Predicting Present and Future Suitable Climate Spaces (Potential Distributions) for an Armillaria Root Disease Pathogen (Armillaria solidipes) and Its Host, Douglas-fir (Pseudotsuga menziesii), Under Changing Climates

Climate change and associated disturbances are expected to exacerbate forest root diseases because of altered distributions of existing and emerging forest pathogens and predisposition of trees due to climatic maladaptation and other disturbances. Predictions of suitable climate space (potential geographic distribution) for forest pathogens and host trees under contemporary and future climate scenarios will guide the selection of appropriate management practices by forest managers to minimize adverse impacts of forest disease within forest ecosystems. A native pathogen (Armillaria solidipes) that causes Armillaria root disease of conifers in North America is used to demonstrate bioclimatic models (maps) that predict suitable climate space for both pathogen and a primary host (Pseudotsuga menziesii, Douglas-fir) under contemporary and future climate scenarios. Armillaria root disease caused by A. solidipes is a primary cause of lost productivity and reduced carbon sequestration in coniferous forests of North America, and its impact is expected to increase under climate change due to tree maladaptation. Contemporary prediction models of suitable climate space were produced using Maximum Entropy algorithms that integrate climatic data with 382 georeferenced occurrence locations for DNA sequence-confirmed A. solidipes. A similar approach was used for visually identified P. menziesii from 11,826 georeferenced locations to predict its climatic requirements. From the contemporary models, data were extrapolated through future climate scenarios to forecast changes in geographic areas where native A. solidipes and P. menziesii will be climatically adapted. Armillaria root disease is expected to increase in geographic areas where predictions suggest A. solidipes is well adapted and P. menziesii is maladapted within its current range. By predicting areas at risk for Armillaria root disease, forest managers can deploy suitable strategies to reduce damage from the disease.

First Report of Armillaria Root Disease Pathogen, Armillaria gallica, on Rhododendron and Quercus rubra in Georgia, USA

Armillaria root and butt diseases, which are a global issue, can be influenced by changing environmental conditions. Armillaria gallica is a well-known pathogen of diverse trees worldwide (Brazee and Wick 2009). Besides A. gallica causing root rot of Hemerocallis sp. and Cornus sp. in South Carolina (Schnabel et al. 2005), little is reported on the distribution and host range of A. gallica in the southeastern USA. In July 2017, three Armillaria isolates were obtained from two naturally occurring hosts in Georgia, USA and cultured on malt extract medium (3% malt extract, 3% dextrose, 1% peptone, and 1.5% agar). One isolate (GA3) was obtained in Unicoi State Park near Helen, Georgia (Lat. 34.712275, Long. -83.727765, elev. 498 m) from the basal portion of Rhododendron sp. with extensive root/butt decay, but no crown symptoms were evident (Supplementary Figure 1). GA4 and GA5 (Lat. 33.902433, Long. -83.382453, elev. 215 m) were isolated from wind-felled Quercus rubra (red oak) with root disease at the State Botanical Gardens in Athens, Georgia. GA4 was associated with a large root ball (ca. 4-m diameter) (Supplementary Figure 2), and GA5 was obtained from a mature tree with infected roots, with characteristic spongy rot of Armillaria root disease. Crown symptoms could not be evaluated because the crowns had been removed before the collections. Several other oaks with Armillaria root disease were noted throughout the State Botanical Gardens. Pairing tests reduced these three isolates (whiteish mycelia with a dark, brownish crust and rhizomorphs), to two genets with GA4 = GA5. Both genets (GA3 and GA4) were identified as A. gallica using translation elongation factor 1α (tef1) sequences (Genbank Nos. MT761697 and MT761698, respectively) that showed ≥ 97% identity (≥ 98% coverage) with A. gallica sequences (KF156772, KF156775). Also, nine replications of somatic pairing tests showed 33 – 67% compatibility with A. gallica (occurs in southeastern USA), compared with 0 – 22% for A. mexicana, A. mellea (occurs in southeastern USA), A. solidipes, and Desarmillaria tabescens (occurs in southeastern USA). To our knowledge, this note represents the first report of A. gallica on Rhododendron and Q. rubra in Georgia, USA, which has experienced severe drought in recent decades (e.g., Park Williams et al. 2017) that could predispose trees to Armillaria infection (e.g., Wargo 1996). Quercus rubra was previously reported as a host of A. gallica in Arkansas (Kelley et al. 2009) and Massachusetts (Brazee and Wick 2009), USA. In Missouri, USA, A. gallica has been reported as a weak pathogen with potential biological control against A. mellea (Bruhn et al. 2000). Other reports from several regions on various hosts suggest pathogenicity of A. gallica is associated with changing climate (Nelson et al. 2013, Kim et al. 2017, Kubiak et al. 2017). Wide genetic variation and/or cryptic speciation within A. gallica may account for differences in ecological behavior (Klopfenstein et al. 2017), but this is difficult to evaluate because Armillaria pathogenicity tests cannot be used on most forest tree seedlings. This study suggests that A. gallica is more widespread than previously known and its adverse impacts on woody plants may intensify over time, depending on the environmental conditions. Further studies are needed to determine environmental influences on A. gallica, the full distribution of A. gallica, and its effects in forests of the southeastern USA.

