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Forest Ecology and Management

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Impact of Sirococcus shoot blight (Sirococcus tsugae) and other damagingagents on eastern hemlock (Tsuga canadensis) regeneration in NortheasternUSA

Isabel A. Muncka,⁎, Randall S. Morinb, William D. Ostrofskyc, Wayne Searlesc, Denise R. Smithd,Glen R. Stanoszd

aNortheastern Area State and Private Forestry, USDA Forest Service, 271 Mast Rd, Durham, NH 03824, United StatesbNorthern Research Station's Forest Inventory and Analysis, USDA Forest Service, C11 Campus Blvd, Suite 200, Newtown Square, PA 19073, United StatescMaine Forest Service, Maine Department of Agriculture, Conservation and Forestry, 18 Elkins Lane, Augusta, ME 04330, United Statesd Department of Forest and Wildlife Ecology, University of Wisconsin-Madison, 1630 Linden Dr, Madison, WI 53706-1598, United States

A R T I C L E I N F O

Keywords:Invasive forest pestsForest pathogensRegeneration qualityTree disease development

A B S T R A C T

In 2009, Sirococcus tsugae was first reported in Maine on eastern hemlock. Our goal was to quantify the impact ofthe shoot blight disease caused by this fungal pathogen of unknown origin on eastern hemlock regeneration.From 2013 to 2014, 59 long-term monitoring plots established by the US Forest Service (USFS) Forest Inventoryand Analysis (FIA) program in New England and New York were surveyed to determine the impact of S. tsugae.Damage by hemlock woolly adelgid (Adelges tsugae), elongate hemlock scale (Fiorinia externa), white-tailed deer(Odocoileus virginianus), or other causes was also recorded. Disease incidence and severity (percentage of shootsblighted and percentage of crown defoliated) were assessed for 20 seedlings per plot. Sirococcus shoot blightsymptoms were present in most plots (90%) and on most seedlings (72%). For the majority of seedlings, blightaffected less than 10% of shoots, but the percentage of shoots blighted did range up to 75%. Similarly, needleloss was limited to less than 25% of the crown for most seedlings. Disease severity was positively correlated withoverstory hemlock density. Using species-specific polymerase chain reaction (PCR) primers, Sirococcus tsugaewas identified from samples collected in the majority of sites (68%) in New England and New York. In permanentplots at the Massabesic Experimental Forest in Maine, disease symptom severity increased from 16% blightedshoots in 2011 to 47% blighted shoots in 2013. Results confirm that Sirococcus shoot blight of eastern hemlock ismore widespread in natural forests of northeastern USA than previously known and that symptoms can be severe(> 75% blighted shoots) in some locations.

1. Introduction

Blighted shoots of eastern hemlock (Tsuga canadensis (L.) Carrière)regeneration were first documented in 2003 during a Maine ForestService survey to assess hemlock woolly adelgid (Adelges tsugae) da-mage. In 2009, the presence of Sirococcus tsugae Rossman, Castl., D.F.Farr & Stanosz on blighted eastern hemlock shoots collected in Mainewas confirmed based on morphology and DNA analyses (Miller-Weeksand Ostrofsky, 2010). This was the first time that S. tsugae was reportedto damage eastern hemlock. In 2010, the identity of S. tsugae isolatesfrom Georgia and their ability to cause disease on eastern hemlock wasconfirmed (Stanosz et al., 2011). That report also included results of apreliminary survey in Georgia which revealed that incidence of blightedshoots on individual trees varied, but was as high as 70%. Prior to these

reports, Sirococcus tsugae had only been reported on Atlas cedar (Cedrusatlantica), Himalayan cedar (C. deodora), western hemlock (Tsuga het-erophylla), and mountain hemlock (Tsuga mertensiana) in western NorthAmerica (Rossman et al., 2008). Since then, the distribution of S. tsugaein Northeastern USA, where eastern hemlock is valued, has remainedunknown.

