Northeastern Naturalist 188 Z.J. Delisle and T. Parshall 22001188 NORTHEASTERN NATURALIST 2V5(o2l). :2158,8 N–1o9. 62 The Effects of Oriental Bittersweet on Native Trees in a New England Floodplain Zackary J. Delisle1,* and Timothy Parshall2 Abstract – Celastrus orbiculatus (Oriental Bittersweet) is an invasive liana that can negatively affect native forests. Infested trees suffer trunk failures, and subsequent alterations in the surrounding forest’s natural successional trajectory frequently occur. We used a dendroecological approach to investigate the effects of Oriental Bittersweet on the growth of Populus grandidentata (Bigtooth Aspen) and Quercus rubra (Red Oak) in Chicopee, MA. We hypothesized that trees infested with Bittersweet would have reduced growth in comparison to uninfested trees. We sampled 136 trees that were infested or uninfested with Oriental Bittersweet and took cross sections of the liana stems to pinpoint the liana’s date of establishment. We found that Oriental Bittersweet had an abrupt negative effect on tree growth after 14 years of infestation, suggesting that a physical disturbance was likely a causal factor. Introduction The bioeconomic cost of invasive species is at an all-time high, nearing $120 billion annually as of 2005 (Pimentel et al. 2005), and it is increasingly evident that the ecology of invasive species has taken increasing precedence within ecological, conservation, and restoration sciences. In forestry, invasive vine and liana ecology is of particular concern because of the direct effects many nonindigenous vines and lianas have on forests (Forseth and Innis 2004, McNab and Meeker 1987, Oliver 1996). Of these invasive vines and lianas, Celastrus orbiculatus Thunb. (Oriental Bittersweet; hereafter referred to as Bittersweet) is at the forefront. This liana has been invading northeastern forests since the 1860s (Del Tredici 2014) and it is now established in at least 33 states (Lynch 2009, Patterson 1974) and 16 national parks (Mehrhoff et al. 2003). Bittersweet has many negative effects on native trees. Individual lianas wrap around trees as they ascend the trunk, while subsequent radial growth of the trunk tightens the liana’s grasp causing girdling and host-stem deformity (Harrington et al. 2003). The aggressive phototactic growth of Bittersweet leads to quick canopy invasions (Ellsworth et al. 2004). Once in the canopy, the lianas can form a blanketlike cover that casts dense shade on the host’s foliage (Hutchinson 1992, McNab and Meeker 1987). This blanket-like cover also causes the host to be more susceptible to weather related damage such as windthrow and ice storms (McNab and Meeker 1987, Siccama et al. 1976). Eventually, the added weight can cause major limb breakage or even trunk failure (McNab and Meeker 1987). 1Department of Biological and Environmental Sciences, Texas A&M University, Commerce, TX 75428. 2Biology Department, Westfield State University, Westfield, MA 01086. *Corresponding author - zdelisle@leomail.tamuc.edu. Manuscript Editor: Thomas Philbrick Northeastern Naturalist Vol. 25, No. 2 Z.J. Delisle and T. Parshall 2018 189 In the northeast, Bittersweet is closely associated with human-induced habitat fragmentation; thus, major travel corridors (e.g., highways, and railroads) are ideal dispersal avenues (Merriam 2003, Silveri et al. 2001). Road networks functioning as dispersal corridors could perpetuate future range expansions, and perhaps they already have because Bittersweet and other lianas are becoming more prevalent in North American ecosystems (Allen et al. 2007, Fikes and Niering 1999, Stewart et al. 2003). Within Bittersweet’s expanding range, the species usually colonizes forests after disturbances from windthrow, ice storms, or timber harvests (Harrington et al. 2003, McNab and Loftis 2002, Silveri et al. 2001). In these disturbed forests, Bittersweet infestations can substantially alter typical successional trajectories by causing a prolonged liana and shrub-dominated community, which ultimately increases liana cover, snags, shrub cover, and invasive flora (Fikes and Niering 1999). Northeastern floodplain forests are especially vulnerable to Bittersweet incursion because of annual flood disturbances, moist circumneutral soil, and high irradiance (Silveri et al. 