Importance of Riparian Forest Buffers in Conservation ...

Importance of Riparian Forest Buffers in Conservation of Stream Biodiversity: Responses to Land Uses by Stream-Associated Salamanders across Two Southeastern Temperate Ecoregions Author(s): Thilina D. Surasinghe and Robert F. Baldwin Source: Journal of Herpetology, 49(1):83-94. Published By: The Society for the Study of Amphibians and Reptiles URL: http://www.bioone.org/doi/full/10.1670/14-003

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Journal of Herpetology, Vol. 49, No. 1, 83–94, 2015 Copyright 2015 Society for the Study of Amphibians and Reptiles

Importance of Riparian Forest Buffers in Conservation of Stream Biodiversity: Responses to Land Uses by Stream-Associated Salamanders across Two Southeastern Temperate Ecoregions THILINA D. SURASINGHE1,2,3

AND

ROBERT F. BALDWIN2

1

2

Department of Biology, Gustavus Adolphus College, St. Peter, Minnesota 56082 USA School of Agricultural, Forest, and Environmental Sciences, Clemson University, Clemson, South Carolina 29634 USA

ABSTRACT.—Stream microhabitats are strongly influenced by adjacent terrestrial land use and other anthropogenic disturbances. Therefore, sensitive stream fauna can be highly imperiled. We investigated relative susceptibility of stream-associated salamanders to riparian land use by studying species-specific responses that influence community assembly. The Piedmont and Blue Ridge ecoregions of the southeastern United States have high aquatic biodiversity, centuries of land use, and increasingly extensive urbanization. We surveyed low-order streams in these regions for salamanders across four riparian land uses (forests, agricultural, residential, and urban) and assessed 15 habitat variables at each sampling site. We found that forested streams were more diverse compared to streams affected by riparian land uses. Our study showed two distinct assemblages of salamanders in response to riparian land use: forest-dependent, large-bodied, long-lived species sensitive to riparian land uses (disturbance avoiders) and cosmopolitan, small-bodied, short-lived species that are relatively resistant to impacts of riparian land uses (disturbance tolerants). These assemblages varied in composition between the ecoregions, with Blue Ridge harboring more land-use–intolerant species. Results indicated that multiple habitat features of the riparian zone (canopy cover, canopy height, leaf litter cover), and stream geomorphology (bank complexity, streambed heterogeneity, sedimentation) are dramatically altered by riparian land uses, and influence the assemblage structure of salamanders. Riparian buffers in both ecoregions are largely unprotected (70% in Blue Ridge, 96% in Piedmont) and are possibly threatened with anthropocentric land uses. Results suggested that conservation of stream salamander communities should be strengthened with protection and restoration of riparian forests, connectivity among riparian forests, and soil-conservation practices.

Conversion of landscapes to human settlements, agriculture, and infrastructure are the primary causes of habitat degradation and biodiversity loss in stream ecosystems (Abell, 2002; Allan, 2004; Dudgeon et al., 2006). Urbanization induces the most devastating impacts on streams where impervious surfaces replace the natural land cover, resulting in dramatic geomorphological, hydrological, chemical, and biological changes (Scott et al., 2002). Impacts of anthropogenic disturbances on stream ecosystems are intricate and highly variable, depending on focal taxa and geography; hence biological responses to land transformations need to be addressed with an ecoregion-wide perspective (Utz and Hilderbrand, 2010). Among species imperiled by land uses, amphibians have generated research attention ranging from global analyses of patterns and causes of decline, to prescriptions for local habitat conservation plans (Houlahan et al., 2000; Ficetola and De Bernardi, 2004; Gallant et al., 2007). Among global amphibian fauna, 32% are considered critically endangered, endangered, or vulnerable because of multiple anthropogenic stressors, and 43% of the extant species suffer population declines, making amphibians among the most imperiled vertebrates (Stuart et al., 2004). Salamanders account for 64% of the amphibian diversity of North America; 22% of North American salamander species are ‘‘globally threatened’’ (IUCN, 2012). Salamanders account for 60–80% of the animal biomass in headwaters and vernal pools (Windmiller, 1996; Peterman et al., 2008). As important consumers of the aquatic and forest-floor ecosystems, they exert a top-down control on lower tropic levels, particularly invertebrate guilds (Burton and Likens, 1975; Wyman, 1998). The high biomass, combined with their trophic function, makes them key players of biogeochemical cycles (Burton and Likens, 1975; Davic and Welsh, 2004). Amphibians are cost-effective sentinels of ecological integrity (Welsh and Ollivier, 1998; Welsh and Droege, 2001). Further, amphibians are sensitive to human-induced environmental 3

Corresponding Author. E-mail: [email protected]

