Impact of Sirococcus shoot blight (Sirococcus tsugae) and other damaging agents on eastern hemlock (Tsuga canadensis) regeneration in Northeastern USA

Forest Ecology and Management 429 (2018) 449–456

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Impact of Sirococcus shoot blight (Sirococcus tsugae) and other damaging agents on eastern hemlock (Tsuga canadensis) regeneration in Northeastern USA

T

⁎

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

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

A R T I C LE I N FO

A B S T R A C T

Keywords: Invasive forest pests Forest pathogens Regeneration quality Tree disease development

In 2009, Sirococcus tsugae was first reported in Maine on eastern hemlock. Our goal was to quantify the impact of the 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 Inventory and 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 shoots blighted and percentage of crown defoliated) were assessed for 20 seedlings per plot. Sirococcus shoot blight symptoms were present in most plots (90%) and on most seedlings (72%). For the majority of seedlings, blight affected less than 10% of shoots, but the percentage of shoots blighted did range up to 75%. Similarly, needle loss was limited to less than 25% of the crown for most seedlings. Disease severity was positively correlated with overstory hemlock density. Using species-specific polymerase chain reaction (PCR) primers, Sirococcus tsugae was identified from samples collected in the majority of sites (68%) in New England and New York. In permanent plots at the Massabesic Experimental Forest in Maine, disease symptom severity increased from 16% blighted shoots in 2011 to 47% blighted shoots in 2013. Results confirm that Sirococcus shoot blight of eastern hemlock is more 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 Forest Service survey to assess hemlock woolly adelgid (Adelges tsugae) damage. In 2009, the presence of Sirococcus tsugae Rossman, Castl., D.F. Farr & Stanosz on blighted eastern hemlock shoots collected in Maine was confirmed based on morphology and DNA analyses (Miller-Weeks and Ostrofsky, 2010). This was the first time that S. tsugae was reported to damage eastern hemlock. In 2010, the identity of S. tsugae isolates from Georgia and their ability to cause disease on eastern hemlock was confirmed (Stanosz et al., 2011). That report also included results of a preliminary survey in Georgia which revealed that incidence of blighted shoots on individual trees varied, but was as high as 70%. Prior to these ⁎

reports, Sirococcus tsugae had only been reported on Atlas cedar (Cedrus atlantica), Himalayan cedar (C. deodora), western hemlock (Tsuga heterophylla), and mountain hemlock (Tsuga mertensiana) in western North America (Rossman et al., 2008). Since then, the distribution of S. tsugae in Northeastern USA, where eastern hemlock is valued, has remained unknown. Eastern hemlock is ecologically and economically important in the Northeast (Dukes et al., 2009). The range of eastern hemlock extends from southeastern Canada to Georgia and Alabama in the south and as far west as Minnesota. Eastern hemlock is considered a foundation species because it defines an ecological community, it is regionally common, locally abundant and creates stable conditions for many other species (Ellison et al., 2005). Currently, the eastern hemlock resource is threatened by exotic pests such as hemlock woolly adelgid and

Corresponding author. E-mail address: [email protected] (I.A. Munck).

https://doi.org/10.1016/j.foreco.2018.07.043 Received 29 June 2018; Received in revised form 23 July 2018; Accepted 25 July 2018 0378-1127/ Published by Elsevier B.V.

