Study Area

The Delaware Water Gap National Recreation Area (NRA; Figure 2) borders the Delaware River in northeastern Pennsylvania and northwestern New Jersey and covers an area of 27,742 ha, with elevations of 84 to 490 m (Mahan et al. 2004). The dominant cover type is forest, with 18,575 ha of hardwood forest, 1,295 ha of coniferous forest, and 2,015 ha of mixed evergreen–deciduous forest (Myers and Irish 1981). Prior to the introduction of the hemlock woolly adelgid at Delaware Water Gap NRA, hemlock was present in >1,000 ha of forest, concentrated in mostly pure stands growing along streams that drain into the Delaware River (Young et al. 2002). Hemlock woolly adelgids were first discovered at Delaware Water Gap NRA in 1989 and were present in more than half of hemlock stands there by 1995 (Evans 2004). However, hemlocks in most stands had not yet experienced significant decline prior to the year 2000, when the baseline avian surveys for our study were conducted (R. Evans and R. Ross personal communication). Research on hemlock in a subset of hemlock stands at Delaware Water Gap NRA showed no change in basal area or relative dominance of hemlock prior to 2003 (Eschtruth et al. 2006). Data from surveys conducted in 2000 therefore provide a reliable baseline of predecline conditions.

FIGURE 2.

Location and outline of study area (Delaware Water Gap National Recreation Area) along the border of Pennsylvania (PA) and New Jersey (NJ) in the northeastern USA, where we studied changes in vegetation structure and avian community composition following the decline of hemlocks due to hemlock woolly adelgid invasion. The Delaware River divides the study area longitudinally from northeast to southwest. Black and green patches within the study area border represent 22 forest stands within which 80 sampling locations were located. Forest stands had previously been designated as either hemlock or hardwood prior to hemlock mortality caused by the hemlock woolly adelgid.

Surveys were conducted in 22 forest stands—11 hemlock and 11 hardwood (Figure 2)—located along first- or second-order streams in Delaware Water Gap NRA. Prior to hemlock mortality, digital GIS vegetation maps had been used to designate stands as either hemlock or hardwood based on the dominance of tree species by canopy area. Stands in which hemlock was the first, second, or third most dominant species were designated as hemlock stands, with all others classified as hardwood (hereafter, ‘hemlock stands' and ‘hardwood stands,' respectively; Young et al. 2002). Subsequent basal area measurements in these 22 stands showed that hemlock accounted for a mean of 53% (range: 25%–77%) of the basal area in hemlock stands, compared with a mean of 3% (range: 0%–14%) in hardwood stands (Mahan et al. 2004). Average stand area was 34.5 ha, and ranged from 2.5 ha to 127.5 ha. These stands were selected as part of a wider research effort to inventory the unique communities associated with hemlock stands in the park. This effort was motivated by the threat posed by the hemlock woolly adelgid's recent arrival (Young et al. 2002). Each of the 11 hardwood and hemlock stands were paired based on similar topographic characteristics. This design minimized nonvegetative differences between paired hemlock and hardwood stands (Young et al. 2002).

Vegetation Surveys

We conducted 2 types of vegetation survey to characterize forest structure and composition and how they changed through time. The first set of measurements occurred along transects at standardized locations within hemlock stands that were originally measured in 1997, prior to significant hemlock decline or mortality (Mahan et al. 2004). These measurements allowed us to examine differences between hemlock basal area pre- and post-hemlock mortality. In each of the 11 hemlock stands, we measured percent hemlock basal area in the winter of 2015–2016 (during the leaf-off period) and compared these values with premortality baseline data collected in 1997. These survey locations did not coincide directly with avian survey locations and instead quantified stand-level hemlock decline over time. The second set of measurements occurred at avian survey locations in 2015, allowing us to examine how contemporary vegetation related to bird distributions. Unfortunately, vegetation was not measured at individual avian survey locations during the 2000 surveys conducted by Ross et al. (2004).

