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Natural Areas Journal 28:395–403

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Divergence in Avian Communities Following Woody

Plant Invasions in a Pine Barrens

Ecosystem

Brian L. Beachy1

George R. Robinson2,3

1 1977-2008

2 Program in Biodiversity, Conservation and Policy

Department of Biological SciencesUniversity at Albany

State University of New York1400 Washington AvenueAlbany, NY 12222, USA

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R E S E A R C H N O T E

1 Corresponding author: grobins@albany.edu; 518-442-4302

ABSTRACT: We compared avian communities and vegetation characteristics in invaded and uninvaded pine barren ecosystems to test whether invasive woody plants were altering native bird communities. We hypothesized that structural changes in vegetation caused by the invasion of fire-intolerant decidu-ous trees were altering bird communities in the Albany Pine Bush, east central New York State. We recorded bird calls at 55 stations during breeding season to estimate abundances of breeding birds in areas dominated by fire-dependent pine-shrub savanna and areas dominated by invasive hardwoods (black locust, Robinia pseudoacacia, and aspens, Populus tremuloides and P. grandidentata). Vegetation surveys were conducted surrounding each station to quantify woody plant composition and structure. Sites characterized as invaded had more vegetation layers, twice as much closed canopy, and higher tree stem densities in all but the largest (> 25 cm dia) size classes. Forty-seven bird species were recorded; thirty-three at both invaded and uninvaded sites. Grassland/shrubland birds, such as prairie warbler (Dendroica discolor), field sparrow (Spizella pusilla), red-breasted nuthatch (Sitta canadensis), and eastern towhee (Pipilo erythrophthalmus), were twice as frequent and three times as abundant at unin-vaded sites. Native bird species characteristic of closed-canopy forest were more frequent and abundant at stations in invaded sites. Multivariate analyses indicate distinct associations of particular birds with unique combinations of vegetation characteristics that differed between invaded and uninvaded points. A campaign of adaptive fire management holds promise to restore critical avian habitat in protected areas of this threatened barrens ecosystem.

Index terms: Albany Pine Bush Preserve, invasive tree species, pine barrens, shrubland birds, vegeta-tion structure

INTRODUCTION

Invasive plant species have received considerable attention in natural resource management (Byers et al. 2002; D’Antonio et al. 2004; Tempel et al. 2004; Lodge et al. 2006). However, despite abundant evidence of their potential to spread and proliferate, specific impacts of plant invasions on native fauna are often subtle and elusive. Specific cases of negative effects of invasive plants and native birds have been documented (e.g., Schmidt and Whelan 1999; Stoleson and Finch 2001), but other results have been equivocal, including some evidence that invasive plants supply habitat needs for native avifauna (Hunter et al 1988; Hudson 1994; Kiviat 1996; Wiliams 1997). In most of these latter cases, the focus has been on individual bird species and their capacity to tolerate invasive plants.

Populations of many neotropical migra-tory birds in eastern North America have experienced recent declines (Robbins et al. 1989; Askins et al. 1990; Hagan and Johnston 1992; Benoit and Askins 1999; Whitt et al. 1999). One of the clearest trends is reduced abundances of successional and scrub-breeding species (Hunter et al. 2001), due in large part to loss of breed-ing habitat (Brawn et al. 2001; Trani et al. 2001). Among the most threatened habitats are natural fire-dependent shrub-scrub eco-

systems, which are difficult to maintain in the highly fragmented landscapes found in much of the eastern United States (Thomp-son and DeGraaf 2001). Classic papers in avian ecology have linked changes in bird communities associated with successional change from open field to closed-canopy woodland (Adams 1908; Johnston and Odum 1956; Shugart and James 1973). Among the most influential effects of forest succession on avian habitat selection are changes in vertical vegetation structure (MacArthur and MacArthur 1961), with avian communities sorting along succes-sional gradients (MacArthur et al. 1962; MacArthur et al. 1966; Roth 1976). Fol-lowing fire suppression, succession to intolerant forest may also include invasive woody species with the potential to further alter avian habitat structure.

