Occurrence and Effect of Chrysomyxa Pirolata Cone Rust on Picea Pungens in Utah

Great Basin Naturalist

Volume 42 Number 2 Article 11

6-30-1982

Occurrence and effect of Chrysomyxa pirolata cone rust on Picea pungens in Utah

David L. Nelson U.S. Department of Agriculture, Forest Service, Ogden, Utah

Richard G. Krebill Arizona State University, Tempe

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Recommended Citation Nelson, David L. and Krebill, Richard G. (1982) "Occurrence and effect of Chrysomyxa pirolata cone rust on Picea pungens in Utah," Great Basin Naturalist: Vol. 42 : No. 2 , Article 11. Available at: https://scholarsarchive.byu.edu/gbn/vol42/iss2/11

This Article is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized editor of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. OCCURRENCE AND EFFECT OF CHRYSOMYXA PIROLATA CONE RUST ON PICEA PUNGENS IN UTAH

David L. Nelson' and Richard G. KrebilF

In Abstract.- a rare 1969 epidemic, spruce cone rust caused by Chrysomyxa piwlata infected 40-100 percent of trees and 20-67 percent of cones on riparian Colorado blue spruce on plots located in a 2200-2400 m elevational zone in Huntington Canyon of central Utah. Uredinial and telial sporulation on Ptjrola spp. began in mid-June, a time closely correlated with opening of pistillate spruce cones. Cone phenology and host habitat, as influenced by elevation, are apparently important factors in the restricted niche of the cone rust fungus in Utah. Several preceding consecutive years with extended periods of spring and fall moisture were associated with occurrence of the epidemic, although no cause-and-effect relationship was established. Weather records indicate that these events are infrequent in this climatic zone, and there was no detectable recurrence of cone rust for at least 9 years following 1969. Outwardly normal seeds developed in diseased cones, but seed germinability was reduced by 25 percent. Ae- cial spore masses between cone scales, cone resinosis, and distortion of cone scales prevented seed dispersal to the extent that the seed crop was effectually destroyed.

Our discovery of a rare outbreak of spruce ern hemisphere (Jcirstad 1940, Savile 1950, cone rust caused by Chrysomyxa pirolata Ziller 1974), extending across North America (Komike) Wint. on Picea pungens Engelm. in and Eurasia. In the contiguous western central Utah (Nelson and Krebill 1970) af- United States, incidence is relatively low, and forded the opportunity to study the nature of on spruce considered only occasional (Hedg- the disease. Mycological collection records cock 1912) compared with Canada, where its provide insight into its distribution; but infor- occurrence is frequent (Can. Dept. Environ. mation on the effect, ecological nature, and 1951-1975). Abundance similar to that in epidemiology of the disease is limited, espe- Canada is evident in Alaska (Cash 1953, Kim- cially for the contiguous western United mey and Stevenson 1957, Zasada and Gre- States. gory 1969), and it occurs on Pyrola (pyrola) or Moneses (single-delight) species in Nevada Review (Arthur 1907-1931), California, Colorado, Idaho, Oregon, Montana, New Mexico, Utah, The spruce cone rust fungus is hetero- Washington, Wyoming (Arthur 1934), South ecious and full cycled (Eraser 1912, Savile Dakota (Peterson 1961), and Arizona (Gil- 1953, Ziller 1974). The aecial and pycnial bertson and McHenry 1969). As in other re- stages form on female cones of Picea spp. gions of its distribution (Ziller 1974), in the Peridermial aecia develop on outer surfaces western United States in certain areas, it is of cone scales (Arthur and Kern 1906). Myce- rather common on Pyrola and Moneses spp., lium of the uredinial and telial stages is sys- but not known on spruce. Prior to this ac- temic and perennial in Pyrola and Moneses count, C. pirolata was known to occur on spp. (Rice 1927, Gaumann 1959). The per- spruce in Colorado, Montana, Oregon (Ar- ennial nature ensures persistence of the rust thur 1934), and Washington (Shaw 1973). during periods unfavorable for infection (Sav- Apparent extension beyond the range of ile 1953). spruce may result from its perennial nature Favorable habitat for C. pirolata occurs on the telial host and a possible lower fre- primarily in the boreal regions of the north- quency of critical requirements occurring for

