produced.

Aeciospores (barberry to grass infection): Aeciospores are produced only on susceptible barberry, and 1 single infected barberry plant can produce as many as 64 billion aeciospores (Schumann and Leonard, 2000). Aeciospores are released from infected barberry leaves and can infect nearby cereal crops. Once aeciospores reach a host, urediospores are produced, thereby completing the life cycle.

Susceptible barberry plants near cereal production areas allow the sexual reproduction of Puccinia graminis, and therefore enable hybridization and creation of new rust races to which cereal cultivars may not be resistant.

Barberry

Not all barberry plants can act as an alternative host for black stem rust. Some species are resistant and therefore, are not infected by Puccinia graminis. There are many hybrids within the barberry genus; most horticultural, and some wild barberry plants, stem from hybridization. Uncontrolled hybridization becomes a problem when rust-resistant cultivars cross with susceptible barberry. Seeds from these crosses may produce both resistant and susceptible plants. To add to the complexity, hybrids from crosses between resistant and susceptible barberry cultivars, may have the appearance of the resistant parent, but possess the susceptibility to black stem rust of the susceptible parent.

Japanese barberry (Berberis thunbergii), the species from which most of the current horticultural cultivars originate, is considered non-host resistant to black stem rust (Bartaula et al., 2019). Non-host resistance means that an entire plant species demonstrates broad-spectrum defense against all genetic variation of a pathogen. However, Japanese barberry can readily hybridize with common barberry, which is a black stem rust susceptible species. Offspring of such hybrids may be capable of producing susceptible off-spring.

Pathways for introduction and spread

Black stem rust

Black stem rust has a complex life cycle that includes a sexual stage (on the alternate host barberry) and an asexual stage (on susceptible grasses and cereals). Spread of black stem rust and resulting infection of cereals can come from aeciospores produced on susceptible barberry plants surrounding the host crops or from the repetitive infection by urediospores. In the southern U.S. and northern Mexico, urediospores continue to propagate on fall-planted cereals from volunteer wheat plants that sprout and become infected in the summer. However, in Canada, urediospores cannot indefinitely re-infect host crops because cold temperatures end the cycle with the production of teliospores that overwinter and can only infect an alternate host in the spring.

In Canada, black stem rust epidemics are considered to have been associated with barberry as, by allowing the sexual stage, the rust can establish early each spring. The numerous aeciospores produced on susceptible barberry spread to cereal hosts and cause infection, and multiple generations of urediospores can then spread the infection rapidly over a wide area. Without susceptible barberry in proximity to susceptible cereal crops, the initial spring inoculum must arrive in Canada from distant sources, such as from the southern U.S. and northern Mexico, thus arriving later in the growing season and at low inoculum levels (Bailey et al, 2003), and resulting in less severe symptoms and losses in cereal cultivars lacking black stem rust resistance.

In addition to causing early infection of host crops, susceptible barberry is also the source of new black stem rust races as the sexual stage allows for gene virulence reshuffling. Over the years, breeders have developed black stem rust resistant cereal varieties. However, these varieties may not be resistant to new, more pathogenic black stem rust races formed on barberry. In warm climates, barberry is not infected by black stem rust as teliospores do not germinate unless exposed to extended periods of freezing temperatures (Schumann and Leonard, 2000). Therefore, new races are less likely to develop as the sexual stage does not occur in warmer regions. Thus, the later spring inoculum from the south that reaches Canada poses a reduced risk of overcoming the resistance bred into current cereal varieties, compared to the inoculum generated on susceptible barberry.

Barberry

After years of eradication programs, common barberry (Berberis vulgaris) can be found in many different parts of Canada but is no longer considered to be commonly found in Canada – especially in the Canadian prairies. Japanese barberry (Berberis thunbergii) has escaped or become naturalized locally in Ontario, Quebec, New Brunswick, Prince Edward Island and Nova Scotia. Three native barberry species (Mahonia aquifolium, Mahonia nervosa and Mahonia repens) are largely restricted to British Columbia but 2 species (M. aquifolium and M. repens) are cultivated in other parts of Canada. Mahonia aquifolium is known to have become locally naturalized in parts of Ontario and Quebec, whereas M. repens is known to have become locally naturalized in parts of Ontario.

Barberry produces attractive fleshy berries that get eaten by birds who then spread the seeds to new areas. The quantity of fruit produced varies depending on the species and cultivar. Seeds can remain dormant in the soil for up to 10 years and have a high germination rate. Barberry is also capable of vegetative reproduction by root sprouts and stem layering.

