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THE AUTHOR

R. J. HOFF is principal plant geneticist with the Intermoun-
tain Research Station’s Forestry Sciences Laboratory in
Moscow, ID. He received a B.A. degree in biology from
Western Washington State University and a Ph.D in
botany from Washington State University.

RESEARCH SUMMARY

In 1985 a needle cast caused by Lophodermium
baculiferum Mayr severely infected a provenance test and
a progeny test of ponderosa pine located in northern
Idaho. Populations of ponderosa pine from northern Idaho-
northeastern Washington and western Montana differed in
their susceptibility to needle cast. Geographic area ac-
counted for most of the variation among populations;
elevation accounted for very little. The populations in the
north-central portion of the collection area were most
resistant, and these were connected with the more sus-
ceptible southern populations by gentle clines. Family
heritability was 0.60; for individuals it was 0.45.

February 1988

Intermountain Research Station
324 25th Street
Ogden, UT 84401

Susceptibility of Ponderosa Pine
to the Needle Cast Fungus
Lophodermium baculiferum

R. J. Hoff

INTRODUCTION

In 1983, a small amount of needle cast was observed in
a plantation of ponderosa pine (Pinus ponderosa Laws.) in
northern Idaho. In 1984, the level of damaged needles had
increased, and by 1985 the damage had become severe.
The causal organism (Lophodermium baculiferum Mayr)
was identified by Sue Hagle, USDA Forest Service, North-
ern Region, Forest Pest Management, and John M. Staley,
Department of Pathology, Washington State University.

Needle cast fungi can substantially decrease growth and
can also cause mortality, especially if the infection is of
current year’s needles. Scots (Pinus sylvestris L.) pine
stands of central Europe have sustained heavy losses due
to L. pinastri (probably L. seditiosum) (Squillace and
others 1975). In North America the same fungus causes
downgrading and mortality of Scots pine (Merrill and
Kistler 1976; Skilling 1975; Skilling and Nicholls 1971).
Transfer of seed of populations of Scots pine with differ-
ing levels of susceptibility to L. pinastri (probably L.
seditiosum) has compounded this disease problem (Scholz
and Stevens 1982; Squillace and others 1975).

The infection process or infection needs of L. baculi-
ferum are not known; neither is there any knowledge
concerning the genetics of resistance of ponderosa pine to
infection by this needle cast. However, data on and
evidence of resistance have been observed for several
other needle cast fungi. For example, Harvey (1976)
observed uninfected individuals within a provenance test
of ponderosa pine that were heavily infected with
Lophodermella morbida Staley & Bynum. Mitchell and
others (1976) reported resistant trees within a plantation
of Corsican pine (Pinus nigra var. maritinea [Acton]
Melville) infected by Lophodermella sulcigena (Rostr.) v.
Hohn. Hoff (1985) reported that the degree of susceptibil-
ity of lodgepole pine (Pinus contorta Dougl.) infected with
Lophodermella concolor (Dearn.) Darker was closely
associated with elevation of the seed collection; within-
family variability was also fairly high, yielding a family
heritability of 0.738.

Conclusions from the large amount of literature on
resistance of Scots pine to Lophodermium needle casts in-
dicate that provenances differ in their response to infec-
tion (Baumanis and others 1982; Martinsson 1979), and
there is a relatively high within-provenance and within-
family variance for resistance (Martinsson 1979; Squillace
and others 1975).

The purpose of this paper is to document the patterns of
variation of infection caused by L. baculiferum on ponder-
osa pine with respect to geographic area and elevation and
to document family variation.

MATERIALS AND METHODS

The Inland Empire Tree Improvement Cooperative has
established several plantations of ponderosa pine in
northern Idaho and western Montana. Trees in two
plantations—one a provenance test, the other a progeny
test—exhibited severe infection by L. baculiferum in 1985.
Infection appeared uniformly heavy over the entire planta-
tion, but there were scattered individuals throughout both
tests that were not infected. These were often surrounded
by severely infected trees.

