CHAPTER 1. Effects of the Canopy Opening on the Understory of an Old Growth Eastern Hemlock-Northern Harwood Forest in South-Central Pennsylvania:

Literature Review

Introduction

Tsuga canadensis (L.) Carr. (eastern hemlock) dominates much of the central Appalachians, provides a major water quality buffer for riparian forests and also provides habitat for many animals including numerous species of birds, small mammals and invertebrates (Swanson and Franklin 1992; Stephenson et al. 1993; Benzinger 1994a). Tsuga canadensis is disappearing across much of its range because of infection by the hemlock woolly adelgid (HWA, Adelges tsugae Annand), an exotic defoliating insect. Changes in canopy cover caused by HWA have been shown to significantly effect the understory of old growth eastern hemlock-northern hardwood forest (Orwig and Foster 1998). Changes such as increased levels of forest-floor light and release of previously suppressed species may destabilize the community (Orwig and Foster 1998), adversely affect hemlock regeneration and engender the loss of sensitive and uncommon plants such as Taxus canadensis Marsh. (Canada yew), Monotropa uniflora (Indian pipe) and various bryophyte species (Evans et al. 1997).

Natural History of the Eastern Hemlock

Tsuga canadensis dominates riparian forests in monospecific stands and stands mixed with Pinus strobus L. as well as certain hardwood species in the central Appalachians and Appalachian Plateau (Orwig and Foster 1998). It is extremely long-lived, becoming sexually reproductive at about 15 years and fully mature at 250 - 300 years, sometimes living as much as 800 years (Godman and Lancaster 1990). Tsuga canadensis is one of the most shade tolerant tree species in the eastern United States and this quality enables it to remain in a suppressed condition in the understory for long periods of time prior to ascention to canopy dominance and this enables it to out-live other species (Godman and Lancaster 1990). Once released from suppression, however, Tsuga canadensis typically grows rapidly to attain a dominant position within the canopy (Godman and Lancaster 1990).

Tsuga canadensis is recognized as a component of the white pine-hemlock (Society of American Foresters type 22), eastern hemlock (type 23) and hemlock-yellow birch (type 24) in the Northern Forest region and the yellow poplar-eastern hemlock type (type 58) in the Central Forest region (Eyre, F.H., ed. 1980). Tsuga canadensis is also found in pure riparian stands that are dim, cool and damp with sparse understory vegetation (Lutz 1928; Rogers 1980). The dense foliage of a healthy Tsuga canadensis stand casts a dark shade and drops an acidic litter onto the soil (Godman and Lancaster 1990). These stands are frequently found in ravines, at stream bottoms and on exposed slopes (Rogers 1978; Kessel 1979). Some species that typically associate with hemlock are Dryopteris species (woodfern), Oxalis montana (common woodsorrel), Coptis groenlandica (goldthread), Lycopodium species (clubmoss) and Carex species (sedges) as well as Dicranum species and Polytrichum species (common mosses) (Rogers 1980; Willis and Coffman 1975).

Tsuga canadensis is very sensitive to fire, drought, wind, and anthropogenic disturbances because it lives in shallow soil, has shallow rooting systems and grows thin bark (Whitney 1990; Foster et al. 1992; Foster and Zebryk 1993). Many of the present-day stands, including the site in this study, are found in geographically or historically protected sites (Rogers 1978; Foster and Zebryk 1993).

Forests of Tsuga canadensis range from northeastern Minnesota through south-central Ontario, into southern Quebec, through New Brunswick and Nova Scotia south to Georgia and Alabama (Fig. 1-1; Godman and Lancaster 1990). Tsuga canadensis is among the eight most abundant species in New England, as measured by biomass (Wharton et al. 1985; Frieswyk and Malley 1986a, 1986b) and either in pure stands or mixed with Pinus strobus, it covers more than 300,000 hectares in New York state alone (Alerich and Drake 1995).