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elongated hemlock scale (Fiorinia externa) (Preisser et al., 2008; Evans et al., 2011; Orwig et al., 2012; Gomez et al., 2015; Case et al., 2017). Browsing by white-tailed deer (Odocoileus virginianus), which have increased in abundance in recent decades, also negatively impacts eastern hemlock regeneration (Eschtruth and Battles, 2008; Frerker et al., 2014; Faison et al., 2016). The impact of Sirococcus shoot blight (SSB) on the eastern hemlock resource, already at risk because of hemlock woolly adelgid (HWA), elongated hemlock scale (EHS), and white-tailed deer predation merits further investigation. There are several Sirococcus Preuss species that cause shoot blight to many conifer species causing damage to new shoots, seedlings and saplings (Nicholls and Robbins, 1984). Sirococcus shoot blight symptoms can become widespread and cause tree mortality under favorable weather conditions (Nicholls and Robbins, 1984). Growth reduction, crown deformation, and mortality attributed to the closely related species Sirococcus conigenus (Pers.) P.F. Cannon & Minter have been documented in young and mature Norway spruce (Picea abies) plantations in Europe (Halmschlager et al., 2000; Halmschlager and Katznsteiner, 2017) and red pine regeneration (Pinus resinosa) in the Great Lake States in the USA (Bronson and Stanosz, 2006; Ostry et al., 2012; Haugen and Ostry, 2013). In mature red pines, symptoms are more severe in the lower crown but can extend to the upper part causing poor crown condition (O'Brien, 1973). In southeastern Alaska, reduced height, terminal-leader kill and mortality of western hemlock regeneration were attributed to Sirococcus shoot blight, most likely caused by S. tsugae (Wicker et al., 1978; Shaw et al., 1981; Rossman et al., 2008). The etiology and epidemiology of S. tsugae on eastern hemlock, however, are not yet understood. The pathogen does not always form fruiting bodies on killed shoots, but other fungi do fruit on diseased shoots complicating disease diagnoses (Miller-Weeks and Ostrofsky, 2010). Therefore, it is important to verify the association of shoot blight symptoms with the pathogenic fungus S. tsugae. The goal of this project is to elucidate the many questions regarding Sirococcus shoot blight on eastern hemlock including its geographic range, symptomatology, etiology, and impact that this disease is having on eastern hemlock regeneration. The specific objectives are to: (i) delineate the geographic range of Sirococcus shoot blight in the Northeastern USA, (ii) verify the association of the pathogenic fungus S. tsugae with both shoot blight and needle loss, (iii) quantify impact of the disease and other damaging agents on eastern hemlock regeneration, and (iv) monitor changes in severity over time. Information pertaining to stand characteristics associated with disease incidence and severity are provided along with baseline data of current disease distribution. This information will help resource managers determine stand susceptibility and assess risk to regeneration activities in already at-risk hemlock forests.

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

Plots No. (%)

Seedlings No. (%)

Sirococcus shoot blight Animal Hemlock woolly adelgid Elongate hemlock scale Hemlock-blueberry rust Circular hemlock scale Other Not damaged

53 (90) 37 (63) 11 (19) 6 (10) 6 (10) 1 (2) 32 (54) 34 (58)

791 (72) 206 (19) 136 (12) 85 (8) 33 (3) 11 (1) 68 (6) 184 (17)

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 symptomatic: June through August of 2012 and June of 2013. We traveled to the center of the selected FIA plot with the aid of a GPS receiver (GPSmap 60CSx, Garmin International Inc., Olathe, KS, USA). At each FIA plot, 20 seedlings defined as hemlocks taller than 30 cm, but smaller than 2.54 cm in diameter at breast height (dbh, 1.3 m from the ground) were surveyed along transects or in quadrants. If available, five seedlings were surveyed in each cardinal direction (north, east, south and west) along transects 40 m long and 4 m wide. If not enough seedlings were present in one direction, additional seedlings were surveyed in the opposite direction. If not enough seedlings were present along transects, additional seedlings were surveyed in quadrants of a circular plot with a 40 m radius. The distance of the seedling farthest from plot center in each transect or quadrant was recorded. The extent of the crown that was defoliated was estimated for each seedling and recorded as: 0 = none, 1 = 1–10%, 2 = 11–25%, 3 = 26–50%, 4 = 51–75%, 5 = 76–99%, 6 = dead (Orwig and Foster, 1998). Severity of damage (defined as the percentage of shoots affected) attributable to each damaging agent, animal, SSB, HWA, EHS, hemlockblueberry rust (Naohidemyces vaccinia), circular hemlock scale (Nuculapsis tsugae), and other, also was estimated for each seedling and recorded using the same 0–6 classes. Sources of damage in the “other” category included: mechanical damage (dead tops or wounds), winter injury, mites (Oligonychus ununguis and Nalepella tsugifoliae), hemlock looper (Lambdina fiscellaria), and spittle bugs (Aphrophora spp.). 2.3. Confirmation of pathogen identity

2. Materials and methods Samples from each FIA plot were kept cool and shipped overnight to the University of Wisconsin-Madison. Eastern hemlock shoots with symptoms of Sirococcus shoot blight were incubated in moist chambers at room temperature for 2–10 days to allow development of pycnidia containing conidia, and single-conidial isolates were obtained. DNA was extracted from isolates grown in potato dextrose broth using a modified Dellaporta procedure (Smith and Stanosz, 1995). The DNA was amplified using the primer pair SirTf and SirTr2 and the amplification conditions described by Smith and Stanosz (2008) to confirm identity of isolates as S. tsugae. Any isolates with negative results for S. tsugae were further tested using the primer pair SirCf and SirCr to in an attempt to determine whether these might be the morphologically similar species S. conigenus. For a small number of shoots that did not yield conidia from which cultures could be obtained, a small piece of symptomatic stem and needle tissue was aseptically removed from the sample and placed in a microcentrifuge tube. The DNA was extracted by the modified Cubero procedure as published in Smith and Stanosz (2006). Testing for the

