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1 Chapter 14: Terrapin Conservation: Mitigating Habitat Loss, Road Mortality, and Subsidized Predators 2 John C. Maerz1, Richard A. Seigel2, and Brian A. Crawford1 3 4 5 6 7 1 8 Introduction 9 D. B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602. 2 Department of Biological Sciences, Towson University, Towson, MD 21252. The majority of animals have complex life cycles that require periodic migration to 10 complementary habitats. As a result, the management of such species can be challenging because it 11 requires assessing and targeting interventions toward multiple threats concurrently. In a previous 12 chapter in this volume, Chambers and Maerz (in review) address the specific impacts and management 13 of terrapin bycatch in commercial and recreational crab pots. While bycatch impacts on terrapin 14 populations are well-documented throughout the species range, a suite of terrestrial factors also 15 interact to impact terrapin populations such that bycatch management needs to be included as a part of 16 a more comprehensive terrestrial-aquatic management strategy (Hart 2005, Crawford et al. 2014a). 17 In this chapter, we address the major terrestrial management issues for terrapins, which include 18 road mortality during nesting migrations, nest depredation by mesopredators, and vegetation effects on 19 nest microclimate and depredation. We first summarize the terrestrial habits of terrapins and their 20 importance relative to aquatic life stages. We note that terrapins spend very little time in terrestrial 21 environments, yet the terrestrial phases of their lives appear to present more numerous and influential 22 threats to population growth. Next we review current knowledge on each major terrestrial threat to 23 terrapins, and we discuss interactions between threats and opportunities for complementary 24 management options. We stress that failure to account for impacts at all life stages may often render 25 management activities targeted at one or a subset of stages ineffective, and we discuss how 1 26 complementary terrestrial management creates flexibility and opportunities for compensatory actions 27 when certain threats cannot be fully remediated. 28 29 Terrapin Life Cycles, Demographic Rates, and Terrestrial Habits 30 Juvenile and adult terrapins primarily live in aquatic environments, with terrestrial habits limited to brief 31 annual migrations of females onto land to nest, and hatchlings dispersing from terrestrial nests to 32 aquatic habitats. Terrestrial movements of juvenile and adult male terrapins are believed to be rare, but 33 individuals have occasionally been encountered (<2% of observations) during road surveys (Szerlag and 34 McRobert 2006, Crawford 2011). Terrapins show similar general nesting behavior throughout the 35 species range, though patterns can vary geographically associated with changes in coastal environments 36 and movement of the species into more inland brackish environments (Roosenburg 1994). Generally, 37 females nest from late spring through mid summer and make multiple nesting migrations within a single 38 breeding season often failing to nest during a migration. Diel nesting patterns may vary geographically, 39 potentially in relation to predation risk. Several studies show daylight nesting of terrapins concentrated 40 around the diurnal high tide (Fig. 1; Burger and Montevecchi 1975, Zimmerman 1992, Goodwin 1994, 41 Butler et al. 2006, Szerlag and McRobert 2006, Crawford et al. 2014b). Nesting during the high tide may 42 reduce the time and distance female terrapins must travel, and may be related to higher survival among 43 nests laid above the high tide line. Daytime nesting also occurs in the late morning through mid 44 afternoon in localities where tidal influences are absent (Seigel 1980). However, approximately half of 45 females nest at night in Sandy Neck Massachusetts (Auger and Giovannone 1979) and females nest 46 primarily at night along the Patuxent River in Maryland (Roosenburg 1994). The terrestrial portions of 47 nesting routes are generally short (<50 m), but can be as long as 1600 m in Massachusetts (Auger and 48 Giovannone 1979). Females typically nest a few meters above the spring high tide (Burger and 49 Montevecchi 1975, Butler et al. 2004) and generally in sandy soils, and females have been reported 2 50 nesting in a variety of vegetation habitats including areas