Armillaria altimontana Is Associated with Healthy Western White Pine (Pinus monticola): Potential in Situ Biological Control of the Armillaria Root Disease Pathogen, A. solidipes

Research Highlights: Two genets of Armillaria altimontana Brazee, B. Ortiz, Banik, and D.L. Lindner and five genets of Armillaria solidipes Peck (as A. ostoyae [Romagnesi] Herink) were identified and spatially mapped within a 16-year-old western white pine (Pinus monticola Doug.) plantation, which demonstrated distinct spatial distribution and interspecific associations. Background and Objectives: A. solidipes and A. altimontana frequently co-occur within inland western regions of the contiguous USA. While A. solidipes is well-known as a virulent primary pathogen that causes root disease on diverse conifers, little has been documented on the impact of A. altimontana or its interaction with A. solidipes on growth, survival, and the Armillaria root disease of conifers. Materials and Methods: In 1971, a provenance planting of P. monticola spanning 0.8 ha was established at the Priest River Experimental Forest in northern Idaho, USA. In 1987, 2076 living or recently dead trees were measured and surveyed for Armillaria spp. to describe the demography and to assess the potential influences of Armillaria spp. on growth, survival, and the Armillaria root disease among the study trees. Results: Among the study trees, 54.9% were associated with Armillaria spp. The genets of A. altimontana and A. solidipes comprised 82.7% and 17.3% of the sampled isolates (n = 1221) from the study plot, respectively. The mapped distributions showed a wide, often noncontiguous, spatial span of individual Armillaria genets. Furthermore, A. solidipes was found to be uncommon in areas dominated by A. altimontana. The trees colonized by A. solidipes were associated with a lower tree growth/survival and a substantially higher incidence of root disease than trees colonized only by A. altimontana or trees with no colonization by Armillaria spp. Conclusions: The results demonstrate that A. altimontana was not harmful to P. monticola within the northern Idaho planting. In addition, the on-site, species-distribution patterns suggest that A. altimontana acts as a long-term, in situ biological control of A. solidipes. The interactions between these two Armillaria species appear critical to understanding the Armillaria root disease in this region.

Screening Almond Rootstocks for Sources of Resistance to Armillaria Root Disease

Prunus dulcis (almond) is one of the most susceptible horticultural crops to Armillaria root disease. Resistance to Armillaria mellea and Armillaria tabescens, the geographically isolated causal fungi that attack almond and closely related Prunus persica (peach), has been evaluated in studies of almond, peach, and other Prunus rootstocks, but not in one comprehensive study. We evaluated the relative resistance to A. mellea and A. tabescens of six clonally propagated almond and peach rootstocks (Bright’s 5, Empyrean 1, Hansen 536, Krymsk 1, Krymsk 86, and Lovell) in comparison with that of clonally propagated Marianna 2624 rootstock (resistant control) and clonally propagated Nemaguard rootstock (susceptible control). Replicate clones used in the growth chamber assay were micropropagated and rooted in vitro before inoculating the culture medium with Armillaria spp. At 2 months, the most resistant and susceptible rootstocks were Krymsk 86 and Hansen 536, respectively, with 27% vs. 89% mortality. This finding was consistent among two isolates of A. mellea and one isolate of A. tabescens in three replicate experiments. Our finding of low mortality among Krymsk 86, Krymsk 1, and Marianna 2624, which all share Prunus cerasifera (Myrobalan plum) parentage, is consistent with past reports of resistance in the field to A. mellea, but conflicts with reports of susceptibility to A. tabescens. Resistance to A. tabescens of genotypes with Myrobalan plum parentage in our assay may reflect the simplified rooting environment of tissue culture medium, which does not perfectly mimic a field trial, in which biotic and abiotic factors may affect host resistance. Nonetheless, our growth chamber assay may provide a more rapid alternative to identify sources of resistance for breeding and to screen progeny of such crosses.

Impact of climate on juvenile mortality and Armillaria root disease in lodgepole pine

Variable and sometimes high levels of mortality in lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) planted in western Alberta have raised awareness of the need to forecast and ameliorate risks to reforestation success. Mortality and health of regeneration during the 12 years following harvest were monitored and evaluated in relation to climate, site and silvicultural treatments. Results suggest that physiological stress related to evapotranspiration is the most prevalent cause of overall juvenile mortality and susceptibility to Armillaria root disease in planted pine. Mortality and disease not only increase at higher rates of drying during the growing season, but an opposite effect is also demonstrated whereby they decrease with increasing spring temperatures. Mechanical site preparation aimed at countering mortality and disease of planted stock with improved soil conditions appears to have good potential for ameliorating adverse climatic effects in juvenile stands.