2.1. Site selection The Forest Inventory and Analysis (FIA) program of the U.S. Department of Agriculture, Forest Service, conducts an inventory of forest attributes across the country (Bechtold and Patterson, 2005). The FIA three-phase random sampling design is based on a tessellation of the United States into hexagons approximately 2428 ha in size with at least one permanent plot established in each hexagon. We used data from permanent plots established by FIA to locate survey sites. To facilitate access and ensure sampling success, we selected FIA plots in public lands with eastern hemlock regeneration and in close proximity to roads. For Maine and New York, we selected up to 20 FIA plots per state. We selected 20 additional FIA plots in the remaining New England states: Connecticut, Massachusetts, New Hampshire, Rhode Island, and Vermont. Within a state, we selected a maximum of three FIA plots per county. To obtain a wide geographic range, we selected FIA plots that met our criteria in the counties with most northern (Aroostook 450

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

presence of S. tsugae and S. conigenus DNA was done using the procedure in the previous paragraph.

Table 2 Percentages of eastern hemlock seedlings which exhibited damage by various agents, categorized by the percentage of shoots affected by those damaging agents. Damaging agent

Sirococcus shoot blight Animal Hemlock woolly adelgid Elongate hemlock scale Hemlock-blueberry rust Circular hemlock scale Other

2.4. Long term monitoring

Percentage of shoots affected 1–10

11–25

26–50

50–75

76–99

73 55 23 14 50 0 47

20 29 32 29 50 27 21

6 12 25 32 0 18 32

1 4 16 24 0 55 0

0 0 4 1 0 0 0

Five permanent plots were established in the USFS Massabesic Experimental Forest (MEF) during 2011. The MEF is located in York County, Maine on flat to gently rolling land up to 137 m above sea level with soils of glacial origin. Plots were established in stand (43.44755, −70.6815833333) with a mean basal area of 24.4 m2/ha. Eastern hemlocks comprised 30% of the basal area and had a mean dbh of 40 cm. White pines (Pinus strobus) comprised 70% of the basal area and had a mean dbh of 69 cm. Each plot center was marked with a metal stake and 20 seedlings per plot were tagged. Seedling height and diameter at base were measured. Seedlings in these plots exhibited symptoms of Sirococcus shoot blight, but were not infested by HWA or EHS. During three consecutive years, 2011–2013, extent of crown defoliation was estimated as described above for each seedling in July. To determine disease progression, the number of blighted shoots and total 451

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Table 3 Effect of damaging agents on eastern hemlock seedling crown defoliation. Mean defoliation rating (SE)a

Damage type “Hemlock wooly adelgid (HWA) & Sirococcus shoot blight (SSB) only” and “HWA & SSB & animal & other” “Elongate hemlock scale (EHS) only” and “EHS & animal & other or SSB” “Animal & SSB only” and “animal & SSB & other” “Hemlock woolly adelgid (HWA) only” and “HWA & animal & other” “SSB only” and “SSB & other” “EHS & HWA only” and “EHS & HWA & animal or other” “Animal only” and “animal & other” “Hemlock-blueberry rust & SSB only” and “rust & SSB & other” “No damage” and “other only”

1.88 1.84 1.62 1.43 1.41 1.40 1.34 1.07 0.97

(0.31) (0.40) (0.17) (0.31) (0.14) (0.33) (0.19) (0.37) (0.15)

**

ab ab* a*** ab ab** ab ab ab b

Plots (N) 7 4 24 7 45 8 18 4 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 multiple comparisons posttests. Stars indicate values statistically significant in pair-wise comparisons from the “No damage” mean. * p < 0.05. ** p < 0.01. *** p < 0.001.

a linear mixed model (PROC GLIMMIX) in SAS taking into account the repeated measures of “year” and the random “plot”. “Year” was a fixed effect, “plot” was a random factor, and the response variable was “mean crown defoliation per plot”. To account for the correlated errors between “years”, an autoregressive order 1 covariance structure was used. Similarly, to establish the effect of time on disease progression, data from permanent plots at the MEF were analyzed using a linear mixed model (PROC GLIMMIX) in SAS taking into account the repeated measures of “sampling date (year)” and the random plot. “Year” and “sampling date” were fixed effects, “plot” was random factor, and the response variable was “percentage of blighted shoots”. To account for the correlated errors between “sampling dates” within “years”, an autoregressive order 1 covariance structure was used. In both analyses above the Kenward-Rogers denominator degrees of freedom adjustment was used. For all models, when main effects were significant (α = 0.05), a Tukey-Kramer test was used to identify differences among means.