of bare sand, exposed and vegetated dunes, 51 short or tall dense grasses, and dense shrubs. Attributes of sandy soils that may be important in nesting 52 habitat selection include access, thermal and moisture conditions, soil composition and texture, 53 disturbance, and predation risk (Burger and Montevecchi 1975, Goodwin 1994, Roosenburg 1994, 54 Feinberg and Burke 2003, Ner 2003, Scholz 2006, Hackney 2010, Grosse et al. in review). Nesting 55 duration is generally short (15 – 120 min) with the majority of time allocated to nest site selection 56 (Roosenburg 1994). Females will often frequently abandon nesting, often in response to disturbance by 57 predators or humans. 58 59 Recommended location for Figure 1 Because terrapin hatching success and sex ratio are dependent on nest incubation temperatures 60 and other factors affected by topography and vegetation structure, one expects female terrapins to 61 show fidelity to natal nest sites or local, interannual nest site selectivity fidelity. Sheridan (2010) used 62 mark-recapture and genetic markers to show natal nest site fidelity among some female terrapins, and 63 other studies show nest site fidelity within and among years (Goodwin 1994, Crawford 2011). Crawford 64 (2011) reports capturing 50% of nesting female terrapins within 50 m of their capture location the 65 previous nesting season, and 80% of females were captured within 200m of their capture location the 66 previous nesting season. Roosenburg (1996) used egg size data to infer that females are more selective 67 about nest sites when they have larger eggs; however, nest site fidelity and selectivity may vary 68 geographically (Roosenburg 1994). Mean incubation time varies with latitude and microhabitat, ranging 69 from as short as 66-69 days in central and northern Florida (Seigel 1980, Butler et al. 2004) to 74 days in 70 New Jersey and 77 days in New York (Scholz 2006). However, local factors such as the presence of 71 vegetation that shades nests can slow development and create greater local variation incubation time 72 than is seen over wide latitudes (Goodwin 1994, Wneck 2010). 3 73 Hatchlings may emerge from nests in the late summer, fall or the following spring, when they 74 appear to disperse into high marsh environments. Burger (1976) reports that hatchling terrapins in New 75 Jersey move quickly into grassy vegetation and downslope, which would be consistent with rapid 76 dispersal bias from elevated nesting areas into marsh vegetation. However, Muldoon and Burke (2012) 77 report that hatchlings emerging in fall in New York tended to move up in elevation rather than down 78 until spring when the behavior reversed. They also report finding hatchlings on land up to nine months 79 after emergence from the nest, which may indicate prolonged terrestrial habits by some individuals or in 80 some environments. Once in the high marsh, hatchlings appear to avoid open water and tend to stay 81 close to vegetation, often burrowing in areas of dense rack (Lovich et al. 1991). Laboratory studies 82 suggest that hatchling and juvenile terrapins may also use the high marsh and terrestrial habitats to 83 reduce osmotic stress that can inhibit growth (Dunson 1985, Kinneary 2008, Holliday et al. 2009). 84 The demographic rates associated with the terrapin life cycle are typical of most turtles 85 including other members of the Emydidae (Heppell 1998, Ernst and Lovich 2009). We have provided a 86 list of stage-specific estimates of terrapin demographic rates and the associated context from across the 87 species range in Table 1. Generally, terrapin life history is characterized by high annual adult survival, 88 and potentially low but highly variable egg survival, and slow growth and low survival from hatching to 89 adulthood. Females generally mature between 6 and 8 years though some smaller subspecies may 90 mature at 4 years, and females lay 1-3 clutches of 5 to 15 eggs per annum. Hatchling sex ratio is 91 environmentally determined, and incubation temperature and egg size can have significant positive 92 effects on juvenile growth and maturation rates (Roosenburg and Place 1995, Roosenburg and Kelley 93 1996). There are few estimates of adult annual survival despite the existence of several multi-year 94 population studies across the species range (e.g., Mitro 2003, Dorcas et al. 2007). Mitro (2003) 95 estimated adult annual survival between 0.94-0.96, which is consistent with