Eastern hemlock is ecologically and economically important in theNortheast (Dukes et al., 2009). The range of eastern hemlock extendsfrom southeastern Canada to Georgia and Alabama in the south and asfar west as Minnesota. Eastern hemlock is considered a foundationspecies because it defines an ecological community, it is regionallycommon, locally abundant and creates stable conditions for many otherspecies (Ellison et al., 2005). Currently, the eastern hemlock resource isthreatened by exotic pests such as hemlock woolly adelgid and

https://doi.org/10.1016/j.foreco.2018.07.043Received 29 June 2018; Received in revised form 23 July 2018; Accepted 25 July 2018

⁎ Corresponding author.E-mail address: imunck@fs.fed.us (I.A. Munck).

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elongated hemlock scale (Fiorinia externa) (Preisser et al., 2008; Evanset al., 2011; Orwig et al., 2012; Gomez et al., 2015; Case et al., 2017).Browsing by white-tailed deer (Odocoileus virginianus), which have in-creased in abundance in recent decades, also negatively impacts easternhemlock regeneration (Eschtruth and Battles, 2008; Frerker et al., 2014;Faison et al., 2016). The impact of Sirococcus shoot blight (SSB) on theeastern hemlock resource, already at risk because of hemlock woollyadelgid (HWA), elongated hemlock scale (EHS), and white-tailed deerpredation merits further investigation.

There are several Sirococcus Preuss species that cause shoot blight tomany conifer species causing damage to new shoots, seedlings andsaplings (Nicholls and Robbins, 1984). Sirococcus shoot blight symp-toms can become widespread and cause tree mortality under favorableweather conditions (Nicholls and Robbins, 1984). Growth reduction,crown deformation, and mortality attributed to the closely relatedspecies Sirococcus conigenus (Pers.) P.F. Cannon & Minter have beendocumented in young and mature Norway spruce (Picea abies) planta-tions in Europe (Halmschlager et al., 2000; Halmschlager andKatznsteiner, 2017) and red pine regeneration (Pinus resinosa) in theGreat Lake States in the USA (Bronson and Stanosz, 2006; Ostry et al.,2012; Haugen and Ostry, 2013). In mature red pines, symptoms aremore severe in the lower crown but can extend to the upper partcausing poor crown condition (O'Brien, 1973). In southeastern Alaska,reduced height, terminal-leader kill and mortality of western hemlockregeneration were attributed to Sirococcus shoot blight, most likelycaused by S. tsugae (Wicker et al., 1978; Shaw et al., 1981; Rossmanet al., 2008). The etiology and epidemiology of S. tsugae on easternhemlock, however, are not yet understood. The pathogen does not al-ways form fruiting bodies on killed shoots, but other fungi do fruit ondiseased shoots complicating disease diagnoses (Miller-Weeks andOstrofsky, 2010). Therefore, it is important to verify the association ofshoot blight symptoms with the pathogenic fungus S. tsugae.

The goal of this project is to elucidate the many questions regardingSirococcus shoot blight on eastern hemlock including its geographicrange, symptomatology, etiology, and impact that this disease is havingon eastern hemlock regeneration. The specific objectives are to: (i)delineate the geographic range of Sirococcus shoot blight in theNortheastern USA, (ii) verify the association of the pathogenic fungus S.tsugae with both shoot blight and needle loss, (iii) quantify impact ofthe disease and other damaging agents on eastern hemlock regenera-tion, and (iv) monitor changes in severity over time. Information per-taining to stand characteristics associated with disease incidence andseverity are provided along with baseline data of current disease dis-tribution. This information will help resource managers determinestand susceptibility and assess risk to regeneration activities in alreadyat-risk hemlock forests.

