Northeastern Naturalist Vol. 23, No. 1 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 151 2016 NORTHEASTERN NATURALIST 23(1):151–162 Potential Influence of Salamanders and Coarse Woody Debris on the Distribution of Dryopteris intermedia in a Hardwood Forest Devin G. Oralls1, Abbey R. Osborn1, and Jack T. Tessier1,* Abstract - Dryopteris intermedia (Common Wood Fern) is more associated with coarse woody debris (CWD) than the surrounding forest floor. Along with microsite-based establishment benefits, dispersal vectors may facilitate this distribution. Some salamanders are associated with CWD and may serve as dispersal agents for spores of the Common Wood Fern. In a deciduous forest of south-central New York State, we assessed the ability of Plethodon cinereus (Red-backed Salamander) and Notophthalmus viridescens (Eastern Newt) to pick up and transport spores and sori fragments from the dorsal side of the frond, and rinsed salamanders to collect and germinate any viable spores from their bodies. We also measured the moisture content of soft CWD, soil beneath hard CWD, and background soil. Both salamander species picked up reproductive components of Common Wood Fern. Wild-caught salamanders of both species had viable spores on their bodies. Soft CWD held more moisture than soil beneath hard CWD and the forest-floor soil. Dispersal by salamanders and the provision of humid habitat by soft CWD may help to explain the abundance of Common Wood Fern near CWD. Introduction Dryopteris intermedia (Muhl. ex Willd.) A. Gray (Common Wood Fern) is the most abundant fern in northeastern US forests (Flinn 2006, Tessier and Raynal 2003, Yorks et al. 2000). This wintergreen fern (Tessier 2008) commonly occurs in microclimates with abundant moisture such as pits and mounds from tree falls (Flinn 2007, Maser and Trappe 1984), and has been documented to occur in high abundance near coarse woody debris (CWD; Flinn 2007, McGee 2001). Its germination has been experimentally shown to benefit from a high-humidity environment. One study demonstrated that elevated humidity in experimental plots could lead to a 4000-times higher chance of gametophyte establishment and a 60-times higher chance of sporophyte establishment when compared with control plots (Flinn 2007). Therefore, moisture is critical to the establishment of Common Wood Fern. Dispersal of spores is also an important factor in fern distribution (Karst et al. 2005). While spores can move throughout a forest, most spores stay near their source plant (Peck et al. 1990, Penrod and McCormick 1996). For example, most spores of Dennstaedtia punctilobula (Michx.) Moore (Hayscented Fern) fall within 4 m of the source plant (Penrod and McCormick 1996) and most spores of Botrychium virginianum (L.) Swartz (Rattlesnake Fern) fall within 3 m of the source plant (Peck et al. 1990). Further, spore abundance for the Common Wood 1Division of Liberal Arts and Sciences, SUNY Delhi, 454 Delhi Drive, Delhi, NY 13753. *Corresponding author - tessiejt@delhi.edu. Manuscript Editor: Douglas DeBerry Northeastern Naturalist 152 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 Vol. 23, No. 1 Fern is greater in primary forests than in the secondary forests (Flinn 2007) that dominate the northeast United States (Dyer 2006). These dispersal limitations suggest that there may be a separate dispersal vector that helps fern spores reach coarse woody debris. Like ferns, salamanders are extremely common in northeastern forests. Plethodon cinereus Green (Red-backed Salamander) is so abundant that its summer biomass (when fern spores are released) can exceed that of birds during the breeding season and equal the biomass of mammals in the northeastern United States (Burton and Likens 1975, Grover 1998, Hairston 1996, Mathewson 2009). This species is most commonly found beneath cover structures such as logs and rocks (Bishop 1943, Jaeger 1980, Richmond and Trombulak 2009) but avoids permanently wet areas (Burger 1935). Red-backed Salamanders roam above leaf litter during wet periods and can climb more than 2 m up plants in search of food (Burton and Likens 1975). Notophthalmus viridescens Rafinesque (Eastern Newt) has a four-stage life cycle. Eastern Newt eggs, larvae, and adults are aquatic, though juveniles (efts) are terrestrial and, therefore, the focus of this study (Chambers 2008, Healy 1975). Eastern Newt efts occur at an average density of 0.03 per m2 in the northeast United States (Healy 1975), and each individual eft roams throughout 266.9 m2 on average in a year (Healy 1975). Eastern Newts need to migrate to ponds for breeding as adults (Hurlbert 1969, Jones and Smyers 2010). They move the most (mean of 2 m per day) during the early summer (when fern spores are released) and less (mean of 0.5 to 1.5 m per day) through mid-summer and fall (Healy 1975). The efts tend to stay on land for 4 to 5 years (Healy 1975) and prefer moist conditions, with the extent and timing of their activity on top of the leaf litter being influenced by rain (Healy 1975). Both macro- and microhabitat features have an