'Intermountain Forest and Range Experiment Station, U.S. Department of Agriculture, Forest Service, Ogden, Utah, located at Shrub Sciences Labora- tory, Provo, Utah 84601. ^Rocky Mountain Forest and Range Experiment Station, U.S. Department of Agriculture, Forest Service, Forestry Sciences Laboratory, Arizona State University, Tempe, Arizona 8528L

262 263 Tune 1982 Nelson, Krebill: Cone Rust on Spruce infection of spruce than for pyrola. Although thur 1934, Brown 1956, Shaw 1973). Damage unclear from the literature, however, it ap- to these species by the disease is apparently pears that collection locations of the rust on minor, with some atrophy and yellowing of Pyrola and Moneses spp. in the West are leaves (Rice 1927, 1935). Disease symptoms within the distributional range of spruce. reported on spruce cones in Canada include Presently a clear extension beyond the range an early yellowing of cone scales, resin flow, of spruce is the occurrence in Guatemala on premature browning, and—following aecial Pyrola secunda L. (Cummins 1943), a great formation— a premature opening of the cones distance from the nearest indigenous spruce (Eraser 1912, Ziller 1974). Distortion or at- in northern Mexico (Martinez 1963). During rophy of cones is not indicated in the liter- the Pleistocene, spruce extended farther ature. Except for Picea breweriana S. Wats., south and the fungus may have survived on Picea chihitahuana Martinez, and Picea rnexi pyrola to the present, when spruce died out, cana Martinez, all native North American rather than spreading southward on pyrola. spruce species are known hosts of C. pirolata Inaccessibility of rusted cones to the casual (Arthur and Kern 1906, Ziller 1957, Can. collector is likely a factor in the apparent Dept. Environ. 1951-1975). Hedgcock (1912) low frequency of this rust on spruce. Also, described infected cones of Engelmann there are no specific, systematic annual sur- spruce {Picea engelmannii Parry) as aborted, veys made in the western United States to de- with the only apparent damage being a re- tect rust diseases as there are in Canada. duction in seed crop. The infection is thought Little knowledge of the epidemiology of to spread completely throughout the cone this fungus exists. Clinton and McCormick (Savile 1950). Damage to seeds in rusted (1919), in Petri dish culture tests, failed to ob- cones apparently can be severe. Rhoads et al. tain infection of excised pyrola leaves using (1918) indicate that no seeds are produced in uredinial inoculum, even though success was infected cones. In the United States (Zasada achieved with other rust fungi. Eraser (1911, and Gregory 1969) and in Canada (Can. 1912, 1925) made a series of phenological ob- Dept. Environ. 1951-1975), reports indicate servations and inoculation studies of the rust that no sound seeds are produced, although in Nova Scotia and Saskatchewan, Canada. no germination studies were reported to sup- He observed that uredinia on pyrola matured port this. Eide (1927) in Norway found that and began releasing spores by early May, and 33 percent of the seeds from rusted cones from telia germinated in late May. Pistillate cones germinated compared to 56.5 percent were opening on spruce in the vicinity. In nonrusted cones. Neger (1924) described dis- little or no seed. In early July, the pycnial state was evident with eased cones as forming found a yellowing of cone scales and a yellow-col- British Columbia, Sutherland (1981) ored resin flow. Several controlled field and that the effect of cone rust on Picea glauca yield, laboratory inoculation tests indicated that (Moench) Voss seed was to reduce about 48 hours of moist environment was suf- weight, and in some cases, the germinative ficient for infection of cones, although the capacity. number of infected cones was low. Sporadic, relatively localized epidemics Environmental requirements for infection appear to characterize the occurrence of C. of pyrola from urediniospores and aecio- pirolata spruce cone rust in the contiguous spores are probably more frequently met western United States. In contrast, in Alaska, rust than for spruce cones from basidiospores be- Zasada and Gregory (1969) reported the south cause of the differing microenvironment of on white spruce over an extensive area the host organs. Pyrola inhabits moist sites in of the Alaska range in 1960, and again in the shade of dense tree stands, compared to 1968 north of the Alaska range near Fair- the exposed tops of spruce trees. This differ- banks. Ziller (1974) attributes an "A" damage ence would be greater in semiarid regions of rating ("causes great or significant damage") piro- the West, and perhaps less so in the Pacific to inland spruce cone rust (caused by C. Northwest. lata) in Canada. Damage ranging from light Many species of Pyrola and two species of to nearly the entire cone crop destroyed in Moneses are known hosts of C. pirolata (Ar- certain localities is reported regularly in the 264 Great Basin Naturalist Vol. 42, No. 2 various provinces of Canada (Can. Dept. En- in the tops of trees were detected by using viron. 1951-1975). Similar severity of dam- binoculars and, when in doubt, impacting the age occm-s in Norway (Jo

