Severity of Endocronartiumharknessii in Two Provenance Stands of Pinusponderosa in Michigan

C. S. THOMAS, Graduate Research Assistant, Department of Botany and Plant Pathology, J. H. HART, Professor, Departments of Botany and Plant Pathology and Forestry, and C. E. CRESS, Professor, Department of Crop and Soil Sciences and Agricultural Experiment Station Statistician, Michigan State University, East Lansing 48824 of the 10-yr growth and survival of trees ABSTRACT from these seed sources was reported by Thomas, C. S., Hart, J. H., and Cress, C. E. 1984. Severity of Endocronartiumharknessii in two Read (16). provenance stands of Pinusponderosain Michigan. Plant Disease 68:681-683. The trees were used to establish I provenance stands of P. ponderosa vars. Transplants (2-1 stock) representing 73 seed sources of Pinusponderosawere planted at two sites 74 ponderosa and scopulorum at two sites km apart in 1968 in southwestern Michigan. Before being planted in Michigan, 0.5% or less of the 74 km apart in southwestern Michigan. stock became infected with Endocronartiumharknessii at a Nebraska nursery. In 1982, disease One stand was planted at Kellogg Forest, severity (number of galls per tree) was recorded for each tree and mapped. P. ponderosa var. Au scopulorum was more severely diseased than P.ponderosa var. ponderosa (P = 0.05). Within P. gusta, MI (spacing of 2.44 X 2.44 i), ponderosavar. scopulorum, two southern ecotypes, Colorado Plains and Southern Rockies, were on rolling glacial moraine with 2-30% more severely diseased than others (P = 0.001). Resistant and susceptible seed sources occurred slopes. The stand was planted in Oshtemo within ecotypes of both varieties. sandy loam and loamy sand. The other stand was planted at Russ Forest, Volinia, MI (spacing of 1.83 X 1.83 m), in Western gall rust (pine-pine rust), ponderosa pine were planted at the U.S. a Brady sandy loam on flat terrain. All caused by Endocronartiumharknessii (J. Forest Service Bessey Nursery, in Halsey, transplants were planted in six-tree, east- P. Moore) Y. Hiratsuka, is an important NE. While at the nursery, 0.5% or less of west plots in five randomized complete disease of ponderosa pine (Pinus the stock became infected with E. blocks at each site. When available, one ponderosa Dougl. ex Laws.). The rust harknessii from a nearby forest and from or two replacement trees were planted causes severe damage on ponderosa pine a windbreak (10,13). Transplants (2-1 between trees five and six of the grown on Christmas tree plantations, stock) of 73 seed sources representing corresponding provenance group. windbreaks, experimental plots, forests, eight ecotypes as defined by Read (15) In 1982, rust severity was recorded for and nurseries (4,12,13,20). (Fig. 1) were shipped to Michigan for each of 4,389 trees, using a disease scale of Previous studies have reported genetic planting in early April 1968. A summary 0-4, where 0 = no infection, 1= 1-5 galls, resistance of pines to rust fungi (11,14). Ponderosa pine shows differences - .- t between varieties (P. ponderosa var. 866 i Ii Ct M ponderosa and P. ponderosa var. -- -- Central Montnd scopulorum Engelm.) in susceptibility to several pests (2,6,8,18). However, 81 High differences in susceptibility between N r5 1 8.--17 Ph/118, - -. ~ 18l~18 I 815 8 1 PFin varieties or ecotypes to E. harknessiihave . 820 7 not been documented for ponderosa pine. Plateau' 81 8 4827 Individual Scots pine (P. sylvestris L.) 865 825 828 M3 - - (4,9) and ponderosa pine (12) have shown :"-- - Black resistance to E. harknessii,but differences Bitterroots1 <,, Hills in susceptibility have not been reported at \836 W- the varietal level. 8 75T The objective of this study was to t-"8721 Et•cs, determine if variation in susceptibility to t eta •'Elevation F. harknessii exists among seedlings of I oke-•. . '• ponderosa pine from different geographic I . R rkS- -_~ sources. A preliminary report of this (• California / / .. . . . work has been published (19). "•tI (•"-Pan

MATERIALS AND METHODS • ! In 1965, seeds from 80 geographic L _• sources throughout the natural range of .

Research supported in part by Mclntire-Stennis \ • Forestry Research Act PL-87-788. ¶ 6 Southern 1

Michigan Agricultural Experiment Station Journal • '-".. -.. Article 11124.t 76 I Accepted for publication 23 April 1984 (submitted --- ' (| for electronic processing). (- ,•

The pu blication costs of this article were defrayed in part by page charge payment. This article must therefore be Fig. 1. Locations of 73 ponderosa pine provenance seed sources. Pinus ponderosa var. ponderosa hereby marked "advertisement" in accordance with 18 includes California, North Plateau, Bitterroots, and Transition ecotypes. P. ponderosa var. U.S.C. § 1734 solely to indicate this fact. scopulorum includes Central Montana, High Plains and Black Hills, East Low Elevation, Central © 1984 The American Phytopathological Society Rockies, Colorado Plains, and Southern Rockies ecotypes (15).

