2010 NORTHEASTERN NATURALIST 17(4):647–658 Possible Impact of Multiflora Rose on Breeding-Bird Diversity in Riparian Forest Fragments of Central Delaware Roger J. Massé1,2,* and Kevina Vulinec1 Abstract - The populations of many North American forest-breeding songbirds have declined over the past few decades, initiating much research regarding the factors influencing avian use of remaining forests, many of which are highly disturbed and impacted by invasive plants. Our objective was to compare the species richness of breeding birds in riparian forest fragments that contain different amounts of the invasive shrub, Rosa multiflora (Multiflora Rose). We conducted 20 point counts in each of three sites from early June until mid-July of 2008 and 2009, and estimated species richness and relative richness using the program COMDYN4. During 2008, species richness was lower at the site with the most Multiflora Rose. However, the number of species at that site increased by 33% from 2008 to 2009, whereas the number of species in the other two sites remained similar. Consequently, we did not detect differences in species richness among sites during 2009. Despite the increase in species richness at the more heavily invaded site, several common ground- to shrub-nesting species did not occur at that site during either year. Multiflora Rose may reduce the species richness of breeding birds in forest fragments, but additional research coinciding with the control and removal of this invasive shrub will be needed to infer such a relationship. Introduction Declines in the populations of many avian species are well documented throughout much of North America. Of particular interest to many researchers are the negative trends exhibited by numerous species of forest-breeding songbirds. Habitat loss and degradation on both breeding and wintering grounds are typically regarded as the most important factors causing the observed trends (Heske et al. 2001, Robbins et al. 1989b, Schmiegelow and Mönkkönen 2002, Sherry and Holmes 1996). The preservation of riparian buffers can ameliorate the negative effects of habitat loss and degradation by providing habitat for wildlife. This is especially true in agriculturally dominated landscapes where riparian buffers are often viewed as important conservation foci (NRCS 2009). The benefit of riparian buffers for avian conservation can be illustrated by considering the species richness of the assemblages found using these areas. For example, 57 species were observed using four riparian habitat types in northwestern Mississippi (Smiley et al. 2007). In Georgia, 48 species 1Department of Agriculture and Natural Resources, Delaware State University, 1200 North DuPont Highway, Dover, DE 19901. 2Department of Natural Resources Science, University of Rhode Island, 102 Coastal Institute in Kingston, Kingston, RI 02881. *Corresponding author - rjmasse@mail.uri.edu. 648 Northeastern Naturalist Vol. 17, No. 4 of breeding birds were documented in riparian forests of different widths along the Altamaha River (Hodges and Krementz 1996). A similar number of breeding birds were found in riparian forests on the Delmarva Peninsula (Keller et al. 1993). Twenty-five species of breeding birds were found in riparian corridors in Clay County, SD compared to just 15 species in more upland woodlots (Gentry et al. 2006). Importantly, riparian forests may promote beta diversity by supporting distinct assemblages of birds compared to more upland sites (Lehmkuhl et al. 2007). Due to the importance of these areas, riparian forests have been studied extensively in an effort to understand the relationships between avian species richness and various habitat features (Fleishman et al. 2003, Hanowski et al. 2005). Most researchers have found that species richness is positively correlated with riparian forest width (Peak and Thompson 2006, Shirley and Smith 2005). In some cases, variation in species richness is better explained by forest width than by vegetation structure (Shirley 2004). Consequently, the protection of wide (e.g., ≥100 m) riparian forests is typically advocated to benefit the greatest number of species (Peak and Thompson 2006, Pearson and Manuwal 2001). The composition or structure of the vegetation within remaining forest fragments may also influence the species richness of avian assemblages (Hanowski et al. 2005, Robbins et al. 1989a). For instance, the presence of some species is positively correlated with shrub cover (Doherty and Grubb 2000), and the establishment of invasive plants can reduce the diversity of breeding birds (Burghardt et al. 2009, Klaus and Keyes 2007). Others have found no effect of non-native plants on songbird populations (Wilcox and Beck 2007). One possible mechanism by which invasive plants