important influence on the abundance of salamanders in the environment. Slopes facing the north tend to be moister than other slopes because the sun’s rays are not as strong, thereby offering better habitat for salamanders (Sariyildiz et al. 2005). Habitats for the Red-backed Salamander and Eastern Newt are near and under coarse woody debris and rocks (Burger 1935). The Red-backed Salamander is most active near seeps due to the high moisture (Grover 1998, Grover and Wilbur 2002) and forages best near cover structures (Grover 1998). High moisture levels provided by CWD help with gas exchange through the skin in the lungless Red-backed Salamander (Grover 1998). Common Wood Fern provides shade (George and Bazzaz 1999), which increases humidity that salamanders prefer (Grover 1998). The spores of the Common Wood Fern, therefore, may get attached to the salamanders’ porous skin and feet, increasing dispersal across the forest (as speculated for fern gemmae by Farrar [1985]). The propensity for these salamander species to live under, on, and around CWD due to the moisture it provides (Bishop 1943, Burger 1935, Grover 1998, Healy 1975, Jaeger 1980, Richmond and Trombulak 2009) and the much greater extent of their annual movement relative to the distance that most fern spores disperse from the parent plant (Peck et al. 1990, Penrod and McCormick 1996) indicate the potential for salamanders to be dispersal vectors for fern spores to CWD. Northeastern Naturalist Vol. 23, No. 1 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 153 These facets of fern and salamander ecology led us to 2 questions related to the abundance of Common Wood Fern near CWD. First, can salamanders function as a dispersal vector for fern spores? Second, does CWD provide more moisture than background soil? These questions led to 2, non-mutually exclusive hypotheses. First, we hypothesized that spores of the Common Wood Fern can get stuck on salamander bodies through physical contact resulting in viable spores being present on salamander bodies. Second, we hypothesized that CWD provides a humid habitat for fern spores thereby promoting germination and survival (Flinn 2007). We predicted that (1) spores will attach to a salamander if it walks through them, (2) viable spores can be rinsed from salamander bodies, and (3) soil associated with CWD will be moister than that in the surrounding area. Field-Site Description We conducted the fieldwork in a north-facing deciduous forest in the town of Delhi, Delaware County, NY (42°14'53"N, 74°56'06"W). The site is dominated in the overstory by Acer saccharum Marshall (Sugar Maple), A. rubrum L. (Red Maple), and Fraxinus americana L. (White Ash). The understory is dominated by Common Wood Fern and D. marginalis (L.) A. Gray (Marginal Wood Fern). Methods Prior to the start of field activities, we obtained permission to conduct the work from SUNY Delhi’s Institutional Animal Care and Use Committee and from the New York State Department of Environmental Conservation. We chose to work with Red-backed Salamanders and Eastern Newts because they are the most common salamanders at our study site. Spore attachment First, we assessed if spores can become attached to salamander bodies. This experiment was necessary to determine the quantity of spores that could become attached to salamander bodies without background variation from spore availability in the environment or spore loss from bodies from prior dispersal of spores. We obtained salamanders for this research component by searching 10-m–wide belt transects for 100 m, or until 10 individuals of each salamander species had been found. Transects were used to provide a guided search path such that our search for salamanders was not biased toward one area or another at the site, and thus would be much less likely to result in finding salamanders in environmental conditions (e.g., wet or dry) that made them more or less likely to collect spores from their surroundings than other salamanders. We placed each salamander onto the dorsal side of a fertile frond of Common Wood Fern in a small, cardboard box and coaxed them to walk across a microscope slide with a thin coat of petroleum jelly (sensu Kimmerer and Young 1995). Petroleum jelly was used to maximize removal of spores from the salamanders in order to get as accurate as possible a count of spores collected from the frond. The Northeastern Naturalist 154 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 Vol. 23, No. 1 frond was 10 cm across and the microscope slide was placed directly adjacent to the frond. The box was the width of the microscope slide. The back end of the box was left intact to offer a shaded area to which the salamanders would prefer to go. Once placed on the frond, each salamander completed the movement across the slide within 10 seconds. We repeated this procedure 10 times with each species of salamander. We restricted the sample size to 10 in order to limit our impact on the populations of these vertebrate animals. The same frond was used for each salamander to minimize the impact of