2001). We employed a dendroecological approach to investigate how Bittersweet has influenced the growth of Populus grandidentata Michx. (Bigtooth Aspen) and Quercus rubra L. (Red Oak) by extracting increment cores, measuring annual growth rings, and dating cross sections of Bittersweet. Field-site Description Our study took place on a floodplain bordering the Connecticut River in Chicopee, MA, located between the north side of the mouth of the Chicopee River (42°08'54.8"N, 72°37'19.7"W), the public boat launch (42°09'10.3"N, 72°37'30.5"W), and the Chicopee Water Pollution-control Facility (42°09'10.1"N, 72°37'19.0"W). This site was used for agriculture from colonial times until the 1960s, at which time the property was purchased by the city of Chicopee to build the wastewater-treatment facility. Ever since the city’s purchase, natural reforestation has progressed on this land. Today, this site is primarily forested by Bigtooth Aspen and Red Oak, but Populus deltoids Bartr. (Cottonwood), Acer saccharinum L. (Silver Maple), and Catalpa speciosa (Warder) Warder ex Engelm. (Northern Catalpa) are also present. Invasive shrubs such as Rosa multiflora Thunb. (Multiflora Rose), Ligustrum obtusifolium Siebold and Zucc. (Border Privet), and Euonymus alatus (Thunb.) Siebold (Burning Bush) are also sparsely distributed here. We chose this site because of the wide range of Bittersweet infestation levels on Bigtooth Aspen and Red Oak (from 100% canopy coverage to none), with several trees already dead from Bittersweet-induced trunk failure. Methods Field sampling We followed Ingwell et al. (2010) and defined infested trees as having more than 75% of their canopies covered with Bittersweet and uninfested trees as having less than 25% of their canopies covered with Bittersweet. We sampled a total Northeastern Naturalist 190 Z.J. Delisle and T. Parshall 2018 Vol. 25, No. 2 of 136 canopy trees (Table 1). Canopy coverage was measured visually (Ingwell et al. 2010, Ladwig and Meiners 2009). We measured the diameter at breast height (DBH) for each tree at 1.3 m above the ground, and extracted a single increment core at this same height on the north side of every tree using an increment borer (4.3-mm core, 3-thread, 0.4572 m length; Haglöf, Sweden) (Speer 2010, Stokes and Smiley 1968). The intensity of environmental factors that drive tree growth (e.g., insolation, climate, hydrology, edaphic qualities, CO2) vary both spatially and temporally (Bowman et al. 2013); thus, we collected all tree cores, liana cross-sections, and dendrometric measurements during Spring 2016 within a relatively small area (6.23 ha). Data analysis We prepared tree cores and measured annual growth increments to an accuracy of 0.005 mm using a Velmex tree ring measuring system (Velmex Inc., Bloomfield, NY). Both authors cross checked core measurements. We determined establishment dates for Bittersweet around all infested trees by cutting cross sections at ground level from the largest lianas growing up a host tree and counting annual growth rings. We considered the age of the oldest individual liana found growing up a host tree to be the Bittersweet establishment date on that particular tree. We converted annual-ring increments to tree basal-area increments (BAI) using the standard formula: BAI = π (Rn 2 - Rn–1 2), where n is the year of growth and R is the tree’s radius (Wang et al. 2012). To assess whether Bittersweet had any impact on the growth of Bigtooth Aspen and Red Oak, we performed several statistical analyses. We used an independent 2-sample, 1-tailed t-test to determine if the infested-tree BAIs for the most recent 3 years (2016, 2015, and 2014) were less than those of uninfested trees. We used the Levene’s test via the car package in R v.3.3.1 (R Core Team 2016) to analyze homoscedasticity and dictate whether to use a Student’s t-test, which uses a pooled-variance method (assuming equal variances), or a Welch’s t-test, which approximates to the degrees of freedom (assuming unequal variances). We compared the total growth of the most recent 3 years because we assumed that the decline in growth only occurs if a tree is heavily infested (i.e., >75% canopy coverage). Bittersweet has extremely rapid growth rates (Ellsworth et al. 2004); therefore, we could not verify that