estimates of adult annual 96 survival for freshwater emydids (Heppell 1998). There are few direct measures or indirect estimates of 4 97 hatchling or juvenile annual survival [aptly referred to as the missing years]. Mitro (2003) estimated 98 juvenile annual survival between 0.446 and 0.565, which is lower than estimates for other emydids 99 (Heppell 1998); however, Mitro (2003) did not distinguish hatchling from juvenile survival. As with other 100 species, hatchling survival is likely to be lower than juvenile annual survival (Heppell 1998). Draud and 101 Zimnavoda (2004) documented 33% mortality of hatchling terrapins over a 29 day period, though this 102 resulted from predation by introduced Norway rats. Crawford et al. (2014a) estimated annual hatchling 103 survival was ~25%, which is consistent with rates estimated for other emydids (Heppell 1998). 104 With such limited data on most terrapin demographic rates, there is little opportunity to 105 evaluate geographic variation for most terrapin demographic rates. We do know that terrapin clutch size 106 increases significantly with latitude with a small concurrent increase in mean age at maturity from 6 to 8 107 years (Table 1). One would expect higher adult or nest survival rates to accompany delayed maturity. 108 Nest or egg survival rates to hatching are highly variable among sites and years such that there are no 109 clear geographic trends in variation. Rather, variation in nest and egg survival is governed by local 110 conditions such as nest and predator abundance and vegetation (Table 1). 111 112 Recommended location for Table 1 All turtle life stages influence population growth and viability, but population growth is not 113 equally sensitive to variation in all demographic rates and all demographic rates are not equally variable 114 or amenable to management (de Kroon et al. 2000). Like other turtles (Heppell 1998, Enneson and 115 Litzgus 2008), terrapin population growth is most sensitive to variation in adult female survival, followed 116 by juvenile and hatchling survival, and finally female fecundity (Mitro 2003, Crawford et al. 2014a). 117 Models of terrapin population growth are consistent with other species that indicate 3-5% additive 118 reductions in female survival are sufficient to cause population declines (Crawford et al. 2014a). Though 119 terrapin population growth is least sensitive to nest or egg survival (Mitro 2003, Crawford et al. 2014a), 5 120 nest or egg survival is naturally and anthropogenically highly variable (Table 1). When one factors in 121 that terrapins have temperature dependent sex determination, which creates a potential for sex-specific 122 nest or egg survival rates, and the existing knowledge about factors that affect nest survival and sex 123 ratios of hatchlings, the nest life stage is more valuable as a management target than is reflected by its 124 elasticity. 125 126 Terrestrial Threats to Terrapin Populations 127 Though terrapins spend a relatively brief portion of their lives in terrestrial habitats, a suite of terrestrial 128 threats can have a disproportionately large effect on terrapin populations. Terrapins are confronted 129 with modified access and alterations to nesting habitats, nesting females can experience high mortality 130 rates along coastal roads, and subsidized predators can increase both adult and egg mortality. Arguably 131 the two largest terrestrial threats, and the two for which there is the greatest amount of research, are 132 vehicle strikes on coastal roads and high nest depredation from subsidized mammalian predators. 133 However, the variety of terrestrial threats that have been identified to date indicates that threats that 134 are localized or have small effects are part of a larger cumulative set of terrestrial threats to terrapin 135 populations. In many cases, terrestrial threats are likely spatially correlated and interact across multiple 136 life stages with dramatic negative consequences to terrapin populations. 