Identification and Distribution of Armillaria Species Associated With

For. Path. 39 (2009) 397–404 doi: 10.1111/j.1439-0329.2009.00600.x 2009 Blackwell Verlag GmbH

Identiﬁcation and distribution of Armillaria species associated with an oak decline event in the Arkansas Ozarks

By M. B. Kelley1, M. K. Fierke and F. M. Stephen

Department of Entomology, University of Arkansas, AGRI 319, Fayetteville, AR 72701, USA. 1E-mail: [email protected] (for correspondence)

Summary Forests in the Ozark Mountains of northern Arkansas recently experienced a widespread oak decline event. Armillaria, a root rot fungus, has been associated with other oak decline events and may have been an important contributing factor to tree mortality in this event. Although Armillaria has been identified from the Ozark Mountains in Missouri, it has never been investigated in the Arkansas Ozarks. Molecular diagnostic techniques were used in this study to identify species of Armillaria present on roots removed from dead trees of two common oak species, northern red oak, Quercus rubra L., and white oak, Q. alba L., from three geographic areas and on three topographic positions – ridges, south- and west-facing benches. Armillaria (A. mellea, A. gallica or A. tabescens) was identified from 31% of root samples taken from 102 trees in seven of nine sample plots. Armillaria mellea, occurred most often (20 samples, both oak species on seven plots) followed by A. gallica (10 samples, northern red oak only on four plots), and A. tabescens occurred twice (on northern red oak in a single plot). Thus, all three Armillaria species occurred on northern red oaks while A. mellea was the only species recovered from white oaks. Results varied by topographic position with samples from tree roots on ridges having the fewest positive identifications, one of 29. West-facing benches had the highest positive samples with 20 of 41 testing positive and trees on south-facing benches were intermediate with 11 of 32 samples from infected trees. This study documents the occurrence of three species of Armillaria in the Arkansas Ozarks and their association with oak mortality resulting from an oak decline event coupled with a red oak borer, Enaphalodes rufulus, outbreak. Further, it documents some potential variation in host ⁄ pathogen combinations and forest site conditions.

1 Introduction Oak-hickory forests in the Ozarks of northwest Arkansas recently experienced an oak mortality event with mortality ranging from a few scattered trees in stands having a diversity of species and age classes, to hundreds of acres of mature red oaks on poor sites (Starkey et al. 2000; Fierke et al. 2007). A number of abiotic and biotic stress factors can lead to oak decline and mortality (Sinclair 1965; Manion 1981). Mortality in this recent event has been primarily attributed to red oak borer, Enaphalodes rufulus (Haldeman) (Coleoptera: Cerambycidae) a native long-horned wood-boring beetle (Stephen et al. 2001; Fierke et al. 2005a,b). Some researchers have speculated that Armillaria (Fr.: Fr.) Staude (Agaricales: Marasmiaceae), a common genus of root rot fungus, may have also contributed to mortality in this event (Starkey et al. 2000; Fierke et al. 2005b) as was documented in the 1990s in the upland Ozark Mountains of Missouri (Bruhn et al. 2000). However, species composition, distribution and possible ecological impacts have never been investigated in the ArkansasÕ Ozarks. Armillaria is often associated with forest decline events (Balch 1927; Carey et al. 1984; Bauce and Allen 1992; Bruhn et al. 1996) and is generally considered a contributing factor ultimately responsible for tree death following some other predisposing stressor (Sinclair 1965; Manion 1981; Wargo and Harrington 1991). Armillaria species exhibit

Received: 1.11.2007; accepted: 10.2.2009; editor: S. Woodward

www3.interscience.wiley.com 398 M. B. Kelley, M. K. Fierke and F. M. Stephen varying degrees of pathogenicity (Gregory et al. 1991). Certain species of Armillaria, such as A. gallica Marxmuller and Romagn., allocate more energy to production of rhizomorphs and are considered to be a more exploratory, less pathogenic and less aggressive species (Gregory et al. 1991). Other species, such as A. mellea (Vahl: Fr) and A. ostoyae (Romagn.) Herink, put more energy into production of mycelia and are therefore considered more pathogenic. Armillaria tabescens (Scop.) Emel is considered moderately pathogenic as it produces short and sparsely branched rhizomorphs (Bruhn and Mihail 2003). The latter three species depend more on root-to-root contact for spread of mycelia or on basidiome production for basidiospore dispersal. Armillaria gallica depends more on penetration of roots by rhizomorphs to establish infection (Bruhn and Mihail 2003). The goals of this research were to document species of Armillaria present in Arkansas Ozark forests as well as determine Armillaria distribution in an initial effort to elucidate contributors to tree mortality. Speciﬁc objectives were to determine Armillaria species presence and relative abundance on (1) dead trees of the two most common oak species, northern red oak, Quercus rubra L., and white oak, Q. alba L., and on (2) the three topographic positions experiencing the greatest tree mortality, ridges, south- and west- facing benches (Fierke et al. 2007).

