Five-needle white pine ecosystems in California, and throughout western North America, are challenged by the interacting threats of an introduced fungal pathogen, Cronartium ribicola
J. C. Fisch. (the cause of white pine blister rust, WPBR), climate-driven outbreaks of mountain pine beetle (MPB) (Dendroctonus ponderosae
Hopkins), climatic warming, historical logging, and a century of fire suppression [1
]. Unique to California is the diversity of five-needle white pine species (subgenus Strobus
] with six species of the nine North American species distributed throughout the State. Many of the five-needle white pine species in California are at or near their southern range limits. In western North America, sugar (Pinus lambertiana
) and western white (P. monticola
Dougl. ex D. Don) pines have been of great economic, as well as ecological, importance. Much is known about the population biology, fire ecology, prevalence and resistance to white pine blister rust, and historical disturbances for sugar pine [4
], but much less is known for western white pine in California.
Western white pine (Pinus monticola
Dougl. ex D. Don) is an important co-dominant species of upper montane forests in California. Over the years this species has been severely affected by C. ribicola
infection, logging, and fire suppression [1
]. In California, western white pine generally occurs in high-elevation forests ranging from 1219 meters on the north coast to 3200 m in the Sierra Nevada. Historically, foresters considered the upper montane to be in the “alpine zone”, ranging in elevation from 150 to 2400 m in the Cascades and North Coast ranges, to over 2700 m in the Sierra Nevada; this zone was generally deemed “too inaccessible to be logged profitably” [14
]. Today, the combined effects of white pine blister rust, logging, fire suppression, and climate-driven outbreaks of mountain pine beetle are affecting populations of western white pine significantly throughout its entire range [2
]. Thus, western white pine forests merit attention today because of their ecosystem values and the consequences of benign neglect.
is a primary management concern in all five-needle white pine ecosystems in western North America. Cronartium ribicola
was introduced into British Columbia around 1910 and arrived in northern California around 1929, spreading southward into the southern Sierra Nevada by 1961 [16
]. While all size classes of western white pine are susceptible to WPBR, individuals most often infected with stem cankers (as opposed to branch cankers) are generally less than 20 cm in diameter at breast height, making stem cankers lethal to small individuals [16
]; this can dramatically alter population structure—by reducing or eliminating small- to intermediate-sized individuals within stands. In a statewide survey of high elevation white pines in California, Maloney [13
] found C. ribicola
infecting 42% (range: 24%–74%) of western white pine trees in the North Coast, 18% (range: 0%–72%) in the Klamath region and 14% (range: 0%–90%) in the Sierra Nevada. Although WPBR can be fatal to all five-needle white pine species, a simply inherited gene in western white pine confers resistance to C. ribicola
]. This gene, designated Cr2
, controls a hypersensitive response in needles that prevents fungal growth [17
] and is analogous to Cr1
, which confers resistance to C. ribicola
in sugar pine [18
are the foundation for naturally occurring resistance to C. ribicola
in sugar pine and western white pine in California.
Fire is an important disturbance agent in mixed conifer forests throughout California, and while fire return intervals in upper montane forests are likely less frequent than in lower-elevation forests, the effects of fire suppression (e.g., stand densification) are evident in these western white pine forest communities [3
]. Studies from upper montane/red fir zone (Abies magnifica
Andr. Murray) and high-elevation forests in California report fire return intervals between 15–76 years (range: five–175 years) [3
]. Given fire suppression policies and estimates of fire return intervals for upper montane and comparable forest types, we assume that many upper montane forests throughout California have missed one–three intervals of fire.
These disturbances (WPBR, MPB, fire exclusion, and logging) and their interactions can have negative population- and genetic-level consequences throughout the range of western white pine in California. At the 1300 km2 scale of the Lake Tahoe Basin, we have taken a landscape approach to understanding the population dynamics, genetic structure, and diversity of western white pine. Our objectives were to determine: (i) the current population structure and trends of western white pine in the Lake Tahoe Basin; (ii) the genetic structure and diversity of extant western white pine populations; and (iii) the landscape-scale frequency of WPBR infection and resistance to WPBR (Cr2) in western white pine. We present our results as a summary of important ecological and genetic factors that should be considered to provide guidance for conservation and management strategies appropriate to a forest tree species at its southern range limit.
