Northeastern Naturalist 200 A. Robillard and B.Johnson 22001155 NORTHEASTERN NATURALIST 2V2(o1l). :2220,0 N–2o0. 81 Edge Effects on Eastern Massasauga Rattlesnakes Basking in Managed Habitat Alexander Robillard1,* and Brent Johnson1 Abstract - Extensive vegetation growth has decreased potential basking sites for an endangered population of Sistrurus catenatus (Eastern Massasauga Rattlesnake [EMR]), and habitat management is needed to restore these sites. Practices that decrease canopy cover can unintentionally impact snakes by increasing exposure, thereby raising predation rates. Basking behavior of slow-moving EMRs often involves remaining cryptic or retreating to avoid detection. We observed several aspects of EMR basking behavior—location, exposure, and defensiveness—relative to distance from habitat edge within 100-m2 square plots of cut shrubs to determine whether the habitat alterations modified EMRs use of the landscape as it related to predator avoidance. EMRs basked throughout the entirety of plots and did not vary their level of exposure or defensiveness based on their distance from the edge of plots. Our results suggest that shrub-cutting in up to 10 m x 10 m areas does not alter predator-avoidance behavior in EMRs. Introduction Ecological traps, which are low-quality habitats occupied by animals in preference to available high-quality habitats, can be incidentally generated by management practices (Battin 2004, Gates and Gysel 1978). Ecological traps are often associated with habitats modified by human activities such as mowing or indirectly through human-mediated invasion by exotic species (Battin 2004). These abrupt environmental changes can misinform individual animals whose habitat preference may remain unchanged despite having the positive effects associated with their adaptation replaced with negative ones (Gates and Gysel 1978, Misenhelter and Rotenberry 2000). Although most of the literature on ecological traps thus far pertains to birds (Battin 2004), some studies have documented habitat-management practices that decrease shrub- and tree-canopy cover, thus creating unintentionally negative impacts on snakes by increasing their exposure and thereby increasing predation rates (Durbian 2006, Setser and Cavitt 2003). Cryptic behavior is an important predator-avoidance technique for many snakes and other reptiles that involves remaining stationary while blending into surroundings (Martins 1996). However, in cooler climates, viviparous snakes must typically bask extensively in order to thermoregulate effectively, and in doing so maintain greater exposure to potential predators (Lourdais et al. 2004). Therefore, some edge habitats may enable better predator avoidance for basking snakes by providing them with vital retreat sites (Blouin-Demers and Weatherhead 2001, DeGregorio 2008, Greene 1988, Harvey and Weatherhead 2006). However, few studies have 1State University of New York College of Environmental Science and Forestry, 1 Forestry Drive, Syracuse, NY 13210. *Corresponding author - ajrobill@syr.edu. Manuscript Editor: Ralph Grundel Northeastern Naturalist Vol. 22, No. 1 A. Robillard and B.Johnson 2015 201 examined the impact that efforts at habitat improvement can have on the behavior of basking snakes (Burger 2001, Harvey and Weatherhead 2006, Hedgecock 1992, Parent and Weatherhead 2000, Prior and Weatherhead 1994). Sistrurus catenatus (Rafinesque) (Eastern Massasauga Rattlesnake [EMR]) is considered threatened or endangered in every state where it occurs with the exception of Michigan, which is considered a stronghold for the species (Szymanski 1998). This species is typically found in early to mid-successional habitats (Bailey et al. 2012, Foster et al. 2009, Johnson and Leopold 1998, Jones et al. 2012, Reinert and Kodrich 1982) and may preferentially bask near retreat sites (DeGregorio 2008, Harvey and Weatherhead 2006, Marshall et al. 2006) such as shrubs or slash piles (DeGregorio 2008, Harvey and Weatherhead 2006). In viviparous snakes like the EMR, effective thermoregulation by gravid females critically influences the fitness and phenotype of developing offspring (Alberts et al. 1997, Blouin-Demers et al. 2000, Lourdais et al. 2004, Shine et al. 1997). At Cicero Swamp Wildlife Management Area (CSWMA) in New York, the resident EMR population is threatened by woody-plant growth that infringes on established basking areas (Johnson and Breisch 1993, Johnson and Leopold 1998, Shoemaker and Gibbs 2010). EMRs at CSWMA are known to bask in places with significantly higher temperatures than nearby random locations, and also in locations that appear to offer greater potential cryptic protection from predators (Shoemaker and Gibbs 2010). Basking EMRs rely on cryptic behavior or flee to avoid potential predators (Greene 1988, Klauber 1982, Parent and Weatherhead 2000). To provide a mix of active warming and cryptic