Invasive Pathogen Threatens Bird-Pine Mutualism: Implications for Sustaining a High-Elevation Ecosystem

Human-caused disruptions to seed-dispersal mutualisms increase the extinction risk for both plant and animal species. Large-seeded plants can be particularly vulnerable due to highly specialized dispersal systems and no compensatory regeneration mechanisms. Whitebark pine ( Pinus albicaulis), a keystone subalpine species, obligately depends upon the Clark\u27s Nutcracker (Nucifraga columbiana) for dispersal of its large, wingless seeds. Clark\u27s Nutcracker, a facultative mutualist with whitebark pine, is sensitive to rates of energy gain, and emigrates from subalpine forests during periods of cone shortages. The invasive fungal pathogen Cronartium ribicola, which causes white pine blister rust, reduces whitebark pine cone production by killing cone-bearing branches and trees. Mortality from blister rust reaches 90% or higher in some whitebark pine forests in the Northern Rocky Mountains, USA, and the rust now occurs nearly rangewide in whitebark pine. Our objectives were to identify the minimum level of cone production necessary to elicit seed dispersal by nutcrackers and to determine how cone production is influenced by forest structure and health. We quantified forest conditions and ecological interactions between nutcrackers and whitebark pine in three Rocky Mountain ecosystems that differ in levels of rust infection and mortality. Both the frequency of nutcracker occurrence and probability of seed dispersal were strongly related to annual whitebark pine cone production, which had a positive linear association with live whitebark pine basal area, and negative linear association with whitebark pine tree mortality and rust infection. From our data, we estimated that a threshold level of similar to 1000 cones/ha is needed for a high likelihood of seed dispersal by nutcrackers ( probability \u3e= 0.7), and that this level of cone production can be met by forests with live whitebark pine basal area \u3e5.0 m(2)/ha. The risk of mutualism disruption is greatest in northernmost Montana ( USA), where three-year mean cone production and live basal area fell below predicted threshold levels. There, nutcracker occurrence, seed dispersal, and whitebark pine regeneration were the lowest of the three ecosystems. Managers can use these threshold values to differentiate between restoration sites requiring planting of rust-resistant seedlings and sites where nutcracker seed dispersal can be expected

Whitebark Pine Stand Condition, Tree Abundance, and Cone Production as Predictors of Visitation by Clark's Nutcracker

Accurately quantifying key interactions between species is important for developing effective recovery strategies for threatened and endangered species. Whitebark pine (Pinus albicaulis), a candidate species for listing under the Endangered Species Act, depends on Clark's nutcracker (Nucifraga columbiana) for seed dispersal. As whitebark pine succumbs to exotic disease and mountain pine beetles (Dendroctonus ponderosae), cone production declines, and nutcrackers visit stands less frequently, reducing the probability of seed dispersal.We quantified whitebark pine forest structure, health metrics, and the frequency of nutcracker occurrence in national parks within the Northern and Central Rocky Mountains in 2008 and 2009. Forest health characteristics varied between the two regions, with the northern region in overall poorer health. Using these data, we show that a previously published model consistently under-predicts the proportion of survey hours resulting in nutcracker observations at all cone density levels. We present a new statistical model of the relationship between whitebark pine cone production and the probability of Clark's nutcracker occurrence based on combining data from this study and the previous study.Our model clarified earlier findings and suggested a lower cone production threshold value for predicting likely visitation by nutcrackers: Although nutcrackers do visit whitebark pine stands with few cones, the probability of visitation increases with increased cone production. We use information theoretics to show that beta regression is a more appropriate statistical framework for modeling the relationship between cone density and proportion of survey time resulting in nutcracker observations. We illustrate how resource managers may apply this model in the process of prioritizing areas for whitebark pine restoration

Loss of foundation species revisited: conceptual framework with lessons learned from eastern hemlock and whitebark pine

Ecologists and conservation biologists often prioritize the study of species that are declining, threatened, or endangered over species that are abundant and ecologically important, such as foundation species (FS ). Because entire ecosystems and their biodiversity depend on FS , we argue that they have high conservation priority. A citation analysis reveals that FS are studied, but often are characterized ambiguously. More effort is needed to identify FS before they, and the ecosystems they define, are at risk of decline or loss. We suggest a new conceptual framework that includes: informed identification of FS in ecosystems; documentation of ecosystem services provided by FS ; a long‐term monitoring strategy to detect threats to FS within specified ecosystems; and, if threats are identified, a comprehensive conservation and adaptive management strategy for FS . We use two widely distributed, rapidly declining North American foundation tree species (Tsuga canadensis [eastern hemlock] and Pinus albicaulis [whitebark pine]) to illustrate this framework. These species exemplify the importance of identifying FS early and conserving or restoring them when they are threatened

Rapid Microsatellite Identification from Illumina Paired-End Genomic Sequencing in Two Birds and a Snake

Identification of microsatellites, or simple sequence repeats (SSRs), can be a time-consuming and costly investment requiring enrichment, cloning, and sequencing of candidate loci. Recently, however, high throughput sequencing (with or without prior enrichment for specific SSR loci) has been utilized to identify SSR loci. The direct “Seq-to-SSR” approach has an advantage over enrichment-based strategies in that it does not require a priori selection of particular motifs, or prior knowledge of genomic SSR content. It has been more expensive per SSR locus recovered, however, particularly for genomes with few SSR loci, such as bird genomes. The longer but relatively more expensive 454 reads have been preferred over less expensive Illumina reads. Here, we use Illumina paired-end sequence data to identify potentially amplifiable SSR loci (PALs) from a snake (the Burmese python, Python molurus bivittatus), and directly compare these results to those from 454 data. We also compare the python results to results from Illumina sequencing of two bird genomes (Gunnison Sage-grouse, Centrocercus minimus, and Clark's Nutcracker, Nucifraga columbiana), which have considerably fewer SSRs than the python. We show that direct Illumina Seq-to-SSR can identify and characterize thousands of potentially amplifiable SSR loci for as little as $10 per sample – a fraction of the cost of 454 sequencing. Given that Illumina Seq-to-SSR is effective, inexpensive, and reliable even for species such as birds that have few SSR loci, it seems that there are now few situations for which prior hybridization is justifiable

A Possible Breeding Record for Clark\u27s Nutcracker

In the late morning of 17 May, 1987, my husband and I drove into Sowbelly Canyon, which is in the Pine Ridge area in northwestern Nebraska. In the canyon, about 3.3 miles from Harrison, we were in a ponderosa pine (Pinus ponderosa)–riparian community ecotone, and were startled to hear and see a flock of Clark\u27s Nutcrackers (Nucifraga columbiana). About 30 adults were perched on branches or flying about the tops of the ponderosa pines. From the abundance of cones, it was clear that there had been a good seed crop the previous fall. Some of the birds were perched on or near cones, sorting through the scales and removing seeds. I saw similar foraging behavior by Clark\u27s Nutcrackers Jeffrey pines (Pinus jeffreyi) during winter and spring in the eastern Sierra Nevada, California (Tomback 1978)

Notes on Cones and Vertebrate-mediated Seed Dispersal of Pinus albicaulis (Pinaceae)

Volume: 28Start Page: 91End Page: 9

POST-FIRE REGENERATION OF KRUMMHOLZ WHITEBARK PINE: A CONSEQUENCE OF NUTCRACKER SEED CACHING

Volume: 33Start Page: 100End Page: 11