Preferred name: Chrysomyxa arctostaphyli
Authority: Dietel
Taxonomic position: Fungi: Basidiomycota: Pucciniomycotina: Pucciniomycetes: Pucciniales: Coleosporiaceae
Other scientific names: Melampsoropsis arctostaphyli Arthur, Peridermium coloradense Arthur & Kern
Common names in English: broom rust of spruce, common yellow witches' broom rust
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Notes on taxonomy and nomenclature EPPO Categorization: A1 list
EU Categorization: A1 Quarantine pest (Annex II A)
view more categorizations online...
EPPO Code: CHMYAR

C. arctostaphyli is a fungal pathogen with a 2-year life cycle alternating between the aecial host Picea spp. and the telial host Arctostaphylos spp. The fungus primarily infects members of the genus Arctostaphylos, which are commonly known as manzanitas, a group of evergreen shrubs and small trees native to North America. C. arctostaphyli is often referred to as manzanita rust because it causes rust-like symptoms on these plants. The pest develops aecia on Picea spp. and the main reported aecial hosts are Picea engelmannii and Picea pungens. Picea glauca, Picea mariana, and Picea rubens are also reported as hosts (Crane, 2000; Sinclair & Lyon, 2005). Arctostaphylos uva-ursi is reported as the most important alternate host of the rust, but Arctostaphylos nevadensis and Arctostaphylos patula have also been reported as telial hosts (Sinclair & Lyon, 2005). A. uva-ursi is present both in North America and in Europe, A. nevadensis and A. patula are only present in Western North America (EFSA, 2018).

For additional information, see Ziller (1974) and Sinclair & Lyon (2005).

Host list: Arctostaphylos nevadensis, Arctostaphylos patula, Arctostaphylos uva-ursi, Picea abies, Picea engelmannii, Picea glauca, Picea mariana, Picea pungens, Picea rubens, Picea sitchensis

C. arctostaphyli is distributed only in natural ecosystems throughout North America wherever the two host genera, Picea and Arctostaphylos, occur together (Crane, 2000). In Canada, the pathogen is widespread (Alberta, British Columbia, Manitoba, New Brunswick, Newfoundland, Northwest Territories, Nova Scotia, Ontario, Quebec, Saskatchewan, and Yukon). In the USA, it is present in the northern and western states (Alaska, Arizona, Colorado, Idaho, Maine, Michigan, Montana, New Mexico, New York, Oregon, South Dakota, Utah, Washington, Wisconsin, and Wyoming). The pathogen has not been reported in Europe and in the EPPO region.

North America: Canada (Alberta, British Columbia, Manitoba, New Brunswick, Newfoundland, Northwest Territories, Nova Scotia, Ontario, Québec, Saskatchewan, Yukon Territory), United States of America (Alaska, Arizona, Colorado, Idaho, Maine, Michigan, Montana, New Mexico, New York, Oregon, South Dakota, Utah, Washington, Wisconsin, Wyoming)

The pest was originally considered to be microcyclyic on Arctostaphylos spp. (Crane, 2000) and the life cycle was debated over several years. However, it is now agreed that C. arctostaphyli has a 2-year life cycle alternating between the aecial host Picea spp. and the telial host Arctostaphylos spp. (Crane, 2000). Aeciospores of the pest are produced during the summer on Arctostaphylos spp. and they re-infect the hosts from the same genus. Basidiospores are produced latter, and they infect a Picea spp. after overwintering, in early summer. The fungus persists in the twig and bud tissues of the brooms in spruce and colonizes the current year’s needles after overwintering, in the spring. Aeciospores are subsequently produced and infect Arctostaphylos spp. (Hennon & Trummer, 2001).

On Arctostaphylos spp.: There are no uredinia and urediniaspores. Telia form on reddish spots that blacken with age, usually hypophyllous, may also be epiphyllous on A. patula; gelatinous, found in groups, confluent when mature, forming pulvinate crusts erumpent through epidermis, 0.3–1.0 mm across (Crane, 2000).