Pine barrens in northeastern North America are characterized by fire-adapted pitch pine (Pinus rigida) mixed with shrub oaks (Quercus prinoides, Q. ilicifolia), prairie grasses, and other fire-tolerant species that coexist in open-canopy, savanna-like land-scapes. Most of the hardwood tree species that invade following fire suppression are native to North America, but historically they have not been primary components of barrens and other shrubland plant com-munities. Highly invasive tree species, both native and exotic, are quick to appear when

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pitch pine communities lose their distur-bance dynamic; and in a matter of decades, their growth and spread lead to soil nutrient enrichment and full-scale loss of barrens plant communities (Little and Garrett 1990; Bernard and Seischab 1995).

We studied an inland pine barrens com-munity that contains a mix of heavily invaded zones and fire-managed pine/shrub habitats. Our research goals were to: (1) quantify differences in avian communities between native pine barrens savannah and habitat dominated by invasive deciduous trees; (2) quantify differences in vertical and horizontal vegetation characteristics in the two habitats; and (3) categorize species-specific relationships, with special attention to grassland/shrubland birds that are undergoing regional declines.

METHODS

Study area

The Albany Pine Bush is an inland pitch pine-scrub oak barrens (Barnes 2003), ranked as a globally rare ecosystem (Ed-inger et al. 2002). Soils are well-drained sand dune deposits that formed on the margins of Glacial Lake Albany during the Wisconsin glaciation (LaFleur 1976; Barnes 2003). Approximately 7000 ha re-main of its original 40 km2 extent (Rittner 1976), of which 1300 ha are currently protected as the Albany Pine Bush Preserve (APBPC 2006). The dominant natural veg-etation is fire-dependent pine-shrub barrens (Milne 1985; Schneider et al. 1991), with an estimated wildfire cycle of 6-15 years (Benton 1976; Edinger et al. 2002), now under active fire management (Zaremba et al. 1991; APBPC 2006). A combination of fire suppression and habitat fragmentation from suburbanization (Zantopp 2000), as well as natural topographic variation, has produced a mosaic of vegetation types (Milne 1985).

Black locust (Robinia pseudoacacia) has recently produced dense stands that sup-press barrens vegetation by shading and soil enrichment (Rice et al. 2004). Native to southeastern North America, where it is classified as an early to mid-successional

forest species (Boring and Swank 1984), it was introduced to the Albany Pine Bush for use in agriculture, escaping to overwhelm many pine-shrub oak stands (Milne 1985; Barnes 2003). Two other invasive trees, both native to the region, are trembling aspen (Populus tremuloides) and big-tooth aspen (P. grandidentata). Both are intolerant of frequent fires, but invade aggressively when released (Laidly 1990; Perala 1990 ). All three species are fast-growing, highly clonal, and capable of long-distance seed dispersal. All three are targets of control campaigns within the Albany Pine Bush Preserve that include girdling, mechanical removal, and chemi-cal application, in combination with fire management (APBPC 2006; N. Gifford, Conservation Director, Albany Pine Bush Preserve Commission, pers. comm.).

The vertebrate fauna of the Albany Pine Bush is relatively species rich (Schneider et al. 1991; Barnes 2003), and includes a number of taxa at or near their north-ernmost range limits (Stewart and Rossi 1981). Previous censuses of avifauna are documented in Treacy (1953) and Kerlinger and Doremus (1981a, b).

Sample point selection

Sample points for recording breeding bird calls were selected to include both invaded and uninvaded areas based on visual as-sessment of dominant vegetation. The majority of these stations were located on walking trails or on fire breaks to reduce travel time between points and to minimize noise when approaching a station. Twenty-eight points were designated as uninvaded and 27 points were designated as invaded. Mean distance to the nearest forest edge was 224 m (± 132 m SD) and to the near-est road was 289 m (± 158 m SD). Mean distance between all point pairs was 237 m (± 65 m SD).

