Re-Establishment of Three Dominant Herbaceous Understory Species Following Fine-Scale Disturbance in a Catskill Northern Hardwood Forest

By Tessier, Jack T

TESSIER, J. T. (Central Connecticut State University, New Britain, CT 06050). Re-establishment of three dominant herbaceous understory species following fine-scale disturbance in a Catskill northern hardwood forest. J. Torrey Bot. Soc. 134: 34-44. 2007.-At the landscape scale, herbaceous understory plant species are limited in return to forested settings by dispersal. At fine-scales, microhabitat characteristics are known to be important in determining the distribution of herbaceous understory plant species. Fine-scale manipulative experiments to determine responses of understory species to disturbance, however, are few and limited to Europe and the Pacific northwest. The Unified Neutral Theory of Biodiversity (UNT) predicts that species enter disturbed habitat in abundances proportional to their neighboring abundance. I assessed the reestablishment of dominant understory plant species (Dryopteris intermedia, Lycopodium lucidulum, and Oxalis acetosella) following small-scale disturbance in a Catskill northern hardwood forest. While reestablishment of all species was significantly and positively correlated with the presence of each species in surrounding areas indicating the importance of dispersal limitation of reestablishment, rates of recovery were species specific. Reestablishment of O. acetosella was far greater than that of the other species. In fact, no sexual reproduction was observed for D. intermedia and L. lucidulum. Cover of D. intermedia and L. lucidulum was significantly and positively correlated with pre-disturbance cover but this was not true for O. acetosella, indicating that for the pteridiophytes, habitat quality (as well as dispersal) was an important factor in reestablishment. Reestablishment therefore was influenced by dispersal and habitat characteristics, was species specific, and did not follow the predictions of the UNT. Thus, small- scale disturbance can have an important effect on the composition of the herbaceous community in northern hardwood forests. Key words: Catskill Mountains, disturbance, Dryopteris intermedia, Lycopodium lucidulum, northern hardwood forest, Oxalis acetosella, understory, Unified Neutral Theory of Biodiversity and Biogeography.

Herbaceous understory plant species of the northeastern United States represent a large component of the species diversity of these forested ecosystems (Gilliam and Roberts 2003, Whigham 2004). Understanding the factors that affect these plant species and managing such ecosystems with this knowledge in mind is therefore critical to the maintenance of biodiversity. The history of natural and anthropogenic disturbance in the eastern United States (Foster and Aber 2004) has led to great interest in the effects of disturbance on understory plant communities (Flinn and Vellend 2005).

Several studies have indicated that forest understory herbaceous plants are limited by dispersal factors as they re-establish in secondary woodlands (e.g., Bossuyt et al. 1999, Butaye et al. 2001, Matlack 1994, 2005, Peterken and Game 1984, Verheyen et al. 2003a). These studies descriptively examined herb movement at the forest or larger scale and have not focused on finer scale disturbances within existing herbaceous communities. Since the rate of return in forest cover in the northeast has leveled off in the past century (Foster et al. 2004), the more important disturbance patterns in the future will be at these fine-scales within these forests. Such disturbances (on the scale of meters rather than hectares) alter light availability and can mix soil horizons or remove some soil horizons completely. These fine-scale disturbances may occur through forestry operations, tip-ups, and other localized disturbances to the forest floor.

Within stands at fine-scales, there is extensive descriptive evidence that niches affect species composition in the understory. Habitat characteristics known to affect herb composition include soil moisture (Anderson et al. 1969, Bell 1974, Davidson and Buell 1967, Hutchinson et al. 1999, Mabry et al. 2000, Sweeney and Cook 2001, Yorks et al. 2000), soil pH (Andersson 1991, Crozier and Boerner 1984, Graae et al. 2004), pit and mound topography (Peterson and Campbell 1993, Struik and Curtis 1962), nutrient availability (Chipman and Johnson 2002, Hutchinson et al. 1999), aspect (Small and McCarthy 2002), coarse woody debris (Lee and Sturgess 2001, McGee 2001, Thompson 1980), leaf litter depth (Sydes and Grime 1981), light availability (Brewer 1980, Davison and Forman 1982, Goldblum and Beatty 1999, Mabry et al. 2000, Whitney and Foster 1988), and stand history (Frelich et al. 2003, Foster and Aber 2004, Sweeney and Cook 2001). These factors and interactions among these factors may be important in explaining the response of these understory plant species to newly opened ecological space.