We evaluated population and genetic characteristics of western white pine in the Lake Tahoe Basin as they relate to stand conditions, land-use, disease, and insect prevalence. Current forest conditions in our study were comparable to Taylor’s [3
] findings in which he identified shifts in density, basal area, and diameter (d.b.h., diameter at breast height) in pre-Euro-American and contemporary upper montane forests of the Lake Tahoe Basin. Western white pine density was lower in pre-Euro-American upper montane forests than in contemporary forests [3
] and this study (53Taylor-Pre-Euro
, and 82Contemp
); basal area was greater (15.5Taylor-Pre-Euro
, and 13.68Contemp
); and d.b.h. was larger (63.9Taylor-Pre-Euro
, 32.1Taylor -Contemp
, and 33.51Contemp
], see Table 1
). Taylor [3
] attributes these forest structural shifts to historical logging and fire exclusion. We also documented negative population trends for three western white pine populations (Blackwood Canyon, Incline Lake, and Heavenly). These three populations, all with low estimated growth rates (λ), have moderate to high incidence of WPBR and/or MPB and some of the highest levels of mortality for western white pine. By contrast, seven populations appear to be stable (λ ≥ 1.0) because of low-to-moderate disease and insect incidence, and the presence of resistance to WPBR. Negative population trends are likely the consequence of historical land-use and altered disturbance regimes.
The effects of genetic drift can be greater when populations are small, and can act faster to reduce genetic variation. The longevity and dispersal capabilities of conifers, such as western white pine, are typically thought to counteract the effects of localized genetic drift. In the Lake Tahoe Basin, western white pine at Incline Lake had the highest drift parameter value (ci
) and moderate to low population densities and low fecundity. Previously, Maloney et al.
] found a similar pattern of high genetic drift for two sugar pine populations in the Lake Tahoe Basin—likely a consequence of historical logging in the region. Since there is clear evidence of early cut-over stands in the upper montane of the Lake Tahoe Basin, particularly in the vicinity of the Incline Lake population, historical logging may very well explain the high genetic drift within this population. Interpreting ci
values requires caution, however, as any changes in local effective population sizes will affect these estimates, and they are based on a single model for population divergence (see [40
Much of the genetic diversity in forest tree species is found within rather than among populations [48
]. Our landscape study reveals values of genetic diversity for western white pine similar to a rangewide study of western white pine by Kim et al.
]. In earlier genetic studies of western white pine by Rehfeldt et al.
] and Richardson et al.
] found that Sierra Nevada populations had low growth potential but high cold tolerance, which may reflect the environmental conditions in the higher elevations of the Sierra Nevada, with short, dry growing seasons. The authors concluded that western white pine throughout its extensive range is a “generalist” species, with weak patterns of genetic variation among populations from a broad range of elevations [50
]. The limitation to this conclusion, at least for California and the Sierra Nevada, is they had little representation from the Sierra Nevada (populations, n
Mountain pine beetle incidence was a significant predictor of western white pine mortality in upper montane forests of the Lake Tahoe Basin. This insect is known to preferentially attack drought-stressed trees when at low population levels [52
], similar to the endemic levels we observed in the Lake Tahoe Basin. Two other predictors of mortality were cation exchange capacity and δ13
C (water-use efficiency). We found that mortality was higher on soils with larger values of CEC, indicative of non-granitic soil types (e.g., volcanic), and in populations of western white pine with phenotypic means for δ13
C having more negative values, as found on volcanic soil types (the more negative the value the less water-use efficient). In summary, for the Lake Tahoe Basin, western white pine mortality is associated with important biotic agents such as MPB and WPBR and with soil properties, particularly as related to traits such as water-use efficiency.
Moderate to high levels of infection by C. ribicola
were found on western white pine in the Lake Tahoe Basin. The major gene for resistance, Cr2
, was identified in only two populations; but pollen receptors (rare resistance alleles in the pollen cloud that pollinated non-Cr2
parent trees) were found in nine of the 10 populations. Blackwood Canyon was the one population with no evidence of pollen receptors and was the population with the highest levels of WPBR infection in this study (45%) (see Figure 4
frequencies in the Lake Tahoe Basin were nearly three-fold higher than what Kinloch et al.
Upper montane forests provide significant biological and hydrological functions and services, including biodiversity, high carbon storage, and deep and long-lasting snowpacks [55
]. In the context of fire suppression, an introduced pathogen, prolonged droughts, and catastrophic wildfires, conservation and management strategies appear to be warranted for this important species and forest type. As in lower elevation forests, restoration treatments that mitigate fire and drought may be appropriate for some locations in the upper montane [58
]. Similar to Taylor [3
], recommendations to reintroduce fire appear necessary if forest conditions allow, to promote natural western white pine regeneration. Without management action, catastrophic wildfires, infection by WPBR, and elevated MPB activity in this forest type may cause significant ecological (e.g., reduced population sizes), environmental (e.g., greater fuels, carbon loss), and genetic losses, including loss of naturally occurring resistance to WPBR, already present in western white pine. Rangewide seed collections and screening for Cr2
are needed for western white pine in California. Such efforts will be needed to enhance collections of rust-resistant western white pine as well as provide a local and diverse seed source for post-wildfire restoration and post-MPB outbreak recovery.