2. Materials and methods

2.1. Site selection

The Forest Inventory and Analysis (FIA) program of the U.S.Department of Agriculture, Forest Service, conducts an inventory offorest attributes across the country (Bechtold and Patterson, 2005). TheFIA three-phase random sampling design is based on a tessellation ofthe United States into hexagons approximately 2428 ha in size with atleast one permanent plot established in each hexagon. We used datafrom permanent plots established by FIA to locate survey sites. To fa-cilitate access and ensure sampling success, we selected FIA plots inpublic lands with eastern hemlock regeneration and in close proximityto roads. For Maine and New York, we selected up to 20 FIA plots perstate. We selected 20 additional FIA plots in the remaining New Eng-land states: Connecticut, Massachusetts, New Hampshire, Rhode Island,and Vermont. Within a state, we selected a maximum of three FIA plotsper county. To obtain a wide geographic range, we selected FIA plotsthat met our criteria in the counties with most northern (Aroostook

County, ME), southern (Orange County, NY), eastern (Hancock County,ME) and western (Allegany County, NY) locations.

2.2. Eastern hemlock regeneration survey

Seedlings were surveyed when current-year shoots became symp-tomatic: June through August of 2012 and June of 2013. We traveled tothe center of the selected FIA plot with the aid of a GPS receiver(GPSmap 60CSx, Garmin International Inc., Olathe, KS, USA). At eachFIA plot, 20 seedlings defined as hemlocks taller than 30 cm, butsmaller than 2.54 cm in diameter at breast height (dbh, 1.3 m from theground) were surveyed along transects or in quadrants. If available, fiveseedlings were surveyed in each cardinal direction (north, east, southand west) along transects 40m long and 4m wide. If not enoughseedlings were present in one direction, additional seedlings weresurveyed in the opposite direction. If not enough seedlings were presentalong transects, additional seedlings were surveyed in quadrants of acircular plot with a 40m radius. The distance of the seedling farthestfrom plot center in each transect or quadrant was recorded. The extentof the crown that was defoliated was estimated for each seedling andrecorded as: 0= none, 1=1–10%, 2= 11–25%, 3=26–50%,4=51–75%, 5=76–99%, 6= dead (Orwig and Foster, 1998). Se-verity of damage (defined as the percentage of shoots affected) attri-butable to each damaging agent, animal, SSB, HWA, EHS, hemlock-blueberry rust (Naohidemyces vaccinia), circular hemlock scale (Nucu-lapsis tsugae), and other, also was estimated for each seedling and re-corded using the same 0–6 classes. Sources of damage in the “other”category included: mechanical damage (dead tops or wounds), winterinjury, mites (Oligonychus ununguis and Nalepella tsugifoliae), hemlocklooper (Lambdina fiscellaria), and spittle bugs (Aphrophora spp.).

2.3. Confirmation of pathogen identity

Samples from each FIA plot were kept cool and shipped overnight tothe University of Wisconsin-Madison. Eastern hemlock shoots withsymptoms of Sirococcus shoot blight were incubated in moist chambersat room temperature for 2–10 days to allow development of pycnidiacontaining conidia, and single-conidial isolates were obtained.

DNA was extracted from isolates grown in potato dextrose brothusing a modified Dellaporta procedure (Smith and Stanosz, 1995). TheDNA was amplified using the primer pair SirTf and SirTr2 and theamplification conditions described by Smith and Stanosz (2008) toconfirm identity of isolates as S. tsugae. Any isolates with negative re-sults for S. tsugae were further tested using the primer pair SirCf andSirCr to in an attempt to determine whether these might be the mor-phologically similar species S. conigenus.

For a small number of shoots that did not yield conidia from whichcultures could be obtained, a small piece of symptomatic stem andneedle tissue was aseptically removed from the sample and placed in amicrocentrifuge tube. The DNA was extracted by the modified Cuberoprocedure as published in Smith and Stanosz (2006). Testing for the

Table 1Occurrence of different damaging agents on eastern hemlock seedlings in 59plots in New York and New England.