Table 4 Pearson correlation coefficients (r) and associated p-values (p) among stand attributes and damage severity or defoliation (N = 59 FIA plots). Damage severitya,b,

Stand attributes

Latitude Slope Total basal area Percent hemlock basal area Percent hemlock seedlings Hemlock overstory trees Percent overstory hemlock trees

Sirococcus

EHS

HWA

Animal

Defoliationb

r p r p r p r

−0.037 0.781 0.142 0.282 −0.096 0.468 0.273

−0.427 0.001 0.186 0.159 −0.19 0.149 0.141

−0.446 < 0.001 0.073 0.585 −0.168 0.202 −0.007

0.023 0.863 −0.05 0.704 0.089 0.503 −0.081

−0.149 0.261 0.252 0.054 −0.275 0.035 0.382

p r

0.036 0.254

0.285 0.223

0.956 0.048

0.543 −0.245

0.003 0.216

p r

0.052 0.148

0.089 0.035

0.719 −0.023

0.062 −0.111

0.101 0.351

p r

0.262 0.381

0.793 0.208

0.863 0.052

0.402 −0.138

0.006 0.466

p

0.003

0.113

0.696

0.297

< 0.001

3. Results 3.1. Eastern hemlock regeneration survey Seedlings with Sirococcus shoot blight symptoms were present in most (90%) of the 59 FIA plots surveyed (Table 1, Fig. 1). Animal browsing (63% plots) and “other” (54% plots) were the second and third 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 seedlings was recorded for only four plots (Fig. 1). Whereas animal damage and SSB were present throughout the region, EHS and HWA were found in more southern areas (Fig. 1). Circular hemlock scale was only observed in one plot in Connecticut. For most seedlings affected by animal browsing, Sirococcus shoot blight, or hemlock-blueberry rust, damage was limited to 1–10% of shoots (Table 2). In contrast, for most seedlings affected by EHS, HWA or circular hemlock scale, ≥11% of shoots were damaged. Damaging agents had a significant impact on seedling crown defoliation (p = 0.0179). For example, mean defoliation rating of seedlings exhibiting damage only from Sirococcus shoot blight (1.41) was greater than the mean defoliation rating (0.97) of seedlings with no damage (p < 0.01, Table 3). In addition, defoliation was generally greater when more than one damaging agent was present (Table 3). Although not statistically significant due to small sample sizes, seedling crown defoliation was less when both EHS and HWA were present together than when either of these were present on their own, indicating a potentially antagonistic relationship between these two damaging agents (Table 3).

a

Severity is defined as the mean proportion of shoots affected by each damaging agent for each seedling per plot. b Severity and crown defoliation were assessed using a 0–6 rating scale.

number of shoots for each seedling were counted three times from midJune 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 random factor, and the response variable was “mean crown defoliation for each damaging agent category per plot”. We used Pearson correlations to examine the relationship between FIA stand attributes (Bechtold and Patterson, 2005): longitude, latitude, slope, total basal area, hemlock basal area, percent hemlock basal area, hemlock seedlings, percent hemlock seedlings, hemlock overstory trees, percent hemlock overstory trees, elevation, seedling count, stand size, aspect, growing stock, all live stocking, and severity by each damaging agent per plot and crown defoliation per plot. Severity is defined as the proportion of shoots affected by each damaging agent. To ascertain the effect of time on crown defoliation, data from permanent plots at the MEF were analyzed using 452

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

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

Several FIA stand attributes were correlated with severity of Sirococcus shoot blight and other damaging agents (Table 4). For example, percentage hemlock basal area, percentage hemlock seedlings (marginally significant), and percentage overstory hemlock trees were positively correlated with Sirococcus shoot blight severity. These stand attributes, excepting percentage hemlock seedlings, and including slope and hemlock trees in the overstory were also correlated with hemlock seedling crown defoliation. Whereas latitude was not correlated with Sirococcus shoot blight severity, it was negatively correlated with HWA and EHS severity as these exotic pests continue to expand their range northwards. Longitude was only (marginally) associated with Sirococcus shoot blight severity because Sirococcus shoot blight severity tended to decrease westwards (r = −0.23, p = 0.08). None of the correlations with other FIA stand attributes were significant (p > 0.1).