basking sites for EMRs at CSWMA (Shoemaker and Gibbs 2010), the New York State Department of Environmental Conservation (NYSDEC) conducted habitat manipulations in 2011 that included cutting tall (>1 m) shrub vegetation within thirty-two 100-m2 square plots. Workers cut shrubs to the ground and removed all fallen vegetation from the plots, which maintained a clearly defined hummockhollow definition. Despite possible benefits, habitat-management practices that decrease shrub cover can increase the rate of predation on snakes by increasing their exposure to predators (Durbian 2006, Setser and Cavitt 2003). Although EMRs at CSWMA used cut plots more than unmanipulated sites for basking (Johnson 2013), the influence of distance to edge habitat on the behavior of basking snakes remained unknown. Therefore, our objective was to determine whether the entirety of a 100-m2 plot provided adequate basking potential for EMRs. By pairing habitat-use surveys (Johnson 2013) with behavioral observations, we hoped to better understand the influence of distance to plot edge (DTE) on EMR basking behavior and site selection. Understanding how EMRs bask in cut habitats in relation to DTE could help to determine ideal dimensions of future habitat manipulations, and help to avoid ecological trapping. Study Site CSWMA, in Onondaga County, NY, is a large wetland complex managed by NYSDEC and comprised of a mix of upland forest and peatland habitats (Johnson and Leopold 1998). A fire in 1892 completely burned an ~1-m-deep layer of peat Northeastern Naturalist 202 A. Robillard and B.Johnson 2015 Vol. 22, No. 1 moss in a 37-ha area of CSWMA now known as the burn area (LeBlanc and Leopold 1992), which serves as core range of resident EMRs (Johnson 1995, 2000). To mitigate the extensive shrub growth in this historically open habitat, 32 experimental 100-m2 plots were cut in the burn area in 2011 (Johnson 2013). This area is distinguished from adjacent habitats by having organic soils with a high occurrence of Vaccinium corymbosum L. (Highbush Blueberry), Ilex mucronata (L.) Powell, Savol. & Andrews (Mountain Holly), and Aronia melanocarpa (Michx.) Elliot (Black Chokeberry) surrounded by trees such as Picea mariana (Mill.) Britton, Sterns & Poggenb. (Black Spruce), Larix laracina (Du Roi) K. Koch (Eastern Tamarack), Acer rubrum L. (Red Maple), and Betula pendula Roth (European White Birch) (Johnson 1995, LeBlanc and Leopold 1992). Methods To record how EMRs basked within the 32 treatment plots, we surveyed each plot once per week from early June to late August in 2011 and from late May through August in 2012. We conducted surveys from the morning into early afternoon. At least 2 observers searched each plot from the edge to the middle and detected EMRs in vegetation by sight or by sound (rattling). Upon finding an EMR, the observers measured its distance to habitat edge, made at least two visual-exposure estimates, recorded the average of at least 2 dorsal infrared (IR)- temperature readings using an Extech IR400 (Extech Instruments, Waltham, MA), and noted the snake’s basking behavior, and then captured and handled them using the methods of Johnson (2013) to determine sex and gravidity and to implant passive integrated transponder tags (AVID Identification Systems, Inc., Norco, CA) to identify individuals. We collected exposure estimates prior to capture by observing the percentage of the snakes that could be seen through vegetation from directly above at standing height. We classified behaviors as either cryptic (i.e., 0 = stationary, not rattling) or defensive (i.e., 1 = rattling and/or retreating), which were adapted from previous observations by Klauber (1982) and Greene (1988) and methods used by Hedgecock (1992). We intentionally limited our analysis of EMR presence relative to DTE to snakes that were engaged by an observer at less than 1-m distances in order to control for possible behavioral effects of our approach distance and direction. The majority of our captures were females, and we limited behavioral analysis to gravid females to account for the possible behavioral bias associated with gravidity (Goode and Duvall 1989, Harvey and Weatherhead 2006). Brodie and Russell (1998) observed Thamnophis sitalis L. (Garter Snakes) at temperatures of 15–30 °C, and noted a positive correlation between anti-predation behaviors (e.g., fleeing) and temperatures up to 30 °C. Thus, for our behavioral observations, we included only snakes whose IR temperature was above 15 °C because colder snakes cannot display response behaviors. We used a chi-square test to compare EMR occurrence to DTE with a null hypothesis of uniform distribution throughout a plot. We observed EMRs across a 10 m x 10 m grid within each plot. In total, we made 87 observations of EMRs across the grids examined, leading to an expectation of 0.87 observations per m2 Northeastern Naturalist Vol. 22, No. 