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Tales From the Blackgum, a Consummate Subordinate Tree

April 19, 2007

By Abrams, Marc D

No species in the eastern United States better exemplifies a ubiquitous yet subordinate tree than does blackgum (Nyssa sylvatica). What enables blackgum to grow nearly everywhere, but almost always at very low densities? It is the longest-lived hardwood species in the eastern United States, with a maximum age that can exceed 650 years. It is inherently slow growing, which most likely explains its great longevity and high shade tolerance; it is also one of the few tree species that are fire resistant as well as shade tolerant. Blackgum can grow in bottomlands or at xeric sites, being tolerant of both flooding and drought. Despite these ecologically beneficial attributes-and the fact that early loggers systematically avoided blackgum because of its tendency to rot-this slow-growing tree is rarely dominant. Blackgum has so far simply persisted as a marginal species. The future of blackgum is uncertain, however, because of the opposing forces of global warming and increased competition from other tree species. This article synthesizes a broad range of ecological studies that relate to the unique behavior of blackgum as a consummate subordinate, something that is poorly understood for this and other similar species in the ecology literature.

Keywords: Nyssa sylvatica, land-use history, witness trees, forest geography, ecophysiology

In many respects, blackgum (Nyssa sylvatica) is enigmatic, and it is certainly unique among eastern US hardwood species. It has a large range and can grow on almost any type of site in the eastern forests (Burns and Honkala 1990, Iverson et al. 1999). Despite its ecological breadth, blackgum almost never obtains overstory dominance, typically representing just 1 % or 2% of the canopy trees. It is the longest-lived hardwood species in the eastern United States, and probably ranks among the longest-lived hardwoods anywhere in the world; The oldest known blackgum tree is 679 years old (Sperduto et al. 2000), and blackgum ages of 450 to 550 years are not unusual. Blackgum often grows in swamps and floodplains, but it also occupies extremely droughty sites (Barnes 1991). It grows best on nutrient-rich sites, but obtains greater importance on nutrient-poor, xeric, and hydric sites. Btackgum is one of the few tree species that combine shade tolerance, drought tolerance, and fire resistance (Harmon 1984, Burns and Honkala 1990). Moreover, it is late successional but can invade disturbed areas such as old fields, burned areas, and mine spoils (Burns and Honkala 1990). If it does so many things so well, why doesn’t it dominate the vast majority of the eastern US forests?

The purpose of this article is to synthesize current scientific knowledge concerning the historical development, present distribution, stand dynamics, growth, and ecophysiological attributes of blackgum to explain why it is relegated to a subordinate status in most forests. This is something that is poorly understood for many marginal temperate tree species in the ecological literature, of which there are many, but none so ubiquitous as blackgum. I will explore studies of paleoecology, land- use history, witness tree distribution from early land surveys, forest and physical geography, dendroecology, fire effects, and ecophysiology to investigate major ecological and environmental changes as they relate to the past and present distribution of blackgum in the eastern United States. I will also examine the potential of blackgum in the current milieu of fire suppression, limited timber cutting, and global change processes. My main objective is to address the following questions:

* What were the distribution and frequency of blackgum in North American forests before European settlement, and what are they in present-day forests?

* What impact did early Euro-American land-use practices have on the frequency and ecological dynamics of blackgum?

* What are the ecophysiological, growth, and life history attributes of blackgum as they relate to being a consummate subordinate tree species?

* What impacts will current and future environmental conditions and management practices have on blackgum dominance and distribution in eastern forests?

Blackgum classification and distribution

Blackgum is widely distributed in the forests of the eastern United States, with a range bounded by southeastern Maine, southeastern Wisconsin, eastern Texas, and Florida (figure 1; Little 1971). Blackgum ranks 15th among 80 common tree species in the eastern United States in the amount of forest area occupied, according to the USDA (US Department of Agriculture) Forest Inventory Analysis (Iverson et al. 1999). Fernald (1950) recognized three principal varieties within the species N. sylvatica (excluding var. dilatata). N. sylvatica van caroliniana is a typically upland blackgum ranging from northern Pennsylvania south to Florida and west to eastern Texas. Fernald’s N. sylvatica var. biflora grows mainly in coastal plain swamps in the Southeast. N, sylvatica var, sylvatica is found in swamps of the Northeast, extending into wetlands of the upper South. However, recent literature recognizes two distinct species (N. sylvatica and Nyssa biflora) among these three varieties, and they will be treated as such for the purposes of this review (Burckhalter 1992). JV. sylvatica combines the varieties sylvatica and carolinina, whereas the variety biflora is now the species N. biflora.

Figure 1. Range map for blackgum (Nyssa sylvaticaj in the eastern United States (adapted front Little 1971).

Blackgum (N. sylvatica) is widely distributed in upland sites across its entire range and in bottomland sites in the Northeast and upper South, whereas swamp tupelo (N. biflora) grows mainly in swamps and estuaries of the coastal plain in the mid-Atlantic and southern states. Swamp tupelo also grows along the Mississippi River and can be found as far north as Illinois. Three other Nyssa species are found in southern forests. Water tupelo (Nyssa aquatica) grows in swamps and floodplains along the Atlantic and Gulf coastal plain and along the Mississippi River up to southern Illinois {Burns and Honkala 1990, Burckhalter 1992). Ogeechee tupelo (Nyssa ogeche) is a small, scarce tree that grows in swamps and along rivers on the southern coastal plain from South Carolina through northern Florida (Burns and Honkala 1990). Finally, bear tupelo (Nyssa ursma) is a shrub or small tree that grows on wet flatwoods and savanna sites and occurs in only six counties in the Apalachicola region of the eastern panhandle of Florida (Burckhalter 1992). In the southeastern evergreen forest region, water tupelo and swamp tupelo are well represented in swamps, bottomland, and floodplains, whereas blackgum occurs mainly in upland forests (Braun 1950, Barnes 1991). In the northern mid-Atlantic and New England, outside the range of water tupelo and swamp tupelo, blackgum occurs in both swamps and uplands. Indeed, blackgum reaches its highest importance values (a measure of the relative frequency, density, and dominance of a species) and ages in the swamps of New England (Sperduto et al. 2000).