variability in spore abundance among salamander runs. The vast quantity of spores on a fertile frond (Wagner and Lim Chen 1965, Whittier and Wagner 1971) relative to the amount that might be removed by any of the salamanders also ensured an effectively similar degree of spore exposure for each salamander run. Salamanders were included as found, resulting in a temporally heterogeneous mix of the 2 species, also precluding a difference in spore availability between the 2 species. As the sampling took place, 6 of 10 Red-backed Salamanders were among the first 10 salamanders caught and 6 of 10 Eastern Newts were among the last 10 salamanders caught, demonstrating species evenness in the order of sampling. We wore lab gloves when handling salamanders to provide them with a smoother surface compared to human skin, thereby offering greater comfort and less stress to the animals. We released salamanders adjacent to the cover structure under which they were found immediately after the procedure. This approach limited their handling to less than 5 minutes, requiring no extended captivity. As a control, we placed a microscope slide with petroleum jelly adjacent to the fern frond in the box, but without allowing a salamander to walk across it. This control provides for a background count of spores that could have been accidentally moved to the slide via handling and placement of the slide in the box adjacent to the frond. We examined the microscope slides with a light microscope at 100x, looking for spores and fragments of sori with spores of Common Wood Fern. This combination of spores and sori with spores allowed us to quantify the total number of reproductive pieces moved by the salamanders. We calibrated our search image by intentionally scraping sori and spores onto a separate microscope slide and viewing these components prior to visually searching the experimental slides. Spore dispersal To assess if salamanders move fern spores on their bodies, we rinsed salamanders with rain water and cultured that water on sterile potting soil. We collected a second set of animals from their habitat for this experiment. Collection, handling, and release of salamanders were conducted as above such that we collected 10 individuals of each species. Immediately upon collection, each salamander was held over a funnel and rinsed with 25 mL of locally collected rainwater. We directed this water onto pre-moistened, sterile potting soil in a 118-mL, square-shaped, plastic food-storage container. We collected control samples by rinsing the ends of our gloved fingers with 25 mL of rain water and collecting that water in soil as above. This control, therefore, took into account any spores that may have contaminated Northeastern Naturalist Vol. 23, No. 1 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 155 the rainwater during collection or that may have been on our fingers or the funnel during the field work. These containers were sealed with their cover to retain moisture and kept in the lab under fluorescent white light until establishment of gametophytes ceased. Moisture content To document the moisture of soil and associated CWD, we established a 10-m– wide belt transect for 100 m. A transect was used to provide an unbiased sampling of the CWD and soil, avoiding any tendency to oversample in areas with abundant CWD due to soil conditions that may make trees prone to falling and thereby confounding the results. For the purposes of this study, we defined CWD as downed wood that was at least 10 cm in diameter (McGee 2000). Along this transect, we searched for both hard and soft CWD. If a gardening trowel could not be easily inserted into the CWD, we categorized it as hard CWD. If a gardening trowel could be easily inserted into the CWD, we categorized it as soft CWD. We collected soil from beneath the hard CWD and from soil under leaf litter that was both 1 m from this CWD along the transect in reverse of our direction of sampling and 1 m away from any other CWD for comparison. From the soft CWD, we collected a sample of the CWD itself along with a sample of soil from under leaf litter 1 m along the transect in reverse of our direction of sampling. The soft CWD itself was sampled because this is the medium in which Common Wood Fern has been shown to be abundant (Flinn 2007, McGee 2001) and it provides a contrast with the soil available in other locations in the field (i.e., forest soil and soil beneath hard CWD). Forest floor soil was collected from near hard CWD and soft CWD to control for variation in soil conditions near the 2 types of CWD (e.g., moist soil and not just decay duration could help to make the soft CWD softer than the hard CWD). We sampled 30 replicates of each soil type. The soil samples were brought to the lab at SUNY Delhi, weighed immediately, and allowed to dry to a constant mass. We then calculated their soil moisture content (Brower et al. 1990 ). Statistical analysis We compared the number of spores and sori components with spores of Common Wood Fern found on the microscope slides and the number of gametophytes