2 Materials and methods

2.1 Study sites Study areas were located in oak-hickory forests in the upper Boston Mountains of the Ozark National Forest. These forests are generally composed of even-aged trees (Soucy et al. 2004) covering approximately 6.5 million hectares (USDA FS 1999). In the Upper and Lower Boston Mountains, the specific area of interest, oaks comprise 97% and 92%, respectively, of the forested area (USDA FS 1999). Sampling occurred within or adjacent to three previously established fixed area 3000 m2 vegetation plots on ridges, south- and west- facing benches located in each of three areas, Fly Gap, White Rock and Oark (UTM Zone 15–S NAD83: Fly Gap – E 0431660, N 3954978 and White Rock – E 412668, N 3949429 and Oark – E 0450792, N 3952369) (Fig. 1) (Fierke et al. 2007). Original stand selection for plot placement was based on presence of northern red oak and signs of red oak borer infestation (although stands were not specifically selected for a greater incidence of either of these, Fierke et al. 2007). Living and dead tree densities as well as relative sizes for trees by topographic position plots are provided in Table 1.

2.2 Sample collection Eighty dead northern red oaks and 26 dead white oaks were sampled from June 2004 to August 2004. Up to 10 northern red oaks and ﬁve white oaks were sampled in each vegetation plot depending on availability of suitable trees. Criteria for sampling was that trees were dead but still standing – so sampled trees varied from recently dead with small twigs to some that exhibited more extensive decay. In plots with ample trees to choose from, sampling was spaced throughout the plot, however, in a majority of plots, all standing dead trees were sampled from within the plot and a few sampled adjacent to the plot. Root samples were collected as it is the easiest way to obtain Armillaria mycelia for molecular diagnostics (Harrington and Wingfield 1995). Root excavation methods were similar to those used in the Missouri Ozarks Armillaria study (J. N. Bruhn, University of Missouri, personal communication). Debris was raked away from the base of a tree to expose the largest lateral root. Soil and rocks were removed with a trowel until a sufﬁcient portion of root bark was exposed. Samples were excised from under a soft portion of root bark as mycelium is often associated with soft rotten wood. One seven by Armillaria in the Arkansas Ozarks 399

Fig. 1. Nine ﬁxed-area vegetation plots were located in three general areas of the Ozark National Forest, Arkansas. Circles encompass three plots within each general area.

Table 1. Mean (±SE) densities and sizes of trees from nine 3000 m2 ﬁxed-area vegetation plots established in three areas on three topographic positions in oak-hickory forests of the Ozark National Forest.

Total Dead Living Dead Living Dead Topographic trees ⁄ ha1, trees ⁄ ha1, RO2 ⁄ ha, RO2 ⁄ ha, WO3 ⁄ ha, WO3 ⁄ ha, position mean dbh mean dbh mean dbh mean dbh mean dbh mean dbh

Ridge 588 ± 39 181 ± 16 238 ± 49 171 ± 17 88 ± 41 7 ± 4 23.4 ± 0.4 22.7 ± 0.5 29.2 ± 0.5 23.2 ± 0.5 18.0 ± 0.7 14.8 ± 1.9 South 578 ± 14 85 ± 14 114 ± 28 38 ± 17 262 ± 88 46 ± 19 22.4 ± 0.4 19.2 ± 0.9 30.0 ± 0.8 22.7 ± 1.2 23.2 ± 0.6 15.2 ± 0.6 West 448 ± 31 90 ± 24 121 ± 19 52 ± 7 98 ± 41 36 ± 42 25.4 ± 0.5 23.6 ± 1.1 34.6 ± 1.0 28.4 ± 1.5 28.0 ± 1.2 16.6 ± 0.9 1Data previously reported in Fierke et al. (2007). 2Red oaks (RO) include Q. rubra, Q. velutina and Q. marilandica. 3White oaks (WO) include Q. alba and Q. stellata.