Tsuga canadensis has an important role in forests as a store of nutrients and as a habitat for birds and small mammals (Brush et al. 1980; Gregory et al. 1991). Tsuga canadensis often grows in nutrient poor, moist soil and is closely associated with streams and soil nutrient banks. As a result, watershed nutrient cycling rates are dramatically affected by hemlock mortality and the subsequent increase in the volume of coarse woody debris (CWD) that often causes elevated levels of nitrate, calcium, aluminum, and magnesium to leach into the lower streams (Jenkins et al. 1999; Yorks and Leopold 1999). Evidence suggests replacement of hemlock by hardwood yields higher pH and nitrogen turnover rate as well as reductions in carbon, nitrogen and exchangeable cations in the forest floor (Jenkins et al. 1999; Finzi et al. 1998a; Finzi et al. 1998b; Mladenoff 1987).

Natural History of the Hemlock Woolly Adelgid

The hemlock woolly adelgid (HWA) is a 0.5 mm long, aphid-like insect that gets its common name from the silken thread that the adelgid uses to protect its eggs (McClure 1987b, 1989). HWA is dispersed by birds, deer, wind and human activities such as logging, and has spread to 11 states, from Massachusetts to Virginia since its introduction from Japan during the early 1920s and its first being reported in Virginia in the early 1950’s (McClure 1987b, 1989).

The HWA is polymorphic and goes through two reproductive generations each year (McClure 1987b, 1989). The adult, called a sisten, lays a single cottony sac containing 50 - 300 eggs, surrounded by a cottony mass, on a hemlock twig sometime between March and May. The nymphs hatch approximately 30 days later, beginning in April, and move to the base of a hemlock needle. These crawlers are one of two forms: progrediens or sexuparae. Both types of the crawler phase settle at the base of a hemlock needle, insert a stylet into hemlock ray parenchyma cells, then feed and develop from nymphs through four instars to maturity by June. The winged sexuparae leave hemlock in search of a suitable species of spruce on which to oviposite. No young of the sexuparae (called sexuales) have ever been observed in North America because of a lack of a suitable species of spruce (McClure 1987a). Progredien adults remain on the hemlock and in June each produces a single cottony egg sac. Sistens hatch in about 30 days, beginning in July, and the sistens crawlers attach at a suitable place to feed on a hemlock twig. They begin to feed but soon enter aestival diapause that lasts until October. Aestivating nymphs then begin to feed again and are mature by February. These sistens begin to oviposite the following March to complete the double generation (McClure 1987b, 1989, 1995b).

The yearly double generation is significant because the HWA population may grow very quickly once it establishes within a stand. Dissemination is rapid in part because the time of activity coincides with the windy time of year (McClure 1989).

The adelgid feeds on the xylem ray parenchyma cells of new growth (Young et al. 1995). There is evidence that the salivary sheaths surrounding the adelgid’s stylet bundle may function to slow plant defense mechanisms and that this may be the cause of Tsuga canadensis’s reaction to the adelgid (Young et al. 1995). Symptoms such as needle loss, defoliation, and bud mortality appear within 1 year and tree mortality appear within 4 years (McClure 1987b, 1991; Young et al. 1995). Tsuga canadensis shows no apparent resistance to HWA and a heavily infested tree has little chance of recovery (McClure 1995b).

HWA is likely native to Japan given samples of the insect collected in Honshu, Japan in 1984 from Tsuga sieboldii Carriere (Southern Japanese hemlock) and the low, steady and relatively harmless presence of HWA in Japan (McClure 1983, 1987b). Japan’s native hemlocks are not harmed by HWA and one reason may be the native predator Pseudoscymnus tsugae which McClure discovered on an exploration of Honshu, Japan in 1992 (McClure 1995a). Pseudoscymnus tsugae has been cultured and researched as the main biocontrol agent for HWA in the eastern United States (Sasaji and McClure 1997).

HWA was detected in North America when identified by Annand in 1928 living on Tsuga heterophylla Sargent (western hemlock) in Oregon (McClure 1987b). Takahashi identified HWA from Tsuga chinensis Pritzel which was collected in Formosa, Taiwan and from Tsuga sieboldii collected in Japan (Takahashi 1937). The vector from the Japan to the US has never been identified (McClure pers. comm.). HWA sometimes kills the northwestern pacific ornamental hemlock Tsuga heterophylla but is not usually harmful in forest environments (Keen 1938; Furniss and Carolin 1977). HWA was reported in Virginia in early 1950’s, in southeastern Pennsylvania in the 1960’s and now occurs in parts of Massachusetts, Connecticut, Rhode Island, New York, New Jersey, Delaware, Pennsylvania, Maryland, Virginia, West Virginia and North Carolina (Fig. 1-1; McClure 1987b, 1989).