On Picea spp.: Spermogonia and aecia on chlorotic, stunted, current-year needles of perennial witches’ brooms of Picea spp. (Bergdahl & Smeltzer, 1983). Spermogonia are subepidermal and aecia are peridermioid, bullet- or tongue-shaped. Aeciospores orange-yellow, spore walls are verrucose without a smooth spot.

C. arctostaphyli overwinters as mycelium in the systemically infected brooms on spruce (Crane, 2000) and as mycelium in the leaves of Arctostaphylos spp. Telia form on Arctostaphylos spp. in early spring and produce basidiospores that cause new infections on spruce, probably through the young needles of newly opened vegetative buds but it is not confirmed yet (Crane, 2000).

For further details see also Savile (1950), Ziller (1974), and Crane (2000).

Symptoms

On Picea spp.: The first symptom of the pest is needle etiolation in summer. Release of dormant buds results in conspicuous, compact, perennial witches' brooms with yellow-green needles on which foul-smelling, subepidermal pycnia are found. These are followed by aecia which give the brooms a yellow-orange appearance. Needles subsequently die and fall in the autumn, leaving the broom to appear dead during the winter. The fungus causes the production of numerous short lateral shoots causing the broom (Hennon & Trummer, 2001). The internodes and needles on the brooms are also shorter than normal (EFSA, 2018). The brooms grow over time and may become up to 2 m tall (Sinclair & Lyon, 2005). Witches' brooms of conifers not caused by rust retain the colour of normal dark-green foliage throughout the year; only a few of their needles are shed. Sometimes cankers, fusiform swellings and secondary brooms form on the branches and trunk. The branch and stem at the base of the broom become swollen due to the infection and may form a canker or gall (EFSA, 2018). Trees lose vigour and spike tops, dead branches and mortality are common. It is rare that more than 25% of Picea spp. trees in a stand are infected; and fewer than 1% of trees in an infected trees bear brooms. The disease is mainly found in spruce stands where the Arctostaphylos spp. host is also found (Hennon & Trummer, 2001). The abundance of brooms showed no trend with stand age (EFSA, 2018).

On Arctostaphylos spp.: The rust is most noticeable in late spring and causes a reddish leaf spot. Orange-brown, waxy telia form in crowded groups on these spots on the underside of leaves.

Morphology

Spermogonia numerous, prominent, dark reddish-brown when dry, subepidermal, sometimes arising between epidermis and hypodermis; in cross section, usually globose or with a slightly flattened base, 80–160 µm wide x 80–114 µm high (Crane, 2000). Spermatia variable in shape and size, globose, ovoid or ellipsoidal, 1.6–4.5 x 1.2–2.5 µm. Aecia amphigenous, crowded along most of the needle length. Aeciospores variable in shape and size, ellipsoidal, ovoid, or polygonal, occasionally globose, subglobose, clavate, or fusiform, often with both ends flattened or with a cap, part of a longitudinal stripe, 16–36 x 12–24 µm. Spores are orange-red, with warts annulate, irregular in shape, often joined laterally into ridges, basal connections lacking; wall hyaline, very thin (0.8 µm). Peridium tubular, dehiscing at apex, outside of cells shallowly concave, smooth, inside of cells shallowly concave, with crowded irregular warts similar to the spores (Crane, 2000).

Black telia are similar to pulvinate crusts erumpent through epidermis, 0.3–1.0 mm across, confluent when mature (Crane, 2000). Teliospores catenulate, oblong, rounded at both ends, wall smooth and colourless, uniformly 10–19 µm high x 6–16 µm wide (Ziler, 1974; Crane, 2000). Basidia curved, four-celled, basidiospores regular in size and shape, globose to subglobose with a tiny apiculus; 6–43 x 5–7 µm (Ziler, 1974; Crane, 2000).