established from rinse water among the control and 2 salamander species using 2 separate Kruskal-Wallis tests due to the small sample size. Following the significant Kruskal-Wallis result when comparing reproductive components moved to the microscope slides, we made post-hoc comparisons among the species and control using Mann-Whitney tests with an adjusted α = 0.01667 to control for the experiment-wise error rate. We compared the moisture of substrate material gathered from the 4 location types (soil beneath hard CWD, soil nea r hard CWD, soft CWD, and soil near soft CWD) using analysis of variance followed by a Tukey’s family error rate means comparison. All statistical analyses were conducted using Minitab version 16 (Minitab, Inc., State College, PA) at α = 0.05, unless otherwise stated. Northeastern Naturalist 156 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 Vol. 23, No. 1 Results While Red-backed Salamanders moved twice as much reproductive components of Common Wood Fern than Eastern Newts, the difference was not statistically significant ( W = 134.0, P = 0.0290; Fig. 1). More reproductive components were found on slides from the 2 salamander species treatments than on the control slides (H2 = 15.21, P < 0.0001; Control vs. v: W = 61.0, P = 0.0005; Control vs. Eastern Newt: W = 74.0, P = 0.0114; Fig. 1). There was no pattern between spore count and order of the sampling in the field, indicating that there was not a decline in spore availability from the frond as the experiment was conducted. Three out of 10 samples of rinse water from each of the 2 salamander species grew fern gametophytes, while none of the control samples did. The lack of gametophytes from the control samples indicates that there was no spore contamination of the gloves used in the experiment. The number of gametophytes grown per sample was not significantly different between species nor from the control (H2 = 3.68, P = 0.159; Fig. 2). The moistest soil was that of the soft CWD (F3,116 = 29.17, P < 0.0001; Fig. 3), while that beneath hard CWD and both adjacent soils did not differ significantly (Fig. 3). The soft CWD held more than twice as much water (405.9 g/100 g dry soil) as the other soil types (158.6 g/100 g dry soil) (Fig. 3). Figure 1. Number of spores or sori components with spores found on microscope slides that had been walked across by each salamander species after being placed on the dorsal side of a fertile frond of Dryopteris intermedia (Common Wood Fern) in the Town of Delhi, NY. Center line represents the 50th percentile, dashed line represents the mean, box represents the 25th and 75th percentiles, and whiskers represent the 10th and 90th percentiles. Treatments with different letters are significantly different at α = 0.05 based on a Kruskall-Wallis test and subsequent Mann- Whitney post-hoc tests. Northeastern Naturalist Vol. 23, No. 1 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 157 Discussion Red-backed Salamanders and Eastern Newts are possible dispersal agents of fern spores (Figs. 1, 2). To our knowledge, this is the first study to document uptake and movement of spores by salamanders. Our first experiment demonstrated Figure 2. Number of gametophytes grown from water used to rinse salamanders from the Town of Delhi, NY. Center line represents the 50th percentile, dashed line represents the mean, box represents the 25th and 75th percentiles, and whiskers represent the 10th and 90th percentiles. Means were not significantly different based on a Kruskall-Wallis test at ɑ = 0.05. Figure 3. Moisture of 4 types of soil in a second-growth hardwood forest in the Town of Delhi, NY, in the summer of 2014. Center line represents the 50th percentile, dashed line represents the mean, box represents the 25th and 75th percentiles, and whiskers represent the 10th and 90th percentiles. Soil types with different letters are significantly different at α = 0.05 based on an analysis of variance and Tukey’s family error rate tests. Northeastern Naturalist 158 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 Vol. 23, No. 1 that both salamander species collect spores from the environment (Fig. 1). Our second experiment showed that viable spores remain on the salamanders as they move from the spore source (Fig. 2). The lower count of viable spores on the freeroaming salamanders compared to the spore count on animals that had just picked up spores from a frond suggests that spores are lost from the salamanders as they move in the environment, indicating dispersal of the spores. Salamanders may move more spores on their bodies than our data suggest because our rinsing experiment took place in early August due to logistical delays, whereas spore release in Common Wood Fern peaks in late June (Flinn 2007) coincident with the time of greatest movement for Eastern Newts (Healy 1975). Salamanders could encounter fern spores under non-experimental conditions as they climb vegetation (Burton and Likens 1975, Trauth et al. 2000) and move in the understory among plants, leaf litter, and soil (Peck et al. 1990, Penrod and