Natural History of the Canada Yew

Taxus canadensis Marsh. (Canada yew) is an evergreen shrub that grows in small colonies throughout the northeastern United States and southeastern Canada (Martell 1974; Allison 1991). It ranges from Newfoundland to Maryland and west to Manitoba and Iowa and serves as common winter browse for both Odocoileus virginianus Rafinesque (white-tailed deer) and Alces alces americana Clinton (moose) (Billington 1949; Beals et al. 1960; Allison 1990a; pers. obs.). Taxus canadensis thrives in humid sites with high soil moisture in mixed and deciduous North American forests and is commonly found at the base of slopes with a northerly or westerly aspect and at the base of concave slopes with northerly or westerly aspects (Allison 1991; Stachowicz et al. 1995).

Taxus canadensis is wind-pollinated and, unlike the other members of its genus, it is monoecious (Chamberlain 1966). Male and female strobili initiate during the summer and mature the following spring (Allison 1991). The male strobilus has 5 - 14 microsporophylls fixed onto a single axis and each microsporophyll has in it 2 - 10 microsporangia and female strobili are uniovulate (Dupler 1920). A single seed forms inside the strobilus after fertilization with a thick, hard coat on which rodent teeth marks have been found (Allison 1991). The fruit, a fleshy red aril, attracts birds as a dispersal agent (Wilson et al. 1996). Taxus canadensis reproduces vegetatively when procumbent branches take root and the connecting branches rot, leaving a clone and making it difficult to determine ramets from genets (Allison 1991).

In the 1960’s, other members of the genus Taxus were discovered to contain the chemical compound paclitaxel, or Taxol^®, a drug effective against cancers of the breast and ovary (Senneville et al. 2001). Taxol^® was initially lethally harvested from the bark of Taxus brevifolia Nutt. which killed the shrub (Senneville et al. 2001). Taxol^® was later discovered in the foliage of Taxus canadensis from which it can be harvested in a sustainable manner (Senneville et al. 2001). Eight other taxane analogues have been identified in the needles of Taxus canadensis and four of these taxane analogues have been isolated for the first time in the genus Taxus from Taxus canadensis foliage (Zhang et al. 2001). Some of these have been shown to inhibit breast adenocarcinoma cell lines (Zhang et al. 2001).

Taxus canadensis has been shown to suffer as the canopy opens through either logging or defoliation and soil moisture and humidity decrease while light levels increase (Nichols 1913; Hosley and Ziebarth 1935; Jenkins et al. 1999).

Study Significance

The loss of the canopy as a result of HWA infestation differs from loss via clearcut or windthrow. Snags come down more slowly and remain as shelter, holding nutrients longer and releasing them more slowly. Gap species have time to establish with less soil erosion and these gap species form habitat for other species (Evans et al. 1996). Orwig and Foster (1998) addressed forest response to HWA in central Connecticut and this study in the central Appalachian region will expand upon that idea by documenting the effects of HWA-induced canopy loss upon the understory of Sweet Root Natural Area, a typical old-growth eastern hemlock-northern hardwood forest. This study will examine the recruitment or release of species within the understory and the changes in the genetic diversity of Taxus canadensis. Sweet Root Natural Area’s many similarities to other Tsuga canadensis-northern hardwood stands make it a valuable site for observing the effects of canopy loss upon the understory. The growth and genetic diversity of populations of Taxus canadensis are of particular interest because the study site is in the southern extreme of its range and the opening canopy cover may result in the loss of plant vigor and finally, genetic diversity.

The study objectives are to: (1) assess changes in understory structure; (2) assess changes in CWD volume; (3) assess changes in Taxus canadensis diversity and vigor, as the canopy opens. Results will be used to predict a pattern of response that helps to deal with HWA infestation, hemlock defoliation, and the results of such as well as to assemble baseline data regarding the population genetics of Taxus canadensis. The working hypothesis is that Tsuga canadensis canopy loss will cause a significant change in the occurrence and growth rate of certain understory species including possible changes in the genetic diversity or vigor of Taxus canadensis.

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