Detection and inspection methods

The disease can be easily identified based on the symptoms, i.e. as dense witches’ brooms on spruce. A key is available to distinguish C. arctostaphyli from other tree rusts in western Canada based on the morphology and symptom descriptions (Ziller, 1974). The most conspicuous symptoms of spruce broom rust occur in early summer, when yellowish infected needles are present on shoots of witches’ brooms (Crane, 2000). After production of spermogonia and aecia, the needles shrivel and fall off, leaving bare, dead-looking brooms during the winter. Brooms can occur on the trunk or branches, and after many years attain a diameter of 1 m or even up to 2 m. Trees with up to 41 brooms have been reported in Newfoundland, CA (Singh, 1978).

Both the ITS and the large subunit (28S) regions in the chromosome were also successfully used for conventional PCR test and barcoding PCR to distinguish C. arctostaphyli from other species as well as in phylogenetic studies (Feau et al., 2011).

The main host commodities on which the pathogen can spread between countries are plants for planting and cut branches of Picea spp. (EPPO, 2018). Both pathways are closed for the EU countries due to the ban on importing plants of Picea spp., other than fruit and seeds, from non-EU countries (EPPO, 2018).

The pathogen could also be introduced on plants of Arctostaphylos spp., a pathway which is not currently regulated in EU countries (or elsewhere in the EPPO region). The most important alternate host, A. uva-ursi is present both in North America and in Europe (Calflora, 2023).

Long-distance dispersal is possible from infected plants of Picea spp. by wind-blown aeciospores, because aeciospores have a very high dispersal capacity and can survive for several months (Crane, 2000; EFSA, 2018).

Economic impact

C. arctostaphyli causes brooms and trees with abundant brooms often grow slowly and might die prematurely (Hennon & Trummer, 2001). Disease may also result in trunk deformations, cankers, growth loss, dead or broken tops and sometimes tree mortality (Sinclair & Lyon, 2005). In Southern Colorado and Northern Arizona (USA), the pathogen could infect many Picea species, but it only causes important damage to P. engelmannii and P. pungens. Nevertheless, the disease is not fatal generally and damage results from death of branches, deformation of trunks, reduced growth, and decay caused by secondary decay fungi which can enter via the rust infection sites (Hennon & Trummer, 2001; Sinclair & Lyon, 2005). In 21 stands of marketable P. engelmannii in Colorado, an average cull factor of 24% due to broken or dead trees’ tops adjacent to dead rust brooms has been reported (Schwandt, 2006). Since diseased trees are liable to shed branches, they also represent a hazard to the public.

Control

Chemical control has not been shown to be effective to manage the disease on spruce (Hennon & Trummer, 2001). Other pest control methods can be applied, namely removal of infected Picea spp. trees through selective thinning. It is also recommended to remove Arctostaphylos spp. within 300 m of Picea spp. stands; this measure can reduce the damage to spruce trees (Hennon & Trummer, 2001). Pruning of brooms may also reduce the risk of breakage and maintain tree vigour in high value trees (Schwandt, 2006). Given that C. arctostaphyli does not normally kill spruce trees, one management option is to take no action, considering that witches’ brooms offer refuge for many birds and small mammals, which may be a desirable feature for some tree or woodland owners (Hennon & Trummer, 2001).

Phytosanitary risk

Since A. uva-ursi is more commonly associated with Picea spp. in Eurasia than in North America, the rust is a potential danger to Picea spp. stands in Europe and Asia (Ziller, 1974).

It is unclear how susceptible P. abies is to the disease and what level of damage the species could sustain. Picea sitchensis is considered a minor host in North America but its susceptibility under European conditions is uncertain. It has been suggested, but not confirmed, that Picea-to-Picea transmission of the pathogen by aeciospores can occur (EFSAb, 2018).