currently infested trees were equally infested >3 years ago. There is an allometric relationship between a tree’s DBH and overall height, canopy dominance, and root coverage (Meyer 2011, Vadeboncoeur et al. 2007) therefore, we performed the same analysis within DBH subsets (≤25.0 cm, 25.1–34.9 cm, and ≥35.0 cm). This approach controls for other growth-inhibiting factors unrelated to Bittersweet. We performed an independent 2-sample, 1-tailed t-test between uninfested and infested BAIs for each individual year following Bittersweet establishment to assess when a Bittersweet-induced growth decline began in infested trees. We conducted all statistical analyses in R v.3.3.1 (R Core Team 2016). We performed numerous tests, which increases the risk of making a Type 1 error; thus, we set statistical significance at an alpha level of 0.01. Northeastern Naturalist Vol. 25, No. 2 Z.J. Delisle and T. Parshall 2018 191 Results Our increment cores indicated that most trees of both species at our study site were established in the late 1980s, with some of the older trees dating to the late 1970s (Table 1). The largest Bittersweet specimens indicated that the species was established in the late 1990s, with a mean establishment date of ~1997 and at least 1 individual was present as early as 1984 (Table 1). None of the tree species, infested or uninfested, had significantly different establishment dates (Kruskal–Wallis oneway nonparametric ANOVA: P = 0.3117), nor were the establishment dates of the Bittersweet growing around the 2 tree species significantly different (Student’s ttest: P = 0.5188; Table 1). The BAIs for the last 3 years were significantly greater for uninfested trees than for infested trees (Fig. 1) for both Bigtooth Aspen (Welch’s t-test: P < 0.0001) and Red Oak (Student’s t-test, P < 0.0001). The larger-DBH Red Oak subsets showed significance in this same comparison (25.1–34.9 cm Student’s t-test: P < 0.0001; >35.0 cm Welch’s t-test: P < 0.0001), while the smallest-DBH Red Oak subset did not show a significant difference (less than 25.0 cm Student’s t-test: P = 0.0919). All 3 Bigtooth Aspen DBH subsets showed a significant difference in this same comparison (less than 25.0 cm Welch’s t-test: P = 0.0099; 25.1–34.9 cm Welch’s t-test: P < 0.0001; >35.0 cm Student’s t-test: P = 0.0001). Figure 1. Mean BAI from 2014 to 2016 for infested and uninfested (A) Red Oak (Student’s t-test: P < 0.0001) and (B) Bigtooth Aspen (Welch’s t-test: P < 0.0001). Table 1. Establishment dates of all infested and uninfested Bigtooth Aspen, Red Oak, and the Bittersweet infesting both species. n Mean Min Max Bittersweet on Bigtooth Aspen 33 1997.4 1984 2007 Bittersweet on Red Oak 33 1998.1 1991 2007 Infested Bigtooth Aspen 33 1987.2 1978 2000 Infested Red Oak 33 1988.2 1979 2002 Uninfested Bigtooth Aspen 30 1986.1 1976 1992 Uninfested Red Oak 40 1988.9 1983 2002 Northeastern Naturalist 192 Z.J. Delisle and T. Parshall 2018 Vol. 25, No. 2 The BAIs of infested Red Oak trees were significantly less than those of uninfested trees in 2012 (Welch’s t-test: P = 0.0004), and in 2013 for Bigtooth Aspen (Welch’s t-test: P = 0.0018; Fig. 2). Preceding these years, the BAIs of infested trees were never significantly less than those of the uninfested trees. This initial significant BAI decline was sustained, at an alpha level of less than 0.01, in all of the following years for both species. Discussion Our results offer strong evidence that trees infested with Bittersweet for many years will experience growth declines not evident in simlar trees that are Figure 2. Annual mean BAI for (A) Bigtooth Aspen and (B) Red Oak immediately north of the Chicopee River mouth, Chicopee, MA. Dotted line indicates the mean year of establishment for Bittersweet. Stars indicate the year significant growth decline begins for each species (Red Oak 2012, Welch’s t-test: P = 0.0004; Bigtooth Aspen 2013, Welch’s t-test: P = 0.0018). Northeastern Naturalist Vol. 25, No. 2 Z.J. Delisle and T. Parshall 2018 193 uninfested. Nearly all of our tests documented a negative relationship between Bittersweet infestation and the growth of Red Oak and Bigtooth Aspen. Infested trees of both species had lower growth than uninfested trees (Fig. 1), and showed a growth decline that was not present in the chronology of