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

3.2. Confirmation of pathogen identity Symptomatic shoots were collected from stands containing the 59 FIA plots where eastern hemlock regeneration was surveyed, an 453

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Crown defoliation category (% )

26-50

introduction to North America in 1904 (Evans and Finkral, 2010). In 2015, S. tsugae was reported for the first time on Atlantic cedar in Britain where both the host and the pathogen are exotic (Perez-Sierra et al., 2015). The pathogen is now widespread in the UK on several conifer 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 that eastern hemlock has received due to the threat posed by hemlock woolly adelgid (HWA) and elongate hemlock scale (EHS). A succession of unusually wet springs since 2006 (Wyka et al., 2017) could have favored an expansion of the pathogen and outbreak of this disease in the Northeast because spring rain would favor reproduction and dispersal of S. tsugae. Other conifer needle diseases, such as needle blight and needle casts of eastern white pine (Pinus strobus) reached an epidemic level during 2011–2013 (Wyka et al., 2017). Although Sirococcus shoot blight was common, damage was typically limited to 10% or less of the shoots in most FIA plots. In permanent plots, however, percent crown defoliation increased from category 1 (1–10%) to category 2 (11–25%) and percent shoot blight increased from 19% to 47% from 2011 to 2013 indicating that in some locations the disease may be intensifying. The second most common cause of damage to eastern hemlock regeneration was browsing by white-tailed deer or moose (Alces alces). Eastern hemlock is preferred winter food and habitat for white-tailed deer and is vulnerable to herbivory (Hosley and Ziebarth, 1935; Hough, 1965; Eschtruth and Battles, 2008). Moose also utilize hemlock stands and browse on eastern hemlock regeneration (Faison et al., 2016). Eastern hemlock regeneration has been negatively impacted by increased white-tailed deer densities (Rooney et al., 2000; Horsley et al., 2003; Frerker et al., 2014; Faison et al., 2016; Frerker et al., 2017). For example, long-term studies confirm that deer herbivory greatly reduced tree regeneration, including hemlock, resulting in shifts in forest understory cover and regeneration failures (Frerker et al., 2014). The relationship between deer abundance and hemlock seedling cover is exponential meaning that impact per deer increases with increasing deer density resulting in very reduced seedling hemlock cover (Eschtruth and Battles, 2008). To make matters worse, canopy decline related to hemlock woolly adelgid (HWA) may result in proportionally greater herbivory impacts (Eschtruth and Battles, 2008). While HWA and EHS were not as frequently encountered as ungulate browsing or Sirococcus shoot blight in this study, they tended to cause more damage to affected seedlings. Cold winter temperatures limit the distribution of HWA and EHS in the north although their range continues to expand (Orwig et al., 2002; Preisser et al., 2008; Orwig et al., 2012; Gomez et al., 2015; Livingston et al., 2017; Schliep et al., 2018). These two insect pests are antagonistic to each other (Preisser and Elkinton, 2008), as HWA avoids settling on foliage previously colonized by EHS (Gomez et al., 2014; Gomez et al., 2015; Schaeffer et al., 2018). Indeed, in the current study, when these two insects co-occurred seedling crown defoliation was less than when they occurred on their own. In contrast, when these occurred together with Sirococcus shoot blight or animal damage, the effect on crown defoliation tended to be additive. These relationships highlight the importance of considering the multiple impacts of native and invasive insects and diseases and other damaging agents such as white-tailed deer on each other and their hosts (Eschtruth and Battles, 2008; Preisser and Elkinton, 2008). Sirococcus shoot blight severity of eastern hemlock seedlings in this study 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), describing greater disease frequency in suppressed or crowded western hemlock trees. He attributed the relationship between disease severity and crowding to low light intensity, a hypothesis that was supported by successful disease development on western hemlock seedlings kept in the dark for 4 days prior to inoculation. In addition to reducing light to favor disease development, overstory trees are likely a source of

A 11-25 B C 1-10

2011

2012

2013

Year

Percentage of blgihted shoots (%)

Fig. 3. Crown defoliation over time in seedlings with Sirococcus shoot blight in permanent plots (N = 5 plots, 20 seedlings per plot) at Massabesic Experimental Forest, Maine. 60 2011 2013

50

A

A

40 30 B

20

B B

10 C

0 June-20

July-7

July-23

Date Fig. 4. Disease progression over time of seedlings with Sirococcus shoot blight in permanent plots (N = 5 plots, 20 seedlings per plot) at Massabesic Experimental Forest, Maine.

effects of year, date, and their interaction on the percentage of blighted shoots were significant (p < 0.0001). The mean proportion of symptomatic shoots per seedling in late July in 2011 was 16% compared to 47% in 2013. Current year shoots became symptomatic by mid-June, their number peaking by mid-July. After mid-July, the number of symptomatic shoots did not change significantly within the same year.