1 A. Robillard and B.Johnson 2015 203 of grid area across the study. To test whether observations were uniformly distributed across the grids, we divided the grids into 1-m-wide nested squares. The first square was a 1-m-wide band around the inside of the perimeter of the 10 m x 10 m grid, the second was 1-m-wide following the inside perimeter of the first band, and we continued in 1-m-wide bands producing 5 bands (i.e. 0–1 m, 1.1–2 m, 2.1–3 m, 3.1–4 m, 4.1–5 m) with areas of 36, 28, 20, 12 and 4 m2 per band. We calculated expected number of observations per band by taking the product of the band’s area and 0.87 observations per m2 for a uniform distribution of observations. We determined deviation from expectation with a chi-square test comparing actual number of observations per band area in a grid to expected numbers (Ries and Debinski 2001). We compared exposure of snakes to DTE using a simple linear regression model. To account for the possible influence of temperature on the DTE of basking snakes, we decided to include this variable in the model based on its significance (α = 0.05). We compared the behavior score of gravid female EMRs to DTE using logistic regression models and similarly chose a best model based on significance of included variables such as exposure and temperature. We performed all analyses on each season separately because there were obvious differences in vegetative cover within the 100-m2 basking plots between years due to growth of vegetation throughout the first field season. Conditions of each capture were variable in terms of microhabitat, and the number of unique individuals captured was low, so we treated the capture of individuals on different days as independent units (Andrews 1971). We constructed all models in R 2.15.1 (R Core Team 2012) and used Minitab (Minitab, Inc.; www.minitab.com) to graphically represent the results. Results and discussion We made 87 observations on 42 individual snakes, resulting in a mean of 2.07 observations per snake (SD = 1.09, skewness = 0.80). We captured 16 of the 42 individuals only once. We found that EMR basking-site selection and behavior did not vary with DTE within the plots, suggesting that habitat manipulations occurring at a 100-m2 scale were not likely to restrict snakes in their use of the landscape. Tests of our observations of EMR DTE in the 100-m2 plots indicated an even distribution in both 2011 (df = 4, n = 57; χ2 = 1.517, P = 0.824) and 2012 (df = 4, n = 39; χ2 = 0.921, P = 0.921) (Table 1). Snake exposure did not vary with DTE or temperature when modeled together in 2011 (n = 49, P = 0.715 ) and 2012 (n = 36, P = 0.218). However, we found that when gravid females basked in more exposed areas, their response behavior was more cryptic (i.e., they remained stationary and did not rattle), even when we included DTE in our model (2011: n = 60, P < 0.001 and 2012: n = 35, P = 0.025) (Fig. 1). Our results suggest that EMRs do not alter their selection of basking sites based on habitat within a 5-m distance from the edge of the cleared plots. DeGregorio (2008) found that EMRs in clear-cuts use areas up to 24.92 ± 1.73 m away from the forest edge, with 85% of snakes located within 2 m of slash piles left on sites. Harvey and Weatherhead (2006) determined that, when available basking sites up to 30 m away from the edge of forests were available, EMRs most often used areas Northeastern Naturalist 204 A. Robillard and B.Johnson 2015 Vol. 22, No. 1 Table 1. Distance to edge (DTE) distribution of Eastern Massasauga Rattlesnakes observed in 100- m2 cleared plots, compared to expected spatial distribution of snakes if equally likely to be found anywhere in the plots. Band DTE (m) Observed Expected χ2 2012 0.0–1.0 12 14.04 0.296 1.1–2.0 13 10.92 0.396 2.1–3.0 8 7.80 0.005 3.1–4.0 4 4.68 0.099 4.1–5.0 2 1.56 0.124 n = 39, df = 4, χ2 = 0.921, P = 0.921 2011 0.0–1.0 18 20.52 0.309 1.1–2.0 17 15.96 0.068 2.1–3.0 13 11.40 0.225 3.1–4.0 8 6.84 0.197 4.1–5.0 1 2.28 0.719 n = 57, df = 4, χ2 = 1.517, P = 0.824 Figure 1. Binary logistic regression models of the behavior score (0 = cryptic, 1 = escape/rattle) indicating that exposed gravid female Eastern Massasauga Rattlesnakes exhibited more cryptic behavior than those under partial or full cover in both 2011 and 2012. Northeastern Naturalist Vol. 22, No. 1 A. Robillard and B.Johnson 2015 205 15–20 m away. Although these previous studies indicate EMRs perceived edge as between 15–25 m, both were conducted in areas of uncut or clear-cut forests (De- Gregorio 2008, Harvey and Weatherhead 2006), whereas our study was located in a mosaic of plots cut within a shrub-dominated area. Because they were connected by trails, our plots could have focused predatory search efforts, potentially making the plots more prone to becoming ecological traps than a clear-cut area. Basking-site selection by EMRs may be an anti-predation tactic or