Northern spruce-rhododendron rust -Chrysomyxa rhododendri

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

Chrysomyxa rhododendri de Bary

Chrysomyxa rhododendri is a heteroecious rust, the aecial stage occurring on needles of species in Picea, and the uredinial and telial stages on the leaves of species of Rhododendron.

Spermogonia amphigenous, subepidermal, globose, yellow, turning brown.

Aecia amphigenous (on both sides of needles), cylindrical, 0.3-1.3 mm diam, single or confluent; peridium white, margin lacerate, peridial cells concave, smooth on outside, internal wall convex, with low irregular warts. Aeciospores in chains, globose, ovoid to ellipsoid, one or both ends flattened, or with a small cap, and indistinct longitudinal stripe, 18-30 x 16-22 µm, pale orange; wall 2-3.3 µm thick including warts.

Aecia amphigenous (on both sides of needles), cylindrical, 0.3-1.3 mm diam, single or confluent; peridium white, margin lacerate, peridial cells concave, smooth on outside, internal wall convex, with low irregular warts. Aeciospores in chains, globose, ovoid to ellipsoid, one or both ends flattened, or with a small cap, and indistinct longitudinal stripe, 18-30 x 16-22 µm, pale orange; wall 2-3.3 µm thick including warts.

Telia hypophyllous, orange-red, in groups or confluent, erumpent, to 1 mm long; teliospores in chains, chains in rows. Spores cuboid to ellipsoid, 20-28 x 12-21 µm, thin-walled, smooth, rounded, densely crowded.

See Crane, 2001.

Notes: Savile (1950) reduced this species to a variety of C. ledi de Bary, basing the name on Uredo rhododendri DC, however, this was an incorrect placement of an anamorph in a teleomorphic genus. His subsequent publication (Savile, 1955) of the variety with a description of the teleomorph, nevertheless, is an illegitimate later homonym of the 1950 taxon, so that the variety name was not validly published (Crane, 2001). Crane (2001) found morphological differences between C. ledi and C. rhododendri originally described and illustrated by de Bary (1879) to be consistent in existing specimens, so retained de Barys species in her examination of North American Chrysomyxa.

Distribution: Chrysomyxa rhododendri has a circumpolar distribution throughout the Northern Hemisphere, but is apparently absent from southern Asia, Tibet, and perhaps Japan (Crane, 2001, 2005). Endemic to alpine and boreal areas of Europe, it was absent from the United Kingdom 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 United States 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, C. reticulata. Crane (2001) also suggests that the American species, C. reticulata, was introduced at least once into the United Kingdom 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 R. lapponicum (L.) Wahlenb., but because telia have not been observed, there is no apparent danger of infection of spruces (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 find 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 center of origin for Rhododendron. Specimens from northeastern Russia and northern China were consistent with the morphology of the European species.

Similarities to other 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 1-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 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 P.E. Crane, known only from North America, differs from C. rhododendri in having smaller urediniospores, mostly less than 20 µm diam, with an area of reticulate ornamentation, and smaller aeciospores, also mostly less than 20 µm diam (Crane, 2001). Caeoma tsukubaense, 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 Fuckel, 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 years 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 likely be identified.

Detection and Inspection methods: 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.

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

Habitat: In Europe, the rust is considered a native of sub-alpine and boreal forests (Bauer and Schwaninger, 2007; Safrankova, 2008).Consequently, 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 (Parmalee, 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.

Plants Affected: 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 Safrankova (2008), and BPI (2009).

Symptoms-Description Infection of Picea results in transverse yellowed bands on the current years new needles, or whole needles may be chlorotic. The white columnar peridia of the aecia project from the undersides of the needles in summer. The needles are shed by winter, leaving bare shoots (Murray, 1955; Bennell, 1985; Bauer and Schwaninger, 2007).