could impact avian species richness is through habitat degradation. In theory, alien plants could degrade habitat quality by reducing the biomass of phytophagous insects (Tallamy 2004), which act as an important trophic link between plants and insectivorous wildlife (Wilson 1987). In some cases, invasive plants may leave species more vulnerable to brood parasitism (Stoleson and Finch 2001) or nest predation (Borgmann and Rodewald 2004, Schmidt and Whelan 1999). However, not all birds nesting in alien plants experience these negative impacts (Heckscher 2004, Schmidt et al. 2005, Van Riper et al. 2008). Given that results related to the influence of invasive plants on forest breeding birds are conflicting, further investigation into this relationship is needed. The objective of this study was to compare the species richness of breeding birds in riparian forest fragments that contain different amounts of the invasive shrub Rosa multiflora Thunb. ex Murr. (Multiflora Rose). We hypothesize that if Multiflora Rose exerts a negative influence on breeding birds, then species richness will be reduced in more heavily invaded sites. 2010 R.J. Massé and K. Vulinec 649 Methods Study sites We examined the species richness of breeding birds in three small riparian forest fragments in central Delaware. Approximately 206,492 ha (40%) of Delaware’s land area are dedicated to agriculture, with nearly 85% of this area consisting of cropland (USDA 2007). Consequently, the landscapes surrounding each site were dominated by agriculture. The Upper Blackbird Creek forest (39°23'23"N, 75°38'17"W) is located near the town of Townsend, DE in New Castle County and is managed by the Delaware National Estuarine Research Reserve. That site is roughly 12.6 ha in size, but is connected to a larger (62-ha) forest fragment; the remainder of which is privately owned. Approximately 828 ha of the landscape within two km of that site are forested. The Finis (39°16'44"N, 75°29'43"W) and Steamboat (39°12'28"N, 75°27'49"W) forests are located near the towns of Smyrna and Little Creek, DE, respectively, in Kent County. Those sites are managed by Bombay Hook National Wildlife Refuge. The Finis site is approximately 13.6 ha in size, but is connected to a larger (39-ha) forest fragment. About 206 ha of the landscape within two km of that site are forested. The Steamboat site is about 12.6 ha in size and completely isolated from surrounding forest. Roughly 40 ha of the landscape within two km of that site are forested. We visited sites prior to final selection to visually examine the composition of the dominant vegetation. Each site consisted primarily of Liquidambar styraciflua L. (Sweet Gum), Liriodendron tulipifera L. (Yellow Poplar), Quercus spp. (oaks), Ilex opaca Ait. (American Holly), Acer rubrum L. (Red Maple), Vaccinium corymbosum L. (Highbush Blueberry), and Viburnum dentatum L. (Arrowwood). Multiflora Rose appeared most abundant in the Upper Blackbird Creek forest followed by the Finis forest. Field methods We established 30-x30-m grids in each site during April 2008 by placing colored flagging along a compass bearing of the longest distance in each site, perpendicular to a property boundary. We spaced subsequent transects parallel to that transect, assigned each flag a number, and recorded its location using a Garmin GPSMAP 76CSx. We randomly chose five locations within each site using a random number generator and conducted one unlimited-radius 10-minute point count (Verner 1988) at each location from 8 June–16 July during 2008 and 2009 to establish the presence of avian species during the breeding season. A single observer conducted each point count. Upon arriving at locations, we allowed five minutes to pass before beginning point counts. We identified species by sight or sound, included only species that were seen or heard within each site, and initiated all point counts between 0530–0800 on mornings with favorable weather conditions (e.g., without rain or strong wind). Prior to the 2009 breeding season, we selected 10 additional locations within each site 650 Northeastern Naturalist Vol. 17, No. 4 using restricted random sampling to increase sampling intensity and improve the dispersion of point-count locations. We divided the flagged locations into 10 groups of approximately equal size and randomly chose one flagged location from each group by drawing from a hat. By chance, none of the locations we selected in 2008 were included in these selections. We conducted point counts at each of these locations using identical protocol. We sampled for Multiflora Rose at systematically selected locations in the Upper Blackbird Creek (n = 25), Finis (n = 30), and Steamboat (n = 23) forests during August 2009. We determined the starting location on the