DOI: 10.1670/14-003

perturbations such as sedimentation, altered hydrothermal regimes, reduced supply of allochthonous organic matter, and watershed deforestation (Corn and Bury, 1989; Welsh and Hodgson, 2008; Olson and Burnett, 2009). Urbanization and agriculture can reduce the diversity of salamanders across many terrestrial and aquatic habitats (Barrett and Guyer, 2008; Baldwin and Demaynadier, 2009; Barrett et al., 2010; Price et al., 2011). Most research on salamanders was limited to a few focal species and to a smaller geographical extent; hence community-level, landscape-scale investigations on salamander occupancy in stream habitats across land-use gradients are scarce. To fill these gaps and contribute to ongoing conservation efforts, we investigated the effects of different riparian land-cover types across two ecoregions (Blue Ridge and Piedmont), on species composition of aquatic plethodontid salamanders, a highly diverse group in our study region. There are 102 species of salamander and 20 species of anurans recorded from Blue Ridge and Piedmont (Dorcas and Gibbons, 2008; Mitchell and Gibbons, 2010). The Blue Ridge is a global hot spot for salamander diversity (approximately 25 aquatic and 25 terrestrial plethodontids) and a center of plethodontid evolution (Arnold, 2000; Highton, 2000). The Piedmont is home to about 12 and 10 species of aquatic and terrestrial plethodontids, respectively (Mitchell and Gibbons, 2010). Our specific objectives were (1) to examine variation of salamander diversity and species-specific responses across the riparian land-use gradient and ecoregions, (2) to determine fundamental environmental variables that shape habitat associations of stream salamanders, and (3) to assess currently protected riparian forest cover and recommend conservation actions that focus on stream ecosystems, including targeted land management, policy, and regulatory actions. MATERIALS

AND

METHODS

Study Site.—The Blue Ridge and Piedmont ecoregions of the southeastern United States (Fig. 1) include a diverse array of land

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T. D. SURASINGHE AND R. F. BALDWIN

FIG. 1. Study site: Blue Ridge and Piedmont ecoregions in the conterminous United States and the southeastern United States.

forms and land-cover types (Abella and Shelburne, 2004) and are rich in biodiversity and endemism (Hackney et al., 1992; Liu et al., 2006; Graham et al., 2010). Extensive cotton farming (an intensive land use) in the Piedmont between early-18th and mid19th centuries altered the region’s stream geomorphology (Galang et al., 2007). During the same time frame, the Blue Ridge experienced extensive deforestation, but forests rapidly returned following land abandonment and delineation of protected areas (Bolgiano, 1998). The aesthetic and recreational advantages of this area led to an amenity-based housing boom, primarily for secondary and vacation homes, creating an extensive wildland–urban interface in recent decades (Radeloff et al., 2005; Theobald and Romme, 2007). In the Piedmont, urban and exurban development have followed farmland abandonment, creating a megaurban corridor (Brown et al., 2005). Sampling Design.—Sampling occurred at 101 low-order (1–3) stream reaches within watersheds < 25 km2 (Vannote et al., 1980), blocked across two ecoregions, in association with four riparian land uses: forested, agricultural, residential, and urban. The classification of the riparian area was based on the dominant (‡ 50%) land-use type within a 500-m radius at each sampling point; similar approaches were used in other research on urban– rural gradients (McKinney, 2002, 2008). Definition of the landcover types was based on Anderson (1976). We selected sites that shared < 50% of the same drainage and used a VisualBasic query to ensure that sampling sites were not spatially autocorrelated (Scott, 2009). We selected a 100-m stream segment per sampling point and surveyed the wet channel and undercut banks for adult and larval salamanders via three repeat upstream passes over the same segment. The survey involved dip netting, overturning movable rocks and logs and searching their surfaces, examining crevices, and scrutinizing surfaces of large rocks and woody debris. We conducted three repeat surveys of stream banks to a distance of 1 m from the wet channel where we overturned all movable rocks and logs and searched through leaf litter, moss, and understory vegetation (Heyer et al., 1994; Dodd, 2010). Surveys were conducted daily between 0800 and 1800 h for 55 sampling days during early April to mid-July for two consecutive years (2010, 2011). Sampling was conducted only on clear-sky, nonrainy days to minimize variability of species detection caused by weather. We identified all captured individuals, recorded the species name and number of individuals captured from each species, and released back to

the capture site. We assessed 15 habitat variables of the wet channel and the riparian zone at each sampling site (Table 1) selected a priori based on stream ecology and natural history of plethodontids (Hicks and Pearson, 2003; Petranka and Smith, 2005). We employed multiple passes and a consistent, trained field crew to increase detection. We plotted species accumulation curves for each land-use type and both ecoregions to assess species detectability visually (Flather, 1996). Statistical and Geospatial Analyses.—We used arcsine square-root transformation to approximate normality for species richness, for all statistical analyses. All our statistical analyses were based on R 2.15.1 (R Core Team, 2013) and JMP 9.0 (SAS Institute Inc., 2012) (a < 0.05), and all the geospatial analyses were based on ArcGIS 10 (ESRI). Variation in Salamander Diversity across Riparian Land-Use Types.—We calculated species richness for each riparian landuse type and performed a one-way ANOVA to determine significant differences among land uses for species richness, followed by LSMeans contrast tests to determine whether species richness was significantly higher for forested streams than other land uses. Identifying Species-Specific Responses and Habitat Associations.— We performed nonmetric multidimensional scaling (NMDS) to identify species assemblages that segregate in response to four land uses (Bray-Curtis dissimilarity matrix, 50 random starting configurations, two-dimension ordinations), followed by a Monte Carlo simulation (1,000 iterations). Based on the ordinations, we classified species into three functional groups (Fig. 3): disturbance avoiders (species predominantly associated with forested streams), disturbance tolerators (species mostly associated with nonforest riparian land uses, but also occurring in forested streams), and disturbance exploiters (species exclusively associated with nonforest riparian land uses). Our classification of species responses to riparian land use was modified from McKinney (2002) and Blair (2001), and describes the habitat use of birds, mammals, and butterflies along an urban–rural gradient based on species adaptability to inhabit human-dominated landscapes. Our study is comparable to both McKinney (2002) and Blair (2001) in that we attempt to describe the community composition of stream-associated salamanders in response to a riparian land-use gradient that may present life-history constraints to native biodiversity similar to an urban–rural gradient. Environmental Correlates of Land-Use Types.—We performed a principal-component analysis (PCA) on the correlation matrix of