The two tests were planted side by side during spring
1974 at the Lone Mountain tree improvement site 25 miles
(40 km) north of Coeur d’ Alene, ID, by the Northern
Region of the Forest Service. The site is flat, with only
slight undulations, at an elevation of 2,488 ft (758 m). The
entire 160-acre (65-ha) site is surrounded by naturally
regenerated ponderosa pine and lodgepole pine with a
lesser mixture of grand fir (Abies grandis [Doug].] Lindl.),
Douglas-fir (Pseudotsuga menziesti var. glauca [Beissn.]
Franco), and western larch (Larix occidentalis Nutt.). This
natural stand is two-layered with the overstory composed
of mature scattered trees (remnants of harvest) and the
lower layer composed of pole-sized trees 20 to 30 ft (6 to
9 m) tall. Most of these natural ponderosa pine were in-
fected with L. baculiferum to some degree.

Provenance Test

The seed came from 92 stands (populations) in north-
eastern Washington, north of the Salmon River in Idaho,
and western Montana (fig. 1). Open-pollinated seed was
collected from five individuals per stand and combined.

The seedlings were grown at a Forest Service nursery
near Coeur d’Alene, ID, in nursery beds for 2 years, then
lifted and planted at the Lone Mountain tree improvement
site in April 1974. The experimental design was a ran-
domized complete block with 10 replications (blocks). Four
progeny of each stand were planted per replication as a
four-tree row plot.

Data were taken by viewing the needles (those produced
in 1983) when the maximum expression of symptoms was
evident, from mid-May to mid-June of 1985. The damage
was evident as straw- to brown-colored needles. It was
assumed that the amount of this damage reflected infec-
tion severity. First, the entire plantation was observed for
20 to 30 minutes to get an idea of the general level and
range of infection. Then observers walked slowly along a
row of trees and placed each tree in one of the following
categories:

118

117

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115 114 ; 112

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Figure 1—Actual levels of infection (percentage) by Lopho-
dermium baculiferum for populations of ponderosa pine.

= no needle tissue infected

= less than 5 percent of needle tissue infected
from 6 to 36 percent of needle tissue infected
= from 37 to 69 percent of needle tissue infected
= more than 70 percent of needle tissue infected.

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Before analysis, the five categories were changed to the
mean proportion of each class, that is: 1 = 0.025; 2 =
0.21; 3 = 0.53; and 4 = 0.85. For computing purposes,

0 = 0.0004.

An analysis of variance was used to determine
significant differences among stands. Multiple regression
analyses were used to relate the degree of infection to
elevation and geographic location of the seed source.
Independent variables included elevation, latitude,
longitude, northwest-southeast coordinates, southwest-
northeast coordinates, and their squares. The northwest-
southeast coordinates equaled latitude x longitude and the
southwest-northeast coordinates equaled (1/latitude) x
longitude. The geographic variables were nested within
two geographic regions: Idaho north of the Salmon River
and Montana west of the Continental Divide (Rehfeldt
1980; Rehfeldt and Wykoff 1981). A stepwise multiple

regression procedure for maximizing R? (SAS 1982) was
completed.

Predicted infection values for geographic areas were
produced using the best fit multiple regression equation
for a constant elevation. Contour lines (isopleths) sepa-
rating statistically equal levels of infection were deter-
mined by using the least significant difference formula
(Steel and Torrie 1960) at a ¢t-value of 0.2. The effect of
elevation was determined by using the regression coeffi-
cients for the elevation factors of the multiple regression
equation to predict infection values for a geographic
intercept.

Progeny Test

Open-pollinated seed from 234 families was collected
from 48 stands in northeastern Washington and Idaho
north of the Salmon River. (Seed from these 48 stands
was also included in the provenance test described above.)

The seedlings were grown as described for the pro-
venance test. The experimental design was a randomized
complete block design but with five replications (blocks).
Four progeny from each family were planted as a four-
tree row plot.