Japanese barberry (Berberis thunbergii) is considered invasive in most of the eastern Canadian provinces (Nova Scotia, Ontario, Prince Edward Island and Québec) (CABI 2020), and is regulated as such by some U.S. states (for example, Massachusetts, New Hampshire, Vermont). The invasive nature of Japanese barberry is due to the combination of multiple and effective reproduction mechanisms, a low rate of plant mortality (Ehrenfeld 1999), and its capacity to tolerate a wide range of environmental conditions, such as full sun to full shade, severe drought and extreme winters (CABI 2020).

Potential economic consequences

Black stem rust is considered to be one of the worst pests of wheat. It can cause complete crop loss within a few weeks in a seemingly healthy-looking crop (Fetch et al, 2011). In Canada, the last major epidemics occurred in 1953 to 1955 and caused hundreds of millions of dollars in losses (Fetch et al, 2011).

Conners (1958) reported that, when susceptible barberry is grown near cereals, yield losses can range from 40% to the destruction of the entire crop. Craigie (1957) also reported that, during the 1916 epidemic in western Canada, 100 million bushels of wheat were lost to stem rust.

Today, the impact of black stem rust in North America has been reduced as breeders have developed cereal varieties carrying a combination of genes conferring resistance to many black stem rust races. However, this resistance could be lost with the increased presence of susceptible barberry plants in cereal production areas as they would allow for gene recombination and the creation of new races that our current cereal varieties may not be resistant to.

For example, Ug99 (TTKSK), a virulent race of black stem rust discovered in Uganda in 1999, was shown to overcome many wheat resistance genes. In 2010, it was estimated that 80 to 90% of global wheat cultivars were susceptible to Ug99 or its variants (FAO, 2010). Another new race, TKTTF, caused severe yield losses during an epidemic in Ethiopia in 2013 to 2014. TKTTF affected Ethiopia's most widely grown variety (Digalu) and grain yield losses of up to 100% were observed over an area exceeding 10,000 ha (Singh et al 2015).

Risk management considerations

Recent scientific literature has documented that some of the approved Canadian barberry species and cultivars that were previously assessed as being resistant to black stem rust may in fact be capable of producing susceptible offspring. Two cultivars, 'Concorde' and 'Royal Cloak', that were thought to be true Japanese barberry are in fact hybrids between B. thunbergii (rust-resistant) and B. vulgaris (rust-susceptible) and have therefore been reclassified as B. × ottawensis (Lubel et al. 2008). 'Tara' Emerald Carousel is known to be a hybrid between B. thunbergii and B. koreana (moderately susceptible to black stem rust) (Levine and Cotter 1932). It is unclear if this hybrid could produce susceptible offspring, but 'Tara' Emerald Carousel is the most prolific seed producer (Brand et al. 2012) amongst all approved cultivars in Canada.

Jin et al. (2014) determined that Mahonia aquifolium and Mahonia repens, both native to Canada and currently exempt from prohibition under the Plant Protection Regulations, could serve as alternate hosts for black stem rust. Therefore, these species require further evaluation to determine if movement prohibition should apply. Restricting their movement outside of their native areas could be considered as a potential risk mitigating measure.

Some of the new, commercialized, resistant cultivars in the U.S. are sterile or produce a limited quantity of seed. These cultivars present an excellent alternative to some of the currently approved cultivars of Japanese barberry that either pose a risk of producing offspring that are susceptible to black stem rust or have an invasive character due in part to the large number of seeds that they produce. The demand for barberry in Canada remains high, with growing interest in new cultivars, which are currently prohibited in Canada but approved for production in the U.S.

The high potential for hybridization between rust-resistant and rust-susceptible barberry, combined with the invasiveness of Japanese barberry, support the need for a continued barberry regulatory program, and highlight the need for a review of the species and cultivars currently exempt from movement prohibitions. Without movement restrictions and removal of potentially susceptible barberry from the list, large numbers of barberry plants capable of producing rust susceptible offspring could continue to be sold and distributed throughout Canada. This could lead to an increased number of susceptible barberry plants and potential creation of new black stem rust races. With the creation of new black stem rust races, cereal breeding programs as well as previous barberry eradication efforts could be compromised.