RIPARIAN LAND USE AND STREAM SALAMANDERS

85

TABLE 1. Habitat variables estimated at the sampling sites and the methods of estimation. The average was calculated from the multiple measurements/estimations taken at a certain sampling location for a given habitat characteristic. Habitat characteristics

Techniques, instruments used for measurements/estimations

3

Stream velocity (m /s) Water depth Streambed heterogeneity Stream substrate particle size Particle-size ratio (stream substrate) Streambed embedness Bank complexity

Water quality Percent canopy cover Canopy height Percent litter cover Litter depth Topsoil thickness (A horizon) Basal area

Measured at 100 random points with a flow meter Measured at 100 random points using a top-set wading rod With the use of the zigzag method (Bevenger and King, 1995), the types of substrates were recorded (supplemental information, SI1), and the percent cover of each substrate type on the streambed was calculated Intermediate axes of the inorganic stream substrate particles were measured. Inorganic particles too large to pick up were measured on the streambed with the meter stick. If the substrate is bedrock, record as 999 mm (Bevenger and King, 1995) Calculated based on length measurements of the intermediate axis of the streambed particles (d84/d50, di indicates the particle size larger than the ith percentile of particles [Wolman, 1954]). The depth of the sediments deposited on the streambed was measured at 50 random points. Assessed at 10 random locations of both stream banks on a scale of 0–10, 0 for lowest heterogeneity and 10 for the highest. Presence of undercut banks, littoral vegetation, moss cover, and roots of woody plants were considered as indicators of high complexity. Water temperature, turbidity, pH, conductivity, and dissolved oxygen, measured at 10 random locations in the wet channel with the use of the 6-series multiparameter water quality sondes (YSI Inc.) Measured at 10 points (at every tenth meter) along the wet channel, facing four cardinal directions per point with a spherical densitometer (concave Model C, Forestry Suppliers Inc.). Measured at 10 points (at every tenth meter) with the use of a clinometer on woody tree species of the overstory layer at each bank Measured at five, 5 · 5–m litter quadrats placed (at every tenth meter), at each bank, along each riparian transect Measured at five random points inside all 5 · 5–m litter quadrats at each bank, along each riparian transect Measured at five random points at each bank, along the riparian transect Measured at five points (at every twentieth meter), with the use of a cruising prism (BAF 10, Forestry Suppliers Inc.) at each bank, along each riparian transect

habitat variables. We selected all PCs that individually explained > 10% of the overall environmental variability and used Pearson correlation coefficients between those selected PCs and habitat variables to verify environmental correlates of derived PCs. Based on these habitat variables and natural history of focal species, we identified potential mechanisms of species responses to riparian land use. Determining the Protected Area Coverage for Riparian Buffers.— We generated 140 m (Olson et al., 2007) and 240 m (Semlitsch and Bodie, 2003) riparian zones (ArcGIS 10) around streams (National Hydrography Dataset) within the Blue Ridge and Piedmont ecoregions. We calculated the extent of buffers located inside and outside mapped protected areas (Protected Area Database of the USA; PADUS Version 1.3) and the management level (USGS Gap Analyses Program) of riparian zones falling within protectedarea buffers. We also calculated the area of riparian habitat that would be subject to improved regulatory and management actions, and catalogued examples of regulatory and management actions. RESULTS Variation of Stream Salamander Diversity across Riparian Land-Use Types.—Species distribution of salamanders differed by ecoregion, with 11 species representing three plethodontids genera (Eurycea, Desmognathus, and Gyrinophilus) in the Blue Ridge, and 7 species of the same genera in the Piedmont (Table 2). Species accumulation curves reached the asymptote after the first few sampling occasions, regardless of ecoregion and land use, suggesting a high rate of species detectability (Fig. 2). Our