Table 1—Model for analysis of variance and expected mean squares

Source of
variation df! Expected mean squares
Block 4 ow + pore + pfo,
Stand 47 ow + Pore + Pbo*-< +pf bos
Family in stand 188 Ow + Poe + PO nc
Experimental error 892 ow + Po.
Within plot 2,644 Ow

Where: b = 5, S = 48, f = 234, f* = 4.8 harmonic mean of families in
stands; p = 3.01 harmonic mean of individuals within plots.

1Degrees of freedom were reduced by 44 for missing plots.

Table 2—Level of infection (percent) by Lophodermium
baculiferum on 2-year-old foliage of ponderosa pine by

Data were taken as described for the provenance test.
Table 1 shows the analysis of variance and expected mean

squares. Heritability was calculated using the following category
formula: Amount of
For individual foliage damaged Test trees
: =e
h2, = 40" ns Category Mean Range Provenance Progeny
o ote o° 7 ——
¢ is 0 0 0 <1 <1
For family 1 2.5 <5 7.4 4.8
p Ong 2 21.0 6-36 36.3 34.2
h'p = . ; 3 53.0 37-69 34.2 32.8
FEW ee 4 85.0 >70 22.1 28.1
Ons + b + 3
where h?, = heritability based on individuals, h?, =
heritability based on families, 40°p/5 is the estimated addi-
Bye variance for individuals, o*7,s for families, and oy, Table 3—Analysis of variance of infection by Lophodermium
O"E» pb, and b are defined in table 1. baculiferum on ponderosa pine
Relationship of infection and the 1985 height was deter-
mined by regression analysis using the GLM procedure Source of Mean
(SAS 1982). variance df’ square F
Block 9 0.136
RESULTS Stand 81 103** 3.32
Block x stand 783 031

Provenance Test

The level of infection by L. baculiferum varied from
none (1 percent of the trees) to almost complete defoliation
of 1983 needles (22.1 percent of the trees). Table 2 sum-
marizes the amount of infection for both tests. Figure 1
shows the actual percentage of damage for each stand.

Analysis of variance of the levels of infection demon-
strated that differentiation among stands for infection was
highly significant (table 3).

Regression coefficients for the multiple regression equa-
tion that produced the best fit are listed in table 4. These
resulted in an R? of 0.37, a mean square of 0.0386 with 9
degrees of freedom, and an error mean square of 0.0072
with 82 degrees of freedom, resulting in an F' value of 5.4,
significant at 1 percent level of significance.

Predicted values from the multiple regression equation
at the mean elevation of all stands—3,282 ft (1,000 m)—
are shown in figure 2. The center line represents the
average predicted value, and lines depicting +1/2LSD
from this mean at the 0.2 level of significance were drawn
north and south from this line.

1Degrees of freedom were reduced by 36 for missing plots.
**Significant at the 1 percent level of probability.

Table 4—Intercept and regression coefficients
from the best fit multiple regression
equation for infection of ponderosa
pine by Lophodermium baculiferum

Factor b value
Intercept — 247.86612619
Elevation — .00008780
Elevation? .00000001
Northwest .01251327
Southwest zone 1 .00678625
Latitude — 1.44985788
Longitude 4.99039460
Longitude zone 1 .49234995
Longitude* — 02442355
(Southwest zone 1)? 3.30576505

118 117

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X+1/2 LSD @.2

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44 +

115 114 113 112

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Figure 2—Predicted levels of infection (percentage) by Lopho-
dermium baculiferum for populations of ponderosa pine derived
from regression coefficients listed in table 4 at a constant eleva-

tion (mean of all stands, 3,282).

Elevation had no effect, as shown in figure 3. The
plotted values are the actual percentages of infection
plotted against elevation. The line (A) represents the
predicted infection level at the southern geographic point
using 44 percent for the collection area. The line was
derived by using the regression coefficients for the eleva-
tion factors listed in table 4.

Progeny Test

The level of infection varied from none (1 percent of the
trees) to nearly complete defoliation of 1983 needles (28.1
percent of the trees). The levels of infection are summar-
ized in table 2.