Research into fine-scale responses of herbaceous plant species to disturbance has found evidence that establishment of new populations is limited by dispersal of propagules (Primack and Miao 1992, Eriksson et al. 1995, Ackerman et al. 1996, Eriksson 1998, Ehrlen and Eriksson 2000), habitat quality (Ehrlen 1995, McKenzie et al. 2000, Gustafsson and Ehrlen 2003), or both (Eriksson and Ehrlen 1992, Van der Meijden et al. 1992, Ehrlen and Eriksson 1996, Tilman 1997). This work has been done mostly in the Pacific northwest (e.g., McKenzie et al. 2000) and in Europe (e.g., Gustafsson and Ehrlen 2003), and herbaceous plants of forest understories have not been examined for this trait in the northeast United States (but see Primack and Miao 1992).

The ability of neutral models to predict the ecological responses of species to disturbance has been known for some time (MacArthur and Wilson 1967, Caswell 1976, Hubbell 1979, Hubbell and Foster 1986), but a recent book on the topic (Hubbell 2001) has evoked a flurry of interest in the utility and accuracy of this model (e.g., Ricklefs 2003, Hubbell 2003, McGill 2003, Volkov et al. 2003, Etienne and Olff 2004, Tilman 2004). At its core, Hubbell’s (2001) Unified Neutral Theory of Biodiversity (hereafter UNT) explains that communities follow a zero-sum game, whereby species are considered to be equal, and the sum of all changes in a community results in no net change in organism abundance in the community. Species therefore replace one another at random through time in the community. Specifically, the UNT predicts that following a disturbance, species replacements are “drawn at random from the species that survive, with probabilities set by their postdisturbance relative abundances” (Hubbell 2001). Given the compatibilities and discrepancies found between the UNT and other models using data from descriptive (and in one case experimental) studies (Chave et al. 2002, Tokeshi and Schmid 2002, Condit et al. 2002, Tuomisto et al. 2003, Clark and McLachlan 2003, Adler 2004, Vandermeer et al. 2004, Obiri and Lawes 2004, Wootton 2005, Dornelas et al. 2006), there is a clear need to evaluate the limits of the UNT (Bell 2001, Hubbell 2003) particularly with experimental studies in ecosystems other than the tropical rainforests where the theory was developed (Chave 2004).

The objective of this study was to examine the recovery of dominant herbaceous understory species from fine-scale disturbance within an intact forest ecosystem. First, I predicted that if dispersal limits reestablishment at finescales as it does at large scales then cover of reestablishing species would be correlated with cover in the adjacent community. second, I predicted that if habitat quality limits reestablishment then cover of reestablishing species would be correlated with the original cover of those species in disturbed plots (a measure of habitat quality). Finally, if the UNT applies to dominant herbaceous forest understory plant species, I predicted that the species would return to disturbed plots in proportion to what is found in the plant community surrounding the disturbed plot.

Materials and Methods. STUDY SITE. This study was conducted within a 5 ha stand of a second-growth northern hardwood forest in the Catskill Mountains near Frost Valley, New York, USA. The canopy is dominated by Acer rubrum L., A. saccharum Marshall, Fagus grandifolia Ehrh., and Betula alleghanienxix Britton with scattered patches of Tsuga canadensis (L.) Carriere. Nomenclature follows Gleason and Cronquist (1991). The understory is dominated by Dryopteris intermedia (Muhl.) A. Gray, Lycopodium lucidulum Michx., and Oxalix acetosella L. with lesser amounts of Arisaema triphyllum (L.) Schott., Claytonia caroliniana Michx., Erythronium americanum Ker Gawler, Panax trifolius L., Trillium erectwn L., Trillium undulatum Willd., and Viola macloskeyi F. Lloyd. This area was last selectively logged in the 1950s and presumably Tsuga canadensis was harvested in the 1800s for the tanning industry. While the surrounding area is hilly to mountainous (including Slide Mountain, the highest peak in the Catskills), this stand is relatively flat, but slopes gently to the south before a quick drop-off that marks the southern border of the experimental area.