Plant Disease/August 1984 681 2 = 6-25 galls, 3 = 26-50 galls, and 4 = restricted initially to the east side of the bility of ponderosa pine ecotypes within a >50 galls. Gall rating, dead trees, and stand by a north-south ridge. A few galls variety. Differences in susceptibility to topography were mapped for each stand. were found on trees on the west side of the western gall rust among individual trees To verify the identity of the rust, stand but were the result of more recent have been observed in ponderosa pine peridermoid teliospores were collected in infections because they were located only (12) and in Scots pine (4). In both cases, 00 gelatin capsules from one gall on each in the upper portion of the crown. Gall heavily infected trees were adjacent to of 30 trees on 20 May 1982 at the Kellogg rating was not closely associated with a trees of the same species with no stand and from one gall on each of three tree's distance from the nearest low area infection. Hutchinson (9) detected 2 trees at the Russ Forest stand on 21 May at Kellogg Forest (R = 0.03). The differences among individual Scots pine 1983. The fungus was identified as E. western gall rust fungus has not spread to trees in susceptibility to E. harknessii in harknessii on the basis of germ tube other pine plantations from these two inoculation tests. morphology as described by Anderson stands. Ponderosa pine has shown varietal and and French (1). individual tree differences in susceptibility DISCUSSION to other pests. Callahan (6) reported RESULTS This study is the first to document varietal differences in susceptibility of Because infection within each stand differences in susceptibility to E. ponderosa pine to the pine reproduction was spotty, we chose to average tetfive harknessii between P. ponderosa vars. weevil (Cylindrocopturus eatoni Buch.). plots (six trees each) within each site to ponderosaand scopulorum. It is also the P. ponderosa var. ponderosa was obtain a more stable gall rating. Analysis first to document differences in suscepti- moderately susceptible; however, P. of variance was performed with the experiment (site) as the blocking variable in a randomized block design. Mean gall Table 1. Severity of western gall rust caused by Endocronartiumharknessii in 73 Pinusponderosa ratings for provenance groups showed provenance groups representing eight ecotypes planted in Michigan similar rankings at each forest stand. Ecotype' Provenance groupx Variances at each stand were similar. The mean gall rating at Kellogg Forest (0.56) Mean Identification Percent Gall was significantly higher than that at Russ Name gall ratingw numberY infection ratingw Forest (0.36, P = 0.001). The mean gall North Plateau 0.33 az 866 9.5 0.10 rating of P. ponderosa var. scopulorum 865 34.0 0.47 (0.48) was significantly higher than that 867 29.0 0.42 of P. ponderosa var. ponderosa (0.35, Bitterroots and LSD . = 0.12). Mean gall ratings for Transition 0.36 a 754 20.0 0.23 0 05 818 33.535.5 0.460.40 eight ecotypes indicated more disease in 819 820 30.5 0.39 southern ecotypes (P = 0.05) (Table 1). Resistant and susceptible provenance 817 27.5 0.32 groups occurred within the same ecotype Central Montana 0.39 a 814 21.5 0.18 of either variety (the higher the 815 16.0 0.19 percentage of infection of each provenance 813 25.5 0.27 group, the higher the gall rating [r = 0.91 ]) 829 26.0 0.35 (Table 1). Provenance groups were 812 35.0 0.55 considered very resistant if no tree had 821 31.0 0.48 Low more than five galls when at least two East adjacent trees in different provenance Elevation 0.36 a 855 18.0 0.29 groups had more than five infections. 757 22.5 0.30 Four provenance groups were consistently 856 15.5 0.27 very resistant (828, 866, 760, and 827). 720 38.0 0.57 Mortality was low (2.5-9%) for all of High Plains and these except 760 from Colorado (30.5%), Black Hills 0.42 a 828 3.0 0.03 which was the southernmost source. 827 11.5 0.13 Michigan's climate may have been too 722 15.5 0.21 cold and moist for trees from this seed 825 14.0 0.17 source because they died of winter injury. 835853 16.519.0 0.250.21 Four provenance groups were consistently 832 16.0 0.18 very susceptible (849, 762, 850, and 863). 