Analysis of variance of the levels of infection shows that
the differences among stands and families within stands
were highly significant (table 5). Table 6 lists variance
components. Heritability based on individuals was 0.45; for
families, 0.60.

There was little relationship between the degree of in-
fection and the heights of the trees in 1985 (fig. 4). The
R? for populations was 0.02 and for families, 0.07.

% NEEDLE CAST DAMAGE

1000 2000 3000 4000 5000 6000 FT
(305) (610) (915) (1920) (1524) (1829) (M)
ELEVATION

Figure 3—Actual levels of infection by
Lophodermium baculiferum for populations of
ponderosa pine plotted against elevation. The
line (A) represents the predicted elevation effect
(derived from the multiple regression equation)
for a constant geographic effect, in this case 44
percent infection.

Table 5—Analysis of variance of infection by Lophodermium
baculiferum on stands and families of ponderosa pine

Source of Mean F
variance df square value
Block 4 0.5673
Stand 47 .2233** 3.60
Family in stand 186 .0620* * 2.51
Experimental error 892 .0257
Within plot 2,644 0173

**Significant at the 1 percent level of probability.

Table 6—Variance components for infection of
ponderosa pine by Lophodermium

baculiferum
Source Variance component
Stand 0.0022
Family in stand .0025
Experimental error .0026
Within plot .0173
DISCUSSION

Geographic location of seed source had the most effect
on the pattern of infection due to this needle cast fungus.
The most resistant populations occurred in the north-
central portion of the collection area. Susceptibility was
most pronounced to the south. What seems to be depicted
are gentle north-south clines of susceptibility to L.
baculiferwm.

We have no data concerning the level of infection for
trees in the stands from which seed was collected. Conse-
quently, there is no way of testing whether the variation
pattern among stands is due to natural selection keyed to
the intensity of the disease or just a chance occurrence.
Nonetheless, the pattern of the damage appears to follow
the climate of the Northern Rocky Mountains. The ex-
treme northern portion of Idaho and adjacent Montana is
the wettest part of the area. Usually May and June, and
often July, are foggy and rainy. This general area con-
tained the stands with the least amount of damage, that
is, highest resistance. On the other hand, the stands in the
extreme southern portion of the collection were from
much drier areas, and their progeny had the greatest
amount of damage.

Thus, it seems reasonable to conclude that resistance to
this needle cast fungus is an adaptive trait that has ad-
justed to sites according to the amount of damage caused
by needle cast.

From a practical standpoint, L. baculiferuwm seems to be
only a minor problem for ponderosa pine because it shows
up only when environmental conditions are favorable and
only year-old or older needles are infected. Ponderosa pine
in the Northern Rocky Mountains occurs in uniform pure

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10 12 14 16 18 FT
(305) (366) (427) (488) (549) (CM)
1985 HEIGHT

Figure 4—Lophodermium baculiferum infection plotted
against 1985 height: A, provenance test; B, family
test.

stands only in the drier habitats where needle cast is likely
to occur even less frequently than in the wetter portion of
the area. Planting pure ponderosa pine plantations would
probably lead to needle cast problems in these wet
habitats. This supports the present prevailing forest
practice of regenerating mixed stands.

The relatively high heritabilities for individuals and
families indicate that substantial gains could be made in
breeding for resistance to this needle cast fungus. For
each unit of 7 (selection intensity), 14 percent gain could
be made with family selection and 10 percent for in-
dividual selection. With proper seed source management,
together with selection of good seed trees for natural
regeneration or a fairly large inclusion of resistant trees in
seed collected for artificial regeneration, additional
resistance is probably not needed, especially if pure stands
are not established. However, with a tree improvement
program where the main purpose is to produce faster
growing trees, knowledge concerning the susceptibility of
the selected trees to this needle cast fungus, as well as to
other diseases and insects, would be valuable to the tree
breeder. It may not be necessary to increase resistance,
but it is certain that resistance should not be decreased.

There appears to be only a slight relationship between
relative height and the degree of damage by this needle
cast fungus. In this case, the faster growing trees were
the most resistant.