CO 24

Uj ^23

^22

O occasional 20 o o

3 5 7 9 11 7313 15 17 STUDY PLOTS LOCATED AT 1.6km INTERVALS 265 June 1982 Nelson, Krebill: Cone Rust on Spruce plot area, 5 to 10 trees were examined Ephraim records for 1956 through 1977 to through binoculars. The record indicated form a basis .for projecting to Huntington "open" or "closed" when the majority of Canyon the hourly precipitation data avail- cones on trees were in either state. In the py- able at Ephraim. plots rola area, three sites were located within a Effect of spruce cone rust.— On half-kilometer; in each site several hundred with rusted cones, cone-bearing limbs were pruner to Pijrola asarifolia Michx. plants were growing. removed from one tree with a pole nonrusted At each observation, all rust-infected plants obtain 5 to 20 rusted and 5 to 20 were examined for rust development. Obser- cone samples. The cones were placed in pa- in the laboratory for one vations were made for (1) emergence of ure- per bags and dried simulated by tap- dinial-telial pustules, (2) rupture of the per- month. Seed dispersal was cones briskly on a table top; the remain- idia, (3) dispersal of urediniospores, and (4) ping germination of teliospores. ing seeds were removed by breaking cones Associated precipitation.— Weather apart. "Dislodged" and "removed" seeds kept data from an hourly recording station at Eph- from rusted and nonrusted cones were raim, Utah (about 38 km southwest of the separate for each plot. Seeds were prepared tests first washing under site), were examined for precipitation during for germination by potential rust-infection periods in an effort to cold running tap water for 24 hours and then characterize the 1969 epidemic. We deter- stratifying between moistened filter paper in mined spring (May through June) and fall Petri dishes. Stratification was for three (mid-August through mid-October) precipi- months at 1 C. Germination tests were made seeds tation totals and extended periods of rainy by placing up to 100 randomly selected weather with 4-10 hours consecutive accu- per plot on moist filter paper in Petri dishes, mulation of 0.25 cm or more precipitation, and then incubating them under 15-25 C-day and 10 or more hours with 0.13 cm or more 15 C-night regime, using an 8-hour day at precipitation. Some of the 4-10 hour periods 1100 ft-c artificial lighting. had 1-2 hour gaps, and some of the 10 or more hour periods had 1-3 hour gaps in the Results hourly accumulation recording. A non- Huntington recording rain gauge in Huntington Canyon Occurrence and habitat.— across the at Stuart Guard Station, which was within Canyon dissects southeasterly from an ele- the cone rust infection zone, yielded total Wasatch Plateau of central Utah Valley 1300 summer (April through September) precipi- vation of about 3000 m to Castle of the canyon, tation amounts. These were correlated with m lower. In the lower reaches

blast (left) and cloud of cone mst spores at Fig. 2. Cone-bearing tip of Colorado blue spruce tree before shotgun impact of shot (right). — h