samples in Blue Ridge forested streams represented 100% of known regional plethodontid diversity; 85% of surveyed forested streams hosted all 11 species we detected. We recorded a total of seven species in forested Piedmont streams, which is 80% of those expected to occur. We did not encounter adult stages of Desmognathus marmoratus (Moore, 1899), Desmognathus monticola Dunn (1916) (Dunn, 1916), Desmognathus ocoee Nicholls (1949) (Nicholls, 1949), or Eurycea wilderae Dunn (1920) (Dunn, 1920) at any of the Piedmont forested streams. Only 10% of Piedmont streams harbored all seven species we detected in the region. Agricultural streams were the lowest in cumulative species richness (three and four species in the Blue Ridge and Piedmont, respectively). Residential and urban streams were also substantially species poor (five and four species in the Blue Ridge and Piedmont, respectively). Richness was greatest in forested streams, in both ecoregions. The average species richness differed significantly among the riparian land uses for both adults (one-way ANOVA: F = 17.10, P < 0.05) and larvae (F = 14.28, P < 0.05). Blue Ridge forested streams had significantly greater species richness of adults (LSMeans Contrast: F = 25.31, P < 0.05) and larvae (F = 21.82, P < 0.05) than in nonforest Blue Ridge streams. Average species richness across land uses in the Piedmont differed by life stage, with no differences found for adults in forest against nonforest streams (F = 2.20, P > 0.05); the larval richness was significantly greater in forest vs. nonforest streams (F = 5.01, P < 0.05). Species-Specific Responses of Stream Salamanders to Riparian Land Uses.—Nine of the 11 salamander species appeared to be sensitive to riparian land uses. Desmognathus fuscus (Rafinesque, 1820) and Eurycea cirrigera (Green, 1831) were cosmopolitan, and Eurycea guttolineata (Holbrook, 1838) only slightly less so. Among

86


FIG. 2. Species accumulation curves for salamanders: (a) adults of the Blue Ridge streams, (b) larvae of the Blue Ridge streams, (b) adults of the Piedmont streams, (d) larvae of the Piedmont streams.

the adult stages, Pseudotriton ruber (Sonnini de Manoncourt and Latreille, 1801), Pseudotriton montanus Baird (1850) (Baird, 1850), Gyrinophilus porphyriticus (Green, 1827), and D. ocoee were not recorded from the Blue Ridge nonforest streams. Similarly, Desmognathus quadramaculatus (Holbrook, 1840) and D. marmoratus were not recorded from any Blue Ridge residential stream

during our survey whereas D. monticola and E. wilderae were not found in the agricultural streams of the Blue Ridge. In the Piedmont, D. quadramaculatus and G. porphyriticus were not encountered in the agricultural or urban streams; P. ruber was only absent from the Piedmont agricultural streams, whereas P. montanus only occurred in the forested streams. Larvae showed

FIG. 3. Diagrammatic representation on salamander segregation (based on species richness, diversity, and evenness) across the riparian land-use and land-cover gradient in Blue Ridge and Piedmont ecoregions.


87

TABLE 2. Species composition and average numbers of individuals captured of each species at the Blue Ridge and Piedmont ecoregions. Number of sampling sites at each land-use type in given in parentheses with column headings. Average numbers of individuals captured Blue Ridge (35) Species name

Adults D. quadramaculatus D. marmoratus D. monticola D. ocoeea D. fuscusa E. wilderaeb E. guttolineatab E. cirrigerab P. ruber P. montanus G. porphyriticus Larvae D. quadramaculatus D. marmoratus D. monticola Larvae of D. fuscus and D. ocoee Larvae of genus Eurycea Larvae of genus Pseudotriton G. porphyriticus a b

Piedmont (66)

Forest (15)

Residential (10)

Agriculture (10)

Forest (14)

Residential (15)

Agriculture (19)

Urban (13)

18.0 5.0 27.0 20.0 12.0 4.7 2 5 1.1 1.5 1.9

0 0 0.3 0 13 0.6 12.7 12.1 0 0 0

0.2 0 0 0 12 0 9.0 13.3 0 0 0

3 0 0 0 20 0 8.6 10.5 0.2 0.2 0.65

0.4 0 0 0 15.5 0 8.5 9.6 0.1 0 0.1

0 0 0 0 12.6 0 7.2 11.2 0 0 0

0 0 0 0 10.7 0 2.3 3.7 0.1 0 0

6 8.3 16.6 5.9 5.5 4.1 6.9

1.4 0 0 25.1 8.7 0 0.3

0 0 0 15.7 8.3 0 0

6.4 1.1 4.2 13.8 4.9 0.27 1.35

0 0 0 14.7 3.1 0.3 0.6

0 0 0 8.0 2.4 0.1 0.9

0 0 0 6.2 2.8 0.5 0.7

Larvae of D. fuscus and D. ocoee were grouped as D. fuscus larvae. All larval species from genera Eurycea and Pseudotriton were also grouped.