uninfested trees (Fig. 2). Many studies have shown that Bittersweet colonizes forest sites after a disturbance event (e.g., Harrington et al. 2003, McNab and Loftis 2002, Silveri et al. 2001). Our results suggest that post-disturbance infestation might have occurred at our site. The average Bittersweet establishment date was 1997, a year during a period when the BAIs were increasing in most trees at this site (Fig. 2). This finding could be indicative of a disturbance within the forest that led to ideal growing conditions for Bigtooth Aspen and Red Oak. The same disturbance that caused this release response in Red Oak and Bigtooth Aspen likely provided the opportunity for Bittersweet establishment itself in the area. Horton and Francis (2014) found similar results; they concluded that Bittersweet was established after a disturbance that caused a release response in the surrounding forest. Release responses after disturbances are well documented in northeastern forests, and they are likely caused by the large influx in nutrients and irradiance just after a disturbance ( Canham 1988). The chronologies of our Red Oak and Bigtooth Aspen show that it took at least 14 y after the establishment of Bitterswet, for trees to show a significant decline in BAI (Fig. 2). Thus, it may take many years for a host tree to show distress after a Bittersweet invasion. This finding gives important insight to land managers who seek to eradicate Bittersweet. Forest management should include post-harvest control of Bittersweet. Eradicating Bittersweet is an extremely difficult, time consuming, and possibly expensive process. Mechanical cutting and herbicidal stump treatment is essential (Dreyer 1988, Lynch 2009); otherwise, prolific root suckering will be triggered and a strong growth response is inevitable (Dreyer 1994, Lynch 2009). However, the lengthy period required for Bittersweet to cause a growth decline gives valuable time for managers to take steps to control an infestation. In addition to the length of time it took for these trees to respond to Bittersweet infestation, the speed of decline in average BAI was rapid, over the course of just 1–2 y, suggesting that a physical disturbance was involved. Many individual trees even showed an abrupt and sustained growth decline in a single year (usually 2012 or 2013). There are 2 significant disturbances on record for the region that could be responsible: a tornado in the vicinity of the study site on 1 June 2011 and an unusually strong snowstorm on 7 November 2012. As demonstrated by our study, disturbances to forests lead to the spread of Bittersweet and growth declines in native trees. Seven of the infested trees that we sampled in this forest have already collapsed from the weight of their Bittersweet infestation, and it is probable that many of the other infested trees will also topple. The 7 trees that collapsed while we were sampling did so in only 2 small areas. These trees collapsing in close groups are most likely a function of a few different ecological processes. Bittersweet can spread across the canopy of several trees. In the case of 1 tree collapsing, inter-tree Bittersweet dispersal often causes multiple trees to be dragged down (Putz 1991). Large canopy gaps created by multiple trees Northeastern Naturalist 194 Z.J. Delisle and T. Parshall 2018 Vol. 25, No. 2 being uprooted could also lead to increased windthrow in the immediate area (Franklin and Forman 1987). Bittersweet-infested trees are extremely susceptible to windthrow, which can topple other nearby infested trees, leading to a perpetually increasing canopy gap. Increasingly large canopy gaps due to inter-tree Bittersweet dispersal and increased windthrow could lead to a completely new and unnatural landscape; converting a once forested floodplain into a vine-dominated community (e.g., Fikes and Niering 1999). Acknowledgments We thank Joseph Kietner, chief operator of the wastewater-treatment facility, for allowing us to sample trees on the property. This research was sparked by unpublished data collected from Cottonwood and Red Oak trees that were infested with Bittersweet in the Westfield State Experimental Forest. Literature Cited Allen, B.P., R.R. Sharitz, and P.C. Goebel. 2007. 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