137 Alterations to Nesting Habitats – Though not initially identified among the pressing threats to 138 sustaining terrapin populations, intensifying coastal land use and associated changes in land cover are 139 emerging as an important factor influencing local and regional terrapin abundance. For example, Wneck 140 (2010) and Winters (2013) report that 38% of the shoreline of Barnegat Bay, NJ has been altered in 141 manners detrimental to terrapin nesting habitat. We know of only one study that has examined the 142 effects of terrestrial land use on terrapin populations at a large spatial extent. Isdell et al. (2013) found 6 143 that terrestrial land use, notably agricultural land use, adjacent to marsh habitat was strongly negatively 144 correlated with terrapin occupancy within the Chesapeake Bay. How agricultural practices affect 145 terrapin populations is unknown, but may be related to effects on nesting habitats through soil 146 disturbance and dense planting of vegetation. 147 The bulk of our knowledge about anthropogenic impacts on nesting habitats is limited to 148 estimates of local effects on terrapin behavior or nest success. Roosenburg (1991) highlighted that 149 increasing coastal development results in the loss of intact shoreline and the common practice of 150 constructing bulkheads to stabilize shorelines. Bulkheads can block terrapin access to proximate, 151 preferred nesting sites, which can increase female nesting migration distances, cause females to nest in 152 suboptimal habitats, or concentrate nests into smaller areas (Roosenburg 1994). Winters (2013) used 153 telemetry to measure the effects of bulkheading on terrapin nesting in Barnegat Bay, New Jersey. She 154 found that bulkheads could increase total travel distance up to 500%. When displacing females 155 concentrates nests in areas, this can lead to higher nest predation rates (Roosenburg and Place 1995). In 156 addition, manmade structures can shade terrapin nesting areas, resulting in longer development times 157 and increased male-biased hatchling sex ratios (Wneck 2010). 158 Coastal development practices that alter soils may also be detrimental to terrapin nesting 159 (Wneck 2010). Terrapins evolved to nest in sandy soils, which have properties such as large particle 160 sizes that improve gas diffusion and lower water potential that can reduce hydric constraints on 161 developing embryos (Roosenburg 1994, Wneck 2010). The common practice of dredging of bays to 162 clear shipping channels, fill uplands, and construct causeways can negatively impact remaining terrapin 163 nesting habitats. In highly developed coastal areas, dredge fill areas and causeways may be the only 164 terrapin nesting habitat available (Wood and Herlands 1997, Wneck 2010). Dredge soils contain high 165 concentrations of organic solids, fine sediments, and salts that would increase gas exchange and hydric 7 166 constraints on terrapin eggs (Wneck 2010). Wneck (2010) demonstrated that terrapin embryos are 167 incapable of developing in fresh dredge soil because the high salt content causes embryos to desiccate. 168 After one year, terrapin embryos could develop in aged dredge, but egg survival was still reduced 169 relative to natural sandy soils. 170 Increasing coastal development also leads to shifts in vegetation that directly affect terrapin 171 nesting success and interact with subsidized predators to affect nest survival. Terrapins prefer to nest in 172 areas of patchy, short vegetation, where nests develop faster and tend to produce a higher proportion 173 of female hatchlings (Burger and Montevecchi 1975, Goodwin 1994, Roosenburg 1994, Feinberg and 174 Burke 2003, Ner 2003, Scholz 2006, Hackney 2010, Grosse et al. in review). The dense planting of dune 175 grasses to control erosion or dense areas of invasive plants can increase terrapin nest failure 176 (Roosenburg 1991, Wneck 2010). Some plant roots will infiltrate and kill terrapin eggs (Lazell and Auger 177 1981), and dense grasses can reduce soil moisture potential, resulting in higher egg failure rates. Dense 178 herbaceous cover or the succession or deliberate planting of trees and shrubs can also reduce terrapin 179 nest survival and skew hatchling sex ratios. Dense vegetation shades nests, resulting in longer 180 development times, higher egg mortality, and male biased hatchling sex ratios (Wneck 2010). 181 Vegetation cover may also interact with predator abundance to affect terrapin nest success. 