Chrysomyxa rhododendri
(European Rhododendron rust)

C. rhododendri is a heteroecious rust fungus; an obligate parasite completing stages of its life cycle on different plants. Mating of haploid strains occurs on species of Picea, followed by the production of asexual aeciospores that infect Rhododendron species. Another asexual form producing urediniospores occurs on Rhododendron, followed by the production of teliospores (the sexual stage). All stages are known from Europe. The fungus was reported in 1954 on Rhododendron in the northwestern USA, but the aecial form has not been found in North America. The fungus is a Regulated Pest for the USA; it has been introduced into the UK, New Zealand and Australia. As an invasive species, this rust is damaging on species of Picea and Rhododendron. As latent infections on Rhododendron can be overlooked, accidental introduction of the rust may occur through the importation of these popular ornamental plants (Savile, 1973).

C. rhododendri has a circumpolar distribution throughout the northern hemisphere, but is apparently absent from southern Asia, Tibet, and perhaps Japan (Crane, 2001; 2005), although Chen (2002) recorded this species in Tibet. Endemic to alpine and boreal areas of Europe, it was absent from the UK until introductions to Scotland and England occurred early in the twentieth century (Bennell, 1985). In subsequent decades, the rust was accidentally introduced into Australia and New Zealand (Bennell, 1985).

This species was reported to be introduced into the USA in 1954 (Gould et al., 1955), but Crane (2001), after examining specimens from California and Washington, determined that those outbreaks on imported cultivated Rhododendron spp. were most likely due to a native rust species, Chrysomyxa reticulata. Crane (2001) also suggests that the American species, C. reticulata, was introduced at least once into the UK on Rhododendron plants and was mistaken for the European species. C. rhododendri in the uredinial stage is found in northern parts of Canada on the native Rhododendron lapponicum, but because telia have not been observed, there is no apparent danger of infection of spruces [Picea] (Savile, 1950;Ziller, 1974). Although C. rhododendri probably does occur on cultivated species and varieties in North America, Crane (2001) suggests that the identity of rusts found on Rhododendron should be verified carefully.

Crane (2005) and Crane et al. (2005) also found that many specimens from southern Asia and Japan identified as C.rhododendri are various native species, so that it is doubtful whether C.rhododendri occurs in the centre of origin for Rhododendron. Specimens from northeastern Russia and northern China were consistent with the morphology of the European species.

In Europe, the rust is considered a native of sub-alpine and boreal forests (Bauer and Schwaninger, 2007; Safránková, 2008). Gould et al. (1955) noted the unexpectedness of the appearance of what was thought to be invasive C. rhododendri on imported rhododendrons in the lowland coastal areas of the Pacific Northwest of North America. Although the species occurs in northern Canada (Parmelee, 1989), no continuous range of infection on native species in the areas south towards the state of Washington was observed. Crane (2001) considers this disparity of habitat to be support for her suggestion that the outbreaks were due instead to a species native to the Pacific Northwest.

Farr et al. (1996) list more than 60 Rhododendron species, varieties, hybrids and cultivars of worldwide origin as hosts of C. rhododendri. Other published lists are also extensive (Bennell, 1985; Roane, 1986). Given that there are Chrysomyxa species that can be confused readily with C. rhododendri (Crane, 2001; 2005; Crane et al., 2005), some of these reports should be reconsidered. There are fewer host species in Picea, but misidentification of the aecial form may also have occurred. Reported aecial hosts are listed in Safránková (2008), and BPI (2009).

Teliospores on rhododendron leaves germinate in spring to produce basidiospores that infect the young spruce [Picea] needles. Minute haploid spermagonia are the mating organs; plasmogamy after fertilization results in the production of aecia on needles during the summer. Aeciospores then infect young rhododendron leaves, and the fungus overwinters in these leaves. Brownish-orange telia, as well as yellow uredinia, develop on the undersides of leaves in spring from the previous year’s infection (Bennell, 1985). Urediniospores are a repeating spore, spreading the organism to susceptible new leaves during suitable conditions of cool temperature, low light, and high relative humidity (Roane, 1986).

Some differences have been noted in interactions between the rust pathogen and various Rhododendron hosts, apparently influenced by local climate. The fungus need not complete the full cycle of stages on both hosts, because it can persist and spread in the uredinial form through one or more generations per year on rhododendrons (Bennell, 1985). The observed absence of infection on spruce in northern Canada indicates that conditions cause this pattern on Rhododendron lapponicum (Parmelee, 1989). On the other hand, because current leaves of deciduous “azaleas” are shed in autumn, infection of the new leaves requires inoculum from spruce or evergreen rhododendrons in the spring (Bennell, 1985). In the UK, naturalized Rhododendron ponticum is susceptible to infection by aeciospores, but not urediniospores, and uredinia do not usually develop on that species (Bennell, 1985). In the highly susceptible Rhododendron charitopes, infection is not limited to leaves, and sporulation can occur on petioles, bud scales, pedicels and cataphylls (Bennell, 1985).

Vialle et al. (2009) have obtained and deposited sequences for the LSU region of rRNA for 10 Chrysomyxa species, including C. rhododendri, but at least an equal number are lacking in the genus.