266 Great Basin Naturalist Vol. 42, No. 2

the vertical displacement is about 900 m Although cones were abundant on spruce, within horizontal distance of 1-3 a km. The no rust was encountered for the first 13 km in canyon depth and northeasterly exposures the lower portion of the canyon. Cone rust provide typical coniferous habitat of the In- was first encountered on Plot 9 at an eleva- termountain West. In the lower, more arid tion of 22 m (Fig. 1). For the next four plots, portions of the canyon, riparian blue spruce a distance of about 7 km, nearly 100 percent was associated with pinyon-juniper {Pinus of the spruce trees were infected. Thereafter edulis Engelm. -Juniperus scopulorum Sarg.), there was less infection until after Plot 15, at narrow-leaf cottonwood (Populus angusti- 2400 m; then none was observed, although folia James), and scattered ponderosa pine cones were present on trees for another 1.6 {Pinus ponderosa Laws.). As elevation in- km. The percentage of cones infected varied creased, Douglas-fir {Pseudotsuga menziesii from 20-67 percent on the six plots where var. glauca [Beissn.] Franco.) was present, rust was encountered. The shotgun method of and then the association changed primarily to detection proved very effective in revealing white fir (Abies concolor [Gord. and Glend.] presence of rusted cones in cases where in- Lindl.), quaking aspen {Populus tremuloides itial detection with binoculars was question- Michx.), and an occasional Douglas-fir, Eng- able. Because our sampling was made during elmann spruce, and subalpine fir {Abies lasio- a prime time for aeciospore dispersal, large carpa [Hook.] Nutt.) in the upper canyon orange clouds of rust spores issued from the (Fig. 1). Pyrola spp. occurred on moist nor- treetops upon impact of the shot (Fig. 2). The therly exposures in dense spruce-fir stands in uredinial stage of the rust was found on Py- the central to upper portion of the canyon rola secunda and P. asarifolia in a spruce-fir (Fig. 1). Both Pyrola secunda and P. asarifolia stand midway between Plots 10 and 11 near were present, the latter limited to springs the confluence of Left Fork and Huntington and seeps. No pyrola was found within the Creek. Although the canyon was not pinyon-juniper zone. searched extensively, this was the only site

PYROLA RUST FUNGUS SPRUCE OVULATE CONES Incipient sori IS Bud stage ^ Peridia fracturing PF Bud elongation <> Urediniospore release UR Cones open Q Teliospore gemination TG Cones closed # No sporulation NS Pyrola rust site kj 1^5/25 0000000#4 Q IS ^ 6/14 • ••••••OO o o o o o o O PF UR ^ 6/29 o o o o o o o o UR

CO 7/79 OQQ NS ^ I ^ 1 '——'——'——'——'——'— \ \ \ \ — \ \ ——— / 3 5 7 9 11 13 15 17 STUDY PLOT NUMBER (1950-2470 meters elev.)

Fig. 3. Phenology of spruce ovulate cones and Chrysomyxa piwlata on Pijrola spp. in Huntington Canyon. June 1982 Nelson, Krebill: Cone Rust on Spruce 267 where the rust was found on pyrola. The an- highest plot. Pyrola leaves with rust sori had nual checks from 1970 to 1978 of the area dried up, and there was no evidence of telial where the 1969 cone rust epidemic occurred germination. failed to reveal the recurrence of any cone Ovulate cones opened and closed within 20 Sponilation of ure- rust. Cones were present each year in varying days in the lower canyon. amounts. dinial-telial sori lasted for 15-20 days begin- Phenology of spruce cone rust.— By 25 ning in mid-June. In 1969, aeciospore dis- May of the year studied, ovulate cones were persal lasted from late August to at least beginning to open at the lowest elevations of through September. Huntington Canyon, but the strobilate buds Associated precipitation.— A com- rainfall at Eph- were still dormant at 2200 m and above, parison of the yearly summer re- throughout the pyrola zone (Fig. 3). Incipient raim and Huntington canyons (Fig. 4) uredinial-telial sori were visible on the lower vealed a close correlation in annual leaf surfaces of pyrola near Plot 10. By 14 fluctuations (correlation coefficient rainfall June, cones had opened and then closed to [r = 0.82]). The mean annual summer the 2100 m level and were open from 2200 m at Ephraim was 12.4 cm compared to 24.8 similar de- to 2300 m in the lower pyrola zone. A few cm at Huntington Canyon, with uredinial peridia were rupturing with some viations from the mean. During the 6 years spore dispersal in progress. Telia were pres- preceding 1969 (the only year of known ent at the base of sori, but there was no evi- spruce cone rust outbreak), the annual pre- dence of germination. By 29 June, cones had cipitation at the Huntington Canyon site was ex- closed at only slightly higher elevation, and above or near the 22-year mean, with no cones were open throughout the upper can- treme years on the low side (Fig. 4). Follow- yon. Urediniospore dispersal was at a peak; ing 1969, there was a downtrend with some teliospore formation was very sparse, and near-mean years, but most were below the there was no evidence of germination. By 15 mean. The frequency of extended spring and precipitation totals at July, all spruce cones were long closed to the fall rainy periods and