In spring, red-brown spots develop on both sides of the leaves of many Rhododendron species, although the yellow pustules of the uredinia are primarily hypophyllous. In some species, uredinia also appear on leaf scars and twigs. Infected leaves are usually dropped the next year, after telia expire, but heavily infected leaves may be dropped before winter; some species retain mature infected leaves for more than two years (Bennell, 1985; Safrankova, 2008).

Biology and Ecology: Teliospores on rhododendron leaves germinate in spring to produce basidiospores that infect the young spruce needles. Minute haploid spermagonia are the mating organs; plasmogamy after fertilization results in 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 years 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, since 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 R. lapponicum (Parmalee, 1989). On the other hand, since 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 Great Britain, naturalized R. 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 R. charitopes, infection is not limited to leaves, and sporulation can occur on petioles, bud scales, pedicels and cataphylls (Bennell, 1985).

Natural dispersal: Rust aeciospores, urediniospores and sporidia (basidiospores) are distributed by wind and rain splash (Bennell, 1985)

Vector dispersal: None identified.

Accidental introduction: Introduction has occurred as the result of importation of rhododendron plants for ornamental purposes (Bennell, 1985). The latency of infections, particularly over winter, makes this likely unless post-entry quarantine is practiced (Savile, 1973). Air travel and transport increase the likelihood of introduction of infected rhododendron plants from the wild, but transport of spruce seedlings with infected needles is unlikely, since the symptoms of current infections are conspicuous (Bennell, 1985).

Economic impact: Although the loss of needles in autumn may usually have a "slight or transient" effect on growth of spruce trees (Hansen, 1997), Mayr et al. (2001) found that intense infections did have an effect on annual increments of wood production in subalpine Picea abies. Because some of the damaged needles are retained (Mayr et al, 2009), their increased transpiration, leading to increased water loss in wintertime, may be another factor affecting tree growth, particularly at the alpine timberline. Furthermore, natural regeneration of P. abies stands and use of the species in afforestation of alpine and boreal areas may be hindered by C. rhododendri, since the reduction of photosynthetic capacity resulting from loss of the newest foliage has a greater effect on seedlings (Bauer and Schwaninger, 2007).

Roane (1986) states that rusts on Rhododendron are not usually a serious problem, although some species and varieties may be severely damaged. Post-entry quarantine that may require more than 6 months (Bennell, 1985) imposes an additional cost on trade in Rhododendrons. Local occurrence of this rust may hinder trade in plants and germplasm.

Environmental impact: Given the difficulty of identifying species, rusts may be introduced to new host species in the centers of their diversity (C. rhododendri to southern China) with unforeseeable consequences for the hosts. The outbreak reported in the northwestern United States (Gould et al., 1955), even if actually due to a native species, is an example of what may happen when susceptible plant species encounter a new rust. Bauer and Schwaninger (2007) suggest that the burden of C. rhododendri attacks is one factor affecting species composition on west-facing slopes of alpine valleys, where Pinus cembra, rather than Picea abies, is predominant in an association with native Rhododendron.

Prevention: Given the possibility of latent infections in Rhododendron, phytosanitary postentry 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 United States in areas climatically favorable for the rust and where spruce and Rhododendron grow together, introduction of any C. rhododendri should be prevented (USDA/APHIS, 2009).

Eradication: Collection and destruction of infected Rhododendron leaves is suggested (Roane, 1986). Bennell (1985) proposes removal of all of the previous years leaves that are retained by, or fallen off of, 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 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 years 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 control of powdery mildew will be effective against rust (Cox, 1993). 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 United Kingdom, P. sitchensis showed resistance to this rust (Bennell, 1985).

Gaps in Knowledge/Research Needs: 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 selection of suitable plants for introduction.

References

Nomenclature

Specimens in BPI

Additional distribution data

Suggested citation: Chalkley, D. Systematic Mycology and Microbiology Laboratory, ARS, USDA. . Invasive Fungi. Northern spruce-rhododendron rust -Chrysomyxa rhododendri . Retrieved November 21, 2009, from http://nt.ars-grin.gov/sbmlweb/fungi/index.cfm .