STUDY SPECIES. Dryopteris intermedia is a shade tolerant (Brach et al. 1993), wintergreen fern common to hardwood forests across the northeastern USA. Lycopodium lucidulum is an evergreen club moss that reproduces via spores and vegetative bulbils, which form in late summer (Barrows 1935). Oxalis acetosella is common to woodland settings across the northern hemisphere in both hardwood and coniferous forests (Lawesson and Wind 2002, Packham 1978, Petersen 1998, van Laar and den Ouden 1998) and is a seasonal-green, herbaceous angiosperm (Tessier 2004). These species were chosen for this study because they are the distinctly dominant herbaceous species in the stand (Tessier and Raynal 2003). FIELD METHODS. As part of a project examining the role of understory herbaceous plants and soil microbes in vernal biogeochemical functioning, I completely harvested all plant material from randomly placed, 1-m2 plots from 1999 to 2001 (Tessier and Raynal 2003). These plots were situated throughout the entire 5 ha study site and plots harvested within each year were distributed across the entire site. Plot corners were marked with flags so that during subsequent years a PVC sampling frame could be placed precisely in the same location. Prior to harvest, I determined the cover of Dryopteris intermedia, L. lucidulum, and O. acetosella in each plot by visual estimate. Cover included plant material from plants rooted within or outside of the plot. I sampled and harvested 30 plots in 1999, 18 plots in 2000, and 18 plots in 2001, for a total of 66 plots. Plant removal involved digging underneath the plants (typically 1015 cm) to remove all above and belowground plant material. This harvesting resulted in a collection of denuded plots ranging in time since disturbance from 1 to 3 years.

In 2002, I resampled each of these plots determining the cover of Dryopteris intermedia, Lycopodium lucidulum, and Oxalis acetosella. I also measured the distance from the edge of the plot to the plant that had established the farthest into the plot for each species. Additionally, I measured the cover of each of the study species in the eight 1-m2 plots adjacent to the harvested plot (along each of the four sides and at all four corners) to determine the character of the immediately surrounding plant community.

This approach is a chronosequence, in that different plots were used in different years and change among years is presumed to be representative of what would happen within any given plot through time. Interannual variability in weather can compromise this assumption as can heterogeneity among plots. The potential effects of interannual variability in weather can not be avoided. The influence of heterogeneity among plots was minimized because these plots were randomly distributed throughout the study site and each year’s harvest included plots from across the entire study site.

DATA ANALYSIS. All data were logio transformed prior to analysis to correct normality. Statistical analyses were performed using SAS version 8.0 (SAS Institute Inc., Gary, North Carolina). I compared differences among species and years in regard to cover, distance into plot, and percent recovery of pre-harvest cover using three species X three year factorial Analysis of Variance (ANOVA) tests within PROC GLM. Because there were no significant species X year interactions in cover and distance into the plots, I determined differences within the main effects using Tukey’s HSD tests at a = 0.05. There was a significant interaction between species and years in terms of percent recovery and I determined those differences by comparing least square means using LSMEANS within PROC MIXED. I used a Pearson correlation to assess the relationship for each species between both the cover and distance grown into the recovering plot and both the mean and maximum cover in adjacent plots within PROC CORR. I compared the three species for the ratio between cover in the recovering plot to both mean and maximum adjacent cover using one-way ANOVAs followed by Tukey’s HSD tests at a = 0.05 within PROC GLM. I used a Pearson correlation to assess the relationship between original cover and both reestablished cover and distance into plot for all species collectively and for each of the species independently using PROC CORR.