Damaging agent PlotsNo. (%)

SeedlingsNo. (%)

Sirococcus shoot blight 53 (90) 791 (72)Animal 37 (63) 206 (19)Hemlock woolly adelgid 11 (19) 136 (12)Elongate hemlock scale 6 (10) 85 (8)Hemlock-blueberry rust 6 (10) 33 (3)Circular hemlock scale 1 (2) 11 (1)Other 32 (54) 68 (6)Not damaged 34 (58) 184 (17)

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presence of S. tsugae and S. conigenus DNA was done using the proce-dure in the previous paragraph.

2.4. Long term monitoring

Five permanent plots were established in the USFS MassabesicExperimental Forest (MEF) during 2011. The MEF is located in YorkCounty, Maine on flat to gently rolling land up to 137m above sea levelwith soils of glacial origin. Plots were established in stand (43.44755,−70.6815833333) with a mean basal area of 24.4m2/ha. Easternhemlocks comprised 30% of the basal area and had a mean dbh of40 cm. White pines (Pinus strobus) comprised 70% of the basal area andhad a mean dbh of 69 cm. Each plot center was marked with a metalstake and 20 seedlings per plot were tagged. Seedling height and dia-meter at base were measured. Seedlings in these plots exhibitedsymptoms of Sirococcus shoot blight, but were not infested by HWA orEHS. During three consecutive years, 2011–2013, extent of crown de-foliation was estimated as described above for each seedling in July. Todetermine disease progression, the number of blighted shoots and total

Fig. 1. Damaging agents of eastern hemlock seedlings on 59 FIA plots in Northeastern USA.

Table 2Percentages of eastern hemlock seedlings which exhibited damage by variousagents, categorized by the percentage of shoots affected by those damagingagents.

Damaging agent Percentage of shoots affected

1–10 11–25 26–50 50–75 76–99

Sirococcus shoot blight 73 20 6 1 0Animal 55 29 12 4 0Hemlock woolly adelgid 23 32 25 16 4Elongate hemlock scale 14 29 32 24 1Hemlock-blueberry rust 50 50 0 0 0Circular hemlock scale 0 27 18 55 0Other 47 21 32 0 0

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number of shoots for each seedling were counted three times from mid-June to the end of July in 2011 and 2013.

2.5. Statistical analyses

To determine the effect of damaging agent on crown defoliation,data from the 59 FIA plots were analyzed using a linear mixed model(PROC GLIMMIX) in SAS (SAS Institute Inc., v. 9.3, 2011, Cary, NC,USA). “Damaging agent” was a fixed effect, “FIA plot” was a randomfactor, and the response variable was “mean crown defoliation for eachdamaging agent category per plot”. We used Pearson correlations toexamine the relationship between FIA stand attributes (Bechtold andPatterson, 2005): longitude, latitude, slope, total basal area, hemlockbasal area, percent hemlock basal area, hemlock seedlings, percenthemlock seedlings, hemlock overstory trees, percent hemlock overstorytrees, elevation, seedling count, stand size, aspect, growing stock, alllive stocking, and severity by each damaging agent per plot and crowndefoliation per plot. Severity is defined as the proportion of shoots af-fected by each damaging agent. To ascertain the effect of time on crowndefoliation, data from permanent plots at the MEF were analyzed using

a linear mixed model (PROC GLIMMIX) in SAS taking into account therepeated measures of “year” and the random “plot”. “Year” was a fixedeffect, “plot” was a random factor, and the response variable was “meancrown defoliation per plot”. To account for the correlated errors be-tween “years”, an autoregressive order 1 covariance structure was used.Similarly, to establish the effect of time on disease progression, datafrom permanent plots at the MEF were analyzed using a linear mixedmodel (PROC GLIMMIX) in SAS taking into account the repeatedmeasures of “sampling date (year)” and the random plot. “Year” and“sampling date” were fixed effects, “plot” was random factor, and theresponse variable was “percentage of blighted shoots”. To account forthe correlated errors between “sampling dates” within “years”, an au-toregressive order 1 covariance structure was used. In both analysesabove the Kenward-Rogers denominator degrees of freedom adjustmentwas used. For all models, when main effects were significant (α =0.05), a Tukey-Kramer test was used to identify differences amongmeans.