840 27.0 0.30 These eight sources represent a conserva- 851 22.0 0.38 tive estimate of very resistant and very 852 30.0 0.39 susceptible provenance groups. For 723 25.0 0.40 instance, although 764 had a low mean 811 20.5 0.33 gall rating (0.11), two trees from this seed 838 15.0 0.33 source had a gall rating of 2. The above8227504 833 44.0 0.49 definition of highly resistant provenance 824 26.0 0.32 groups eliminates groups such as 764 as 701 50.5 0.78 well as groups that had low mean gall 839 26.0 0.38 ratings caused by escape from inoculum. 704 13.5 0.20 Infection centers were identified when 822 26.0 0.43 80% of the trees had ratings of 3 or higher. 836 40.5 0.81 Infection centers appeared to be 703 33.5 0.54 distributed throughout the stand at Russ 727 40.5 0.75 Forest. At Kellogg Forest, infection 850 48.5 0.88 37.5 0.75 centers occurred on the east side of the 846702 43.5 0.80 stand surrounding four initially infected 834 31.5 0.63 trees (as indicated by basal galls). Spread (continued on next page) of the rust appeared to have been 682 Plant Disease/Vol. 68 No. 8 Table 1. (continuedfrom precedingpage) Plains and Central Rockies ecotypes, and Ecotypev Provenance groupx G.least Hawksworth, in the Southern personal Rockies communica- ecotype (F. Mean Identification Percent Gall tion). If E. harknessii is less adapted to Name gall ratingw numberY infection ratingw the more southern climates or if it spread Central Rockies 0.46 ab 760 10.0 0.10 to those areas last, there would be less 763 27.5 0.32 selection pressure for resistance to 764 11.0 0.11 western gall rust. This may be the case 857 19.0 0.32 because the southern ecotypes have the 831 28.5 0.40 highest mean gall ratings in Michigan. 845 39.0 0.51 80830 230.523.5 0.35 ACKNOWLEDGMENTS 761 30.5 0.40 We thank W. Lammien and G. Kowalewski for 848 35.5 0.52 technical assistance. 849 64.0 0.94 844 847 42.5 0.80 44.0 0.80 LITERATURE CITED b847 44.0 0.8 1. Anderson, G. W., and French, D. W. 1965. Colorado Plains 0.67 b 861 25.5 0.43 Differentiation of Cronartium quercuum and 759 37.5 0.64 Cronartium coleosporoides on the basis of 858 32.0 0.55 aeciospore germ tubes. Phytopathology 860 40.0 0.55 55:171-173. 859 48.0 0.72 2. Austin, L., Yuill, J. S., and Brecheen, K. G. 1945. 758 39.0 0.74 Use of shoot characters in selecting ponderosa 762 50.0 0.92 pines resistant to resin midge. Ecology 724 35.5 0.84 26:288-296. Southern Rockies 0.65 b 869 19.0 S.69 19.0 0.30 3. Axelrod,forests, California,D. I. 1976. and HistoryNevada. ofUniv. coniferous Calif. 767 49.0 0.69 Publ. Bot. 62 pp. 765 42.5 0.67 4. Baxter, D. V. 1967. Disease in Forest 862 38.5 0.68 Plantations: Thief of Time. Cranbrook Inst. Sci. 864 46.0 0.82 Bull. 51. 251 pp. 766 18.5 0.51 5. Bowman, I. 1911. Columbia Plateaus and Blue 863 45.0 0.88 Mountains: Vegetation. Pages 206-207 in: Forest LSD 0.05 23.4 0.43 759Physiography. pp. John Wiley & Sons, New York. Pinusponderosavar-ponderosa includes North Plateau and Bitterroots and Transition ecotypes. 6. Callaham, R. Z. 1960. Observations on pine P. ponderosa var. scopulorum includes Central Montana, East Low Elevation, High Plains susceptibility to weevils. Pac. Southwest For. and Black Hills, Central Rockies, Colorado Plains, and Southern Rockies ecotypes. Range Exp. Stn. Tech. Pap. 51. U.S. For. Serv. wGall ratings were based on number of galls per tree: 0 = none, 1= 1-5, 2 = 6-25, 3 = 26-50, and 4 12 pp. >50. 7. Cross, A. T., and Taggart, R. E. 1982. Causes of 'Values reported as a mean of two forest stands. Each forest stand was planted in five randomized short-term sequential changes in fossil plant complete blocks of six-tree, east-west plots. Two extra trees were planted when available between assemblages: Some considerations based on a trees five and six. miocene flora of the northwest United States. Identification numbers are those used by Read (15). Detailed forest stand information about seed .Ann. Mo. Bot. Gard. 69:676-734. 8. Hawksworth, F. G., and Wiens, D. 1972. Biology sources is available for gall rating, mortality, and percentage of infection from the first author, and Classification of Dwarf Mistletoes zNumbers followed by the same letter are not significantly different (P = 0.05) according to (Arceuthobium). U.S. Dep. Agric. Agric. Duncan's new multiple range test. Handb. 