Blackgum is a component of 35 forest cover types, but it is not a dominant species in any of them (Burns and Honkala 1990). These types include a remarkable breadth of ecological conditions, encompassing xeric post oak-blackjack, bear oak, and chestnut oak; mesophytic tulip poplar, red oak, and white oak; and swamp types dominated by Atlantic white cedar, pond cypress, and swamp chestnut oak. Blackgum reaches its best development on well-drained, light- textured soils; alluvial stream bottoms; and loamy lower slopes and coves (Burns and Honkala 1990).

Paleoecological evidence of blackgum

Blackgum has a very long history in the eastern United States, dating back to the early part of the Holocene epoch and beyond. In Tennessee and Kentucky, Nyssa pollen in bogs and lake sediment dates to about 8400 years before the present (Delcourt et al. 1983). In a lake in northwestern Florida, Nyssa pollen existed as far back as 33,000 years ago (Watts et al. 1992). Low levels of Nyssa pollen dating back 4000 to 10,000 years were recorded on nearly all sites across 11 bogs and lakes in central Appalachia and the New Iersey coastal plain (Watts 1980). In the Hudson Highlands of eastern New York, Nyssa pollen dates back about 7000 years (Maenza-Gmelch 1997). At Harvard Forest in central Massachusetts, Nyssa dates back to approximately 8000 years before the present (Foster and Zebryk 1993). On Martha’s Vineyard, an island in Massachusetts, Nyssa pollen in bogs on glacial moraines dates back 2400 years ago, with a modest increase in the amount deposited in the last 300 years associated with European settlement (Foster et al. 2002); blackgum typically grew there in mature mesic forests with a low incidence of fire. In all of these studies, the amount of blackgum pollen was very low relative to that of the regional dominants, oak and pine.

Blackgum in the presetttement forest

Early land surveyors in the eastern United States notched or otherwise marked “witness trees” to identify property corners and other boundaries (Whitney 1982, Black and Abrams 2001); they were required to note the species of the witness trees in the survey records. For many areas, witness trees constitute the only quantitative information on forest composition before Europ\ean settlement. Despite some potential biases in tree selection and landforms by the surveyors, witness tree data represent an invaluable historical resource concerning species abundance in the early forest (Black and Abrams 2001).

Before European settlement, blackgum occurred at low density in forests throughout much of the eastern United States (table 1). Blackgum represented less than 1% of the witness trees in the original hardwood and conifer forests of southern and central New England and eastern New York (Cogbill et al. 2002), and only 1% of the original forests of northern New Jersey (Russell 1981). Small amounts of blackgum were recorded in coves in the forests of northern and central Pennsylvania (Abrams and Ruffher 1995). Physiographic and parent-material analyses indicate that blackgum witness trees were broadly distributed across 10 different site types in southeast Pennsylvania, but their frequency never exceeded 2.5% (Black and Abrams 2001).

In eastern West Virginia, blackgum represented 1% to 2% of the witness trees across ridges, side slopes, and cove forests in the Ridge and Valley physiographic province, and 1% to 4% of trees in northwest-facing slopes and cove forests in the Allegheny Mountains (table 1; Abrams et al. 1995, Abrams and McCay 1996). Occasional blackgum trees were recorded in 18th-century surveys for the Piedmont and coastal plain forests of northern Virginia (Orwigand Abrams 1994a). On the Allegheny Plateau of northeastern Ohio, blackgum made up 2% to 3% of the presettlement oak-hickory forest types on coarse-textured till and residual soils, but did not occur on fine-textured, glaciated soils that supported beech-maple forests (Whitney 1982). Blackgum accounted for 2.4% of the composition of the original forests, dominated by white oak, beech, and sugar maple, in the Bluegrass region of north-central Kentucky (Campbell 1989). In southern Illinois, blackgum represented 1% to 3% of the witness trees across sites ranging from ridgetops to north- and south-facing upper and lower slopes to stream terraces (Fralish et al. 1991).

Blackgum witness trees had a relative density of 3% to 10% in floodplain and bottomland forests and of 1% or less in upland forests of north-central Florida (table 1; Delcourt and Delcourt 1977). Blackgum represented less than 1% of the presettlement forests of northern Florida, and was typically found on well- drained, rich soils (Schwartz 1994). Blackgum averaged 1 % of the witness trees across a range of sites in the presettlement Piedmont forests of central Georgia, but had a maximum representation of 3% on floodplains, north-facing lower slopes, and cove forests (Cowell 1995). Blackgum represented 1% to 2.6% of the original pine-oak- hickory and mixed-mesophytic forests in east-central Alabama (Black et al. 2002). In the upland forests of northern Mississippi, blackgum represented about 1% of the witness trees on upland sites dominated by mixed-oak species and 0% to 5% on lowland sites dominated by holly, beech, maple, and white oak (Brewer 2001). In the presettlement forests on the Gulf Coastal Plain of southeastern Texas, blackgum occurred at densities ranging from less than 1% to 5% in upland pine and oak forests, but from 7% to 19% in moist stream floodplains and swamps (Schafale and Harcombe 1983). Indeed, Schafale and Harcombe (1983) designated a blackgum-sweetgum forest type in swampy areas intermixed with better-drained pine-oak forests.

Table 1. Percentage of witness tree species in forests within the range of blackgum in the eastern United States before European settlement.

These studies suggest that blackgum was widely distributed throughout its range in the pre-European settlement forest, but typically represented only 1 % to 2% of the composition of most forests. The few examples of higher blackgum density occurred in floodplain, bottomland, and swamp forests in the southern coastal plain. However, much of the Nyssa found in southern swamps and bottomland included N. biflora and N. aquatka, rather than strictly N. sylvatica. Blackgum probably occurred at high levels in certain swamps and bogs in the northern mid-Atlantic and New England states (outside the range of N. biflora and N. aquatica), but early surveyors typically avoided such sites, so very few witness tree data exist (Black and Abrams 2001).

Blackgum distribution and physiography in present-day forests

Braun (1950) noted that blackgum occurred in a large proportion of stands in the mixed-mesophytic and oak-chestnut forests of the central and southern Appalachians, but was never abundant. Over 50 years later, this review of the forest ecology literature generally supports this conclusion. An analysis of 707 oak-, chestnut-, and hickory-dominated forests, from 32 states in the eastern United States, reported that the genus Nyssn was a first-ranked species in only 3 forests and a third-ranked species in 7 forests (Monk et al, 1990). Blackgum occurred mainly in the southern mixed hardwoods with white oak and beech, where it had an average importance value of 3%. In all other oak community types, its importance value was less than 3%. In the USDA Forest Inventory Analysis, blackgum had an average importance value of 2.6% and ranked 44th among 80 common tree species (Iverson et al. 1999), Relative importance values of 5% to 10% in that study were noted in small areas of Virginia, Tennessee, and Alabama.

In southern and eastern New England, blackgum is an occasional tree found across a range of wet to dry habitats. In New Hampshire, the overstory cover of blackgum ranges from 10% to more than 40% in blackgum-red maple basin swamps (Sperduto et al. 2000). On Cape Cod, in eastern Massachusetts, blackgum occurred in 5% to 31% of the sample plots in upland oak, pine, and maple forests, but had relatively low cover in each (Motzkin et al. 2002). Blackgum had a relative importance value of 8% in a xeric, old-growth, pitch pine rock-outcrop forest in the Shawangunk Mountains of New York (Abrams and Orwig 1995). In the coastal forests of Long Island, New York, blackgum had importance values of 0% to 10%, with its highest importance on the wettest extremes of the moisture gradient (Clark 1986). Blackgum became established in some forests after the hurricane that leveled forests in eastern New York in 1938 and after a fire in 1964, and was also invading old fields (Clark 1986).

Across the entire state of Pennsylvania, blackgum represents 1.6% of all trees greater than 5 inches (12.7 centimeters) in diameter (Iverson et al. 1999). Throughout the state of Maryland, blackgum is broadly distributed and a component of the following forest types: bald cypress association on riparian sites, river birch-sycamore association on bottomland sites, chestnut oak association on dry ridges, and basket oak-willow oak-loblolly pine and tulip poplar associations on the coastal plain and floodplains (Brush et al. 1980). Blackgum trees had 4% to 6% relative importance in mature pine, oak, and mixed-hardwood forests across 58 forest stands on welldrained, sandy loam soils of the coastal plain and Piedmont in northern Virginia (Orwig and Abrams 1994a). Blackgum had an average importance value of 3.4% (range = 0% to 23%) in 14 bottomland hardwood forests in the Virginia coastal plain (Parsons and Ware 1982); blackgum had its highest importance (8.5% to 23%) in the ones that experienced more frequent flooding and had higher soil moisture and higher levels of calcium and nitrogen.

In the Piedmont of North Carolina, blackgum was the 11th-ranked dominant, behind three oak species, four hickory species, dogwood, red maple, and black cherry (Peet and Christensen 1980). In the Great Smoky Mountains, blackgum was broadly distributed but a minor component (1% to 3%) of most hardwood and pine forests (Whittaker 1956). It reached its maximum distribution (10% to 16% of composition) in subxeric and xeric forests dominated by chestnut oak and table mountain pine, respectively. Blackgum exhibited very little potential, compared with chestnut oak, red oak, and red maple, to capture overstory gaps created by chestnut mortality following the chestnut blight in the early 1900s. In an old-growth southern mixed-hardwood forest dominated by magnolia, beech, and sweetgum in northern Florida, blackgum represented 7.5% of basal area and 10% of the overstory tree density (Batista and Platt 2003); over a 14-year period, blackgum exhibited low tree recruitment, low radial growth rate, and low mortality, and was characterized as being persistent and resistant to the impacts of a major hurricane.

Dendroecotogy of blackgum

The use of tree rings provides a highly accurate method for dating species recruitment and assessing the magnitude and frequency of disturbance events and climatic impacts on tree growth. This section will explore four dendroecological examples of forests with a significant blackgum component.

Dendroecotogy of an old-growth, rettct bogforesL A 440-year dendroecological history was conducted for Bear Meadows, an old- growth, relict bog forest in the Ridge and Valley province of central Pennsylvania (figure 2; Abrams et al. 2001). The forest is dominated by eastern hemlock (49% relative importance value), black spruce (16%), red maple (15%), yellow birch (9%), and blackgum (5%). Four blackgum trees were older than 400 years (441-year maximum), and another five were over 300 years old (figure 3). Many blackgum and hemlock trees recruited from the years 1560 and 1700, respectively, until 1890. However, the majority of the other trees, including black spruce, balsam fir, red maple, white pine, and yellow birch, recruited during a 40-year period following selective logging of the forest in the 1890s and fires in 1900 and 1914. These events also promoted a large amount of recruitment for hemlock, but not for blackgum. Blackgum is rare in its inability to recruit in large numbers following major d\isturbance events, even for a late- successional tree species.

Figure 2. Blackgum (central and left trees in foreground) and hemlock (right tree in foreground) growing on an organic peat soil at Bear Meadows Natural Area, a bog in central Pennsylvania. The bark pattern is highly characteristic ofblackgum, with variable knobby and smooth light gray patterns on the lower trunk. Photograph: Marc D, Abrams.

Figure 3. Age-diameter relationship for all cored trees (top panel) and mean standardized ring-width index (lower panel) for the 20 oldest blackgum trees at the Bear Meadows Natural Area in central Pennsylvania (adapted from Abrams et al 2001).

Master tree-ring chronologies-sets of ring-width sequences corresponding to known conditions and dates-revealed a large increase in ring width (and thus growth) associated with logging in 1888 (figure 3). Marked decreases in growth occurred after the 1900 fire, and to a lesser extent after the 1914 fire. Significant increases in tree-ring growth also occurred before European settlement, indicative of major or moderate standwide disturbance events. Representative cores of blackgum and hemlock illustrate the variation in growth patterns and frequency of tree ring release dates from major and moderate disturbances (figure 4). Blackgum exhibited fairly constant, low radial growth, averaging about 0.5 millimeters (mm) per year. Even when released as a result of a disturbance event, radia) growth of blackgum increased only to a maximum of about 1.0 mm per year. In contrast, hemlock typically had a higher average growth rate, 1.3 mm per year, and growth variation between 0.3 and 4.0 mm per year. Core analysis showed that over time blackgum averaged 130 years with a growth rate of less than 0.5 mm per year, compared with only 35 years at that growth rate for hemlock. Both species exhibited a large number of release events over the last 250 to 400 years, with hemlock having a greater number of major releases and blackgum having a greater number of moderate releases. The longest duration between tree-ring releases before reaching an upper canopy position was 142 years for blackgum, compared with 50 years for hemlock. This suggests that blackgum may be even more shade tolerant than hemlock and can persist with highly suppressed growth for longer periods in mature forests between release events.

Dendracotogy of a xeric talus dope forest. A study by Mikan and colleagues (1994) investigated the dynamics of an oldgrowth chestnut oak forest on a dry talus slope in southeastern Pennsylvania. This community is situated near the center of a 19th-century charcoal iron settlement, where area forests were repeatedly clear-cut on short rotations for fuel for over a century. Chestnut oak trees up to 367 years in age dominated the uppermost canopy layer (32% relative importance value). Red maple (17%), black birch (17%), yellow birch (14%), and blackgum (7%) shared the codominant canopy position along with chestnut oak, and dominated the intermediate and overtopped canopy positions. Age determinations indicated that chestnut oak recruited continuously from 1625 until 1920 (figure 5). A major disturbance around 1770 stimulated a large amount of recruitment for chestnut oak and a moderate number of blackgum in the subsequent 30 years. The ability of blackgum to recruit following the 1770 disturbance may be due to the fact that it was competing only with chestnut oak at that time. An examination of individual tree-ring chronologies in the forests indicates that blackgum can persist in an understory position for as many as 125 years before having a radial growth release in a canopy gap. A second major disturbance around 1915, probably a result of the chestnut blight, stimulated large amounts of red maple, black birch, and yellow birch, but little chestnut oak or blackgum. Less frequent cutting in the surrounding forests and reduced occurrence of fire facilitated the establishment of maple and birch species in the early 20th century.

The results of the study by Mikan and colleagues (1994) indicate that a fundamental change has occurred in the forest dynamics of the eastern United States. Disturbances that occurred before European settlement facilitated the recruitment of the historical dominants (in this case, chestnut oak and blackgum), whereas disturbances that occurred after 1900 facilitated the recruitment of a new suite of species, some considered native invasives. Although the shade tolerance of blackgum is most likely superior to that of red maple, it appears now to be easily outcompeted by the red maple on this and other sites. Blackgum was not able to prosper in this forest in the wake of the chestnut blight because of growing competition from the faster-growing red maple and birch. These opportunistic species may further inhibit chestnut oak and blackgum recruitment into the foreseeable future.

Figure 4. Individual tree-ring chronologies and dates of major (arrow) and moderate (asterisk) disturbances resulting in tree-ring releases for six selected blackgum and hemlock trees at the Bear Meadows Natural Area in central Pennsylvania (adapted from Abrams et al. 2001).

Impacts of loggig on tree recruitment in Virginia coastal plain forestt. The composition, structure, and dendroecology of a mature pine-hardwood floodplain forest were studied at the George Washington Birthplace National Monument in eastern Virginia (Abrams and Black 2000). Sweetgum (27% relative importance value), loblolly pine (26%), American holly (23%), blackgum (7%), and several oak species (12%) dominate the forest. Blackgum trees recruited in large numbers from 1840 to 1910, whereas all the other tree species recruited after 1910 (figure 6). A dramatic increase in tree-ring growth of blackgum occurred in the late 1880s, and current age structure indicates that the forest was selectively logged of pine and economically valuable hardwoods at that time. Loggers avoided the low-value, decay-prone blackgum. This late 19th-century disturbance stimulated the recruitment of blackgum (probably from preexisting regeneration and root suckers) for a 30-year period, after which numerous loblolly pines and more moderate numbers of hardwood trees became reestablished.

Forest succession at the study site started after agricultural abandonment at least several decades before 1840 (the date of the oldest blackgum trees), possibly around 1813, when the Washington family sold the property. Loblolly pine is a typical pioneer-tree species in old-field succession on the southeastern coastal plain. Blackgum is a late-successional tree species, but can invade old fields in the southeastern United States after 30 or 40 years. Only sporadic blackgum recruitment occurred during the peak recruitment period for loblolly pine in the early 20th century. Loblolly pines at the site range in age from 64 to 105 years old, and stopped recruiting after canopy closure in 1945. Despite its shade tolerance, blackgum exhibited no recruitment from 1945 to 1985. This is an unusual example because of the large amount of blackgum recruitment following logging of all other tree species in the 1880s and the lack of blackgum recruitment later as the forest matured. Both aspects can probably be explained by the ability of blackgum to recruit in low-competition environments and, conversely, by its inability to recruit in high-competition environments.

Figure 5. Age-diameter relationship for all cored trees (top panel) and mean standardized ring-width index (lower panel) for the 24 oldest chestnut oaks at Hopewell Furnace National Historic Site, southeastern Pennsylvania (adapted from Mikan et at 1994).

Figure 6. Age-diameter relationship for all cored trees (top panel) and mean standardized ring-width index (lower panel) for the 20 oldest blackgum trees at the George Washington Birthplace National Monument in eastern Virginia (adapted from Abrams and Black 2000).

In another dendroecological example from Virginia, cutting of three mixed-oak forests in the late 1800s removed all tree species except blackgum (figure 7; Orwig and Abrams 1994b). Large amounts of tree recruitment occurred in the 40-year period following logging, including white oak, scarlet oak, red oak, black oak, hickory, tulip poplar, and sweetgum, but little or no blackgum. The main reason for this seems to be the very slow growth rate of blackgum, which averaged only 0.7 mm per year. This compares with an average radial growth rate of 2.5 mm per year in tulip poplar (Orwig and Abrams 1994b). In these forests, some understory blackgum trees up to 200 years old have never been released. Other blackgum trees remained highly suppressed for the first 170 years of their life, but were still capable of a tenfold increase in radial growth (from 0.2 mm to 2.0 mm per year) when a canopy gap was created. However, the great limitation for blackgum comes in the face of intense anthropogenic disturbances, such as major logging events, after which it is readily outcompeted by a variety of other tree species. It seems likely that the only reason blackgum is still a significant component in this and many other forests in the eastern United States is that it was not cut during the early logging period.

Ecophysiological and life history attributes

Table 2 summarizes the ecophysiological and life history attributes of blackgum. Blackgum is thought to exhibit a large degree of genotypic and phenotypic variation between populations. Keeley (1979) found differences in growth, flooding tolerance, survival, and physiology among upland, floodplain, and swamp populations of blackgum. In particular, upland populations of blackgum from Georgia are not tolerant of flooding. In a synthesis of southern tree species, Barnes (1991) concluded that blackgum is only weakly tolerant of flooding as compared with swamp tupelo and water tupelo. Burckhalter (1992) reported differences in flavonoid productionamong blackgum seed sources.

In southern Appalachian forests, where blackgum is present in most stands but is nowhere abundant, its recruitment was limited by low seed production and the low density of its bird-dispersed seeds (Clark et al. 1998). Blackgum fruits, which are high in crude fat, fiber, and nutrients, are an important food source for a variety of animals, including black bears and over 30 species of songbirds and game birds (Burns and Honkala 1990). Blackgum seeds generally have high germination rates following several months of moist, cold stratification. Deer browse the foliage of young sprouts of blackgum, but its payability may diminish with age (Burns and Honkala 1990). Blackgum is not seriously plagued by many insects or disease (to the point of inducing mortality), although it is prone to stem rot. Btackgum seedlings are present in most stands where blackgum occurs in the overstory, but almost always in numbers well below those of the more dominant tree species. For example, in a bog forest in central Pennsylvania, blackgum seedling density per hectare (ha) was 1130, compared with 99,000 and 250,000 for red maple and hemlock (Abrams et al. 2001). Out of a total of 84,440 seedlings per ha in an old-growth white oak-white pine forest in West Virginia, only 600 were blackgum (Abrams et al. 1995). However, larger numbers of regenerated blackgum have been reported in certain upland oak forests in Virginia and Pennsylvania, suggesting the potential for blackgum to increase as these stands mature or through stump sprouting and root suckering following clear-cutting (Orwig and Abrams 1994a, Signell et al. 2005).

Table 2. Ecopkysiological and life history attributes of blackgum (Nyssa sylvatica,).

Figure 7. Age-diameter relationship for all cored trees (top panels) and mean standardized ring-width index (lower panels) for the five oldest blackgum trees at the Fredericksburg and Spotsylvania National Military Parks in north-central Virginia (adapted from Orwig and Abrams 1994b).

Blackgum adults produce a very thick bark, often knobby and sometimes with high ridges reminiscent of chestnut oak, that provides a high degree of fire protection (figure 2). The bark thickness of blackgum is adequate for a 50% survival rate, given a surface fire frequency of about 14 years (Harmon 1984). This compares with the 23-year fire frequency required for 50% survival of red maple. A study of postfire tree mortality for six species in mixed-oak forests in Virginia concluded that chestnut oak and blackgum have greater fire resistance than (in decreasing order) pignut hickory, northern red oak, scarlet oak, red maple, and serviceberry (Regelbrugge and Smith 1994). However, a comparison of forest stands burned over the last 25 years with unburned stands in the Ridge and Valley of eastern Pennsylvania found blackgum trees at a similar level of relative importance (3.2% to 6.0%), suggesting that recurring fire or fire suppression had little impact on blackgum dominance (Signell et al. 2005).

Blackgum has low shoot or height growth relative to many other eastern hardwoods and also is among the slowest in its radial growth (table 2). Compared with four other tree species in Tennessee (white oak, chestnut oak, red maple, and tulip poplar), blackgum had the lowest radial growth rate in saplings and overstory trees (Hanson et al. 2001). In gap environments, the height growth of blackgum was similar to that of red maple, but significantly lower than that of sweetgum, sassafras, and white oak (Orwig and Abrams 1995). In a greenhouse study of biomass responses in six eastern tree species, blackgum typically had among the lowest growth rates for both roots and shoots when exposed to varying amounts of light and nutrients (Latham 1992), However, it exhibited the largest changes in root-to- shoot ratio with increasing resources, suggesting a high degree of morphological plasticity in the species (Latham 1992). Blackgum can send out root suckers, and, like almost all hardwood species, younger blackgum trees have vigorous stump sprouting ability (Burns and Honkala 1990).

The high shade tolerance of blackgum allows it to persist in the understory for well over a century and then be released by gap events to grow into the forest canopy (Mikan et at 1994, Orwig and Abrams I994b). However, its relatively low height potential often relegates blackgum to an intermediate or codominant canopy position (Burns and Honkala 1990, Ware 1992). Indeed, in an old-growth forest in southeast Pennsylvania, chestnut oak was the overwhelming canopy dominant, while blackgum trees of a similar age were in the codominant and intermediate canopy classes (Mikan et al. 1994). In second-growth mixed-oak and pine forests in northern Virginia, blackgum was typically relegated to the intermediate and overtopped canopy classes (Orwig and Abrams 1994b). However, other studies involving canopy class distribution indicate that blackgum can become an occasional canopy dominant (Abrams and Black 2000, Abrams et al. 2001).

Blackgum has low nutrient requirements, which enables it to grow successfully in nutrient-poor ridges and swamps (Barnes 1991, Farrell and Ware 1991). It is very tolerant of low-pH soils. It has moderately thick leaves with low photosynthetic rates, similar to those of red maple and sugar maple, and well below those of the faster-growing white oak and chestnut oak (Wilson et al. 2001). The osmotic potential of fieldgrown blackgum is similar to that of dogwood and sugar maple, but is higher (less negative) than that of red maple, chestnut oak, and white oak (Tschaplinski and Gebre 2003). Blackgum grown in a greenhouse has low gas exchange rates and very limited osmotic adjustment, quickly closes its stomata, and experiences leaf mortality with soil drying (Auge and Moore 2002). Blackgum experienced prolonged reductions in radial growth for up to six years following drought events in Virginia (Orwig and Abrams 1995). Overall, these studies suggest that the success of blackgum on xeric sites is due to its being a drought avoider, meaning that it shuts down physiologically in the face of even mild or moderate drought. Blackgum can tolerate January temperatures as low as – 8.6C, but is limited in this regard relative to other dominant tree species in the northeastern and Lake States regions (Iverson et al. 1999). Thus, a lack of extreme cold tolerance appears to play a role in the restricted distribution of blackgum in northern forests.

Grime (1977) characterized three primary strategies in plants relative to ecology and evolutionary theory: competitive, stress tolerant, and ruderal, Compared with other tree species in the eastern United States, blackgum belongs in the stress-tolerant group, although it is not an evergreen. Hubbell (2001) is a key proponent of the neutral theory of biodiversity and biogeography. He believes that ecophysiologicaJ and morphological trade-offs result in equal (or neutral) fitness or competitiveness for most species. Moreover, he argues, most species are not particularly highly specialized in resource requirements, and demography and dispersal are more dominant ecological factors determining species importance. In the case of blackgum vis–vis the neutral theory, slow growth is apparently counterbalanced by very high shade tolerance (low carbon requirements) and longevity, allowing for great persistence in forests. The low importance of blackgum on most sites may be attributed to low seed production and the low density of its bird- dispersed seeds, rather than to its inability to compete well.

Phytosoctology In a changing worid

The wide ecological breadth of blackgum is related to its ability to grow and survive on almost every physiographic, edaphic, moisture, and nutrient site class in the eastern United States. Its vast distribution across upland forests before European settlement suggests a moderate to high degree of fire resistance conferred from its thick bark (Harmon 1984). There are few late-successional tree species, such as blackgum, that are also fire resistant. In terms of ecophysiology, blackgum has low nutrient requirements and avoids the deleterious effects of moisture stress by being a drought avoider, quickly shutting its stomata at the early stages of moisture stress. At the opposite extreme, blackgum can also tolerate flooding and can dominate northeastern bogs.

Box 1. Tree genera and species with primarily bird-dispersed seeds In eastern US forests.

It appears that the percentage of blackgum has remained about the same or increased somewhat in parts of the eastern forest. For example, in southeastern Pennsylvania and northern Virginia, blackgum increased from about 1% to 2% in the presettlement forest to 6% to 7% at present (Orwig and Abrams 1994a, Mikan et al. J 994, Black and Abrams 2001). Perhaps more than any other tree species, blackgum had the best opportunity to increase throughout much of the eastern forest because it was systematically avoided by early loggers as a result of its low economic value and tendency to rot. Indeed, the dendroecological studies reviewed here indicate that blackgum often represents one of the few tree species that predates the original cutting of the forests (Orwig and Abrams I994b, Abrams and Black 2000, Abrams et al. 2001). Moreover, blackgum is shade tolerant and would appear to have had the opportunity to increase in eastern forests after the early 1900s, given the absence of subsequent cutting and fire. Despite these potential advantages, blackgum has gained very little, showing little or no significant increase in recruitment during the 20th century. Similarly, the chestnut blight provided little opportunity for blackgum expansion (Wnittaker 1956, Mikan et al. 1994). In contrast, red oak, chestnut oak, red maple, and black birch had large increases in recruitment following European settlement in much of the eastern forest (Abram\s 1998). Therefore, had blackgum not been spared the axe during the early logging period, its regeneration most certainly would have been outcompeted by more opportunistic tree species, and its numbers would have declined dramatically.

Why is blackgum unable to dominate uplands and all but a few lowland forests? Given its unrivaled ecological breadth, it appears that blackgum should be able to capture just about any microsite with which its seeds come into contact. The reason it does not become dominant appears to be its inherent slow growth. Tree-ring studies consistently show that blackgum is among the slowest- growing tree species in the eastern forest, typically growing less than 1.0 mm per year (Orwig and Abrams 1994b, Abrams et al. 2001). This compares with an average growth rate of 2.0 to 3.0 mm per year in many other eastern tree species. Blackgum also tends to have low height growth and root growth (Latham 1992), and many faster- growing tree species can easily overtop it. This is particularly true when other species are released during moderate to intense disturbance events, which typically are of little or no benefit to blackgum. The low density of blackgum in most forests may also be related to the fact that its seeds are primarily bird dispersed. A compilation of all the major bird-dispersed tree genera and species in the eastern United States indicates that none of them rank among the most dominant trees (box 1). Bird-ingested seeds have the opportunity of long-distance travel, but typically have low numbers at any one location (Hubbell 2001). This is consistent with blackgum’s occupation of a large range of sites, but almost invariably at low densities.

The widespread distribution of blackgum throughout the eastern forest can be attributed to a few key features. It is long lived; has low minimum requirements for water, light, and nutrients; and can tolerate fire, intense windstorms, and flooding. It is shade tolerant and can persist in a suppressed condition in forest understories for up to two centuries, probably longer than any tree species in the eastern United States. Although it rarely prospers as a result of catastrophic disturbances, it seems to persist despite them. The characterization of blackgum as persistent and resistant (Batista and Platt 2003) seems to apply throughout its range. The combination of being drought adapted, wind resistant, and tolerant of shade, wind, flood, and fire is unique among eastern trees.

Based on its ecophysiological attributes, blackgum should do best on low-resource and low-tree-density sites, such as swamps, xeric uplands, and mine spoils. The real enigma is how blackgum survives on better-quality sites with high tree density and competition from mesophytic species. Although few studies have specifically addressed this question, it seems likely that blackgum finds the occasional temporal or spatial opportunity (safe site), outpersists and outlives the competition because of its ecological tolerances and longevity, and then slowly grows into the forest canopy. Blackgum is facilitated by canopy gaps, but it is not strictly dependent on them (Orwig and Abrams 1994b). Blackgum may increase through root suckering following logging events.

In terms of range and ecological breadth, there is only one dominant tree species that compares with blackgum, and that is red maple. Red maple occurs throughout the eastern deciduous forest and can grow on almost all site classes, from wet to xeric (Abrams 1998). Like blackgum, it is shade tolerant; has low water, light, and nutrient requirements; and can survive long periods in shaded understories in a highly suppressed state. Although red maple is less fire tolerant than blackgum, this has not been a limitation in the eastern United States, where forest fires have been almost totally suppressed since the early 1900s. In contrast, red maple is much more prolific in terms of seed production and seedling numbers, is faster growing in high light, and is highly opportunistic in response to disturbances relative to blackgum (Abrams 1998). Red maple is rare in its ability to establish during all stages of forest succession, and it now dominates understories and forest canopies throughout much of the eastern forest.

What does the future hold for blackgum? From European settlement until the early 1900s, it persisted through one of the most disruptive periods in the history of the eastern US forest. With the likelihood of continued fire suppression and forest maturation in the region, there is little question that red maple will be a major player across the eastern forest biome {Abrams 1998). Blackgum will never rival red maple in the super-dominant category. It appears that anything blackgum can do, red maple can do far better. Future successional changes in eastern forests may actually further limit blackgum’s dominance. This is attributable to increased competition from a wide variety of native and exotic invasive species, of which red maple is just one. Hubbell (2001) believes that plant communities are saturated and that increases in the abundance of one or more species occur at the expense of others. This does not bode well for blackgum. Alternatively, global change models involving future increases in carbon dioxide and temperature predict that blackgum will increase in various locations throughout the eastern United States (Iverson et al. 1999), and it does appear to be increasing in some upland oak forests from changes in land-use history. The outcome of these opposing factors (increased competition versus global and land-use changes) for blackgum is unknown, though the hope is that blackgum will continue to capture the occasional microsite and persist in forests as it has done for thousands of years. Its large ecological breadth, longevity, and low resource requirements should help it prevail in this regard.

Acknowledgments

This article benefited greatly from conversations with and suggestions from Robert Peet, Stewart Ware, Greg Nowacki, and David Orwig. An earlier draft of the paper was critically reviewed and improved upon by Robert Peet. I want to thank Sarah Johnson and Rebekah Wagner for help with figure graphics.

References cited

Abrams MD. 1998. The red maple paradox. BioScience 48:355-364.

Abrams MD, Black BA. 2000. Dendmecological analysis of a mature loblolly pine-mixed hardwood forest at the George Washington Birthplace National Monument, eastern Virginia. Journal of the Torrey Botanical Club 127: 139-148.

Abrams MD, McCay DM. 1996. Vegetation-site relationships of witness trees (1780-1856) in the presettlemenl forests of eastern West Virginia. Canadian Journal of Forest Research 26: 217-224.

Abrams MD, Orwig DA. 1995. Structure, radial growth dynamics and recent climatic variations of a 320-year-old Pittus rigida rock outcrop community. Oecologia 101: 353-360.

Abrams MD, Ruffner CM. 1995. Physiographic analysis of witness- tree distribution (1765-1798) and present forest cover through north- central Pennsylvania. Canadian Journal of Forest Research 25:659- 668.

Abrams MD, Orwig DA, DeMeo TE. 1995. Dendroecological analysis of successionsl dynamics for a p resettlement-origin white pine-mixed oak forest in the southern Appalachians, USA. Joumal of Ecology 83:123-133.

Abrams MD, Copenheaver CA, Black BA, van de Gevel S. 2001. Dendroecology and climate impacts for a relict old-growth, bog forest in the Ridge and Valley Province of central Pennsylvania, USA. Canadian tournai of Botany 79:58-69.

Auge RM, Moore JL 2002. Stomatal response to non-hydraulic root- to-shoot communication of partial soil drying in relation to foliar dehydration tolerance. Environmental and Experimental Botany 47: 217- 229.

Barnes BV. 1991. Deciduous forests of North America. Pages 219- 344 in Rhrig E, Ulrich B, eds, Temperate Deciduous Forests. Ecosystems of the World, vol. 7. Amsterdam: Elsevier.

Batista WB, Platt Wl. 2003. Tree population responses to hurricane disturbance: Syndromes in a south-eastern USA old-growth forest. Journal of Ecology 91: 197-212.

Black BA, Abrams MD. 2001. Analysis of temporal variation and species-site relationships of witness tree data in southeastern Pennsylvania. Canadian Journal of Forest Research 31:419-429.

Black BA, Foster HT, Abrams MD. 2002. Combining environmentally dependent and independent analyses of witness tree data in east- central Alabama. Canadian lournal of Forest Research 32:2060-2075.

Braun EL. 1950. Deciduous Forests of Eastern North America. Philadelphia; Blakiston.

Brewer JS. 2001. Current and presentement tree species composition of some upland forests in northern Mississippi. lournal of the Torrey Botanical Society 128: 332-349.

Brush GS, Lenk C, Smith J. 1980. The natural forests of Maryland: An explanation of the vegetation map of Maryland. Ecological Monographs 50:77-92.

Burdchalter RE. 1992. The genus Nyssa (Comaceae) in North America: A revision. Sida 15:323-342.

Burns RM, Honkala BH. 1990. Silvics of North America, vol. 2: Hardwoods. Washington (DC): US Department of Agriculture. Agricultural Handbook 654.

Campbell JJN. 1989. Historical evidence of forest composition in the Bluegrass region of Kentucky. Pages 231-246 in Rink G, Budelsky CA, eds. Proceedings of the 7th Central Hardwood Forest Conference. St. Paul (MN): USDA Forest Service. North Central Forest Experiment Station. General Technical Report NC-132.

Clark JS. 1986. Coastal forest tree populations in a changing environment, southeastern Long Island, New York. Ecological Monographs 56:259-277.

Clark JS, Macklin E, Wood L. 1998. Stages of spatial scales of recruitment limitation in southern Appalachian forests. Ecological Monographs 68: 213-235.

Cogbill C, Burk J, Motzkin G. 2002. The forests of presettlement New England, USA: Spatial and compositional patterns based on town proprietor surveys. Journal of Biogeography 29: 1-26.

Cowell CM. 1995. Presettlement Piedmont forests: Patternsof composition and disturbance in central Georgia. Annals of the Association of American Geographers 85:65-83.

Delcourt HR, Delcourt PA. 1977. Presettlement magnolia-beech climax of the Gulf Coastal Plain: Quantitative evidence from the Apalachicola River Bluffs, north-central Florida. Ecology 58: 1085- 1093.

Delcourt H, Delcourt PA, Webb T III. 1983. Dynamic plant ecology: The spectrum of vegetation change in time and space. Quaternary Science Review 1: 153-175.

Dyer IM. 2001. Using witness trees to assess forest change in southeastern Ohio. Canadian Journal of Botany 31: 1708-1718.

Farrell JD, Ware S. 1991. Edaphic factors and forest vegetation in the Piedmont of Virginia. Bulletin of the Torrey Botanical Club 118:161-168.

Fernald ML 1950. Gray’s Manual of Botany. 8th ed. New York: American Book Company.

Foster DR, Zebrvk TM. 1993. Long-term vegetation dynamics and disturbance history of a lingo-dominated forest in New England. Ecology 74: 982-998.

Foster DR, Hall B, Barry S, clayden S, Parshall T. 2002. Cultural, environmental and historical controls of vegetation patterns and the modern conservation settings on the island of Martha’s Vineyard, USA. Journal of Biogeography 29: 1381-1400.

Fralish IS, Cooks FB, Chambers JL, Harty FM. 1991. Comparison of presettlement, second-growth and old-growth forest on six site types in the Illinois Shawnee Hills. American Midland Naturalist 125:294- 309.

Grime JP. 1977. Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. American Naturalist 11: 1169-1194.

Hanson PJ, Todd DE, Amthor JS. 2001. A six-year study of sapling and large-tree growth and mortality responses to natural and induced variability in precipitation and throughfall. Tree Physiology 21:345- 358.

Harmon ME. 1984. Survival of trees after low-intensity surface fires in Great Smoky Mountains National Park. Ecology 65:796-802.

Hubbell SP. 2001. The Unified Neutral Theory of Biodiversity and Biogeography. Princeton (NJ): Princeton University Press.

Iverson LR, Prasad AM, Hale Bf, Sutherland EK. 1999. Atlas of Current and Potential Future Distributions of Common Trees of the Eastern United States. Radnor (PA): USDA Forest Service, Northeastern Research Station. General Technical Report NE-265.

Keeley JE 1979. Population differentiation along a flood frequency gradient: Physiological adaptations to flooding in Nyua sylvalica. Ecological Monographs 49:89-108.

Latham RE. 1992. Co-occurring tree species change rank in seedling performance with resources varied experimentally. Ecology 73:2129-2144.

Little EL. 1971. Atlas of United States Trees, vol. 1: Conifers and Important Hardwoods. Washington (DC): USDA Forest Service. Miscellaneous Publication no. 1146.

Maenza-Gmelch TE. 1997. Holocene vegetation, climate and fire history of the Hudson Highlands, southeastern New York, USA. The Holocene 7: 25-37.

McIntosh RP. 1962. The forest cover of the Catskill Mountain Region, New York, as indicated by land survey records. American Midland Naturalist 68:409-423.

Mikan CJ, Orwig DA, Abrams MD. 1994. Age structure and successional dynamics of a presettlement-origin chestnut oak forest in the Pennsylvania Piedmont. Bulletin of the Torrey Botanical Club 121: 13-23.

Monk CD, Imm DW, Potter RL. 1990. Oak forests of eastern North America. Castanea 55:77-96.

Motzkin G, Eberhardt R, Hall B, Foster DR, Harrod J, MacDonald D. 2002. Vegetation variation across Cape Cod: Environmental and historical determinants. Journal of Biogeography 29:1439-1454.

Orwig DA, Abrams MD. 1994a. Land-use history (1720-1992), composition, and dynamics of oak-pine forests within the Piedmont and Coastal Plain of northern Virginia. Canadian Journal of Forest Research 24: 1216-1225.

____. 1994b. Contrasting radial growth and canopy recruitment patterns in Liriodendron tulipifera and Nyssa sylvalica: Gap- obligate versus gap-facultative tree species. Canadian Journal of Forest Research 24:2141-2149.

____. 1995. Dendroecological and ecophysiological analysis of gap environments in mixed-oak understoreys of northern Virginia. Functional Ecology 9:799-806.

Parsons SE, Ware S. 1982. Edaphic factors and vegetation in Virginia Coastal Plain swamps. Bulletin of the Torrey Botanical Club 109:365-370.

Peet RK, Christensen NL. 1980. Hardwood forest vegetation of the North Carolina Piedmont. Veroffentlichungen des Geobotanischen Institutes der ETH, Stiftung Riibel, Zurich 69:14-39.

Regelbrugge JC, Smith DW. 1994. Postfire tree mortality in relation to wild-fire severity in mixed-oak forest in the Blue Ridge of Virginia. Northern Journal of Applied Forestry 11:90-94.

Russell EWB. 1981. Vegetation of northern New Jersey before European settlement. American Midland Naturalist 105: 1-12.

Schafale MP, Harcombe PA. 1983. Presettlement vegetation of Hardin County, Texas. American Midland Naturalist 109: 355-366.

Schwartz MW. 1994. Natural distribution and abundance of forest species and communities in northern Florida. Ecology 75:687-705.

Seischab FK. 1992. Forests of the Holland Land Company in western New York, circa 1798. New York State Museum Bulletin 484: 36-53.

Signed SA, Abrams MD, Hovis JC, Henry SW. 2005. The impacts of fire on stand structure and tree regeneration in Central Appalachian mixed-oak forests. Forest Ecology and Management 218: 146-158.

Sperduto DD, Nichols WF, Crowley KF, Bechtel DA. 2000. Black Gum (Nyssa sylvatica Marsh) in New Hampshire. Concord (NH): Department of Resources and Economic Development, Division of Forests and Lands.

Tschaplinski TJ, Gebre GM. 2003. Leaf water potential, osmotic potential, and solute accumulation of several hardwood species as affected by manipulation of throughfall precipitation in an upland Querctis forest. Pages 121-139 in Hanson PI, Wullschleger SD, eds. North American Temperate Deciduous Forest Responses to Changing Precipitation Regimes. New York: Springer.

Ware S. 1992. Where are all the hickories in the Piedmont oak- hickory forest? Castanea 57:4-12.

Watts WA. 1980. Late Quaternary vegetation of central Appalachia and the New Jersey Coastal Plain. Ecological Monographs 49:427-469.

Watts WA, Hansen BCS, Grimm EC. 1992. Camel Lake: A 40,000-yr record of vegetation and forest history from northwest Florida. Ecology 73: 1056-1066.

Whitney GG. 1982. Vegetation-site relationships in the presetttement forests of northeastern Ohio. Botanical Gazette 143:225-237.

Whittaker RH. 1956. Vegetation of the Great Smoky Mountains. Ecological Monographs 26; 1-80.

Wilson KB, Baldocchi DD, Hanson P). 2001. Leafage affects the seasonal pattern of photosynthetic capacity and net ecosystem exchange of carbon in a deciduous forest. Plant, Cell and Environment 24:571-583.

doi:10.1641/B570409

Include this information when citing this material.

Marc D. Abrams (e-mail: agl@psu.edu) is Steimer Professor in the School of Forest Resources, Pennsylvania Stale University, University Park, PA 16802. & 2007 American Institute of Biological Sciences.

Copyright American Institute of Biological Sciences Apr 2007