similar trends compared to adults, where the occurrence of all but D. fuscus and Eurycea spp. varied substantially among riparian land uses (Table 2). NMDS ordinations suggested two types of habitat associations in the Blue Ridge: disturbance avoiders and disturbance tolerators (Figs. 4a, 3b; stress from two-dimensional solution, adults: 0.076, larvae: 0.096, Monte Carlo stress for adults: 0.270, larvae: 0.250). Among adults, eight species (73%) were disturbance avoiders: D. marmoratus, D. monticola, D. ocoee, D. quadramaculatus, E. wilderae, P. ruber, P. montanus, and G. porphyriticus. Disturbance tolerators comprised three species: Eurycea cirrigera, E. guttolineata, and D. fuscus. Among larvae, five species (71%) were disturbance avoiders: D. marmoratus, D. monticola, D. quadramaculatus, Pseudotriton sp., G. porphyriticus); the rest (Eurycea spp. and D. fuscus) were disturbance tolerators. The NMDS ordinations for the Piedmont suggested the same two functional groups but with different species compositions compared to the Blue Ridge (Figs. 2d and 3c; stress from twodimensional solution, adults: 0.098, larvae: 0.09, Monte Carlo stress for adults: 0.267, larvae: 0.262). Disturbance avoiders were P. ruber and P. montanus. Disturbance tolerators consisted of D. quadramaculatus, D. fuscus, E. cirrigera, E. guttolineata, and G. porphyriticus. The ordination segregated the larvae of D. marmoratus, D. monticola, and D. quadramaculatus with forested streams and hence they were considered disturbance avoiders whereas the remainder (D. fuscus, G. porphyriticus, Eurycea and Pseudotrition) did not show distinctive segregation patterns and were regarded as disturbance tolerators. Environmental Correlates of Land-Use Types and Richness.—A number of habitat variables showed substantial variation among different riparian land uses (SI2). Water chemistry parameters (dissolved oxygen [DO], turbidity, and conductivity) showed notable variation among different land-use types of the Blue Ridge. Stream substrate particle size, streambed heterogeneity, substrate composition, stream bank complexity, and riparian

features were markedly different between forested and nonforest streams. The habitat variability across land uses was more prominent in the Blue Ridge than in the Piedmont. From the PCA on the habitat variables (SI3) of Blue Ridge streams, we extracted the first 2 PCs that cumulatively explained 63% of the overall variability (PC1: 51%, PC2: 12%, SI3). PC1 showed strong positive correlations with streambed heterogeneity, percent coarse woody debris (CWD), topsoil depth, canopy cover, canopy height, litter cover, and bank complexity; and negative correlations with streambed embeddedness and percent sand. These habitat variables represented the stream-channel morphology and the structure of the riparian zones. PC2 positively correlated with discharge-related variables such as depth variation and velocity variation, and negatively correlated with conductivity. For Piedmont streams, we extracted the first two PCs that cumulatively explained 28% of the habitat variability (PC1: 18%, PC2: 10%). PC1 correlated positively with habitat variables that govern the stream-channel morphology, i.e., stream-bank complexity, inorganic substrate size, and streambed heterogeneity, and correlated negatively with stream embeddedness. PC1 also represented variables that characterized the riparian zone such as topsoil thickness and percent litter cover. PC2 showed strong correlations with velocity and streambed heterogeneity. Protected Area Coverage of Riparian Zones.—Protected areas covered only 30% of the Blue Ridge riparian buffers (Table 3). This pattern intensifies in the Piedmont, where the unprotected extent of stream buffers is 96%. Nearly 80% of the protected Blue Ridge stream buffers are located within federal lands, and 10% are protected by state and local governmental agencies. Similarly, 55% and 13% of the protected Piedmont buffers fall within federal and state protected areas, respectively. In both ecoregions, 60% of protected buffer zones are subjected to multiple uses; only 11–12% of protected buffer zones sustain historical disturbance regimes.

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FIG. 4. NMDS ordinations of salamander assemblages at Blue Ridge and Piedmont Ecoregions. The closer the Euclidean distance between the species scores and the site scores in the ordination space, the stronger the ecological association among species recorded and the sites surveyed. (a) Adults of Blue Ridge ecoregion, (b) larvae of Blue Ridge ecoregion, (c) adults of Piedmont ecoregion, (d) adults of Piedmont ecoregion. Thick circles: disturbance avoiders. Monte Carlo simulations with 1,000 iterations revealed that our NMDS ordination plots are substantially different from random ordinations. Thin circles: disturbance tolerators. Species legend: adults—Ecirr: E. cirrigera, Eglut: E. guttolineata, Ewildr: E. wilderae, Dfus: D. fuscus, Dmont: D. monticola, Dmarm: D. marmoratus, Doco: D. ocoee, Dquad: D. quadramaculatus, Purub: P. ruber, Pmon: P. montanus, Gprop: G. porphyriticus. Larvae—Dmon_L: D. monticola, Dmam_L: D. marmoratus, Dquad_L: D. quadramaculatus, Dfus_L: D. fuscus, Eur_L: Eucrycea, Psed_L: Pseudotriton, Gyro_L: G. porphyriticus.

DISCUSSION Differential Species Diversity at Different Riparian Land Uses.— Blue Ridge forested streams in our study had the greatest salamander diversity. Streams associated with altered riparian landscapes (agriculture, residential, and urban) were species depauperate. Our general findings agreed with other studies on amphibian responses to habitat conversion in the southeastern United States (Price et al., 2006; Barrett and Guyer, 2008; Price et al., 2011) and other temperate biogeographic regions (Southerland et al., 2004; Beebee and Griffiths, 2005; Riley et al., 2005;

Baldwin et al., 2006). Species-rich salamander communities we observed in Blue Ridge forested streams can most likely be attributed to high streambed heterogeneity, associated with mature mixed-mesic hardwood forests and fast-flowing highly oxygenated cold water (Hairston, 1949; Beachy and Bruce, 1992; Beachy, 1993; Bruce et al., 1994). Streams associated with nonforest riparian land cover experience dramatic modifications in biogeochemistry, thermal regimes, hydrodynamics, and microhabitat structure (Grimm et al., 2008; Gardiner et al., 2009). Land development in the Blue Ridge is relatively patchy because of amenity-based establish-