The main phytosanitary measures are listed in the Standard PM 8/2 (3) Coniferae for C. arctostaphyli (EPPO, 2018). Import of plants for planting (except seeds) and cut branches of Coniferae including Christmas trees, originating in countries where C. arctostaphyli is present is allowed only from pest-free areas (EPPO, 2018). Import of wood, isolated bark of Coniferae originating in countries where C. arctostaphyli is present is allowed (EPPO, 2018) as the fungus is an obligate biotroph that grows and reproduces only in living plant tissue and spreads by windblown spores formed on needles.

The pathogen could also be introduced on plants of Arctostaphylos spp., a pathway which is not currently regulated, especially since the main alternate host (A. uva-ursi) grows across Europe (mainly in mountain range, such as the Pyrenees, Alps, Carpathians, Scandinavian mountains, Grampians, the Balkan Mountain range) (EFSA, 2018). Import prohibition of Arctostaphylos spp. plants for planting would be a suitable measure to reduce the risk of introduction.

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EPPO (2018) EPPO Standard PM 8/2(3) Commodity-specific phytosanitary measures. Coniferae. EPPO Bulletin 48(3), 463–494. https://doi.org/10.1111/epp.12503

EPPO (2021) EPPO Global Database page on EPPO A1 and A2 lists of pests recommended for regulation as quarantine pests. PM 1/002(30). https://gd.eppo.int/standards/PM1/ (accessed on 1^st September 2023).

Feau N, Vialle A, Allaire M, Maier W & Hamelin RC (2011) DNA barcoding in the rust genus Chrysomyxa and its implications for the phylogeny of the genus. Mycologia 103, 1250–1266. https://doi.org/10.3852/10-426

Hennon PE & Trummer L (2001) Spruce broom rust. USDA Forest Service Leaflet R10-TP-100. USDA Forest Service, Anchorage, Alaska, USA. https://www.fs.usda.gov/detail/r10/forest-grasslandhealth/?cid=fsbdev2_038391 (accessed on 1^st August 2023).

Pady SM (1941) Further notes on the witches' brooms and the sub-stomatal pycnia of Melampsorella. Transactions of the Kansas Academy of Science 44, 190–201. https://doi.org/10.2307/3624881

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CABI and EFSA resources used when preparing this datasheet

EFSA Panel on Plant Health (PLH), Jeger M, Bragard C, Caffier D, Candresse T, Chatzivassiliou E, Dehnen-Schmutz K, Gilioli G, Gregoire J-C, Jaques Miret JA, MacLeod A, Navajas Navarro M, Niere B, Parnell S, Potting R, Rafoss T, Rossi V, Urek G, Van Bruggen A, Van der Werf W, West J, Winter S, Boberg J, Gonthier P and Pautasso M, 2018. Scientific opinion on the pest categorisation of Chrysomyxa arctostaphyli. EFSA Journal 2018, 16(7), 5355, 20 pp. https://doi.org/10.2903/j.efsa.2018.5355

This datasheet was extensively revised in 2023 by Kateryna Davydenko, Ukrainian Research Institute of Forestry and Forest Melioration and Swedish University of Agricultural Science. Her valuable contribution is gratefully acknowledged.

EPPO (2024) Chrysomyxa arctostaphyli. EPPO datasheets on pests recommended for regulation. https://gd.eppo.int (accessed 2024-12-21)

This datasheet was first published in the EPPO Bulletin in 1979 and revised in the two editions of 'Quarantine Pests for Europe' in 1992 and 1997, as well as in 2023. It is now maintained in an electronic format in the EPPO Global Database. The sections on 'Identity', ‘Hosts’, and 'Geographical distribution' are automatically updated from the database. For other sections, the date of last revision is indicated on the right.

CABI/EPPO (1992/1997) Quarantine Pests for Europe (1^st and 2^nd edition). CABI, Wallingford (GB).

EPPO (1979) EPPO Data Sheet on Quarantine Organisms no 8: Chrysomyxa arctostaphyli. EPPO Bulletin 9(2), 39-43. https://onlinelibrary.wiley.com/doi/epdf/10.1111/j.1365-2338.1979.tb02449.x