Basal area measurements in 2015 followed the same protocol used in 1997 (Mahan et al. 2004). For each stand, we established 2 transects perpendicular to the stream channel within the forest stand: 1 transect at either end of a predetermined 80-m or 160-m stream length (80 m for first-order streams and 160 m for second-order streams, based on the original study design). For each transect, we established sampling points 15 m from the stream edge on either side of the stream, with subsequent points established at 30 m intervals on either side. Using a compass and handheld GPS unit (GPSmap 60CSx; Garmin, Olathe, Kansas, USA), we established sampling points to a maximum distance of 75 m from the stream edge for first-order streams and 135 m for second-order streams. We terminated transects at the maximum distance or at the edge of the stream's watershed (whichever came first). At each waypoint, we used a 10-factor prism to measure basal area for trees ≥10 cm in diameter at breast height, following standard point-sample timber cruising methods (Burkhart et al. 1984). Each standing tree was recorded as living or dead and identified as hemlock or not hemlock.

To examine the relationship between contemporary vegetation and bird communities, we measured hemlock condition and associated vegetation variables at each of the 80 avian survey locations during the summer of 2015. We established a 50-m radius plot at each location and divided the plot into 4 quadrants based on the cardinal directions. We then established 4 sampling points 25 m from the center of the plot, one in each intercardinal direction, plus a fifth sampling point at the plot center. We rated the average condition of all hemlock trees within a 10-m radius of each of the 5 sampling points on a scale of 1 to 5 (in half-unit increments) using the following scale: 1 = complete mortality; 2 = severe limb die-off and needle loss, with live branches remaining along less than the top ⅓ of the tree; 3 = significant limb die-off and needle loss, but live branches remaining along the top ⅓–⅔ of the tree; 4 = minor limb die-off and needle loss, with live branches remaining along more than the top ⅔ of the tree; and 5 = healthy, with no evidence of limb die-off or needle loss. This metric for evaluating hemlock condition is consistent with the pattern of loss of hemlock foliage and branches, which typically follows a systematic bottom-to-top pattern. We also measured hemlock basal area at the 5 points in each plot, using the same method used at points for the stand-level basal area measurements described previously.

Finally, in 2015, we estimated vegetation coverage from ground level to the canopy in the 50-m radius plots in which avian point count surveys were conducted (protocol adapted from Marshall et al. 2016). Plots were divided into 4 equal quadrants and we estimated vegetation volume in 4 height categories: 0.0–0.5 m; 0.5–2.0 m; 2.0–5.0 m; and >5.0 m to the upper limit of the forest canopy (hereafter referred to as the ground layer, understory, midstory, and canopy). For each level of each quadrant, we estimated the volume of space filled by vegetation, recorded as a percentage to the nearest 10% (essentially a percent cover estimate in a 3-dimensional space). We subdivided these percentage estimates to the nearest 5% based on 4 vegetation types: (1) hemlock; (2) deciduous species; (3) coniferous species other than hemlock; and (4) rhododendron (Rhododendron spp.), laurel (Kalmia spp.), and other broadleaf evergreens. We averaged all vegetation measurements from quadrants and subpoints to generate a single metric for each survey location.

Avian Surveys

We compared the results of surveys conducted in 2015 and 2016 with baseline surveys conducted in 2000 by Ross et al. (2004) to measure changes in avian community composition following hemlock decline. In each of the 3 study years, we surveyed 80 locations across the 11 pairs of hemlock and hardwood stands, with 45 locations in hemlock stands and 35 in hardwood stands. Survey locations were a minimum of 250 m apart and a minimum of 150 m from the edge of the respective stand type. Due to these distance limitations, the number of survey locations per forest stand varied from 1 to 6. In 2015 and 2016, we returned to the same locations surveyed in 2000 whenever possible. However, for 6 of the survey locations, records from surveys in 2000 indicated the forest stand, but not the exact location, where the survey was done. In these cases, we used field notes and guidance from Robert Ross (the observer in 2000) to establish the survey locations as closely as possible to where the original surveys were done.