3. Results

3.1. Eastern hemlock regeneration survey

Seedlings with Sirococcus shoot blight symptoms were present inmost (90%) of the 59 FIA plots surveyed (Table 1, Fig. 1). Animalbrowsing (63% plots) and “other” (54% plots) were the second andthird most common causes of damage to eastern hemlock regeneration(Table 1). Seedlings without damage were found in the majority of plots(58%) (Table 1), but absence of any damage to eastern hemlock seed-lings was recorded for only four plots (Fig. 1). Whereas animal damageand SSB were present throughout the region, EHS and HWA were foundin more southern areas (Fig. 1). Circular hemlock scale was only ob-served in one plot in Connecticut. For most seedlings affected by animalbrowsing, Sirococcus shoot blight, or hemlock-blueberry rust, damagewas limited to 1–10% of shoots (Table 2). In contrast, for most seedlingsaffected by EHS, HWA or circular hemlock scale, ≥11% of shoots weredamaged.

Damaging agents had a significant impact on seedling crown defo-liation (p=0.0179). For example, mean defoliation rating of seedlingsexhibiting damage only from Sirococcus shoot blight (1.41) was greaterthan the mean defoliation rating (0.97) of seedlings with no damage(p < 0.01, Table 3). In addition, defoliation was generally greaterwhen more than one damaging agent was present (Table 3). Althoughnot statistically significant due to small sample sizes, seedling crowndefoliation was less when both EHS and HWA were present togetherthan when either of these were present on their own, indicating a po-tentially antagonistic relationship between these two damaging agents(Table 3).

Table 3Effect of damaging agents on eastern hemlock seedling crown defoliation.

Damage type Mean defoliation rating (SE)a Plots (N)

“Hemlock wooly adelgid (HWA) & Sirococcus shoot blight (SSB) only” and “HWA & SSB & animal & other” 1.88 (0.31) ab** 7“Elongate hemlock scale (EHS) only” and “EHS & animal & other or SSB” 1.84 (0.40) ab* 4“Animal & SSB only” and “animal & SSB & other” 1.62 (0.17) a*** 24“Hemlock woolly adelgid (HWA) only” and “HWA & animal & other” 1.43 (0.31) ab 7“SSB only” and “SSB & other” 1.41 (0.14) ab** 45“EHS & HWA only” and “EHS & HWA & animal or other” 1.40 (0.33) ab 8“Animal only” and “animal & other” 1.34 (0.19) ab 18“Hemlock-blueberry rust & SSB only” and “rust & SSB & other” 1.07 (0.37) ab 4“No damage” and “other only” 0.97 (0.15) b 34

a Mean crown defoliation rating per plot (standard error). The following classes was used to rate the extent of the crown defoliation: 0= none, 1=1–10%,2=11–25%, 3=26–50%, 4= 51–75%, 5= 76–99%, 6= dead. Values with the same letter are not significantly different (α=0.05) by Tukey-Kramer multiplecomparisons posttests. Stars indicate values statistically significant in pair-wise comparisons from the “No damage” mean.* p < 0.05.** p < 0.01.*** p < 0.001.

Table 4Pearson correlation coefficients (r) and associated p-values (p) among standattributes and damage severity or defoliation (N=59 FIA plots).

Stand attributes Damage severitya,b,

Sirococcus EHS HWA Animal Defoliationb

Latitude r −0.037 −0.427 −0.446 0.023 −0.149p 0.781 0.001 <0.001 0.863 0.261

Slope r 0.142 0.186 0.073 −0.05 0.252p 0.282 0.159 0.585 0.704 0.054

Total basal area r −0.096 −0.19 −0.168 0.089 −0.275p 0.468 0.149 0.202 0.503 0.035

Percent hemlockbasal area

r 0.273 0.141 −0.007 −0.081 0.382

p 0.036 0.285 0.956 0.543 0.003Percent hemlock

seedlingsr 0.254 0.223 0.048 −0.245 0.216

p 0.052 0.089 0.719 0.062 0.101Hemlock

overstorytrees

r 0.148 0.035 −0.023 −0.111 0.351

p 0.262 0.793 0.863 0.402 0.006Percent overstory

hemlock treesr 0.381 0.208 0.052 −0.138 0.466

p 0.003 0.113 0.696 0.297 <0.001

a Severity is defined as the mean proportion of shoots affected by each da-maging agent for each seedling per plot.

b Severity and crown defoliation were assessed using a 0–6 rating scale.