Leaves, particularly the undersides, of Picea and Rhododendron plants must be examined under low power magnification for the presence of sporulating structures (spermogonia, aecia, uredinia, telia). Where small yellow to red spots appear, these should be re-examined after incubation. A period of post-entry quarantine should be sufficient to detect latent (overwintering) infections (Savile, 1973; Bennell, 1985). Aeciospores from Picea and urediniospores from Rhododendron should be examined at high magnification, including SEM, in order to identify the rust species.

A number of species of Chrysomyxa occur on either Picea or Rhododendron, or on both, and new species are likely to be identified in areas where plants in these genera are part of the native flora. The work of Crane (2001; 2005) and Crane et al. (2005), including descriptions of new species, demonstrates the continuing need to clarify identities and relationships in the genus. Species are identified and distinguished by aeciospore and urediniospore size, shape and ornamentation and by peridial wall form and cell ornamentation; characters that require close and careful examination. All teliospores in this genus are one-celled and produced in chains; they do not provide many diagnostic characters. When Chrysomyxa rusts appear on introduced plants, the species known from the source area as well as the area of introduction should be considered. According to Crane (2005), “Detailed, well-illustrated descriptions of these rusts are needed for identification”, and Crane (2001) provides such descriptions and a key to nine species of the genus on spruce [Picea] and Rhododendron. Some rusts are known only from the asexual uredinial stage on rhododendrons, without connection to a telial stage or aecial host, although they may appear likely to be related to Chrysomyxa (Crane, 2001; 2005; Crane et al., 2005).

Among recently-described species, Chrysomyxa reticulata, known only from North America, differs from C. rhododendri in having smaller urediniospores, mostly less than 20 µm diameter, with an area of reticulate ornamentation, and smaller aeciospores, also mostly less than 20 µm diameter (Crane, 2001). Caeomatsukubaense, described by Crane et al. (2005) from Asian specimens that were originally identified as C. rhododendri, differs in urediniospore surface ornamentation, observable using scanning electron microscopy (SEM), as well as in the sequence of the large subunit of rDNA.

Puccinia rhododendri, an autoecious rust on native rhododendrons, has been occasionally reported from Europe (Gaumann, 1959). In the genus Puccinia, teliospores are usually two-celled and urediniospores are echinulate (Wilson and Henderson, 1966).

According to Sinclair and Lyon (2005), yellowing and defoliation may occur to the current year’s needles of certain spruce species as a result of fluoride injury. Chlorosis develops from needle tips and the affected portion eventually turns red-brown. Older needles also develop symptoms, but more slowly. Other sensitive species growing nearby would show injury symptoms, and a source of the air pollutant could be identified.

Due to the variable regulations around (de)registration of pesticides, your national list of registered pesticides or relevant authority should be consulted to determine which products are legally allowed for use in your country when considering chemical control. Pesticides should always be used in a lawful manner, consistent with the product's label.

Prevention

Given the possibility of latent infections in Rhododendron, phytosanitary post-entry quarantine of imported plants is inevitable (Roane, 1986). Bennell (1985) notes the need to prevent introduction of new pathotypes of C.rhododendri to areas where the species already occurs. Clearly, if the species is, in fact, not present in the USA in areas climatically favourable for the rust and where spruce [Picea] and Rhododendron grow together, introduction of any C.rhododendri should be prevented (USDA/APHIS, 2008).

Eradication

Collection and destruction of infected Rhododendron leaves is suggested (Roane, 1986). Bennell (1985) proposes removal of all of the previous year’s leaves that are retained by, or fallen off, the plants as part of an eradication effort in gardens or nurseries; an alternative would be complete destruction of heavily infected plants.

Containment

The rust can be spread locally by the distribution of infected Rhododendron plants or cuttings from a nursery or other garden (Bennell, 1985). Measures suggested to prevent this include timing of transport to the early spring, so that sporulation from latent infections would soon be evident, or removal of the previous year’s leaves; the potential source of inoculums.

Cultural Control

Adequate aeration in Rhododendron plantings should reduce the humidity and free moisture needed for spore germination (Bennell, 1985; Roane, 1986). Planting should be avoided where the alternate host is growing or the alternate host should be removed in the vicinity of the more valuable planting of either spruce or rhododendron (Bennell, 1985; Hansen, 1997).

Chemical Control

Although Bennell (1985) discussed the use of various fungicides, such as zineb, triadimefon and oxycarboxin, as a complement to eradication efforts, Roane (1986) does not propose their use for rust control. In any case, most fungicides applied to rhododendrons for the control of powdery mildew will be effective against rust (Cox, 1993). The use of fungicides is not the preferred strategy to protect young spruce trees (Hansen, 1997).

Host Resistance

Although many are recorded as susceptible to C. rhododendri (Bennell, 1985; Roane, 1986), knowledge of the species, hybrids and varieties of Rhododendron may allow selection of appropriate plants for a particular area. Many hybrids are more susceptible than their parents (Bennell, 1985). Among Picea species used in plantations in the UK, Picea sitchensis showed resistance to this rust (Bennell, 1985).

The work of Crane (2001; 2005) and Crane et al. (2005) demonstrates that further information is needed, including detailed descriptions of known and not-yet identified species within the range of their hosts. Comparative data on susceptibility of species or cultivars to known or new rust species would aid in quarantine efforts as well as in the selection of suitable plants for introduction.

19/08/09 Original text by: