Agents that played a more significant role in initiation than in expansion of gaps included spruce beetle, root and butt rots (other than Armillaria root disease), and dwarf mistletoe. Overall, spruce beetle was the most important agent in initiating canopy gaps and it tended to kill the largest, and probably oldest, Picea trees. Root- and butt-rot fungi were also important in initiating gaps. These fungi, unlike Armillaria ostoyae, tended to kill trees scattered throughout the canopy. Root and butt rot diseases were important on Picea, but especially so on Abies.
Eastern dwarf mistletoe may be underestimated as a contributor to gap initiation, because it was difficult to discern if the infections caused mortality. After many decades this obligate parasite can cause witches’ brooms, stem deformation, growth loss and mortality of Picea in the north-eastern USA (Hawksworth & Shigo 1980). Thus, symptoms of mistletoe infection are prominent on the oldest Picea trees, the same trees most susceptible to spruce beetle. For every two gapmakers attributed to mistletoe, there were three more that were obviously infected by mistletoe but killed by spruce beetle.
Although stem decays are important mortality agents in some old-growth forests (Hennon 1995; Lewis & Lindgren 1999), they were relatively unimportant at Crawford Notch, particularly in conifers. As hardwood species continue to increase in importance in the canopy and as their branches become increasingly wounded by wind and ice, we predict that stem decays will become more important mortality agents.
gap expansion and extensive disturbance
We had considered that larger patches of disturbance (> 0.1 ha) may represent ‘catastrophic disturbance’ that is qualitatively different from gap-phase disturbance and caused by different agents (White 1979; Peet 1992). However, at the elevations where extensive disturbance occurred (800 m and above), mortality in extensive disturbance plots was caused by the same agents as caused mortality in gap plots. Extensive disturbances in this forest appear to arise by expansion and coalescence of smaller canopy gaps. At Crawford Notch, particularly at higher elevations, the causes of gap expansion play a major role in forest dynamics.
Wind was a major cause of gap expansion, particularly at the middle and upper elevations of our study. Mortality due to wind can result from chronic wind stress, windthrow or windsnap. Chronic wind stress is a less organized manifestation of the same phenomenon that leads to fir waves at higher elevations in the White Mountains and Adirondack Mountains of the USA and in the Yatsugatake Mountains of Japan, where winter winds are very strong and directional (Iwaki & Totsuka 1959; Sprugel 1976). An increase in wind exposure leads to crown damage from rime ice and associated wind, and to root damage from root movement and underlying rocks. Growth slows and, ultimately, death may result (Harrington 1986; Marchand et al. 1986; Rizzo & Harrington 1988a). Although chronic wind stress was very important in expanding canopy gaps, none of the 33 single-tree gaps we encountered was caused by chronic wind stress.
Windthrow and windsnap in the absence of substantial decay are more obvious results of wind, but such mortality tended to expand gaps rather than cause large disturbance patches. It might at first seem surprising that, although wind is a very important agent of disturbance, evidence of large, catastrophic blowdown was not observed. Such blowdowns occur when exceptionally severe episodes of wind occur in areas where they do not usually occur. At Crawford Notch, in contrast, winter winds tend to be sustained and from a consistent direction. Crown shaping and pruning, and root growth, lead to wind-tolerant trees and extensive blowdowns are rare in the absence of hurricanes. When exposure is suddenly increased, however, some form of wind damage may develop, leading to mortality. Thus, wind is a chronic rather than a catastrophic phenomenon in these forests (Harrington 1986).
Further evidence of the complex consequences of wind in this system is the broken branches on hardwoods and the snapped tops on conifers, particularly on gap margin trees. Abies was particularly impacted by such snapping, contributing to its importance as a gap expander. In addition to reducing the crowns of these trees, and possibly killing them directly, the broken branches and stems serve as infection courts for stem-decay fungi that contribute to later mortality. Crown dieback of exposed hardwood tree species at mid- to upper elevations was particularly evident.
Armillaria ostoyae is also a common cause of gap expansion, especially at low and middle elevations. Establishment of new infections by long-distance dispersal is rare (Worrall 1994), so it may be expected that the disease causes more gap expansion than initiation. Using resources from previously colonized root systems, the pathogen spreads readily to neighbouring trees, either via root contacts or by growth through soil in the form of rhizomorphs. Thus, expanding centres of mortality may occur. The pathogen may have developed in root systems of the large spruce trees killed by the spruce beetle in the late 1970s, using these dead trees as a food base from which to attack adjacent saplings or weakened larger trees (Wargo & Harrington 1991).
long-term dynamics and spruce beetle
This study reports recent disturbance after a major outbreak of spruce beetle. The proportion of Picea as gapmakers far exceeded its proportion in the live canopy, particularly in terms of basal area. The rate of such disturbance is clearly not constant through time.
We use the term episodic disturbance for disturbance of large magnitude concentrated in time but not necessarily in space. Episodes of disturbance concentrated in large patches (Runkle 1985b) are often referred to as catastrophic disturbance. The disturbance that has affected the dominant Picea differs from a typical catastrophic disturbance in that it affects only one species in the forest, only the largest trees are killed, and it is not spatially aggregated.
Episodic disturbance affecting long-lived, dominant trees due to agents such as bark beetles may occur once every hundred or more years. However, the impacts may be long-term and complex, including altered forest structure and composition, with synchronous patterns of stand development across the landscape. In the southern Appalachians, high recruitment of Picea, apparently following extensive disturbance, occurred between 1790 and 1850. However, the incidence of small disturbances (resulting in periods of release of non-canopy Picea trees) did not show a decrease after 1850 (Wu et al. 1999). These patterns highlight the distinction between episodic disturbance and the more general forms of gap-phase disturbance. Based on reports of widespread Picea mortality over the last century and a half, and on dendrochronological evidence, Battles & Fahey (1996) concluded that periods of high Picea mortality and increases in gap fraction might be part of the long-term Picea–Abies disturbance regime in the northern Appalachians.
At Crawford Notch in 1991, Picea comprised nearly 50% of the dead basal area but less than 20% of the live canopy basal area. Large, dead Picea that emerged from the continuous canopy visually dominated the lower to middle elevations. Because Picea is a relatively slow-growing and long-lived species, these patterns strongly suggest a recent episode of elevated Picea mortality. Foster & Reiners (1986) recognized that there had been recent, increased mortality of large Picea in Crawford Notch and suggested that the forest was not in a steady state as a result. Worrall & Harrington (1988) provided evidence that the spruce beetle was primarily responsible for the observed mortality of the largest spruce at those elevations. Observations in 1983 (Harrington, personal observation) and the chronology of spruce beetle activity presented here indicate that the spruce beetle outbreak peaked about 1980. On a regional scale, the spruce beetle may also account for substantial portions of Picea mortality reported elsewhere in the north-eastern USA (Scott et al. 1984; Johnson et al. 1986).
When at low population levels, spruce beetle tends to reproduce in diseased and windthrown trees. When such habitat becomes abundant, populations may increase to a point where beetles overwhelm and kill healthy trees. Older, larger trees are the best habitat and produce the most successful brood of beetles, with 25 cm d.b.h. normally considered a minimum size of Picea rubens for successful beetle reproduction (Weiss et al. 1985). Vast, self-sustaining outbreaks may occur when a triggering event (such as a large blowdown) facilitates initial population rise and large trees are abundant to sustain the outbreak.
In the latter part of the 19th century, outbreaks of spruce beetle killed millions of trees in north-eastern USA (Hopkins 1901, 1909; Weiss et al. 1985). It is estimated that one-third to one-half of the merchantable spruce trees in the Adirondack Mountains of New York was killed in the 1880s (Johnson et al. 1986), and another major outbreak occurred in northern New England and eastern Canada in 1897–1901 (Hopkins 1909). Cutting of most stands of large spruce and subsequent fires near the turn of the century almost eliminated stands of large Picea rubens in the northern Appalachians, and outbreaks of the spruce beetle were smaller and less frequent in the 20th century (Weiss et al. 1985). As trees again reach large sizes, particularly in the few remaining old-growth stands such as Crawford Notch, however, spruce beetle outbreaks can still have significant ecological impact in initiating gaps and exposing other trees to Armillaria root disease and wind.
Our results suggest that forest disturbance regimes may be sufficiently complex that equilibrium or steady-state conditions in tree species abundances and forest structure are unlikely. At Crawford Notch, for example, nearly synchronous mortality of large Picea should be followed by increased regeneration of all tree species, especially Betula spp., though variation in gap size, expansion rate and seedbed will assure spatial heterogeneity of species composition in these forests. The regenerating stand will not be precisely even-aged because gap expansion may continue over several decades. Non-expanding, single-tree gaps should regenerate primarily Picea and Abies, mainly via release of advance regeneration (Runkle 1985b; White et al. 1985; Veblen 1986; Battles & Fahey 2000). Larger nonexpanding gaps, involving a few canopy trees, should allow the regeneration of mid-tolerant tree species such as Betula alleghaniensis, which cannot establish under a continuous canopy (Forcier 1975; McClure & Lee 1993). Slowly expanding gaps may favour a mix of the shade-tolerant and mid-tolerant species, but rapid gap expansion should enable shade-intolerant taxa such as Betula cordifolia and Sorbus americana (or S. decora) to join the mix, though the amount of birch may depend on seedbed availability (Battles & Fahey 2000).
Hardwoods that have been exposed by gap initiation and expansion will suffer crown damage due to wind and deteriorate as decay fungi invade broken branches and wounds. The canopy and subcanopy Abies that are released now will begin to die from root diseases, stem decays, windthrow and chronic wind stress as they reach 100 years of age. A similar pattern occurs in Picea glauca × engelmannii-Abies lasiocarpa forests of British Columbia (Lewis & Lindgren 1999). These smaller-scale disturbances may be tied to stand developmental conditions and susceptibility, but they are not tightly synchronized, as is the case with insect population outbreaks. In this way, gap-phase disturbance cycles are nested within the larger cycle of episodic disturbance in what might be termed a ‘nested bicycle’ system. Eventually a new cohort of Picea, already present in the understorey, will dominate, and as these Picea trees increase in size, the stage will be set for another large outbreak of spruce beetle.