Vegetation sampling

Vegetation sampling was modeled after Shugart and James (1973). Two 100-m x 2-m strip transects were sampled in oppo-site directions from each sampling point. All trees with diameter (dbh) > 5 cm were

identified and measured, using five size classes: 5-10 cm, 11-15 cm, 16-20 cm, 21-25 cm, and > 25 cm. Standing dead trees were included because they serve as avian habitat elements. Clones were not delineated and tree density was estimated as number of stems. Within each 10-transect-meter interval, at a randomly chosen point, vegetation layers were counted within a circle of 1-m radius. Five layer classes were used: a grass/sedge layer and four height categories of woody plants: < 1 m, 1-2 m, 2-3 m, and > 3 m. The first three categories were further divided into fruit-bearing and non-fruit bearing shrubs and trees, and the tallest category was recorded as open or closed canopy.

Point count surveys

Point counts were conducted between 14 May and 4 July 2001, primarily using methods outlined by Hutto et al. (1986) and Ralph et al. (1995). Stations were moni-tored four times, eight minutes each, during the study period, 30 min after sunrise until 9:00 A.M. Bird species were identified by sight and/or sound and were recorded in two distance intervals, 0-50 meters and beyond 50 meters (Ralph et al. 1995). A species was recorded only once unless heard or seen simultaneously or nearly simultaneously from different locations. No counts were conducted during windy or rainy conditions.

Data analysis

For the results reported here, data were restricted to information recorded within 50 m of each sampling point to assure independence of all bird records and to assure homogeneity of vegetation cover within transect samples. Individual bird species were compared using two indices of abundance: frequency for each habitat type, and average number of individuals (Hutto et al. 1986). Contingency tests (Fisher’s Exact Test) were used to compare presence/absence against habitat type (in-vaded or uninvaded). Mean abundance per species in each habitat type was compared with Mann-Whitney U-tests.

Diameter size class distributions were

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compared among the main tree species – pitch pine, black locust, and the aspens – and pooled for invaded versus uninvaded sites; differences in density and frequency were analyzed with paired T-tests. Princi-pal components analysis (PCA) was used to reduce all vegetation measures to two principal axes (on which all sample points were ordinated) and identified as invaded or uninvaded.

Canonical correspondence analysis (CCA; ter Braak 1986; ter Braak and Šmilauer 1998) was used to explore relationships between key elements of vegetation structure, including densities of invasive trees, and avian taxa. For this analysis, only bird species recorded at > 5 points (N = 29 species) were included. Graphi-cal and statistical tests were performed using SPSS™ 10.1, SYSTAT™ 9.0, and CANOCO™ 4.0 software.

RESULTS

Vegetation differences: uninvaded vs. invaded zones

Densities of tree stems in smaller size classes were substantially higher at invaded sites, whereas densities of larger trees were statistically similar between site types (Table 1). The much larger numbers of small stems produced a mean difference in total tree density of 437.7 stems per ha (t = –5.46, df = 53, p < 0.05). No differ-ences were detected among site types in total basal area, numbers of woody plant species, or number of standing dead stems.

Size distributions, however, were distinctly different for the main tree species between invaded and uninvaded sites (Figure 1). Mean pitch pine dbh was significantly greater at invaded points (mean difference = 5.6 cm, t = –3.24, df = 145, p < 0.05), because no small individuals were found in invaded areas (Figure 1A). Aspens and black locust found at invaded points tended to be primarily in the smaller size classes, indicating high reproductive potential (Figure 1B, C). Ordination of sample points shows considerable variability in composite vegetation structure (Figure 2), but substantial separation of uninvaded and invaded sites along the x-axis, which is associated with low-growing vegeta-tion (L1, L2F, and L3) versus closed tree canopy (L5C) (Table 2). Pairwise correla-tions between aspen and black locust were negative for both density (r = –0.356; N = 55, p = .008) and basal area (r = –0.345; N = 55, p = .01).