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Several FIA stand attributes were correlated with severity ofSirococcus shoot blight and other damaging agents (Table 4). For ex-ample, percentage hemlock basal area, percentage hemlock seedlings(marginally significant), and percentage overstory hemlock trees werepositively correlated with Sirococcus shoot blight severity. These standattributes, excepting percentage hemlock seedlings, and including slopeand hemlock trees in the overstory were also correlated with hemlockseedling crown defoliation. Whereas latitude was not correlated withSirococcus shoot blight severity, it was negatively correlated with HWAand EHS severity as these exotic pests continue to expand their rangenorthwards. Longitude was only (marginally) associated with Sir-ococcus shoot blight severity because Sirococcus shoot blight severitytended to decrease westwards (r=−0.23, p=0.08). None of thecorrelations with other FIA stand attributes were significant (p > 0.1).

3.2. Confirmation of pathogen identity

Symptomatic shoots were collected from stands containing the 59FIA plots where eastern hemlock regeneration was surveyed, an

additional 7 FIA plots that did not have sufficient regeneration toconduct seedling surveys, and the Massabesic experimental forest(MEF). Symptomatic shoots collected after July, did not readily yieldconidia when incubated and yielded negative PCR results. Samplesfrom most locations (66% of 67 plots investigated) were PCR positivefor Sirococcus tsugae (Fig. 2). In contrast, S. conigenus was not found.Previously, S. tsugae had only been confirmed to occur in the North-eastern USA in Maine. The known geographic range in which this pa-thogen is causing damage to eastern hemlock regeneration is greatlyexpanded to include six additional states: Connecticut, Massachusetts,New Hampshire, New York, Rhode Island, and Vermont.

3.3. Long term monitoring

Mean seedling height in these plots was 84.33 cm (±4.98 SE) andmean diameter at base 1.14 cm (±0.03 SE). Year had a significanteffect on defoliation (p < 0.0001) as defoliation increased from 2011to 2013 (Fig. 3). The percentage of blighted shoots also increased overtime through the growing season and from 2011 to 2013 (Fig. 4). The

Fig. 2. Locations PCR-positive for Sirococcus tsugae.

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effects of year, date, and their interaction on the percentage of blightedshoots were significant (p < 0.0001). The mean proportion of symp-tomatic shoots per seedling in late July in 2011 was 16% compared to47% in 2013. Current year shoots became symptomatic by mid-June,their number peaking by mid-July. After mid-July, the number ofsymptomatic shoots did not change significantly within the same year.

4. Discussion

Sirococcus tsugae was the most widely distributed and frequentlyobserved damaging agent of eastern hemlock regeneration in this study,which is remarkable considering that eastern hemlock was only re-cently confirmed to be a host of this pathogen (Stanosz et al., 2011). Itis not known if S. tsugae is native to eastern USA, was introduced fromwestern North America, or originated elsewhere. To determine theorigin of this fungus, population genetic analyses should be conducted.Unfortunately, exotic forest pathogens can spread very quickly postintroduction. For example, the chestnut blight pathogen which is winddispersed, decimated chestnut populations within 40 years of its