182 Roosenburg and Place (1995) found that shaded nests in dense grass had higher survival rates but 183 produced almost 100% male hatchlings. Burger (1977) reports high mammalian depredation of terrapin 184 nests in wooded, shrub and edge habitats, and Hackney (2010) found that terrapin nests in shrub or 185 edge habitats closer to marshes had a higher probability of being depredated compared to nests in open 186 sandy areas farther from the marsh. Grosse et al. (in review) demonstrated experimentally that shaded 187 nests in shrub habitats had lower survival rates as a result of higher depredation by raccoons, and 188 surviving nests in shaded shrub habitats produced 100% male hatchlings. In contrast, open, grassy 189 habitats had the highest nest survival rates and produced 100% female hatchlings (Grosse et al. in 8 190 review). Collectively, these studies show that altered terrestrial vegetation can influence nest survival 191 and hatchling sex ratios, and that increasing shrub or tree cover may interact with increases in 192 subsidized mammalian predators to increase nest mortality. 193 194 Subsidized Terrestrial Predators –Mortality of terrapins on land, particularly nest and hatchling 195 mortality, is clearly related to subsidized predator abundance. Known terrestrial predators of adult 196 terrapins are raccoons and foxes, while terrestrial nest and hatchling predators include ghost crabs, 197 grackles, crows, foxes, raccoons, armadillos, introduced Norwegian rats and red imported fire ants. 198 Many studies report anecdotal predation on adult female terrapins by raccoons, but detailed reports of 199 such occurrences are uncommon (Figure 2). Seigel (1980) and Feinberg and Burke (2003) documented a 200 relatively high number of adult female terrapins killed by raccoons over two year periods in Florida and 201 New York respectively, which indicates that adult mortality could be high during nesting migrations in 202 areas where human activities subsidize predators. Burger and Montevecchi (1975) and Roosenburg 203 (1994) suggest that high mammalian predation risk may be a selective pressure promoting diurnal 204 nesting habits by female terrapins. 205 206 Recommended location for Figure 2 The available literature also indicates that terrapin nest and juvenile survival rates can be high in 207 areas with few predators, but can be extremely low in areas of high natural or introduced predator 208 density (Table 1). Numerous studies show raccoon predation is the biggest determinant of terrapin nest 209 success, and in many studies of sites with high raccoon densities throughout the species’ range, 210 raccoon’s routinely depredate as much as 95% of nests (Feinberg and Burke 2003, Butler et al. 2006). 211 Several studies note that mammalian depredation of nests generally occurs within 48 hours of nesting 212 (Burger 1977, Roosenburg 1991, Goodwin 1994, Munscher et al. 2012, Crawford et al. 2014a), and as 9 213 mentioned previously, nests in shrubby or wooded habitats may be more vulnerable to mammalian 214 predators . Several studies also document that predators are significant sources of mortality for 215 hatchlings in the nest and after emergence (Feinberg and Burke 2003, Butler et al. 2006). A study in 216 Oyster Bay Harbor, New York documented that introduced rats depredated 67% of terrapin hatchlings 217 within 30 days of emerging from nests (Draud and Zimnavoda 2004). 218 219 Roads - Roads have become a pervasive fixture on most landscapes with conservation 220 implications for many species. In the Eastern and Gulf Coasts of the United States respectively, 60 to 221 80% of areas are within 400 m of a road (Riitters et al. 2003) and are experiencing the fastest annual 222 increases in traffic density (Baird 2009). In the case of terrapins and other turtle species, models predict 223 road mortality to cause substantial declines of turtle populations on a regional scale (Fahrig et al. 1995, 224 Gibbs and Shriver 2002, Andrews et al. 2008, Litvaitis and Tash 2008, Langen et al. 2009, Beaudry et al. 225 2010). 226 Roads can affect terrapin populations through the permanent loss of habitat, increased 227 mortality from vehicle strikes, and by creating a barrier to movement that restricts movements of 228 individuals between terrestrial and aquatic habitats (for reviews of road impacts on various taxa see 229 Forman and Alexander 1998, Trombulak and Frissell 2000, Andrews et al. 2008, Fahrig and Rytwinski 230 2009). In general, turtles use complex habitat networks for migrating, mate-searching, nesting, and 231 hibernating that often bring them across roadways (Gibbs and Shriver 2002, Aresco 2005, Brennessel 232 2006, Beaudry et al. 2008, Langen et al. 2009). Road mortality is particularly high among terrapins 233 because they are slow moving, do not avoid roads, and cannot flee from oncoming cars (Gibbs and 234 Shriver 2002, van Langevelde and Jaarsma 2004, Fahrig and Rytwinski 2009). Moreover, because turtle 235 road mortality is generally related to movements for breeding and nesting (Wood and Herlands 1997, 10 236 Gibbs and Shriver 2002, Beaudry et al. 2010), it disproportionately affects mature females (Steen et al. 237 2006, Grosse et al. 2011, Crawford et al. 2014a). Among studies that have monitored terrapin activity 238 on roads, > 98% of individuals impacted were adult females (Wood and Herlands 1997, Hoden and Able 239 2003, Szerlag and McRobert 2006, Crawford et al. 2014b). Since turtle populations are strongly governed 240 by high adult female survival, even minor additive road mortality can lead to rapid population decline. 241 Despite documentation of high numbers of terrapins killed on roads throughout the species 242 range, there are relatively few studies that evaluated the local or regional impacts of roads on terrapins 243 or factors that cause terrapin mortality on roads to vary. At the regional scale, Grosse et al. (2011) 244 conducted a statewide assessment of the relationship between commercial crabbing and roads on 245 terrapin abundance in Georgia, and found that proximity to roads did not correlate with terrapin 246 abundance or sex ratio statewide. However, they did find that terrapin abundance was notably low on 247 causeways that bisect marshes to barrier islands. Wood and Herlands (1997) reported high numbers of 248 terrapins killed on roads annually along causeways that bisect marshes en route to densely populated 249 beaches in New Jersey. Crawford et al. (2014a) directly estimated adult female terrapin mortality on the 250 9-km Downing-Musgrove Causeway to Jekyll Island, Georgia and found that mean annual adult female 251 mortality from vehicle collisions during nesting migrations was 11%, and ranged annually over a three 252 year period between 4.4% and 16.4%. They estimated that even the lowest annual additive mortality of 253 4.4% from vehicle collisions was sufficient to cause the terrapin population to decline, and consistent 254 with the high rate of female mortality, they estimated that terrapin populations in the creeks adjacent 255 to the causeway had greater than a 4:1 male biased sex ratio. Similarly, Avissar (2006) reported that the 256 sex ratio of the terrapin population along the Garden State Parkway in New Jersey, where terrapin road 257 mortality is frequent, has increased from 0.61 to 5.7 between 1989 and 2003, and mean terrapin 258 carapace length declined over the same 14 year time period consistent with a loss of older adult 259 females. 11 260 261 Recommended location for Figure 3 262 Causeways constructed through marshes create a significant “ecological trap” for females 263 terrapins (Schlaepfer et al. 2002). With increasing coastal development, elevated causeways through 264 the marsh become the only available nesting habitat for terrapins. Female terrapins are naturally 265 attracted to nest in open, elevated habitat in proximity to the marsh (Szerlag and McRobert 2006), and 266 it is often the case that portions of the causeway most proximate to the road are mowed to maintain 267 short vegetation (Figure 3), while areas more proximate to the marsh may be planted or overgrown with 268 shrubs. This makes the most attractive parts of causeways for nesting those that are immediately 269 adjacent to the road (Wood and Herlands 1997, Crawford et al. 2014b). Traffic volumes on coastal roads 270 peak between May and August (Baird 2009), which overlaps with the terrapin nesting season 271 throughout the range of the species (Seigel 1980, Zimmerman 1992, Wood and Herlands 1997, Feinberg 272 and Burke 2003, Crawford et al. 2014b), and because female terrapins often nest proximate to the 273 diurnal high tide, they are likely to be active on roads during the day when traffic volume is highest. It is 274 under these conditions that we observe the highest numbers of terrapin-vehicle collisions. For example, 275 in New Jersey, Hoden and Able (2003) documented 450 terrapins killed on 8 km of Great Bay Boulevard 276 near Tuckerton between 1999 and 2002, and Wood and Herlands (1997) documented 4,020 terrapins 277 killed on 28 km causeways to the Cape May Peninsula between 1989 and 1995. Between 2009 and 278 2013, Crawford et al. (2014b) documented 757 female terrapins killed along 9 km of the Downing- 279 Musgrove Causeway to Jekyll Island, Georgia. 