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TABLE 3. Degree of protection provided by protected area network (U.S. Geological Survey [USGS] Protected Area Database) to stream buffer zones of different widths: 140 m and 240 m. The surface area under each stewardship category and GAP status (USGS GAP analyses) is provided. The parenthetical values indicate the percentage cover of stream buffers within each landownership category and each GAP status category calculated as a fraction of total protected buffer area within each ecoregion. *Percent values for protected and unprotected buffers were calculated as a fraction of the total land area of each ecoregion. Land area (km2) and percent coverage Blue Ridge Land stewardship categories

Landowner Federal Jointly owned Local government Native American Nongovernmental organization Private State Unknown landowner Total protected buffers* Total unprotected buffers* GAP (land management) status Disturbances proceeded Disturbances suppressed Managed for multiple uses GAP status unknown

140-m buffer

Piedmont 240-m buffer

140-m buffer

240-m buffer

4,030 1 80 69 15 422 262 9 4,886 12,245

(82.5) (0.02) (1.6) (1.4) (0.3) (8.6) (5.4) (0.2) (29.1) (70.9)

8,068 2 174 131 33 892 571 18 9,888 22,422

(81.6) (0.02) (1.8) (1.3) (0.3) (9.0) (5.8) (0.2) (29.3) (70.7)

1,345 2 50 0 69 599 323 17 2,405 54,526

(55.9) (0.1) (2.1) (0) (2.9) (24.9) (13.4) (0.7) (4.0) (96.0)

2,576 3 0 95 118 1,117 638 37 4,585 104,144

(56.2) (0.1) (0) (2.1) (2.6) (24.4) (13.9) (0.8) (3.8) (96.2)

1,036 548 2,930 373

(21.2) (11.2) (60.0) (7.6)

1,970 1,106 6,028 785

(19.9) (11.2) (61.0) (7.9)

55 283 1,464 602

(2.3) (11.8) (60.9) (25.1)

110 551 2,818 1,101

(2.4) (12.0) (61.5) (0.1)

ments, impoundments, small-scale agriculture, and golf courses (Theobald, 2003). Such habitat alterations produce highly fragmented landscapes where forested streams are embedded in a mosaic of land uses with impeded habitat connectivity at different spatial scales in the watershed as well as in the stream channel (Becker et al., 2007). Residential and agricultural land uses are sources of agrochemicals, fine sediments, and organic wastes that dramatically alter the trophic status of streams and ultimately suppress growth, reproduction, and survival of salamanders (Barrett et al., 2010). Low diversity of salamanders in the Piedmont across all riparian land uses may be attributed to historical (1820–1940) cotton farming (Harding et al., 1998) and timber industries (Wear, 2002). Streams in altered landscapes and those with longer histories of intensive land use may develop simplified salamander assemblages (Willson and Dorcas, 2003; Price et al., 2006, 2011, 2012). Piedmont streams exist in landscapes with longer and more intensive land uses, have fewer species, and are more species tolerant of anthropogenic activity. Forested streams in the montane Blue Ridge landscapes have more species, and more of those adapted to relatively pristine conditions. Despite postfarming forest regeneration, sediment influx from erosion gullies into streams exceeds export, leading to in-stream sediment accumulation, which decreases microhabitat and resource availability (Jackson et al., 2005; Galang et al., 2007). Early European settlements substantially altered the landscape structure, leaving unstable, eroded stream banks, mobile sand layers overlying streambeds, and high silt content in most Piedmont streams (Brender, 1974). Excess sedimentation is often associated with egg mortality and reduced growth among stream salamanders (Guy et al., 2004). Higher diversity of larval assemblages in Piedmont nonforest streams compared to adults could be a result of passive drift subsequent to storms with increased discharge from the Blue Ridge (Barrett et al., 2010). Because of lack of suitable habitats, larvae may not reach adulthood in Piedmont streams. Discon-

tinuity of riparian forests may prevent active dispersal between the two ecoregions (Cecala, 2012). Species-rich Piedmont streams in our survey were located at Blue Ridge foothills, where such movements are facilitated through continuous forested corridors (Burbrink et al., 1998; Grant et al., 2010). Inimical effects of land development have been recorded for multiple aquatic taxa; declining stream fish diversity (Jayaratne and Surasinghe, 2011; Pease et al., 2011), macroinvertebrate diversity (Moore and Palmer, 2005; Hedrick et al., 2010), and biotic integrity index (Helms et al., 2005) were reported following watershed urbanization. Our results support that landscape-level processes associated with intensive land use may likewise be influencing stream salamanders. We observed strong differences in species richness and community composition of stream salamanders in response to the riparian land uses between the two ecoregions. The habitat segregation was more prominent in the Blue Ridge compared to the Piedmont. Differential responses to watershed development have been observed among lotic fauna occupying disparate ecoregions (Utz and Hilderbrand, 2010; Utz et al., 2010). Ecoregion-wide geomorphic attributes, i.e., physiography, geological setting, and climate, shape regional hydrodynamics and channel structure (Utz and Hilderbrand, 2010; Utz et al., 2011). There are many such distinctions between these two ecoregions that may have partly contributed to disparate species responses. Blue Ridge is characterized by low to high mountains (260– 1,670 m), steep escarpments (topographic relief: 305–1,070 m), and high-gradient streambeds largely composed of boulders (Bolgiano, 1998; Abella and Shelburne, 2004). Such stream substrates provide ample cover for disturbance avoiders, and the high stream velocity originating from the high gradient may have flushed fine sediments from interstices (Lowe and Bolger, 2002). In contrast, the Piedmont is characterized by dissected, hilly irregular plains (elevation range: 223–583 m, topographic relief: 30–122 m), and moderate-gradient streambeds composed of cobble, gravels, and small boulders (Griffith et al., 2002; U.S. Environmental Protection Agency, 2002; Scott, 2009). Such