14 cm portion of root bark was removed using a hammer and chisel and was placed in brown paper bags, transported in an ice chest, and stored in a refrigerator at 4C. Upon dissection, small amounts of visible mycelium were removed from root samples using sterile forceps for molecular diagnostics. Four samples, from two ridges, did not yield mycelia for extraction. 400 M. B. Kelley, M. K. Fierke and F. M. Stephen 2.3 Species identification Species identification was accomplished using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP) as per Szalanski et al. (2000). DNA was extracted from mycelia using Qiagen DNeasy extraction kits (Qiagen Sciences, Valencia, CA, USA). The intergenic spacer region of ribosomal RNA (rRNA) (Anderson and Stasovski 1992) was amplified using primers LR12R (Veldman et al. 1981) and O-1 (Duchesne and Anderson 1990). RFLP was accomplished using the enzyme Alu I as this enzyme delineates North American isolates of A. mellea, A. gallica and A. tabescens (Harrington and Wingfield 1995). DNA sequencing was outsourced to the University of Arkansas for Medical Sciences and results were compared to sequences for each species on GenBank to validate species identifications (GenBank accession numbers: A. mellea – AF163616, A. gallica – AF451825 and A. tabescens – AF451835).

2.4 Fruiting body survey Visual surveys of vegetation plots in the Fly Gap area were made on 30 August, 27 September and 1 November, 2006 for Armillaria fruiting bodies. Fruiting was observed on 1 November and all nine ﬁeld plots were visually surveyed 1 and 8 November, 2006. All trees within plots were inspected around the tree base. Armillaria fruiting bodies were noted if present. Unfortunately, peak fruiting likely occurred in mid-October based on the degraded state of many of the fruiting bodies, and so decomposing fruiting bodies growing in caespitose clusters at the base of dead trees were noted (A. mellea, A. gallica and A. tabescens exhibit this gregarious growth habit). A few living and dead northern red oak trees within these vegetation plots were cut for other research and are referred to as stumps in the results section for the fruiting survey.

2.5 Statistical analysis Nominal logistic analysis in JMP 6.0 (SAS Institute 2005) at a = 0.05 was used to determine likelihood of occurrence for Armillaria species within each area, on different topographic positions, and on northern red oaks or white oaks. Samples from the four trees that did not yield mycelia were not included in these analyses.

3 Results

3.1 Molecular sampling Three species of Armillaria were identified in root samples – A. mellea, A. gallica and A. tabescens. Armillaria was identified from 32 (31%) of 102 root samples from seven of the nine vegetation plots (Table 2). Twenty-four of the 76 (31.5%) northern red oaks sampled had Armillaria and eight of 26 (31%) white oaks were positive. Likelihood of occurrence was 2 not significantly different between tree species for A. mellea (v 1,102 = 1.2, p = 0.28), but was 2 significantly different for A. gallica (v 1,102 = 6.8, p = 0.009). Armillaria mellea was recovered from 12 of 76 northern red oaks sampled and eight of 26 white oaks. Armillaria gallica was identified from 10 northern red oaks and none of the white oaks. Armillaria tabescens was not statistically analysed as there were only two positive samples for this species. Both of these samples were from northern red oaks and located on a south-facing plot. Trees from which these samples were taken were distributed among seven of the nine vegetation plots. Likelihood of occurrence for A. mellea and A. gallica was not significantly 2 2 different among the three geographic areas (v 2,102 = 3.1, p = 0.21 and v 2,102 = 5.0, p = 0.08, respectively). Sixteen of 38 root samples from trees in Fly Gap plots tested Armillaria in the Arkansas Ozarks 401

Table 2. Results from molecular diagnostic tests on mycelia samples from primary roots of standing dead NRO and WO as well as a visual survey for fruiting bodies.