"Regression Correlation Huntington Canyon r = 0.82 (Upper) o o

Eph raim

(Low e r } o o

50-- Spruce Cone Rust 40 Epidemic — 10 20 30 ^ HUNTINGTON CANYON PRECIR cm

22-Year Mean

20--

-"^ '^ 10 A-/ V- -V v \V/

' H \ 56 58 60 62 64 66 68 70 72 74 76 78 ANNUAL SUMMER PRECIPITATION (April -SeptJ 1956-1977

from 1956 through 197 Fig. 4. Comparison of summer rainfall at Ephraim and Huntington canyons 268 Great Basin Naturalist Vol. 42, No. 2

Ephraim follow a similar pattern (Fig. 5). A An evaluation (Table 1) revealed that non- continuity of extended periods of rainy rusted cones yielded an average of 204 ap- weather during spring and fall occurred at parently sound seeds, and rusted cones 188. Ephraim during the 4 years preceding 1969 Seeds likely to disperse readily averaged 113 that did not occur in the following 8 years. for nonmsted and 13 for rusted. A check of Years with similar extended rainy periods fol- overwintered cones (12 nonmsted, 9 rusted) lowing 1969 (1970, 1972, 1973, 1975) were at the Huntington Canyon site the following interrupted by dry seasons. summer showed an average of 18 seeds per Effect of spruce cone rust.— Our obser- cone remaining in nonmsted cones and 86 in vations of Chrysomyxa pirolata cone-rust rusted cones. Viability of seeds extracted symptoms were hmited to mid-September, from cones as determined by germination when aecia were well open. Depressed re- tests is indicated in Table 2. Of seeds dis- sinous areas were common on infected cones, lodged by tapping cones, 71.0 percent germi- usually on one side. The resinous areas ap- nated from nonrusted cones compared to peared to have developed more slowly or in- 48.9 percent from msted cones. Remaining completely, resulting in a slight twisting of seed extracted by breaking cones apart ger- the cone. Cone scales opened prematurely on minated at 53.3 percent for nonmsted and rusted compared to nonmsted cones, and 34.8 percent for rusted.

were often twisted and malformed (Fig. 6). Not all infected cones appeared to be com- Discussion and Conclusions pletely infected; or at least in some parts of the cone, no aecial development occurred, Occurrence, habitat, and phenology.— and cone scales did not open prematurely. In Huntington Canyon located in central These areas were usually on the upper por- Utah's high plateau country, Chrysomyxa tion of cones (Fig. 7). Aecia formed primarily pirolata cone rust of blue spruce was ob- in a zone peripheral to the seeds (Fig. 8). served in a rare epidemic phase. Cone mst

tota I

5 7

I' S5

3 5 S2

' ' ' * ' 65 66 67 68 69 ^ 70 7? ^ 72 ^ 73 ^ 74 ^ 75 ^ 76 ^ 77 YEARS of RECORD 1965-1977

Fig. ,5. Extended hourly rainy periods and spring and fall precipitation at Ephraim, Utah. 269 June 1982 Nelson, Krebill: Cone Rust on Spruce was limited to the spruce-fir zone where Py- tudes. The uredinial-telial sporulation period rola spp. also occurred. Riparian blue spruce lasted for 15-20 days, beginning in mid-June. extended to lower elevations in the pinyon- The 1972 spring season was later than nor- juniper zone where neither cone infection mal, and therefore spore dispersal could oc- nor pyrola were found. Cones were present cur from May through June into early July. on spruce above and below the cone rust Teliospores did not develop fully, and tiiere zone. Studies by Eraser (1911, 1912, 1925) in- was no germination evident. This result was dicate that pistillate cones are susceptible to likely because of the dry spring of 1972 (Figs. infection when cone scales open for pollina- 4 and 5). This also may have speeded the tion; however, the precise period of suscep- death of pyrola leaves upon which sori tibility has not been established. In our study, formed. Fraser (1911), in eastern Canada, and the period of cone opening observed was Rice (1927), in the New England states, ob- closely correlated with the onset of uredinial- served that teliospore formation followed telial sporulation. During the single season urediniospore formation by several weeks. observed, cones at lower elevations opened Although there was poor telial formation in and closed 20 days or less prior to when the our study, it appeared to be almost simulta- rust fungus began sporulation. Phenological neous with uredinial formation as Savile progress in cone development with elevation, (1950) reported, and is typical of the Chryso- (Ziller Peri- it appears, could limit the distance of in- myxa rust fungi in general 1974). fection from a point inoculum source. In ods of rainy weather may be necessary for Norway (Roll-Hansen 1967), the greatest in- abundant teliospore formation. cidence of cone rust was found at higher ele- Even though the aecial-pycnial stage on vations and more northern latitudes; how- spruce is apparently relatively rare in the ever, abundant infection of pyrola occurred southern distribution of this cone rust on the elsewhere. The cause was attributed to unfa- North American Continent, it is significant vorable climatic conditions for infection of that the sexual stage does occur. There is spruce cones in these areas. Chrysomyxa piro- then the chance for genetic recombination