initial transect by selecting one of the first two flags by flipping a coin, and then selected every odd- or even-numbered flag thereafter. Though not completely random, systematic sampling is preferred in many situations and is able to produce unbiased estimates (Valentine et al. 2009). Following selection, we pulled one cardinal direction from a hat and established a 0.00785-ha circular plot (5-m radius) at 5 m in the chosen direction from each flag. We believe this added an element of randomness and helped to reduce any bias we may have introduced when establishing transects. Within each plot, we counted the number of Multiflora Rose stems and visually estimated the percentage of Multiflora Rose ground cover. Statistical analysis We analyzed point-count data for species richness and relative richness using the program COMDYN4 (Hines et al. 1999). This program allows users to input incidence (e.g., presence/absence) data, accounts for heterogeneity in species detection, and calculates numerous statistics related to community dynamics based on the jackknife estimator (Burnham and Overton 1979, Hines et al. 1999, Nichols et al. 1998). Estimation of these parameters is contingent upon detection frequencies obtained during sampling periods. COMDYN4 also performs chi-square tests to compare average detection probabilities (Hines et al. 1999) and determine how well the data fits model Mh, the model upon which the programs estimator is based (Burnham and Overton 1978, Nichols et al. 1998). The jackknife estimator of species richness is among the least biased and most precise nonparametric methods available (Colwell and Coddington 1994, Walther and Martin 2001). We calculated descriptive statistics for Multiflora Rose stem density and percent ground cover in each site. Because data were not normally distributed, and could not be normalized using standard transformations, we tested for differences between sites using the Mann-Whitney test. We used Minitab 15 for all calculations. Results We observed 15 species in the Upper Blackbird Creek forest, 22 species in the Finis forest, and 25 species in the Steamboat forest during 2008 (Fig. 1a). From the same locations, we recorded 20 species in both the 2010 R.J. Massé and K. Vulinec 651 Upper Blackbird Creek and Finis forests and 21 species in the Steamboat forest during 2009 (Fig. 1b). During 10 additional point counts in 2009, we encountered 22 species in the Upper Blackbird Creek forest and 26 species in both the Finis and Steamboat forests (Fig. 1c). In total, we documented the occurrence of 26 species in the Upper Blackbird Creek forest and 29 species in both the Finis and Steamboat forests during the 2008 and 2009 breeding seasons (Table 1). Figure 1. Bird species accumulation curves for the Upper Blackbird Creek (UBC), Finis (FIN), and Steamboat (STE) forests of central Delaware based on point counts conducted from 8 June–16 July of 2008 (a) and 2009 (b and c). 652 Northeastern Naturalist Vol. 17, No. 4 Model Mh of the program COMDYN4 satisfactorily fit point-count data from all sites, years, and sample sizes (P ≥ 0.07). Furthermore, average detection probabilities did not differ between sites or years (P ≥ 0.10). From 2008–2009, estimated species richness ranged from 16–25 in the Upper Blackbird Creek forest, 21–32 in the Finis forest, and 28–34 in the Steamboat forest. The Finis and Steamboat forests contained approximately 47% and 67% more species, respectively, than the Upper Blackbird Creek forest during 2008 (P < 0.05). However, differences in species richness did not exist among sites during 2009 (Table 2). From 2008–2009, the number Table 1. Bird species detected in the Upper Blackbird Creek (UBC), Finis (FIN), and Steamboat (STE) forests of central Delaware during 20 point counts conducted from 8 June–16 July of 2008 and 2009. *Species detected during ≥1 point count. Species Migratory status1 UBC FIN STE Agelaius phoeniceus L. (Red-winged Blackbird) S * * Archilochus colubris L. (Ruby-throated Hummingbird) N * Baeolophus bicolor L. (Tufted Titmouse) R * * * Buteo jamaicensis Gmelin (Red-tailed Hawk) S * * Cardinalis cardinalis L. (Northern Cardinal) R * * * Carduelis tristis L. (American Goldfinch) S * Coccyzus americanus L. (Yellow-billed Cuckoo) N * * * Colaptes auratus L. (Northern Flicker) S * * * Contopus virens L. (Eastern Wood-Pewee) N * * * Corvus brachyrhynchos Brehm (American Crow) R * Cyanocitta cristata L. (Blue Jay) S * * * Dendroica petechia L. (Yellow Warbler) N * * Dumetella carolinensis L. (Gray Catbird) S * * Empidonax virescens Vieillot (Acadian Flycatcher) N * Geothlypis trichas L. (Common Yellowthroat) S * * Hylocichla mustelina Gmelin (Wood Thrush) N * * Melanerpes carolinus L. (Red-bellied Woodpecker) R * * * Melospiza melodia Wilson (Song Sparrow) S * Molothrus ater Boddaert (Brown-headed Cowbird) S * * * Myiarchus crinitus L. (Great Crested Flycatcher) N * * * Oporornis formosus Wilson (Kentucky Warbler) N * Passerina caerulea L. (Blue Grosbeak) N * * Passerina cyanea L. (Indigo Bunting) N * * * Picoides pubescens L. (Downy Woodpecker) R * * * Picoides villosus L. (Hairy Woodpecker) R * * * Pipilo erythrophthalmus L. (Eastern Towhee) S * * Piranga olivacea Gmelin (Scarlet Tanager) N * * Poecile carolinensis Audubon (Carolina Chickadee) R * * * Quiscalus quiscula L. (Common Grackle) S * Seiurus aurocapilla L. (Ovenbird) N * Sitta carolinensis Latham (White-breasted Nuthatch) R * * * Strix varia Barton (Barred Owl) R * Thryothorus ludovicianus Latham (Carolina Wren) R * * * Toxostoma rufum L. (Brown Thrasher) S * * * Turdus migratorius L. (American Robin) S * * * Vireo griseus Boddaert (White-eyed Vireo) S * * Vireo olivaceus L. (Red-eyed Vireo) N * * * Zenaida macroura L. (Mourning Dove) S * 1Neotropical migrant (N), short-distance migrant (S), or permanent resident (R). 2010 R.J. Massé and K. Vulinec 653 of species in the Upper Blackbird Creek forest increased by about 33% (P < 0.05), whereas the number of species in both the Finis and Steamboat forests remained similar. Despite a significant increase in species richness in the Upper Blackbird Creek forest from 2008–2009, Common Yellowthroat, Eastern Towhee, and Gray Catbird were never encountered at that site during either year. We did not detect Multiflora Rose in the Steamboat forest. Multiflora Rose stem density per plot in the Upper Blackbird Creek forest (median = 7, range = 0–14) was greater (W = 880.5, P = 0.0007) than in the Finis forest (median = 0, range = 0–21). Likewise, percent Multifora Rose cover per plot in the Upper Blackbird Creek forest (median = 10, range = 0–50) was greater (W = 911.5, P = 0.0001) than in the Finis forest (median = 0, range = 0–10). Discussion We found that the species richness of breeding birds varied among similar-sized riparian forest sites containing different amounts of Multiflora Rose. Estimated species richness tended to be lowest in the site with the most Multiflora Rose. During 2008, the Finis and Steamboat forests contained roughly 47–67% more species than the Upper Blackbird Creek forest. However, species richness was similar among sites during 2009. This change likely resulted from an increase in species richness in the Upper Blackbird Creek forest of about 33% from 2008–2009. Nevertheless, we detected fewer species in the Upper Blackbird Creek forest—the site where Multifora Rose was most abundant. We assumed that 5 point counts would be sufficient for estimating species richness given the small size of the sites we investigated. However, Table 2. Relative richness between sites and years estimated as the ratio of the observed number of bird species at occasion two to the observed number of bird species at occasion one (Hines et al. 1999, Nichols et al. 1998). For each comparison, estimates >1.00 indicate a higher number of species in the second site or year relative to the first. Confidence intervals that exclude 1.00 indicate significant differences in species richness between sites or years. Comparison Year Relative richness (95% confidence interval) UBC/FIN 2008 1.47 (1.13–1.86) UBC/STE 2008 1.67 (1.27–2.07) FIN/STE 2008 1.14 (0.84–1.56) UBC/FIN 2009 1.00 (0.82–1.18) UBC/STE 2009 1.05 (0.76–1.32) FIN/STE 2009 1.05 (0.76–1.33) UBC/UBC 2008/2009 1.33 (1.07–1.58) FIN/FIN 2008/2009 0.91 (0.74–1.18) STE/STE 2008/2009 0.84 (0.55–1.10) UBC/FIN 2009* 1.18 (0.91–1.43) UBC/STE 2009* 1.18 (1.00–1.42) FIN/STE 2009* 1.00 (0.84–1.27) *Sampling design consisting of ten point counts selected using restricted random sampling. 654 Northeastern Naturalist Vol. 17, No. 4 species richness is most accurately estimated once species-accumulation curves have reached a clear asymptote (Magurran 2004). Since our curves did not reach convincing asymptotes until we used larger sample sizes (n = 10), we recommend that our estimates of species richness be interpreted with caution. However, it appears that species-accumulation curves for these sites can approach their asymptote in as few as 6 point counts (Fig. 1c). On the other hand, our data may allow for meaningful comparisons in terms of relative richness. When average detection probabilities do not differ, relative richness is most efficiently estimated as the ratio of species observed at two occasions (Nichols et al. 1998). Thus, estimates of relative richness, along with their 95% confi- dence intervals, can be used to examine differences in species richness (e.g., Meyers and Pike 2006). Therefore, we can conclude that species richness was lowest in the Upper Blackbird Creek forest during 2008 and that