280 At finer spatial scales, terrapin mortality along a road can be spatially and temporally diffuse or 281 clustered. Areas of concentrated activity or mortality on roads are known as threat hot spots, and 282 periods of concentrated activity are known as threat hot moments (Beaudry et al. 2008, Beaudry et al. 283 2010). Crawford et al. (2014b) found that 30% of terrapins road mortalities occurred over a 2-year 12 284 period were distributed among three hot spots representing only 0.8 km (9%) of the 9-km causeway to 285 Jekyll Island, Georgia (Figure 4A). These hotspots were spatially stable across years, likely reflecting high 286 interannual nest site fidelity among females at that site. Crawford et al. (2014b) found no clear 287 relationship between terrapin road mortality and proximity to the tidal creek or shrub or grass cover 288 above the high marsh; however, they did find a positive relationship between road mortality and high 289 marsh vegetation. Female terrapins nested more frequently along the roads proximate to areas of well- 290 vegetated high marsh. The use of more densely vegetated high marsh during nesting migrations may be 291 related to minimizing exposure to high summer temperatures or predators. Crawford et al. (2014b) also 292 demonstrated that terrapin occurrences on roads are more concentrated in the earlier part of the 293 nesting season and 52% of terrapin road mortality is concentrated within a 3-hr window around the 294 diurnal high tide when females generally prefer to nest (Figure 4B). By integrating information on the 295 spatial and temporal predictability of terrapin activity, there is the potential to development 296 management strategies to target high terrapin vehicle mortality on coastal causeways. 297 298 Recommended location for Figure 4 299 300 Integrated Management of Terrestrial Threats 301 Multiple factors often contribute to wildlife population declines such that management activities that 302 focus on single threats may compromise the ability of any management effort to stabilize or recover 303 declining populations. Ultimately, conservation efforts for declining species like the terrapin should 304 identify, integrate, and find management solutions for multiple terrestrial threats as part of a holistic 305 framework if management is to be successful (Heppell et al. 1996). Evidence from a range of sites 306 indicates that road mortality and nest mortality from subsidized and introduced predators are 307 independently, sufficiently high such that intervening in one threat without addressing the other is 13 308 unlikely to stabilize or recover terrapin populations. Moreover, the issues of roads, predators, and 309 vegetation changes are interrelated such that their management can and should be coordinated. Below 310 we highlight those interconnections as management opportunities. 311 Without question, directly targeting subsidized predatory mammals such as raccoons around 312 important terrapin nesting areas would have a large positive effect on terrapin recruitment and 313 population recovery. Multiple studies across the species’ range show raccoon and other mammal 314 predation in the largest current determinant of terrapin nest survival. Crawford et al. (2014) modeled 315 the joint impacts of road mortality and mammalian nest depredation on terrapin population growth and 316 found that even complete elimination of road mortality would not stabilize or recover the terrapin 317 population without a concurrent reduction in nest predation. Nest predation rates in their model were 318 notably lower than those reported in other studies, indicating that predator management must be a 319 required element of any terrapin management plan. However, we note that mammalian predator 320 control can be a sensitive issue, and we caution that a failure to consider public reaction to mammal 321 control may result in a general lack of support for terrapin conservation. Nonlethal predator controls 322 can be effective for protecting small numbers of known nests, and Mitro (2003) modeled the benefit of 323 protecting a proportion of terrapin nests and found that protecting as few as 5% of nests was sufficient 324 to increase fecundity by 47% and significantly increase the population growth rate. In some cases, 325 nonlethal predator exclusion can be integrated to improve other management actions such as barriers 326 or manmade nesting that function primarily to prevent road mortality (discussed further below). 