Pest risk management options

In April 2021, the CFIA presented 3 pest risk management options for mitigating the risk of black stem rust by prohibiting susceptible barberry plants in Canada, while permitting trade of species and cultivars that are resistant to black stem rust for consultation. Pros and cons are presented for each approach.

Option 1: Maintain status quo

Under this option, the CFIA maintains, in Schedule I of the Plant Protection Regulations, the current list of barberry species and cultivars that are exempt from the prohibition of movement. The current CBCP that describes import, propagation and domestic movement requirements for barberry continues to apply.

Pros:

Cons:

Option 2: Replace the list of exempt species and cultivars with assessment criteria that will be used to determine which species and cultivars should be added to or removed from the list of barberry species or cultivars that are exempt from movement prohibition

Under this option, the list of species and cultivars that are exempt from prohibition is removed from Schedule I of the Plant Protection Regulations. Exemption criteria used for assessment are described in Schedule I. Species or cultivars meeting the criteria are approved for production in Canada and the CFIA maintains the list of approved species and cultivars in D-01-04: Plant protection import and domestic movement requirements for barberry (Berberis, Mahoberberis and Mahonia spp.) under the Canadian Barberry Certification Program and makes it available to the public. The CBCP is revised to update production practices, requirements and inspection criteria. Cultivars that are currently approved are evaluated based on the latest available science, and cultivars that are determined to pose a risk to the control of black stem rust are removed from the list of cultivars exempt from movement prohibition, and subsequently removed from the marketplace using a phased approach.

Pros:

Cons:

Option 3: Prohibit all barberry species and cultivars

Under this option, importation, propagation or domestic movement of any barberry species or cultivar is prohibited in Canada. The list of species and cultivars that are exempt from prohibition is removed from Schedule I of the Plant Protection Regulations. Barberry species and cultivars are removed from the marketplace using a phased approach.

Pros:

Cons:

Risk management decision

Consultation

Comments on this risk management document were solicited from stakeholders from March 30, 2021 until April 30, 2021. All comments received were reviewed and taken into consideration, and additional information was added to the risk assessment summary section of this document to provide clarification. The majority of partners and stakeholders expressed support for option 2 as the most reasonable and science-based option.

Decision

Based on the risk assessment, and after analyzing all comments received, the CFIA has decided to move forward with a modified Option 2. The CFIA is reviewing the options for regulatory changes and currently plans to update Schedule I to reflect that only approved species and cultivars, as per the publically available list, are exempt from the movement prohibition. The desired outcome is a flexible approach for the addition and removal of cultivars based on science, while continuing to prohibit the movement of barberry species and cultivars that are not resistant to black stem rust. Assessment criteria developed in consultation with stakeholders will be used by the CFIA to evaluate barberry species and cultivars. The assessment criteria and the list of exempt species and cultivars will be available to the public via the CFIA website.

This option protects the grain industry by allowing for a more responsive approach to risk mitigation of black stem rust, while supporting market opportunities for the horticulture industry. It is scientifically based and aligns with the CFIA's plant health mandate. It will also allow the CFIA, in consultation with stakeholders, to strengthen the CBCP. In addition, new black stem rust resistant cultivars, currently prohibited in Canada, could present an alternative to some of the currently approved cultivars that have an invasive character or that may be capable of producing susceptible offspring.

A notice to industry, presents recommendations for those barberry cultivars that were identified as potential obstacles to the control of black stem rust during the risk assessment process. Until the regulatory change is complete, the CFIA strongly recommends that no plants of 'Concorde', 'Royal Cloak' and 'Tara' Emerald Carousel cultivars be moved into or propagated in Alberta, Saskatchewan or Manitoba due to the risks associated with the possible emergence of new strains of black stem rust from the progeny of these cultivars and their potential impacts to wheat production in these provinces. Respecting this recommendation would limit the risk of susceptible offspring in the area considered most at risk to black stem rust.

Next steps

As implementation of Option 2 requires a regulatory change, the CFIA is in the process of reviewing options for revisions to Schedules I and II of the Plant Protection Regulations. The CFIA will also develop the assessment criteria in consultation with stakeholders that will be used to exempt species and cultivars and will begin review of the CBCP to update production practices, requirements and inspection criteria. The CFIA will circulate the assessment criteria and updated CBCP for stakeholder consultation. The CFIA will also consult with impacted stakeholders in the development of a transition prior to the removal of any exempt cultivars from the list.

Endorsement

This risk management document has been approved by the Chief Plant Health Officer.

References

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