REFERENCES

Baumanis, I.; Pirags, D.; Spalvins, Z. 1982. Resistance
trials of Scotch pine clones in the Latvian SSR. In:
Resistance to disease and pests in forest trees: Pro-
ceedings of the third international workshop on the
genetics of host-parasite interactions in forestry.
Wageningen, The Netherlands: Center for Agricultural
Publishing and Documentation: 448-449.

Harvey, G. M. 1976. Epiphytology of a needle cast fungus,
Lophodermella morbida, in ponderosa pine plantations in
western Oregon. Forest Science. 22: 223-230.

Hoff, R. J. 1985. Susceptibility of lodgepole pine to the
needle cast fungus Lophodermella concolor. Res. Note
INT-349. Ogden, UT: U.S. Department of Agriculture,
Forest Service, Intermountain Forest and Range Experi-
ment Station. 6 p.

Martinsson, O. 1979. Testing Scots pine for resistance to
Lophodermium needle cast. Studia Forestalia Suecica.
150: 1-63.

Merrill, W.; Kistler, B. R. 1976. Seasonal development and
control of Lophodermium pinastri in Pennsylvania.
Plant Disease. 60: 652-655.

Mitchell, C. P.; Millar, C. S.; Haworth, M. N. 1976. Effect
of the needle-cast fungus Lophodermella sulcigena on
growth of Corsican pine. Forestry. 49: 153-158.

Rehfeldt, G. E. 1980. Cold acclimation in populations of
Pinus contorta from the northern Rocky Mountains.
Botanical Gazette. 141: 458-463.

Rehfeldt, G. E.; Wykoff, W. R. 1981. Periodicity of shoot
elongation among populations of Pinus contorta from
the northern Rocky Mountains. Annals of Botany. 48:
371-377.

SAS Institute, Inc. 1982. SAS user’s guide: statistics.
Cary, NC: SAS Institute. 494 p. ,

Scholz, F.; Stevens, B. R. 1982. Buffering of pH in plant
organs and resistance against fungi. In: Resistance to
diseases and pests in forest trees: Proceedings of the
third international workshop on the genetics of host-
parasite interactions in forestry. Wageningen, The
Netherlands: Center for Agricultural Publishing and
Documentation: 176-186.

Skilling, D. D. 1975. Lophodermium needle cast of pines.
In: Forestry nursery diseases in the United States.
Agric. Handb. 470. Washington, DC: U.S. Department
of Agriculture, Forest Service: 67-68.

Skilling, D. D.; Nicholls, T. H. 1971. Lophodermium
pinastri—a new disease problem in Scotch pine
Christmas tree plantations. Plant Disease. 55:
1116-1117.

Squillace, A. E.; La Bastide, J. G. A.; Van Vredenburch,
C. L. H. 1975. Genetic variation and breeding of Scots
pine in the Netherlands. Forest Science. 41: 341-352.

Steel, R. G. D.; Torrie, J. H. 1960. Principles and pro-
cedures of statistics. New York: McGraw-Hill. 481 p.

Hoff, R. J. 1988. Susceptibility of ponderosa pine to the needle cast fungus Lophoder-
mium baculiferum. Res. Pap. INT-386. Ogden, UT: U.S. Department of Agriculture,
Forest Service, Intermountain Research Station. 6 p.

In 1985 a needle cast caused by Lophodermium baculiferum Mayr severely infected
a provenance test and a progeny test of ponderosa pine located in northern Idaho.
Populations of ponderosa pine from northern Idaho-northeastern Washington and
western Montana differed in their susceptibility to needle cast. Geographic area
accounted for most of the variation among populations; elevation accounted for very
little. The populations in the north-central portion of the collection area were most
resistant, and these were connected with the more susceptible southern populations
by gentle clines. Family heritability was 0.60; for individuals it was 0.45.

KEYWORDS: disease resistance, Pinus ponderosa, heritability

ve US. GOVERNMENT PRINTING OFFICE: 1988—573-039/61,050 REGION NO. 8