All counts in 2000 were conducted by a single observer (R. Ross), as were all counts in 2015 and 2016 (M. Toenies), and survey methodology in 2015–2016 followed the methodology of surveys in 2000. Observers conducted early season point counts (following the recommendations of Ralph et al. 1995) from May 31 to June 14 in 2000, from May 30 to June 14 in 2015, and from June 1 to June 10 in 2016. In the 2 later years, we also conducted a second set of point counts at each survey location, which occurred from June 15 to July 7 in 2015 and from June 16 to June 23 in 2016. Counts occurred in the morning (between 0530 and 1000 hours) and only during suitable weather conditions: no precipitation and wind speed ≤19 km hr⁻¹ (3 or less on the Beaufort scale). At each point, we measured ambient noise to the nearest tenth of a decibel using a sound meter (GM1351 Digital Sound Level Meter, Shenzhen Jumaoyuan Science and Technology, Shenzhen city, Guangdong province, China) aimed in each of the 4 intercardinal directions (later years only). We disregarded brief noise peaks from sources such as loud bird vocalizations or infrequent traffic noise.

After waiting 5 min to limit the effects of any disturbance on bird activity, observers counted all birds heard or seen in a 10-min period. Observers recorded whether each bird was detected during the first or second 5 min of the count, as well as the distance at which the bird was first observed (0–50 m or >50 m). Observers in both 2000 and 2015–2016 practiced distance estimation prior to avian surveys in order to accurately place detections into the 2 distance bands. Because observers were likely to vary in their abilities to detect more distant birds, subsequent analyses included data for bird detections from <50 m only. This helped to minimize detection differences between observers in 2000 vs. 2015–2016. We conducted counts on dates in 2015 and 2016 that coincided as closely as possible with the same calendar date and time of day as the original count for that point in 2000.

Analyses

Vegetation

Hemlock condition measured at avian survey locations indicated that hemlock woolly adelgid infestation had affected hemlocks at nearly all survey locations in hemlock stands, although no locations had experienced complete hemlock mortality. The proportion of 2015–2016 survey locations with hemlocks in each of the 5 hemlock condition scores were: 7% healthy; 27% minor defoliation and limb death; 53% significant defoliation and limb death; 13% severe defoliation and limb death; and 0% complete tree mortality. Between pre-adelgid (1997) and post-adelgid (2015) basal area measurements, hemlock declined to varying degrees across the sampled stands, with the severity of decline correlated with current vegetation characteristics. Across hemlock stands, hemlock accounted for a mean of 56% of the total basal area in 1997, but had declined to 46% by 2015 (Figure 3, Appendix Table 4). Between 1997 and 2015, mortality in hemlock stands also increased, with standing dead trees accounting for a mean of 2% of the total basal area in 1997, compared with 15% in 2015 (Appendix Table 4). Greater initial hemlock basal area in the premortality surveys in 1997 was correlated with greater subsequent loss of hemlock basal area (r = 0.51, 95% confidence interval = 0.24–0.71). In addition, the degree of decline from one hemlock stand to another was correlated with several vegetation variables measured at individual survey locations (Table 1). Greater decline at the stand level was correlated with poorer hemlock condition, more standing dead hemlocks, and greater deciduous vegetation volume in the understory at survey locations.

FIGURE 3.

Mean hemlock basal area (with standard error bars) in 1997 and 2015 across sampled hemlock stands in the Delaware Water Gap National Recreation Area, northeastern USA. In general, stands that had more hemlock prior to hemlock woolly adelgid infestation experienced greater decline following infestation. For 2 stands with low initial hemlock basal area, the mean percentage of hemlock basal area was slightly greater in 2015.

TABLE 1.

Correlation matrix between vegetation variables related to hemlock decline. Hemlock decline (the difference in hemlock basal area between 1997 and 2015) was measured at the forest stand level, while all other variables were measured at individual survey locations. The hemlock health variable is based on a scale on which greater values indicate healthier hemlocks. Asterisks following r values indicate significance level (* P < 0.05, ** P < 0.01), and nonsignificant correlations are represented by dashes.