a response to movements of prey species (DeGregorio 2008, Theodoratus and Chiszar 2000). Similarly, research has shown that predator avoidance may be a secondary driver of preference for edges of fragmented habitat for other serpent species such as Pantherophis obsoletus (Say) (Black Rat Snake; Blouin-Demers and Weatherhead 2001, Carfagno and Weatherhead 2006). Basking EMRs that behave less cryptically (i.e., rattling or fleeing) upon being disturbed are likely at higher risk for predation, although basking snakes may flee successfully more often when basking near the cover of a habitat edge (Greene 1988, Prior and Weatherhead 1994). Consequently, we might expect EMRs to expose themselves less and use the cover offered from regrowth more the farther into a basking plot and farther from the refuge of the edge habitat they are located. Our results indicate that exposure of basking EMRs is not influenced by their DTE. Uniformity in EMR exposure relative to DTE might be influenced by the surrounding vegetative growth. In 2011, manipulated plots were generally devoid of shrub cover throughout, potentially limiting the EMRs to homogeneous exposures with limited retreat sites thereby restricting their ability to seek refuge and lower their exposure. However, in 2012 plots contained more vegetative growth, but exposure of EMRs was still not influenced by their DTE, suggesting that the regrowth of vegetation was fairly uniform within the plots. It is possible that exposure of snakes was more closely linked to the microtopography of plots and corresponding availability of retreat sites within them. We recommend that future studies should focus on the effects of retreat-site availability on EMR exposure. The resulting data might prove valuable in optimizing future management efforts. Because EMRs that behave less cryptically might be at higher risk for predation (Greene 1988, Prior and Weatherhead 1994), we expected snakes basking in the middle of plots, farther from the safety of the edge, to behave more defensively than snakes closer to the edge. Our comparison of behavior relative to DTE showed that the likelihood of observing EMRs fleeing, rattling or remaining cryptic was similar at any DTE. Rattlesnakes, which are generally slow and bulky serpents, rely mostly on defensive behaviors, such as rattling and, more commonly, remaining cryptic, to avoid predation (Greene 1988, Hedgecock 1992, Klauber 1982, Weatherhead and Madsen 2009). Striking is considered a last-resort defensive behavior for rattlesnakes because it is energetically and physiologically expensive; it is more likely an offensive endeavor (Glaudas et al. 2005). Remaining cryptic is the primary EMR predator-avoidance strategy, and so these snakes generally do not respond defensively to short-term disturbances such as human presence (Harvey and Weatherhead 2006, Hedgecock 1992, Parent and Weatherhead 2000). Northeastern Naturalist 206 A. Robillard and B.Johnson 2015 Vol. 22, No. 1 Our study examined the habitat utilization by EMRs and the effect on their behavior through management actions such as shrub-cutting. We found that basking behavior of gravid EMRs becomes more cryptic with increased exposure. This cryptic strategy might be an adaptation for gravid females, which are known to expose themselves more than other EMRs (Harvey and Weatherhead 2006), because such exposure aids in the development of their unborn offspring (Alberts et al. 1997, Blouin-Demers et al. 2000, Lourdais et al. 2004, Shine et al. 1997). Gravidity might limit an EMR’s potential to escape while fleeing (Parent and Weatherhead 1994), thereby explaining why gravid individuals tend to remain cryptic rather than move defensively when disturbed. The relationship between defensive behavior and exposure of basking EMRs may differ for non-gravid adults relative to gravid females, and should be considered in future studies. Cryptic behavioral differences between gravid and non-gravid periods and between sexes should also be identified to isolate the origins of this behavior. Based on our results, EMR basking-site selection and behavior do not vary within a cleared plot size of 100-m2, suggesting that the snakes’ use of the habitat might not be influenced by habitat manipulations at this scale. We recommend further study of EMR decision-making and specific predation counts to determine the full effects that plot-clearing and DTE has on predation rates. Further study is also needed to determine EMR basking behavior in cleared plots greater than 100- m2. Further examination of cryptic basking behaviors might highlight necessary adjustments to habitat management that could enhance techniques used to conserve EMRs and other threatened snakes. Acknowledgments The New York State Department of Environmental Conservation hosted our study and provided logistical support. 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