Avian communities: invaded vs. uninvaded zones

Fifty-one species were identified, 47 within the 50-m point count radius (Appendix 1). Over one-third (18 species) were found at fewer than six points each. Three species found in this study had not been previ-ously reported as breeding in the Albany Pine Bush – blue-winged warbler (Vermi-vora pinus), hooded warbler (Wilsonia citrine), and blue-headed vireo (Vireo solitarius). Nine species were significantly correlated with either invaded or uninvaded sites (Table 3). The six recorded more frequently at uninvaded points are charac-

Stems/ha (± SD)dbh (cm) Uninvaded Invaded pdbh 1 (5-10) 123.2 (111.8) 335.2 (172) < 0.01dbh 2 (11-15) 76.8 (65.9) 216.7 (115.2) < 0.01dbh 3 (16-20) 60.7 (67.2) 161.1 (120.0) < 0.01dbh 4 (21-25) 66.1 (74.6) 85.2 (90.7) 0.40dbh 5 (> 25) 91.1 (93.3) 57.4 (64.6) 0.13

Table 1. Mean number of stems per hectare in five diameter at breast height (dbh) size classes, with single standard deviations (SD) in uninvaded (N = 28) and invaded (N = 27) sites in the Albany Pine Bush. P-values are from paired t-tests.

Figure 1. Size distributions of the dominant tree species measured at uninvaded (N = 28) versus invaded (N = 27) sites. Aspen (C) refers to both Populus tremuloides and P. grandidentata.

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teristic of grasslands and open shrublands; those found more frequently at invaded sites are characteristic of closed canopy deciduous forests (Table 2).

Species-specific associations with vegetation structure

The CCA biplot (Figure 3) provides insight into how groups of bird species correlate with vegetation characteristics. Although many are clustered near the centroid, sev-eral species congregate in the lower right quadrant, primarily shrub birds of open habitat, closely corresponding to those identified as more prevalent at uninvaded sites (Table 3). Distinctly different avian communities are associated with black locust (Figure 3, upper left quadrant) ver-sus aspens (Figure 3, lower left quadrant), although both tree species are characteris-tic of mid- to late-successional stages of deciduous forest in the region.

DISCUSSION

Although forest trees naturally invade shrublands, an ancient process in ecotone dynamics (Petita et al. 2004), anthro-pogenic activities tend to accelerate the invasion process, often by disrupting historic disturbance dynamics (Hobbs and Huenneke 1992; Davis et al. 2000). Once established, invasive trees clearly have the potential to alter ecosystem function and displace native plant communities (e.g., Vitousek et al. 1987; Richardson 1988), but their consequences for avifauna are poorly understood and are subject to debate (e.g., Cohn 2005).

We found significant differences in the bird communities between invaded and uninvaded points. Eastern towhee (Pipilo erythrophthalmus), field sparrow (Spizella pusilla), prairie warbler (Dendroica pinus), and house wren (Troglodytes aedon) are all birds commonly found in open wood-land and shrubland. Their prevalence at uninvaded points was expected, because these sites were dominated by an open pitch pine-scrub oak habitat. Pine warbler (Dendroica pinus) and red-breasted nut-hatch (Sitta canadensis) were also more prevalent at uninvaded points, and both of these species are often associated with mature coniferous habitat (Ehrlich et al. 1988). In contrast, red-eyed vireo (Vireo

Figure 2. PCA ordination of nine vegetation layers recorded in two 50 m X 2 m strip transects at 55 sample points, 28 invaded and 27 uninvaded. Factor loadings and eigenvalues are reported in Table 2.

Vegetation Layers Component 1 Component 2L1 (grass/low shrub) -0.771 0.260L2 (tree/shrub to 1 m) 0.112 0.349L2F (fruiting shrub to 1 m) -0.700 0.280L3 (tree/shrub 1-2 m) -0.773 0.061L3F (fruiting shrub 1-2 m) 0.610 0.084L4 (tree/shrub 2-3 m) -0.368 -0.382L4F (fruiting tree/shrub 2-3 m) 0.629 0.069L5O (tree > 3 m, open canopy) 0.044 -0.880L5C (tree > 3 m, closed canopy) 0.805 0.258

Eigenvalue 3.25 1.27% variance explained 36.1 14.1

Table 2. PCA factor loadings for the two vegetation structure axes used to ordinate sample sites (N = 55) in Figure 2.