At the 56 point count locations with hemlock present, we also found strong correlations between our measures of vegetation variables. Better hemlock condition was negatively correlated with the number of hemlock snags. Hemlock health was also negatively correlated with both canopy hemlock volume and hemlock basal area at individual survey locations (Table 1), as hemlocks tended to be healthy only where they were sparse. This reflects a similar relationship to the stand-level correlation between initial hemlock basal area and degree of subsequent decline.

Changes in Bird Communities through Time

Across the 3 seasons of surveys of the 80 point count locations, observers detected a total of 58 species that met the criteria for inclusion in our analyses (see Appendix Table 3 for a full listing of these species and the number of surveys during which each species was detected). Of the 3 detection covariates included in our models, 1 (ambient noise) had a mean negative effect on detection probability, although this effect was nonsignificant based on a 95% credible interval (β = −0.18, 95% credible interval [CI]: −0.38 to 0.04). Survey date and time of day did not affect detection probability (see Appendix Table 5 for mean and species-specific effects of all detection covariates).

Several species groups showed strong changes in occupancy in hemlock stands over time, relative to changes in hardwood stands (see Appendix Table 3 for occupancy estimates for all species in the 2 stand types in both time periods). Occupancy increased for the species groups associated with the shrub layer (β = 1.35, 95% CI: 0.56–2.21), forest edge (β = 1.13, 95% CI: 0.13–2.17), and mature deciduous forest (β = 1.00, 95% CI: 0.28–1.69; Figure 4A). The snag-nesting species and early successional species groups also both showed positive mean effects to hemlock decline (β = 0.712, 95% CI: −0.63 to 2.01, and β = 1.12, 95% CI: −1.64 to 3.05, respectively), although the 95% credible intervals overlapped zero for both. Despite fairly strong positive effects for these 2 groups, especially the early successional species, precision for these mean effects was the lowest of all groups, likely a result of fewer detections for most species in both groups.

FIGURE 4.

(A) Avian species group responses and (B) individual avian species responses to hemlock decline and die-off in hemlock-dominated stands relative to hardwood-dominated stands in the Delaware Water Gap National Recreation Area, northeastern USA. Error bars represent 95% credible intervals. The effects shown here are the beta slope coefficients on a logit scale for an interaction between time period (2000 vs. 2015–2016) and forest type (hemlock vs. hardwood). Thus, these coefficients represent the effect of time period on occupancy in hemlock stands after controlling for observed effects occurring in hardwood stands. Species with <5 total detections are excluded here.

The hemlock-associated species showed a strong negative mean effect that clearly contrasted with the positive effect on all other species groups (β = −1.22, 95% CI: −2.47 to −0.06; Figure 4A). The 95% credible interval for this group was broader than that of most species groups, likely due to low power given the scarcity of hemlock-associated species in the hardwood stands, which acted as the control for comparison. At a species-specific level, responses were similar across the 5 species in the group, although the effect was slightly stronger and more precise for the Acadian Flycatcher (Figure 4B).

As the mean effects for the species groups would suggest, the individual species that showed the strongest positive relationships with hemlock decline were mostly species associated with either the shrub layer (Veery [Catharus fuscenscens], Worm-eating Warbler [Helmitheros vermivorum], and Wood Thrush [Hylocichla mustelina]); the forest edge (Blue Jay [Cyanocitta cristata], Great Crested Flycatcher [Myiarchus crinitus], and Brown-headed Cowbird [Molothrus ater]); or both of these habitats (Rose-breasted Grosbeak [Pheucticus ludovicianus] and Cedar Waxwing [Bombycilla cedrorum]; Figure 4B). All of the species associated with deciduous forest, snags, and early successional habitat also showed positive responses, although of all species in the latter 2 groups, only 1 species—the Veery—showed an effect with a nonoverlapping 95 % credible interval.