41. 234 pp. 9. Hutchinson, W. G. 1935. Resistance of Pinus sylvestris to a gall-forming Peridermium. ponderosavars. scopulorum and arizonica Ponderosa pine populations became Phytopathology 25:819-843. (Engelm.) Shaw were highly susceptible. discontinuous and isolated several times 10. Johnson, D. W. 1979. Examination of Bessey Ponderosa pines with resinous new in the recent geological past (3). During Nursery stock for western gall rust. Biol. Eval. shoots were highly susceptible to resin the Tertiary period, large-scale volcanism R2-79-6. U.S. For. Serv. Rocky Mt. Reg., Lakewood, CO. 3 pp. midge (Retindiplosis sp.), whereas trees was followed by arid periods (7). During 11. Kinloch, B. B., Jr. 1972. Genetic variation in with glaucous or glabrous new shoots the Pleistocene period, alpine glaciation resistance to Cronartium and Peridermium rusts were highly resistant (2). Glabrous shoots disrupted the continuous mixed mesic in hard pines. Pages 445-462. in: Biology of Rust were common for southern ecotypes of forests. As the glaciers advanced, the high Resistance in Forest Trees. U.S. Dep. Agric. Misc. Publ. 1221. 681 pp. ponderosa pine (15). Arceuthobium altitudes became colder and the low 12. McNabb, H. S., Jr., and Shurtleff, M. C., Jr. vaginatum (Willdenow) Presl. occurs on altitudes became dryer. Occasionally, as 1957. Notes on stem rusts of hard pines in Iowa. P. ponderosa vars. arizonica and the cold and dry regions merged, pine was Proc. Ia. Acad. Sci. 64:187-188. scoulrubt otonP.podeos vr. eliminated from some slopes (3,5). 13. Peterson, G.WX.1973. Dispersal of aeciospores of scpuormn . onersava.Peridermium utno harknessii in central Nebraska. ponderosa (8). This, however, is due to Microcyclic rusts could have evolved Phytopathology 63:170-172. the limited geographic extent of the from macrocyclic rusts caused by the 14. Peterson, R. S., and Jewell, F. F. 1968. Status of mistletoe because inoculations show that selection pressure of short summers (17). American stem rusts of pine. Annu. Rev. P. pndeosavari suceptble poneroa Croartumqercum Ber.) Myab ex 15.Phytopathol. 6:23-40. P. pndeosavarponerosissuseptble Cronrtim qercum Berk) Myab ex 15.Read, R. A. 1980. Genetic variation in seedling to this mistletoe (F. G. Hawksworth, Shirai f. sp. banksianae may have been progeny of ponderosa pine provenances. For. personal communication). Rabbits and divided by the advancing glaciers and in Sci. Monogr. 23. 59 pp. porcupines preferred to feed on P. the west evolved into E. harknessii. P. 16. Read, R. A. 1983. Ten-year performance of ponderosa var. ponderosa rather than P. ponderosa var. ponderosa was diverging ponderosa pine provenances in the Great Plains of North America. U.S. For. Serv. Res. Pap. ponderosa var. scopulorum, but the in this region as well. Because P. RM-250. 17 pp. opposite was true for deer (18). ponderosa var. ponderosa is the least 17. Savile, D. B. 0. 1971. Coevolution of the rust The bases of resistance are unknown. susceptible to E. harknessii, it could be fungi and their hosts. Q. Rev. Biol. 46:211-218. Thesouherectyes nitateshot hatthefunus ascoevolved longer with 18. Squillace, A. E., and Silen, R. R. 1962. Racial The outern cotpesinitateshootht te fugushasariation in ponderosa pine. For. Sci. Monogr. elongation much later than other this variety than with other varieties of 2. 27 pp. ecotypes (15). Because spores infect new ponderosa pine. 19. Thomas, C. S., Hart, J. H., and Cress, C. E. 1983. shoots as they elongate, the southern In the western United States, frequency Severity of Endocronartium harknessii on Pinus ecotpesmaybet moexposd o nauralinfctin i gretes inthe 20.ponderosa. (Abstr.) Phytopathology 73:838. ecoype ma beexpsedtoore of atual nfetio isgretes inthe 20.Walla, J. A., and Stack, R.WX.1979. Western gall inoculum or to conditions more suitable- Black Hills and East Low Elevation rust in North Dakota. Plant Dis. Rep. for efficacy of inoculum. ecotypes, much less in the Colorado 63:432-433.

Plant Disease/August 1984 683