introduction to North America in 1904 (Evans and Finkral, 2010). In2015, S. tsugae was reported for the first time on Atlantic cedar inBritain where both the host and the pathogen are exotic (Perez-Sierraet al., 2015). The pathogen is now widespread in the UK on severalconifer hosts and has also been reported in Germany (Perez-Sierra et al.,2016). It is possible that S. tsugae is native to eastern North America,but was only recently detected because of the increased attention thateastern hemlock has received due to the threat posed by hemlockwoolly adelgid (HWA) and elongate hemlock scale (EHS). A successionof unusually wet springs since 2006 (Wyka et al., 2017) could havefavored an expansion of the pathogen and outbreak of this disease inthe Northeast because spring rain would favor reproduction and dis-persal of S. tsugae. Other conifer needle diseases, such as needle blightand needle casts of eastern white pine (Pinus strobus) reached an epi-demic level during 2011–2013 (Wyka et al., 2017). Although Sir-ococcus shoot blight was common, damage was typically limited to10% or less of the shoots in most FIA plots. In permanent plots, how-ever, percent crown defoliation increased from category 1 (1–10%) tocategory 2 (11–25%) and percent shoot blight increased from 19% to47% from 2011 to 2013 indicating that in some locations the diseasemay be intensifying.

The second most common cause of damage to eastern hemlock re-generation was browsing by white-tailed deer or moose (Alces alces).Eastern hemlock is preferred winter food and habitat for white-taileddeer and is vulnerable to herbivory (Hosley and Ziebarth, 1935; Hough,1965; Eschtruth and Battles, 2008). Moose also utilize hemlock standsand browse on eastern hemlock regeneration (Faison et al., 2016).Eastern hemlock regeneration has been negatively impacted by in-creased white-tailed deer densities (Rooney et al., 2000; Horsley et al.,2003; Frerker et al., 2014; Faison et al., 2016; Frerker et al., 2017). Forexample, long-term studies confirm that deer herbivory greatly reducedtree regeneration, including hemlock, resulting in shifts in forest un-derstory cover and regeneration failures (Frerker et al., 2014). Therelationship between deer abundance and hemlock seedling cover isexponential meaning that impact per deer increases with increasingdeer density resulting in very reduced seedling hemlock cover(Eschtruth and Battles, 2008). To make matters worse, canopy declinerelated to hemlock woolly adelgid (HWA) may result in proportionallygreater herbivory impacts (Eschtruth and Battles, 2008).

While HWA and EHS were not as frequently encountered as un-gulate browsing or Sirococcus shoot blight in this study, they tended tocause more damage to affected seedlings. Cold winter temperatureslimit the distribution of HWA and EHS in the north although their rangecontinues to expand (Orwig et al., 2002; Preisser et al., 2008; Orwiget al., 2012; Gomez et al., 2015; Livingston et al., 2017; Schliep et al.,2018). These two insect pests are antagonistic to each other (Preisserand Elkinton, 2008), as HWA avoids settling on foliage previously co-lonized by EHS (Gomez et al., 2014; Gomez et al., 2015; Schaeffer et al.,2018). Indeed, in the current study, when these two insects co-occurredseedling crown defoliation was less than when they occurred on theirown. In contrast, when these occurred together with Sirococcus shootblight or animal damage, the effect on crown defoliation tended to beadditive. These relationships highlight the importance of consideringthe multiple impacts of native and invasive insects and diseases andother damaging agents such as white-tailed deer on each other and theirhosts (Eschtruth and Battles, 2008; Preisser and Elkinton, 2008).

Sirococcus shoot blight severity of eastern hemlock seedlings in thisstudy was positively correlated with percentage hemlock basal area,percentage hemlock seedlings, and percent hemlock overstory trees.This is in agreement with a previous report by Funk (1972), describinggreater disease frequency in suppressed or crowded western hemlocktrees. He attributed the relationship between disease severity andcrowding to low light intensity, a hypothesis that was supported bysuccessful disease development on western hemlock seedlings kept inthe dark for 4 days prior to inoculation. In addition to reducing light tofavor disease development, overstory trees are likely a source of

Year2011 2012 2013

Cro

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tego

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Fig. 3. Crown defoliation over time in seedlings with Sirococcus shoot blight inpermanent plots (N=5 plots, 20 seedlings per plot) at MassabesicExperimental Forest, Maine.