To illustrate how the effects discussed above translated into changes in species occurrence, we calculated changes in occupancy over time for each species (Figure 5B) using back-transformations of the logit-scale slope coefficients. For each species group, we also calculated changes in species richness over time by summing estimated changes in occupancy for all species in the group (Zipkin et al. 2009; Figure 5A). Occupancy declined for all hemlock-associated species, with the greatest decline in the Black-throated Green Warbler (mean change in occupancy = −30%, 95% CI: −45% to −14%). Summed across species, the declines in occupancy for this group indicated that survey locations in hemlock stands lost an average of ∼1 hemlock-associated species over time (mean change in species richness = −1.03 species per survey location, 95% CI: −1.52 to −0.59). In contrast to the hemlock specialists, all other species groups showed significant increases in species richness over time (Figure 5A). Species richness increased the most for groups associated with mature deciduous forest (mean change in richness = 1.16 species per survey location, 95% CI: 0.53–1.76). While the species groups associated with the shrub layer and forest edge showed the strongest positive relationships with hemlock decline (Figure 4A), many of the species in these groups also had very low occupancy estimates (see Appendix Table 3). By contrast, the deciduous forest–associate group included several of the species with the highest occupancy estimates (e.g., Red-eyed Vireo [Vireo olivaceus], Ovenbird [Seiurus aurocapilla], and Scarlet Tanager [Piranga olivacea]). Thus, compared with species associated with the forest edge and shrub layer, the overall high occupancy of deciduous forest associates resulted in greater absolute changes in occupancy and species richness for this group (Figure 5), despite a slightly weaker positive relationship with hemlock decline (Figure 4).

FIGURE 5.

Changes through time in (A) avian species richness of species groups (see Appendix Table 3 for species groups) and (B) occupancy of bird species in hemlock stands relative to changes in hardwood stands in response to hemlock decline and die-off in the Delaware Water Gap National Recreation Area, northeastern USA. Error bars represent 95% credible intervals. Between 2000 and 2015–2016, species richness declined for hemlock-associated species and increased for all other species groups. Species with <5 total detections are excluded here.

Homogenization of Bird Community through Time

After finding declines in hemlock specialists and increases in other avian species within hemlock stands, we examined the similarity of bird communities in the 2 forest types (hemlock vs. hardwood) during each of the 2 time periods (pre- and post-decline). Our goal was to test the prediction that, with a decline in hemlock, the avian community in hemlock stands would become more similar to that in hardwood stands. Bray–Curtis similarity indices showed that communities in hemlock and hardwood stands were indeed more similar postdecline (index = 0.71) than predecline (index = 0.60). Furthermore, the contemporary avian community in postdecline hemlock stands was slightly more similar to that in hardwood stands than that in predecline hemlock stands (index = 0.80). This highlights a shift in hemlock stands away from a unique species assemblage and toward the community composition of the surrounding landscape of primarily hardwood forest.

Differences in Occupancy among Hemlock Survey Locations

Vegetation surveys from 2015 and avian surveys from 2015–2016 allowed us to examine how avian community composition following hemlock decline was related to characteristics of vegetation structure that were affected by the hemlock woolly adelgid invasion, including canopy hemlock volume, deciduous understory volume, and hemlock health. Canopy hemlock volume was positively related to the probability of occupancy of the hemlock-associated species group (β = 1.03, 95% CI: 0.19–1.97; Table 2). Canopy hemlock volume had only weak effects on the probability of occupancy of most of the other species groups, although the effect for the early successional species group was much greater than that for the other groups (β = 0.47, 95% CI: −0.34 to 1.90); this effect was significant for the Veery (β = 0.65, 95% CI: 0.03–1.36).

TABLE 2.

Beta coefficients from models examining the effects of 3 variables on the probability of occupancy of hemlock forest stands by avian species groups: (1) hemlock volume in the canopy (>5 m height category); (2) an interaction between hemlock abundance (basal area) and hemlock health; and (3) deciduous vegetation volume in the understory (0.5–2.0 m height category). Asterisks indicate effects with 95% credible intervals that do not overlap zero. Mean effects are shown, with SD in parentheses. See Appendix Table 3 for species groups.