lata cone rust is rare in Canadian Pacific and diversification of the rust fungus without Coast areas compared to other parts of west- dependence on migration of genes from em Canada (Ziller 1974). Climate and telial northern latitudes on Pyrola. hosts did not appear to be limiting since the Associated precipitation.— The close closely related Chrysornyxa monesis Ziller oc- correlation of Huntington Canyon and Eph- curs on Sitka spruce {Picea sitchensis [Bong.] raim summer precipitation fluctuations al- Carr.) cones and Moneses uniflora (L.) A. lowed some confidence in projecting the Gray in coastal areas (Ziller 1974). Our study Ephraim hourly record. Other than elevation, did not include investigation of variation in most differences are probably accounted for duration of favorable moisture during precip- by short-term thunderstorms. Duration of ex- itation periods with elevation. However, evi- tended rain at Huntington Canyon, however, dence suggests that host phenology as well as was likely longer because the total precipi- habitat as influenced by elevation is a factor tation was nearly twice the amount at Eph- in the progressively narrower niches of the raim. Rainy periods of four hours or more in spruce cone-rust fimgus proceeding south- spring and fall were infrequent in the 13- ward across the continent from northern lati- year-record studied (Fig. 5), and therefore the

Table 2. Effect of Chrysomyxa pirolata cone rust on viability of blue spruce seed. Table 1. Effect of Chrysornyxa pirolata cone rust on

blue spruce s< 270 Great Basin Naturalist Vol. 42, No. 2

coincidence of susceptible cones, favorable that are readily dislodged from cones over a moisture, and fungus is inoculum also prob- long period. If these possibilities are true, it ably infrequent. Based on spring rainy peri- would lend support to the importance of fall ods, the chance for favorable moisture for in- rainy periods. Because of the systemic-per- fection during springs of 1970, 1973, and ennial nature of the pyrola rust infection, an 1975 appears just as positive as 1969, al- important factor in the need for consecutive though no cone infection was detected. years of favorable moisture would be the Perhaps, then, a continuity of extended number of years rusted pyrola plants live. spring and fall rains over several years is nec- Effect of spruce cone rust.— Symptoms essary for an epidemic. With dry seasonal in- of C. pirolata cone rust of Colorado blue terruptions, the fungus population could de- spruce observed in this study wer^ somewhat cline to levels that do not permit detectable different from what is reported in the liter- amounts of cone infection even though spring ature for other species of spruce. Depressed rains during some years may be favorable. resinous areas on infected cones appeared to There is, however, no cause-and-effect rela- cause slight twisting of the cones. Portions of tionship established here. There is not infected cones appeared to be rust free, or at enough reliable knowledge about the epide- least there were areas where no aecia miology of C. pirolata cone rust to relate epi- formed. Aecial pustules formed primarily in a demics to weather records in a precise sense. zone peripheral to the seeds, which may be The urediniospores produced on the Pyrola related to the amount of seed damage. The spp. observed in this study adhered rather disease appeared to have only a slight effect strikingly, suggesting that dispersal may be on development of seeds. There was about a primarily by rain splash, thus restricting in- 25 percent reduction in seed germinability tensification of the rust in the uredinial phase with seed from rusted cones. This indicates to the immediate locality. Widespread dis- that cone rust of blue spruce is less damaging persal of the fungus to pyrola would then to seed development than reported for other seem to be more dependent on aeciospores species of spruce. Relatively few seeds could