McCormick 1996). Flinn (2007) clearly demonstrated that high humidity benefits fern germination and survivorship. The moisture in the soft CWD, therefore, provides important habitat for young ferns (Fig. 3), and the salamander species we studied are commonly found in these areas (Burger 1935, Grover 1998). In our study area, we found 10 individuals of each species within 100 m of a 10-m belt transect each time we searched for them in and around CWD. Collectively, these results show that dispersal by salamanders and the moisture in old CWD may both help to explain the prevalence of Common Wood Fern near CWD in forests (Flinn 2007, McGee 2001). Dispersal of fern spores by salamanders could significantly chan ge the distance and location of dispersal. First, these salamanders move greater distances than most fern spores that don’t have the aid of active transport. Most fern spores fall within 4 m of the adult plant (Peck et al. 1990, Penrod and McCormick 1996). Eastern Newts can move 2 m per day during the time when Common Wood Fern spores are released (Healy 1975) and male Red-backed Salamanders can move as far as 10 m or more per day during the growing season (Liebgold et al. 2011). Second, these salamanders are associated with the high-moisture environment of CWD (Fig. 3; e.g., Healy 1975, Richmond and Trombulack 2009) that dramatically raises the germination and establishment success of the Common Wood Fern (Flinn 2007). Therefore, these salamanders are likely to increase the dispersal distance of spores of the Common Wood Fern and to move them to a suitable location for germination and survival. Other animals are known to disperse spores. Ants are known to disperse moss gemmae (Rudolphi 2009), and slugs can disperse moss spores (Kimmerer and Young 1995). Fungal spores can be dispersed by worms and birds (McIlveen and Cole 1976) and in the feces of small mammals (Zaharick et al. 2015). Following dispersal of propagules, microsite can play an important role in the establishment of plants (Beatty 1984, Flinn 2007, Peterson and Campbell 1993). The increase in moisture content through decay class in CWD (Maser and Trappe 1984) provides the cover and moisture preferred by Red-backed Salamanders (Grover 1998), further encouraging dispersal of fern spores to CWD and establishment of ferns (Flinn 2007, McGee 2001, Peck et al. 1990). Northeastern Naturalist Vol. 23, No. 1 D.G. Oralls, A.R. Osborn, and J.T. Tessier 2016 159 This evidence of spore dispersal by salamanders suggests that amphibian decline may have a significant impact on movement of fern spores. While these salamander species are very common and abundant in northeastern forests (Burton and Likens 1975, Healy 1975), amphibians are experiencing a global decline in abundance (Hof et al. 2011), and body size in the Red-backed Salamander is decreasing in the southern part of its range due to climate change (Caruso et al. 2014). Depending on future changes in climate (Peterson et al. 2013) and land use (Thompson et al. 2013), the ability of fern spores to get to the microhabitat that benefits them most (Flinn 2007) may be hampered if salamander abundance decreases. Other questions relating to salamanders’ role in spore disperal deserve study. Given that the gut contents of Red-backed Salamanders include ants and beetles (Hamilton 1932), spores attached to these insects may show up in the feces of salamanders and serve as an additional dispersal mechanism mediated by salamanders. Vegetation has been found in the stomachs of both of these salamander species (Cochran 1911, Ries and Bellis 1966), further suggesting that feces could be an additional dispersal mechanism in need of quantification. Spores of other species that salamanders can move need to be identified. The burrowing capacity of salamanders (Heatwole 1960) raises the possibility that they may play a role in the development of deep spore banks (Dyer and Lindsay 1992). An important next step is to document how readily spores move from the bodies of the salamanders to soil and CWD. Given this potential for salamanders to be important to fern dispersal, current and potential reductions in amphibian abundance may impact fern distribution and should be studied (Caruso et al. 2014, Martel et al. 2 014). In conclusion, the movement of fern spores by salamanders, the presence of fern spores on salamander bodies, and the high moisture content of soft CWD offer a mechanism for the observed abundance of Common Wood Fern adjacent to CWD. Further study should address alternative dispersal mechanisms by salamanders, additional species that salamanders can disperse, and the impact of amphibian decline on plant dispersal. Acknowledgments The authors thank an anonymous donor for funding, Karen Teitelbaum for assistance with obtaining permission for the study from the New York State Department of Environmental Conservation, SUNY Delhi for the use of the study site, and anonymous reviewers for constructive comments on the manuscript. Literature Cited Beatty, S.W. 1984. 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