FIG. 1. Main effects of cover in and distance grown into plots recovering from complete harvest among dominant herbaceous understory species (Dryopteris intermedia, Lycopodium lucidulum, and Oxalis acetosella) and number of years of recovery for these species in a northern hardwood forest of the Catskill Mountains, NY, USA. The center line of each box represents the median value. The top and bottom of the boxes represent the 75lh and 25lh percentiles, respectively. The top and bottom whiskers represent the 90lh and 10lh percentiles, respectively. Outliers (data points above the 90th or below the 10th percentiles) are represented by dots. Species and years with different letters within a frame are significantly different at a = 0.05. Results are based on ANOVA and Tukey’s HSD.

Results. Species differed in their total cover and the distance that they had grown into the recovering plots (Fig. 1). Lycopodium lucidulum had the least cover in recovering plots. Oxalis acetosella traveled the farthest into recovering plots and L. lucidulum traveled the least distance into the plots among the three species. Oxalis acetosella therefore was the best able to reestablish in the recovering plots.

Years of recovery resulted in small but significant differences in cover and distance of growth into plots (Fig. 1). Overall cover of the three focus species and distance into the plots were highest in year two plots. All three species were therefore able to quickly reenter the recovering plots.

Table 1. Pearson correlation coefficients of cover or distance grown into a recovering plot compared to mean or maximum cover in adjacent intact plots for herbaceous understory species in a northern hardwood forest of the Catskill Mountains, USA. All coefficients are significant with/”-values of < 0.0001. For all species n = 66.

The cover of each species and its distance grown into the recovering plot were significantly and positively correlated with both mean and maximum cover in adjacent plots (Table 1). Dryopteris intermedia had the lowest correlations in this regard. All three species are therefore dependant on local populations to reestablish in recovering plots.

The species differed in percent recovery among years (Fig. 2). Percent recovery was higher for Oxalis acetosella than both Dryopteris intermedia and Lycopodium lucidulum in all three years. O. acetosella reached its predisturbance cover in one year and had dramatically higher cover in years two and three compared to pre- disturbance cover. Percent recovery was highest for O. acetosella in two year plots.

There were differences among species in the ratio of cover to both mean and maximum adjacent cover (Fig. 3). Oxalis acetosella had a higher ratio in both categories than the other two species and therefore reestablished in recovering plots faster than the other species relative to the availability of adjacent populations.

FIG. 2. Differences among dominant herbaceous understory species in percent return of cover during 3 years of recovery after complete harvest in a northern hardwood forest of the Catskill Mountains, NY, USA. Error bars represent one standard error. Means with different letters are significantly different at a = 0.05. Results are based on linear contrasts.

There was a significant and positive correlation between pre- disturbance cover and both reestablished cover and distance into plot for all species together, Dryopteris intermedia, and Lycopodium lucidulum, but not for Oxalis acetosella (Table 2). Therefore O. acetosella was the only species that was more abundant after disturbance than before disturbance and was not limited by habitat quality to reestablish in the disturbed plots.

Discussion. The results of this study indicate that there are differences among species in their ability to enter newly opened ecological space and that both dispersal and habitat quality are important determining factors in the reestablishment of herbaceous understory species after fine-scale disturbance. All of these species appear to depend on the presence of adjacent populations for recovery, in accordance with the UNT (Hubbell 2001). This result corroborates my first prediction suggesting that dispersal limits reestablishment for all of these species. Dispersal often limits recovery at the level of stands in the landscape (e.g., Bossuyt et al. 1999, Butaye et al. 2001, Matlack 1994, 2005, Peterken and Game 1984, Verheyen et al. 2003a). Life history traits are known to have a large impact on dispersal (Verheyen et al. 2003b) since sexually reproducing species tend to have a better ability to disperse into new stands than clonal species (Matlack 1994) and those with ingested seeds have a particular advantage (Brunei and von Oheimb 1998, Grashof-Bokdam and Geertsema 1998, Matlack 1994, 2005).