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olivaceus) and rose-breasted grosbeak (Pheucticus ludovicianus) are commonly found in closed-canopy deciduous forest canopies (in this case created by invasive tree clones in absence of historic wildfire). Chestnut-sided warbler (Dendroica pen-sylvanica) was also found more often at invaded sites (in this case younger stands of black locust and aspens).

Our original selection criteria for invaded and uninvaded sites were supported by measured differences in vegetation struc-ture and composition, and our finding that the avian community varies with these differences was expected. Similar results have been reported from other fire-depen-dent ecosystems using a larger number of habitat variables (Kirk and Hobson 2001). In particular, differences in layering and tree stem densities are likely to be primary reasons for the low numbers of ground foragers at invaded points. For example, eastern towhee, which has experienced drastic population declines in the region (Hagan 1993), avoids areas with high densities of small trees (Greenlaw 1996; Bell and Whitmore 1997) where loss of understory and ground cover creates unsuit-able habitat (Krementz and Powell 2000). Prairie warbler has similarly strong habitat associations in pine barrens (Morimoto and Wasserman 1991).

Our designated “invasive” trees include

Abundance FrequencySpecies uninvaded invaded p uninvaded invaded pRed-eyed Vireo 0.03 0.23 0.00 0.11 0.44 0.01Red-breasted Nuthatch 0.37 0.11 0.01 0.64 0.33 0.02House Wren 0.25 0.07 0.02 0.50 0.19 0.01Chestnut-sided Warbler 0.03 0.15 0.03 0.11 0.33 0.04Pine Warbler 0.04 0.00 0.04 0.14 0.00 0.04Prairie Warbler 0.13 0.01 0.05 0.21 0.04 0.05Eastern Towhee 0.63 0.15 0.00 0.71 0.26 < 0.01Field Sparrow 0.07 0.00 0.01 0.21 0.00 0.01Rose-breasted Grosbeak 0.05 0.19 0.01 0.11 0.44 0.01

Table 3. Differences in species abundances (average number of individuals per point count) and frequencies of occurrence (proportion of points at which species was detected) in uninvaded and invaded areas. Probabilities (p values) are derived from Chi-square tests (1 df) for abundance and Mann-Whitney U-tests (1 df) for frequency.

Figure 3. CCA biplot of vegetation attributes and individual abundances for bird species recorded at > 5 sample stations. Species codes are reported in Table 1. Grp. A = NOCA, RBGB, WDTH; Grp. B = DOWP, REVI, WBNH; Grp. C = AMRO, BLJA, EWPE, HAWP; Grp. D = BCCD, GGCFC, HOWR, MODO, TUTI; Grp. E = RBNH, SCTA, VEER. See Appendix 1 for species codes. Eigenvalues: X-axis = 0.348, Y-axis = 0.218. Combined, the two axes explain 56.1% of the variance in species-vegetation correlations.

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two wide-ranging and locally-indigenous species plus a non-indigenous species that is native to other parts of North America. Distinctions between successional change and disruptive invasion into a protected nat-ural system are sometimes difficult to draw (Pickett and Thompson 1978; Cronk and Fuller 1995), particularly when the invad-ers have been in the vicinity for millennia. However, in the case of managed natural areas, a legitimate category of “home-grown exotics” has been suggested ( i.e., native species with invasive traits that get expressed in anthropogenic contexts) (Cox 1999). Vegetation management in Albany Pine Bush Preserve, including removal of black locust and aspen populations, was planned in response to decades of habitat fragmentation and fire suppression.