No. of samples (+) NRO (+) WO (+) Fruiting Area and plot NRO, WO A. mellea A. gallica A. tabescens A. mellea bodies1

Fly Gap Ridge 8, 0 1 – – – 0 Fly Gap South 10, 5 – 2 2 1 2 Fly Gap West 10, 5 6 2 – 2 3 White Rock Ridge 8, 3 – – – – 4 White Rock South 2, 3 – – – 1 1 White Rock West 10, 1 – 5 – 1 3 Oark Ridge 10, 0 – – – – 0 Oark South 8, 4 3 – – 2 0 Oark West 10, 5 2 1 – 1 0 Totals 76, 26 12 10 2 8 13 1Indicates Armillaria fruiting bodies or decomposing fruiting bodies exhibiting Armillaria char- acteristics. NRO, northern red oaks; WO, white oaks.

positive for Armillaria. Seven of 27 samples from trees in White Rock plots tested positive and nine of 37 were positive in Oark plots. Trees on west-facing benches had the highest frequency of Armillaria occurrences with 20 of 41 (48.8%) samples testing positive. South- facing trees had 11 of 32 (34.4%) and ridge trees only had one of 29 (3.5%) test positive for Armillaria. There were signiﬁcant differences among topographic positions for A. mellea 2 2 (v 2,102 = 6.6, p = 0.037) and A. gallica (v 2,102 = 11.2, p = 0.004). Armillaria mellea was identiﬁed on a single ridge tree, seven times from trees on south-facing benches, and 12 times from trees on west-facing benches. Armillaria gallica was not found on ridge trees, but was found twice on trees from south-facing benches and eight times from trees on west-facing benches.

3.2 Fruiting body survey Armillaria fruiting bodies or rotting caespitose fruiting bodies were noted at the base of 13 trees in ﬁve of the nine plots during visual surveys in 2006 (Table 2). There were no Armillaria or rotting caespitose fruiting bodies noted for the Fly Gap ridge plot. There was a white oak and a northern red oak stump with rotting fruiting bodies in the Fly Gap south plot. One standing dead northern red oak, one northern red oak stump, and one standing dead white oak in the Fly Gap west plot had rotting fruiting bodies around them. Two recently dead standing northern red oaks on the White Rock ridge plot had Armillaria fruiting bodies at their bases and one dead white oak and one dead post-oak, Q. stellata Wangenh., had rotting fruiting bodies around their bases. Three northern red oak stumps in the White Rock west plot had rotting fruiting bodies at their bases. There were no trees within the White Rock south plot with Armillaria fruiting bodies; however, there was a standing dead northern red oak just outside the plot with rotting fruiting bodies at the base. There were no trees in the Oark plots with Armillaria fruiting bodies.