the number of species at that site increased from 2008 to 2009 (Table 2). Of the species we observed in the Upper Blackbird Creek forest, all but one (Kentucky Warbler) were encountered, either during or outside of point-count sessions (e.g., when walking to locations or collecting unrelated data), in the Finis and Steamboat forests. In contrast, three of the species we detected in the Finis and Steamboat forests were never encountered during or outside of point-count sessions in the Upper Blackbird Creek forest. These included Common Yellowthroat, Eastern Towhee, and Gray Catbird. We believe these species were not simply missed during sampling, but rather, did not occur in the Upper Blackbird Creek forest, given their relative commonness in the region, typically conspicuous habits (e.g., loud and persistent singing), and that average detection probabilities did not differ between sites or years. Despite a significant increase in species richness in the Upper Blackbird Creek forest from 2008–2009, these otherwise common ground- to shrub-nesting species that we might have expected to find there remained absent. Multiflora Rose could reduce the species richness of breeding birds by discouraging the presence of some ground- to shrub-nesting species such as those mentioned above. This possibility is especially true given that invasive plants frequently degrade habitat quality by modifying habitat structure (Collier and Vankat 2002, Flanders et al. 2006, Knight et al. 2007). In southeastern Pennsylvania, properties landscaped with native plants supported higher bird abundances and species richness than properties landscaped with non-native plants (Burghardt et al. 2009). Moreover, breeding-bird diversity of upland Pinus spp. (pine) forests in Georgia is reduced in areas where invasive trees have become established (Klaus and Keyes 2007). It is possible that differences in forest structure other than the degree of Multiflora Rose influenced the species richness of the breeding birds at the sites we examined. For example, the removal of tree basal area from riparian forests can alter breeding-bird assemblages by promoting the occurrence of early successional species and limiting the occurrence of forest interior species (Hanowski et al. 2005). However, differences in the size (Doherty 2010 R.J. Massé and K. Vulinec 655 and Grubb 2000, Shirley 2004) and amount of forest cover within 2 km of a site (Robbins et al. 1989a) may be the most important factors influencing species richness. Despite being part of a larger forest fragment and existing in a more forested landscape, the Upper Blackbird Creek forest appeared to provide habitat for fewer species than either the Finis or Steamboat forests. This observation contradicts with what could be expected based on forest size and landscape composition. Thus, differences in forest structure among these sites may exert a greater influence on species richness than in other areas. In a separate analysis of 11 forest-structure variables, the only consistent differences among all three sites were the stem density and percent cover of Multiflora Rose (Massé 2009). Our results should be viewed as preliminary observations regarding the possible impact of Multiflora Rose on the species richness of breeding birds in forest fragments. Future monitoring and additional research concurrent with the removal and control of this invasive shrub are needed to more clearly understand how Multiflora Rose influences breeding-bird diversity. A critical flaw in our study is that it is limited to just three sites over a period of two years. As a result, we are not able to determine whether or not there is a correlation between breeding-bird diversity and Multiflora Rose invasion. Consequently, research is needed in other regions, in additional sites with varying amounts of Multiflora Rose, and for extended periods to determine the consistency of our results in other landscapes and whether or not breeding birds exhibit a threshold response to the abundance of this alien shrub. We hope that our preliminary results stimulate such work. Acknowledgments Funding for this research was provided by Grant # NA060AR4810164 from the National Oceanic and Atmospheric Administration through the Educational Partnership Program under the Environmental Cooperative Science Center. We would like to thank the Delaware National Estuarine Research Reserve and Bombay Hook National Wildlife Refuge for the use of their properties, and A. Anoruo, B. Scarborough, R. Barczewski, and two anonymous reviewers for helpful comments on an earlier version of this manuscript, and J. Massé for her help while setting up transects. Literature Cited Borgmann, K.L., and A.D. Rodewald. 2004. 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