DateJune-20 July-7 July-23

Perc

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ge o

f blg

ihte

d sh

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Fig. 4. Disease progression over time of seedlings with Sirococcus shoot blightin permanent plots (N= 5 plots, 20 seedlings per plot) at MassabesicExperimental Forest, Maine.

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inoculum to understory seedlings. In Alaska, pre-commercial thinningsthat reduced tree densities in western hemlock stands also reducedseverity of Sirococcus shoot blight (Shaw et al., 1981). Reducing standdensity would have increased the spacing in the stand, both altering thedistance for inoculum to travel among hosts as well as increasing lightintensity. Thinning may also be an effective management strategy toreduce damage by HWA (Brantley et al., 2017). In greenhouse experi-ments, increasing light intensity resulted in reduced HWA densities andimproved eastern hemlock seedling growth (Hickin and Preisser, 2015;Brantley et al., 2017). Light intensity was also an important factor inanother pathogen of hemlock, laminated root rot (Phellinus weirii) ofwestern hemlock, as shading increased susceptibility of seedlings to thispathogen (Matson and Waring, 1984). Furthermore, eastern hemlockseedling abundance increases with increasing light intensity (Rooneyet al., 2000; D'Amato et al., 2009). Silvicultural treatments that wouldopen up the canopy increasing light intensity and scarifying the soilwould likely both favor the establishment of eastern hemlock re-generation and potentially reduce the negative impact of its damagingagents. Given the importance of eastern hemlock in eastern NorthAmerica, the limited success of biocontrol agents in reducing damageby HWA (Sumpter et al., 2018), and the ubiquitous presence of Sir-ococcus shoot blight, testing the effect of silvicultural treatments onSirococcus shoot blight and HWA severity would provide valuable in-formation for the restoration of this foundation species.

5. Conclusions

In this study we quantified the impact of Sirococcus shoot blight oneastern hemlock regeneration. Sirococcus shoot blight is widespreadand common in hemlock stands of the Northeastern US. Under somestand conditions, and particularly during extended years of wet springweather, hemlock shoot blight can result in significant damage toyoung, regenerating hemlock. In permanent plots, percentage of shootsand crown defoliation increased over time for eastern hemlock seed-lings with Sirococcus shoot blight. We identified stand characteristicswhich favor disease development and should be used to formulate in-itial silvicultural management. Sirococcus shoot blight severity wascorrelated with eastern hemlock basal area and proportion of overstoryhemlock trees suggesting that reducing hemlock basal area or hemlockdensity may reduce damage by Sirococcus shoot blight. Although, S.tsugae was the focal organism of our study, we also quantified the im-pact of other damaging agents such browsing by ungulates, nativediseases and insects, and exotic insect pests: hemlock woolly adelgidand elongate hemlock scale. Presence of more than one damaging agentgenerally had an additive effect on crown defoliation. Additional stu-dies are necessary to discern the geographic origin of Sirococcus tsugaeand implications of Sirococcus shoot blight damage to eastern hemlockregeneration.

Author contributions

IAM, WS, and WDO developed field methodology and conductedfield work. IAM and RSM analyzed data. DRS and GRS conducted labwork. IAM wrote the manuscript. All authors provided editorial advice.

Acknowledgements

This study was funded by USDA Forest Service grants 12-CA-11420004-210 and 12-DG-11420004-195. We are grateful for the co-operation Liz Burrill, Mariko Yamasaki and John Stanovick from theUSFS Northern Research Station for aid with FIA data, plot establish-ment at the Massabesic Experimental Forest, and statistical assistance,respectively. We would also like to thank Rebecca Lilja (USFS) for mapcreation and Justin Williams, Michael Simmons, Maria Vasta andEdward Jordan for field assistance. Thank you to the two anonymousreviewers who have improved the quality of the manuscript.

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