4. Discussion Sirococcus tsugae was the most widely distributed and frequently observed damaging agent of eastern hemlock regeneration in this study, which is remarkable considering that eastern hemlock was only recently confirmed to be a host of this pathogen (Stanosz et al., 2011). It is not known if S. tsugae is native to eastern USA, was introduced from western North America, or originated elsewhere. To determine the origin of this fungus, population genetic analyses should be conducted. Unfortunately, exotic forest pathogens can spread very quickly post introduction. For example, the chestnut blight pathogen which is wind dispersed, decimated chestnut populations within 40 years of its 454

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References

inoculum to understory seedlings. In Alaska, pre-commercial thinnings that reduced tree densities in western hemlock stands also reduced severity of Sirococcus shoot blight (Shaw et al., 1981). Reducing stand density would have increased the spacing in the stand, both altering the distance for inoculum to travel among hosts as well as increasing light intensity. Thinning may also be an effective management strategy to reduce damage by HWA (Brantley et al., 2017). In greenhouse experiments, increasing light intensity resulted in reduced HWA densities and improved eastern hemlock seedling growth (Hickin and Preisser, 2015; Brantley et al., 2017). Light intensity was also an important factor in another pathogen of hemlock, laminated root rot (Phellinus weirii) of western hemlock, as shading increased susceptibility of seedlings to this pathogen (Matson and Waring, 1984). Furthermore, eastern hemlock seedling abundance increases with increasing light intensity (Rooney et al., 2000; D'Amato et al., 2009). Silvicultural treatments that would open up the canopy increasing light intensity and scarifying the soil would likely both favor the establishment of eastern hemlock regeneration and potentially reduce the negative impact of its damaging agents. Given the importance of eastern hemlock in eastern North America, the limited success of biocontrol agents in reducing damage by HWA (Sumpter et al., 2018), and the ubiquitous presence of Sirococcus shoot blight, testing the effect of silvicultural treatments on Sirococcus shoot blight and HWA severity would provide valuable information for the restoration of this foundation species.

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5. Conclusions In this study we quantified the impact of Sirococcus shoot blight on eastern hemlock regeneration. Sirococcus shoot blight is widespread and common in hemlock stands of the Northeastern US. Under some stand conditions, and particularly during extended years of wet spring weather, hemlock shoot blight can result in significant damage to young, regenerating hemlock. In permanent plots, percentage of shoots and crown defoliation increased over time for eastern hemlock seedlings with Sirococcus shoot blight. We identified stand characteristics which favor disease development and should be used to formulate initial silvicultural management. Sirococcus shoot blight severity was correlated with eastern hemlock basal area and proportion of overstory hemlock trees suggesting that reducing hemlock basal area or hemlock density may reduce damage by Sirococcus shoot blight. Although, S. tsugae was the focal organism of our study, we also quantified the impact of other damaging agents such browsing by ungulates, native diseases and insects, and exotic insect pests: hemlock woolly adelgid and elongate hemlock scale. Presence of more than one damaging agent generally had an additive effect on crown defoliation. Additional studies are necessary to discern the geographic origin of Sirococcus tsugae and implications of Sirococcus shoot blight damage to eastern hemlock regeneration. Author contributions IAM, WS, and WDO developed field methodology and conducted field work. IAM and RSM analyzed data. DRS and GRS conducted lab work. IAM wrote the manuscript. All authors provided editorial advice. Acknowledgements This study was funded by USDA Forest Service grants 12-CA11420004-210 and 12-DG-11420004-195. We are grateful for the cooperation Liz Burrill, Mariko Yamasaki and John Stanovick from the USFS Northern Research Station for aid with FIA data, plot establishment at the Massabesic Experimental Forest, and statistical assistance, respectively. We would also like to thank Rebecca Lilja (USFS) for map creation and Justin Williams, Michael Simmons, Maria Vasta and Edward Jordan for field assistance. Thank you to the two anonymous reviewers who have improved the quality of the manuscript. 455

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