We did not investigate habitat-specific behaviors, such as movements among vegetation patches (Keller et al. 2002) or following an avian community through a successional sequence (Holmes and Sherry 2001). However, based on inference from community-level patterns observed during a single season, we discovered an impor-tant, unforeseen benefit of conservation management. Management plans for the Albany Pine Bush Preserve have been developed primarily for the protection of rare insects, in particular the federally-listed endangered Karner Blue butterfly, Lycaedis melissa samuelis (Zaremba 1991; Wilson 1992), as well as preservation of a rare inland barrens ecosystem (APBPC 2006). It now appears that campaigns to reduce invasive trees and to restore barrens’ habitats will also serve shrubland birds that are elsewhere in decline.

ACKNOWLEDGMENTS

We thank Neil Gifford of the Albany Pine Bush Preserve Commission for helpful advice and access to study sites, Ken Able and Charles Smith for expert advice and consultation, and anonymous reviewers for comments and careful editing. This re-search was conducted in partial fulfillment of the M.A. in Biodiversity, Conservation, and Policy Program, University at Albany, SUNY, for B.L. Beachy.

Brian Beachy lost his life to cancer on March 26, 2008. During the preparation of the manuscript, he was a doctoral candidate in Forest Science, Michigan Technological University.

George Robinson is Associate Professor of Biological Sciences, University at Albany, SUNY. His research interests include for-est ecology, biological conservation, and invasive species biology.

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Common name binomial codeAmerican Crow Corvus brachyrhynchos AMCRAmerican Goldfinch Carduelis tristis AMGFAmerican Robin Turdus migratorius AMROBaltimore Oriole Icterus galbula NOORBlack-capped Chickadee Poecile atricapilla BCCDBlue Jay Cyanocitta cristata BLJABlue-headed Vireo Vireo solitarius BHVIBlue-winged Warbler Vermivora pinus BWWABrown Creeper Certhia americana BRCRBrown Thrasher Toxostoma rufum BRTHBrown-headed Cowbird Molothrus ater BHCBCedar Waxwing Bombycilla cedrorum CEWAChestnut-sided Warbler Dendroica pensylvanica CHSWChipping Sparrow Spizella passerina CHSPCommon Yellowthroat Geothlypis trichas COYTDowny Woodpecker Picoides pubescens DOWPEastern Bluebird Sialia sialis EABLEastern Kingbird Tyrannus tyrannus EAKBEastern Towhee Pipilo erythrophthalmus EATOEastern Wood-Pewee Contopus virens EWPEField Sparrow Spizella pusilla FDSPGray Catbird Dumetella carolinensis GRCBGreat Crested Flycatcher Myiarchus crinitus GCFCHairy Woodpecker Picoides villosus HAWPHermit Thrush Catharus guttatus HETHHooded Warbler Wilsonia citrina HOWAHouse Wren Troglodytes aedon HOWRIndigo Bunting Passerina cyanea INBUMourning Dove Zenaida macroura MODONorthern Cardinal Cardinalis cardinalis NOCANorthern Flicker Colaptes auratus NOFLOvenbird Seiurus aurocapillus OVBDPileated Woodpecker Dryocopus pileatus PIWPPine Warbler Dendroica pinus PIWAPrairie Warbler Dendroica discolor PRWARed-breasted Nuthatch Sitta canadensis RBNHRed-eyed Vireo Vireo olivaceus REVI

(continued)

Appendix. List of bird species detected in 50 m radius point counts among 55 point count stations in the Albany Pine Bush.

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ROOFCommon name binomial codeRed-tailed Hawk Buteo jamaicensis RTHKRose-breasted Grosbeak Pheucticus ludovicianus RBGBRuffed Grouse Bonasa umbellus RUGRScarlet Tanager Piranga olivacea SCTASong Sparrow Melospiza melodia SOSPTufted Titmouse Baeolophus bicolor TUTITurkey Vulture Cathartes aura TUVUVeery Catharus fuscescens VEERWhite-breasted Nuthatch Sitta carolinensis WBNHWood Thrush Hylocichla mustelina WDTH

Appendix. Continued.