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smaller substrates offer limited habitats for salamanders; moderate discharge (because of moderate stream gradient) may not have effectively flushed fine sediments from interstices. The rugged terrain of the Blue Ridge has limited urban and agricultural expansions compared to the Piedmont (Wear and Bolstad, 1998). The Blue Ridge has a greater coverage of protected areas than in the Piedmont. Such regional differences in conservation attention may have also account for differential species distribution and diversity. Species-Specific Responses to Riparian Land Uses.—Most of the disturbance avoiders in the Blue Ridge were large (snout-to-vent length [SVL] 70–120 mm) or medium (SVL 45–55 mm) sized, and are microhabitat specialists (Hairston, 1986; Kozak et al., 2005). Desmognathines and Gyrinophilus select large interstitial spaces underneath large rocks and undercut banks as their preferred microhabitats, whereas other Spelerpines choose woody debris as refugia (Mitchell and Gibbons, 2010) and oviposit in rocky interstices and woody debris (Lowe and Bolger, 2002; Bruce, 2003). Given their habitat selectivity, disturbance avoiders are vulnerable to siltation, low pH, and urban effluvia (O’Driscoll et al., 2010). The food base of salamanders is composed of terrestrial (Lepidopeterans) and aquatic insect larvae (Ephemeropterans and Trichopterans) that are themselves sensitive to habitat quality (Felix and Pauley, 2006). When terrestrially active, disturbance avoiders require high humidity, low temperature, deep leaf litter, and large woody debris (LWD); these needs can be provisioned by intact riparian forest canopy (Semlitsch and Bodie, 2003; Willson and Dorcas, 2003; Olson and Burnett, 2009; Price et al., 2012). Disturbance avoiders have greater investments for longterm reproductive success: prolonged growth (5–6 yr), delayed sexual maturity, and longer (> 1 yr) larval periods (Bruce and Hairston, 1990; Tilley and Bernardo, 1993). These life-history strategies may become a liability under riparian land development, because fitness could be impaired during sensitive, prolonged larval stages or before sexual reproduction (Semlitsch et al., 1988). Larger-bodied species have more extensive home ranges, greater resource needs, and higher energy demands. These requirements may predispose larger-sized salamander species to be more susceptible to landscape-level habitat alterations (Lips et al., 2003; Sodhi et al., 2008). Disturbance tolerators are small bodied (SVL 30–40 mm), have a slender morphology, and are microhabitat generalists. Their microhabitats comprise a broader variety of refugia and oviposition sites such as cobbles, pebbles, gravel beds, woody debris, and crevices (Southerland, 1986). Small body size does not require large interstices allowing them to tolerate some degree of sedimentation. Their terrestrial activities are not dependent on intact riparian vegetation (Bruce, 2005). Gut content analyses revealed diverse prey preference, including pollution-tolerant invertebrates (Holomuzki, 1980). Relatively stable populations of disturbance-tolerant species exist elsewhere in North America that underwent notable land-cover transformations (Means, 2005; Pauley and Watson, 2005; Ryan and Douthitt, 2005). However, despite the relatively high tolerance to anthropogenic stressors, disturbance tolerators may eventually suffer population declines given the high rate of residential development observed in our study region (Surasinghe et al., 2012). Previous long-term studies suggested that D. fuscus and E. cirrigera may completely disappear from urbanization-impacted watersheds (Price et al., 2012; Scheffers and Paszkowski, 2012). Land-use associations of D. quadramaculatus and G. porphyriticus differed markedly between the two ecoregions; we