Fig. 6. Chrysomyxa pirohta rust-diseased Colorado blue spruce cones (three left) and nonrusted cones (three right). Note the twisted, malformed nature of the rusted compared to nonrusted cones. 1 June 1982 Nelson, Kkebill: Cone Rust on Spruce 271 272 Great Basin Naturalist Vol. 42, No. 2

Gaumann, E. 1959. Die Rostpilze Mitteleuropas, Bul- Rice, M. A. 1927. The haustoria of certain rusts and the cher Co., Bern. Beitrage zur Kryptogamenflora relation between host and pathogen. Bull. Torrey der Schweiz, Bd. 12. Bot. Club 54:63-153. GiLBERTSON, R. L., AND J. McHenry. 1969. Checklist 19.35. The cytology of host-parasite relations. Bot. and host index for Arizona rust fungi. Univ. of Rev. 1:327-354. Ariz. Agric. Expt. Sta. Tech. Bull. 186. 40 pp. Roll-Hansen, F. 1967. On diseases and pathogens of Hedgcock, G. G. 1912. Notes on some western Ure- forest trees in Norway, 1960-1965. (Om sykdom- dineae which attack forest trees. Mycologia mer og patogener pa skograernei Norge, 4:141-147. 1960-1965). Saertrykk av Meddelelser fra Det JdRSTAD, I. 1935. Uredinales and Ustilaginales of Norske Skogforseiksvesen. Vollebekk, Norge. Nr. Trcindelag. Det Kyi Norske Videnskabers Selskabs 80, Bind XXI, pp. 174-246. Skrifler NR 38. 90 pp. Savile, D. B. O. 1950. North American species of 1940. Uredinales of northern Norway. Skr. utg. Chrysomyxa. Canadian Jour. Resc. 28:318-330. av. Det. Norske Vindensk.-Akad. i, Oslo. I. Mat.- 1953. Short-season adaptations in the rust fimgi. Naturv. Klasse. 1940. No. 6. 145 pp. Mycologia 45:75-87. KiMMEY, W., AND A. Stevenson. 1957. J. J. A forest dis- Shaw, C. G. 1973. Host fungus index for the Pacific ease survey of Alaska. Plant Dis. Reptr. Suppl. Northwest— I. Hosts;— II. Fungi. Washington Agr- 247. 87-98. pp. ic. Expt. Sta. Bull. 765, 766. Martinez, M. 1963. Las Pinaceas Mexicanas, 3d ed. Sutherland, J. R. 1981. Effects of inland spruce cone Universidad Nacional Autonoma de Mexico, rust, Chrysomyxa pirolata Wint., on seed yield, Mexico City. 401 pp. weight and germination. Canadian For. Serv., Neger, F. W. 1924. Die krankheiten unserer Res. Notes l(2):8-9. Waldbaume und der wichtigsten Gartengeholze. Zasada, J. C, and R. a. Gregory. 1969. Regeneration 2d ed. Ferdinand Enke, Stuttgart. 296 pp. of white spruce with reference to interior Alaska: Nelson, D. L., and R. G. Krebill. 1970. Effect of a literature review. USDA For. Serv. Chrysomyxa pirolata cone rust on dispersal and Res. Pap. PNW-79, viability of Picea pungens seeds. Phytopathology 37 pp. Abstr. 60:1305. ZiLLER, W. G. 1957. Fungi of British Cokmibia depos- ited in Peterson, R. S. 1961. Notes on western rust fungi. I. the herbarium of the Forest Biology Labo- Chrysomyxa. Mycologia 53:427-431. ratory, Victoria, BC, Canada. For. Biol. Div., Sci. Rhoads, a. S., G. G. Hedgcock, E. Bethel, and C. Serv., Agric. Dept., Ottawa, Canada. Hartley. 1918. Host relationships of the North 1974. The tree rusts of western Canada. Canada American rusts other than Gymnosporangiums, Dept. Environ., Canadian For. Serv. Publ. No. which attack conifers. Phytopathology 8:309-352. 1329. 272 pp.