Compared with canopy hemlock volume, the percent deciduous vegetation volume in the understory (0.5–2.0 m height category) had larger effects on the probability of occupancy of more of the species groups, although credible intervals overlapped zero for all groups (Table 2). The hemlock-associated species group showed a negative mean effect of this variable on the probability of occupancy (β = −0.40, 95% CI: −0.86 to 0.04), whereas all other species groups besides snag-nesters showed at least weak positive effects for this covariate, with the strongest positive effect shown by the shrub layer–associated species (β = 0.24, 95% CI: −0.06 to 0.56).

As the results of our vegetation analysis showed, there was a strong negative correlation between the amount of hemlock and hemlock health. This could lead to potential confounding of effects when measuring the responses of birds to vegetation characteristics, and therefore we modeled the effects on avian species groups of the interaction between hemlock basal area and hemlock health. The interaction was significant for the hemlock-associated species (Table 2) but not for the other groups. We found that hemlock associates were positively associated with greater hemlock basal area. Once the basal area of hemlocks was controlled for, we also found a positive relationship between the occurrence of hemlock associates and hemlock health (Figure 6).

FIGURE 6.

Mean occupancy of hemlock-associated bird species in relation to the interaction between hemlock health and hemlock basal area. In areas with healthy hemlock trees, the probability of occupancy of hemlock-associated birds increases abruptly as the basal area of hemlocks increases, while the probability of occupancy increases more gradually in heavily degraded hemlock forest.

Changes in Vegetation Structure

The results of our vegetation analyses are consistent with findings from previous research on vegetation in dying hemlock forests. For example, Orwig and Foster (1998) found that hemlock mortality in Connecticut, USA, also resulted in a rapid increase in understory growth, including that of deciduous seedlings. As these other vegetation communities eventually replace hemlock stands, not only in our study area but across the extent of hemlock decline, more homogenized landscapes are likely to develop at a large scale (Orwig et al. 2002). Additionally, the pattern of greater hemlock mortality in stands with greater hemlock basal area, and the corresponding inverse relationship between hemlock basal area and hemlock health at survey locations, hold implications for hemlock forest loss in light of the continued spread of the hemlock woolly adelgid. While other tree species have been known to experience density-dependent effects inflicted by pest species (Bell et al. 2006), this relationship has not previously been well documented in the case of hemlock woolly adelgids and eastern hemlocks, although Orwig and Foster (1998) found a weak relationship between hemlock stand size and hemlock mortality. This pattern indicates that hemlocks and their associated communities may persist longer where the density of hemlock trees is lower.

Changes in Avian Community Composition through Time

Communities across a Gradient of Die-off Severity

Compared with the other species groups, the closer relationship between hemlock specialists and the vegetation variables that we modeled may explain the greater precision that we observed in estimates of effects on this group in relation to vegetation metrics at survey locations. The strong positive effect of hemlock abundance on occupancy, combined with a high correlation between abundant hemlock and poor hemlock condition, indicates that areas with high hemlock basal area may currently present a tradeoff to hemlock specialists. These bird species still persist with reduced but relatively high probabilities in locations with sufficiently high basal area or healthy hemlock (Figure 6). However, continued adelgid infestation is likely to reduce hemlock health in low basal area stands and reduce basal area in dense and unhealthy stands. This suggests a potential tipping point, where the rate of decline of hemlock associates will accelerate in the future. Still, the relationships that we observed may have implications for the management of hemlock woolly adelgid infestations. For example, if management practices are able to maintain either (1) sufficient basal area of even highly degraded hemlock, or (2) relatively healthy hemlock even at a fairly low basal area (∼16 m² ha⁻¹), then the presence of hemlock specialists may be maintained (Figure 6).

Given the geographically widespread nature of hemlock loss and other forest die-offs, vegetation community responses may vary considerably depending on the rate of die-off, the species composition of replacement communities (including the potential for invasion by nonnative plants), variation in disturbance regimes, and numerous other factors. The responses of bird communities to this variability in vegetation changes will undoubtedly be variable as well. Further research at larger scales could better explain how the avian community response that we observed may vary with respect to this heterogeneity in vegetation restructuring following hemlock die-off.