recorded both species across all riparian land uses in the Piedmont but only at forested streams in Blue Ridge (Fig. 4). Interregional differences in species responses to urbanization have been recorded previously for stream fish and macroinvertebrates (Utz and Hilderbrand, 2010; Utz et al., 2011). Likewise, substantial differences in the geomorphology, hydrology, edaphic, and bioclimatic variables may have influenced the distribution and community organization of stream salamanders across different riparian land uses of these two ecoregions (Griffith et al., 2002). As riparian disturbances appear to affect competitively dominant large-bodied Desmognathines disproportionately, small-bodied plethodontids (D. fuscus, E. cirrigera, and E. guttolineata) are released from the competitive pressure, allowing them to monopolize scarce resources in nonforest streams such as microhabitats and food (Barrett et al., 2010). These small-bodied species have shorter larval periods (0.5–2 yr) and faster growth, and reach early reproductive maturity, allowing a faster generation time, which is a great advantage ensuring reproductive success under stressful conditions (Tilley and Bernardo, 1993; Bruce, 2005). Environmental Variables Governing Species Responses to Riparian Land Use.—The PCA identified primary environmental parameters that drove habitat associations of stream-dwelling salamanders, which emphasized the importance of undercut banks, heterogeneous streambed, fast-flowing cold water, deep topsoil, and mature riparian canopy. These features are characteristic of less anthropogenically disturbed streams, and sustain physiological optima for highly diverse salamander communities (Hicks and Pearson, 2003). Heterogeneous stream substrates enriched with woody debris provide interstitial refugia necessary for cover, foraging, hibernation, aestivation, and oviposition; high velocity maintains high dissolved oxygen and removes sediments (Semlitsch, 2000; Semlitsch and Bodie, 2003; Crawford and Semlitsch, 2008; Peterman et al., 2008). Our findings on the importance of riparian habitats align with other studies that underscored the necessity to conserve terrestrial wetland buffers (Semlitsch and Bodie, 2003; Baldwin et al., 2006; Howard et al., 2012). Our findings also highlighted the potential impacts of soil erosion and nutrient-rich runoff on salamanders. High degree of sedimentation smothers interstices, destroys eggs, and prevents recruitment of macroinvertebrates (Bruce, 1986; Petranka and Smith, 2005). Plethodontids are intolerant to high temperatures and suffer mortality, reduced growth, and decreased activity (Feder, 1983). Human-impacted riparian zones have highvolume runoff contaminated with nutrients and pollutants (e.g., agrochemicals) whereas forest-floor runoff is low in volume, less erosive, and nutrient low (Collins and Storfer, 2003; Clinton and Vose, 2006). Forest cover along Blue Ridge streams is relatively extensive and less impacted by historical land use (Wear and Bolstad, 1998). Recommended Conservation Actions.—Policy is a powerful tool, as it is applicable over many kilometers of streams and across ownership and management boundaries. Protection of low-order stream ecosystems is not mandated for many U.S. states; for instance, in the southeastern United States, the average stream buffer width in public properties ranges from 12 to 20 m, which is insufficient to meet life-history needs of amphibians (Lee et al., 2004). The Clean Water Act offers only limited protection for intermittent streams (Zedler, 2003). Policy reformations that might help conserve salamander habitats include 1) strengthening riparian zoning laws: exclusion of riparian zones from development, crop production, and intensive resource extraction

RIPARIAN LAND USE AND STREAM SALAMANDERS (Ekness and Randhir, 2007); 2) regulating land uses in the uplands to achieve watershed-level conservation goals and to enhance overland connectivity among low-order streams (Lowe et al., 2006); 3) restricting amenity-based development in riparian zones and headwaters (Baldwin and Demaynadier, 2009); and 4) clustering development to minimize road construction. Management activities including bank stabilization, erosion controls, introduction of mix-aged native woody and understory species to the riparian zone, and restoration of historical geomorphology of degraded streams, can have positive cumulative effects (Aust, 1994). Conservation easements are a rapidly growing form of land protection in the United States (Rissman et al., 2007) with over 100,000 catalogued in the National Conservation Easement Database. Riparian forest conservation could become a top priority in easement establishment (i.e., modifying easements to ensure preservation of riparian forests), prioritizing easements in stream-embedded private lands, and targeting easements to protect headwater streams as ‘‘patch reserves’’ (Olson et al., 2007; Rissman et al., 2007). Within existing protected areas, the management level of riparian buffers could be raised to zeroimpact zones with re-establishment of historical disturbance regimes and ecosystem processes (e.g., flood pulses, supply of in-stream woody debris) (Welsh, 2011). Benefits of protecting riparian zones extend beyond amphibian conservation, and include maintenance of water quality, discharge, and productivity; moderation of stream microclimate and dissolved oxygen; improved soil water infiltration, nutrient and sediment retention, and downstream supply of nutrients and organic matter; bioremediation of toxic compounds; stabilization of stream channel and bank; river corridors facilitating dispersal for multiple taxa; and sustaining aquatic biodiversity. The Blue Ridge and Piedmont riparian forests are home to a number of rare and threatened species of reptiles (bog turtle, timber rattlesnake), small mammals (Indiana Bat), birds (Cerulean warbler), and flora (Apalachicola wild Indigo); persistence of many species is dependent on riparian zones maintained within the bounds of natural disturbance (Hackney et al., 1992; Martin et al., 1993). Acknowledgments.—The Riverbanks Zoo, Highlands Biological Station, and the Department of Biological Sciences and the Creative Inquiry program of Clemson University funded this research. The South Carolina Department of Natural Resources helped with information sharing. We are indebted to assistance from M. Scott and B. Brown. Undergraduates of Clemson University helped as field technicians. We appreciate comments on the manuscript from K. Barrett. Approvals on animal use and care protocols (Clemson University AUP 2010-013) and research permits (SC DNR permit No: 10-2011; SC State Park Service permit No: N-18-10; U.S. Forest Service permit No: FS2400-8) were obtained.

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