4 Discussion Our findings are similar to the recent reports of Armillaria in the Missouri Ozarks (Bruhn et al. 2000). We identified the same three species, A. mellea, A. gallica and A. tabescens, and found A. mellea to be the most widely distributed and abundant species with a total of 20 402 M. B. Kelley, M. K. Fierke and F. M. Stephen positive identifications from mycelia samples removed from dead northern red oak and white oak roots in seven of the nine plots surveyed. Armillaria mellea was the only species found infecting white oaks in this study (31% of samples). White oaks are becoming more dominant in the Ozarks (Johnson and Law 1989) and may become the dominant tree species in the Arkansas Ozarks (Heitzman 2003). As A. mellea is considered pathogenic and it was present on a high percentage of dead white oaks, it is likely to be an important contributor to white oak mortality in these forests. Armillaria gallica was identified on 10 trees from four of the vegetation plots sampled. It has historically been considered saprophytic (Korhonen 1978; Rishbeth 1982); however, other reports imply that A. gallica rhizomorphs can completely cover roots of healthy trees and are therefore in a position to infect when conditions become suitable (Rishbeth 1985). Armillaria gallica may be pathogenic to some conifers in southern Ontario forests (McLaughlin 2001) and is likely a primary pathogen of mixed hardwood forests in California (Baumgartner and Rizzo 2001). Some trees harbouring A. gallica in the current study had recently died, indicating that A. gallica likely infected them prior to their demise. This contrasts to the Missouri study which only rarely associated presence of A. gallica with declining or recently dead trees (Bruhn et al. 2000). It may be that with tree health severely compromised by other agents, e.g. red oak borer, A. gallica may be occupying more than a saprophytic role in ArkansasÕ forests. Armillaria tabescens was collected twice from trees in the Fly Gap south plot and these were the only occurrences in the nine plots sampled. This plot had a small ephemeral stream within it (there were none in the other plots) and one tree harbouring A. tabescens was located directly adjacent to the stream and the other tree that tested positive was within 5 m of the stream. Armillaria tabescens produces rhizomorphs more readily under conditions of high moisture and increased oxygen availability (Mihail et al. 2002). This explanation may not be acceptable, however, considering findings from the Missouri Ozarks where A. tabescens was identified most often on ridge summits (Bruhn et al. 2000). But, as with this study, the association remained unexplained by the collected data and apparent disparities in A. tabescens habitats may be due to limited inoculum centres and difficulty in field identifications of these species (Bruhn et al. 2000). On the basis of molecular diagnostics, Armillaria was conspicuously absent from trees on ridges. Compared to other landforms, ridges have poorer soils with high solar insolation, shallow-rocky soils and reduced soil moisture (Bates 1923; Potzger 1939). Armillaria gallica mainly spreads by production of rhizomorphs (Rishbeth 1985), which do not grow well under dry, rocky conditions (Bruhn et al. 1997). Only one of the 33 trees from the ridge plots tested positive for A. mellea. Ridge samples were desiccated and flaky compared to samples from trees on south- and west-facing benches and four of the trees on ridges did not yield mycelia. This may mean that ridge samples were not optimal source material for molecular identification. To test this idea, samples with mycelia present were collected under more optimal conditions, i.e. in late May (spring) of 2006, from 10 additional trees in the Fly Gap ridge plot. Again, however, none tested positive for Armillaria, even though there appeared to be visual evidence of Armillaria infection (mycelia and rhizomorphs). If, indeed, collected samples were Armillaria that did not test positive, it means that it is more difficult to get quality DNA for PCR from mycelia on tree roots from these sites, i.e. local conditions may lead to relatively rapid DNA degradation. Alternatively, it may be that Armillaria was present (rhizomorphs), but that the mycelia sampled was not Armillaria. Either of these scenarios would lead to under-reporting of the incidence of Armillaria presence and ⁄ or abundance of a particular species. During visual examinations of trees for Armillaria fruiting bodies, there was no evidence of Armillaria on the ridge plots at Fly Gap or Oark. There were two dead northern red oaks in the White Rock ridge plot with Armillaria fruiting bodies as well as a dead white oak and a dead post-oak with rotting caespitose fruiting bodies characteristic of Armillaria. Armillaria in the Arkansas Ozarks 403 These observations contrast to molecular findings from this plot as none of the 11 tree roots sampled tested positive for Armillaria (and two of the original northern red oak roots sampled did not yield mycelia for DNA extraction). Not all trees originally surveyed molecularly could be definitively associated with presence or absence of fruiting bodies as they either were not permanently marked or they had fallen over and roots were exposed. There were, however, several trees ⁄ stumps in the Fly Gap south and west plots and the White Rock west plot with rotting fruiting bodies associated with them that tested positive molecularly for Armillaria. All trees that tested positive did not have evidence of fruiting bodies, although an absence of fruiting bodies was not unexpected as all species of Armillaria do not produce fruiting bodies annually (Bruhn et al. 2000). This research confirms the occurrence of Armillaria in the Arkansas Ozarks and its association with oak mortality resulting from an oak decline event coupled with a red oak borer, E. rufulus, outbreak. Differences in Armillaria species occurrence on different oak species and on different topographic positions were documented. Other stand variables, such as soil type, percent rock, soil moisture content, tree species richness and diversity, or other topographic positions, east- or north-facing benches, may also be important factors influencing occurrence and distribution of Armillaria in the Arkansas Ozarks. Knowledge of distribution and species composition of Armillaria in these forests provides important information on possible contributors to the recent oak mortality event and patterns of tree mortality.

Acknowledgements Authors thank Dr Allen Szalanski and the Insect Genetics Lab at the University of Arkansas for advice and use of facilities; Jarrett Bates and Joshua Jones for ﬁeldwork; and Dr Johann Bruhn and Dr Jeanne Mihail for suggestions, insight and help at the onset of this project. We also thank Tom Harrington for edits and advice on an earlier version of the manuscript. Funding was provided by the University of Arkansas Agricultural Experiment Station and grants from the Forest Health Protection Special Technology and Development Program and Forest Health Monitoring programs, Pineville, LA and Atlanta, GA, plus grants from the USDA Forest Service, Southern Research Station, Asheville, NC.

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