Both Dryopteris intermedia and Lycopodium lucidulum have life history traits that could limit their ability to colonize open space. While L. lucidulum can establish through vegetative spread, spores, and bulbils, it grows the best in horticultural settings through cuttings (Barrows 1935). This result suggests that vegetative spread is the most effective way for L. lucidulum to enter adjacent new habitat and this process appears to be slow, since this species stayed the closest to the edges of recovering plots (Figure 1). In contrast, Lezberg et al. (1999) who found that shallowly rooted species spread readily in coniferous forests of the Olympic Peninsula in Washington State. Dryopteris intermedia reproduces via spores, which can be enormous in number, but this species produces unisexual gametophytes, therefore its ability to produce new sporophytes is more limited than in other fern species (Xiang et al. 2000).

FIG. 3. Differences among dominant herbaceous understory species of a northern hardwood forest of the Catskill Mountains, NY, USA in terms of the ratios between cover in plots recovering from complete harvest to the mean and maximum cover of that species in adjacent plots of the understory community. The center line of each box represents the median value. The top and bottom of the boxes represent the 75th and 25th percentiles, respectively. The top and bottom whiskers represent the 90th and 10th percentiles, respectively. Outliers (data points above the 90th or below the 10th percentiles) are represented by dots. Species with different letters within a frame are significantly different at alpha = 0.05. Results are based on ANOVA and Tukey’s HSD. Table 2. Pearson correlation coefficients of pre-disturbance cover to reestablishment cover and distance into plot for herbaceous understory species in a northern hardwood forest of the Catskill Mountains, USA. For all species n = 66.

Oxalis acetosella exhibits a number of lifehistory traits that may give it an advantage in entering open ecological space (Roberts and Gilliam 2003). It can reproduce effectively and spread via vegetative means (Packham and Cohn 1990) or through sexual means (Berg 2002, Bierzychudek 1982). In fact, O. acetosella can throw its seeds upon maturity (Berg 2000). Large seeded species in general (such as O. acetosella relative to Dryopteris intermedia and Lycopodium lucidulum) are better able to establish at new sites (Burke and Grime 1996). Both approaches would help O. acetosella enter newly available, adjacent space. The changes brought on by the harvesting may have also helped O. acetosella spread quickly. This species is sensitive to drought (Brunei and Tyler 2000, Packham 1978, Tyler 2001) and low pH (Okland 1995, Rodenkirchen 1992, 1998, Wissemeier and Rodenkirchen 1994, Zerbe 2002). The harvest of all herbaceous species from the disturbed plots for this experiment removed competing roots and would have increased soil moisture and potentially assisted O. acetosella with reestablishment and survival. Soils in this stand have a very low average pH of 3.6 (Tessier and Raynal 2003) and the soil disruption from the harvesting required for this study may have raised the pH by mixing in mineral soil and more base cations into the organic horizon. Disturbances to soil would be common in association with tree tip- ups, foraging by animals, and timber harvest and O. acetosella may be adapted to taking advantage of such opportunities. The decrease in cover of O. acetosella in the third year may represent a decline due to leaching of base cations from the newly uplifted soil by acid deposition (Tessier et al. 2002). While variation in weather patterns among years may have driven differences among species, the repeated dominance by O. acetosella in recovery (Figure 2) suggests a true pattern that is not an artifact of the chronosequence experimental design.

The results of this study also indicate that Dryopteris intermedia and Lycopodium lucidulum are affected by pre-disturbance habitat quality in their reestablishment efforts, but Oxalis acetosella is not. The significant positive correlation between original cover and both reestablishment cover and distance into plot for the pteridiophytes indicates that the habitat quality in the disturbed location has a significant bearing on their ability to survive there. In contrast, since there was not a significant correlation among these factors for O. acetosella, habitat quality was either not important to this species or the quality of the habitat was universally acceptable within this stand. Since O. acetosella could reestablish so well in the disturbed plots, it is likely that dispersal is more important to this species in this stand. However, changes in the habitat as a result of the experimental harvesting may have improved the habitat quality for O. acetosella and therefore masked any influence of original habitat quality on reestablishment by O. acetosella. If this latter case is true, it is likely that the pteridiophytes are reestablishing based on habitat traits that were most likely not affected by the disturbance (light quality and quantity) but O. acetosella is more influenced by habitat traits that were quite likely affected by the disturbance (root competition, soil pH [see above]). These results therefore corroborate my second prediction of habitat limitation for the pteridiophytes but not for O. acetosella.

While all species were dependent on adjacent populations to recover in the disturbed plots, these results do not support the prediction of the UNT that species following a disturbance re-fill ecological space in proportion to their abundance in the resulting community (Hubbell 2001). If the community assembly rules of the UNT applied in this case, the ratio of cover within the disturbed plot to mean and maximum adjacent cover would not be different among species. Oxalis acetosella has a higher ratio than the other species (Figure 3) and therefore these results contradict the UNT for these species. Individualistic responses (Gleason 1917, 1926) to disturbance have also been seen in herbaceous plant species of the Pacific northwest of the United States (Halpern 1989). Oxalis acetosella has a clear advantage over the other two species in colonizing adjacent open space. In fact, even after 3 years, Dryopteris intermedia, which was the most dominant species in the understory (Figure 1), did not have a new sporophyte in any of the recovering plots (personal observation). Its cover was made up entirely of individuals that had arched their fronds into the recovering plots from sporophytes rooted outside of the recovering plots. Oxalis acetosella used its neighboring source populations more efficiently than did the other two species. This pattern was clear across years (Figure 3) suggesting that year to year variation in weather patterns was not a driving factor in the efficiency of O. acetosella in using its source populations. Relative to the size of the surrounding population (Figure 3), O. acetosella was the most prolific species in the recovering plots.

Continual change in forest understory communities limits the ability to determine if these populations have completely recovered. However, some additional recovery can be expected since Oxalis acetosella had a cover in year three that was well above that in the preharvest plots (Figure 2). Additionally, while Lycopodium lucidulum had reached pre-harvest cover, Dryopteris intermedia was below preharvest cover levels (Figure 2.) and had yet to develop new sporophytes within the plots. In the coming years, I expect O. acetosella to decrease in cover as D. intermedia increases in cover and likely outcompetes O. acetosella for light in the recovering plots.

Since the recovery of all three species was significantly and positively correlated with the abundance of the adjacent population, dispersal is likely an important mechanism limiting recovery at fine- scales within intact forests as it is at larger scales. However, since pre-disturbance cover was significantly and positively correlated with reestablishment cover in two of the three species, habitat suitability and niche availability at fine-scales has an important influence on the recovery of some understory species as well. Future studies should measure the rate of propagule production in conjunction with population regrowth. Additionally, manipulative studies could examine how the presence of various habitat traits affects the recovery of these populations at small scales. These studies would help to elucidate the relative importance of these two mechanisms in controlling recovery of understory species at fine- scales.

Clearly, fine-scale disturbances can affect the composition of understory plant communities in the northeast United States. Further work should experimentally examine the relative importance of dispersal and niche availability to these processes and examine responses of additional species. Understanding these phenomena will be important in the management of the secondary forests that are abundant in the northeast United States.

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Jack T. Tessier1,2

Department of Biology, Central Connecticut State University, New Britain, CT 06050

1 The author thanks the Frost Valley YMCA for the use of their forested property; the New York City Department of Environmental Protection and the US Forest Service in cooperation with the US Geological Survey, Troy, NY for funding; Lisa Tessier, Kim Anderson, Tim Schreiber. Karl Didier, Steve Fuller, Dave Kubek, Scott Jones, Kim Kiernan, Tom Touchet, Greg McGee, and Thad Yorks for field assistance; and Thomas Mione, Marcel Holyoak, Lisa Tessier, Jerry Jarrett and anonymous reviewers for constructive comments on the manuscript.

2 Email: TessierJ@ccsu.edu

Received for publication December 15, 2005, and in revised form October 4, 2006.

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