327 However, predator excluders do not always work (Grosse et al. in review), they can require considerable 328 investments of personnel time, and the effect is lost if nest protection interventions are stopped. In 329 these regards, nest protection may not be an effective long-term solution for population management. 330 Road mortality is the other known major terrestrial threat for which management solutions will 331 be essential to recover terrapin populations, particularly in marshes adjacent to coastal causeways. The 14 332 identification of hot spots and hot moments of movements by terrapins across roads creates 333 opportunities for targeted management actions to address terrapin road mortality. Barriers (e.g., Fig 334 5A) that prevent animals from crossing roads are effective at reducing wildlife-vehicle collisions when 335 placed at previously-observed hot spots (Clevenger et al. 2001, Aresco 2005). For example, researchers 336 at the Wetlands Institute in New Jersey installed short barrier fences in 2004, composed of silt fencing, 337 Tenax mesh material, or corrugated plastic pipes, along 10 km of the Stone Harbor Boulevard and other 338 roads known to be hot spots of terrapin mortality. In areas where barriers were installed, the numbers 339 of terrapins killed on the roads was reduced 80% to 100% (R. Wood, unpublished data). 340 Installing fences along roadsides may reduce terrapin-vehicle collisions, but it can have negative 341 impacts and limitations to consider when including barriers as a management option. Fencing materials 342 and annual maintenance are costly, and therefore may only be efficient at when used strategically at 343 local hot spots of terrapin activity on roads. In this regard, the use of hot spot information could be 344 valuable for conservation management (Crawford et al. 2014b); however, the identification of hot spots 345 can present its own logistical challenges. Generally causeways bisecting marshes are likely to be large 346 hot spots of terrapin mortality; however, determining where hot spots are located along a particular 347 causeway may require multiple years of intensive monitoring. Though Crawford et al. (2014) found that 348 terrapin road mortality hot spots were positively correlated with densely vegetated areas of high marsh, 349 this relationship was not highly predictive. Further, large proportions of roads may lie adjacent to 350 extensive areas of marsh vegetation and thereby limit the utility of this relationship for management 351 purposes. No other factors to predict hot spots have been identified beyond the general understanding 352 of terrapin nesting habitat preferences. This may suggest that hot spots exist in part because of terrapin 353 propensities for nest site fidelity, making them hard to predict . Roosenburg and Place (1994) note that, 354 where it occurs, nest site fidelity can interact with spatially variable nest survival to result in increasing 355 terrapin nest density. While Crawford et al. (2014) found hot spots were stable over a few years, it is not 15 356 yet known whether local hot spots are stable longer periods of time or whether temporally stable hot 357 spots would occur at sites where terrapins do not exhibit nest site fidelity. 358 Even when hot spots occur and are identified, fencing can have secondary negative effects on 359 turtles, and cannot address the more diffuse components of road mortality. Fencing can negatively 360 impact adult turtles by increasing the time they spend searching for suitable nest sites and exposing 361 them to elevated risk of thermal stress or predation (Aresco 2005). Turtles will often nest along barriers, 362 which provides mammalian predators a means to more efficiently find and destroy nests. Fences also 363 serve as barriers to dispersal between habitats that may be important in population dynamics. Finally, 364 50% or more of terrapin-vehicle collisions may be highly diffuse over large areas but sufficient to cause 365 population declines (Crawford et al. 2014b, a). In these cases the scale of materials and labor required to 366 install and maintain fencing may be economically and logistically infeasible. 367 368 Recommended location for Figure 5 369 370 Artificial nest mounds may be a solution to complement the use of barriers to reduce terrapin 371 road mortality and improve nesting success at hot spots. Nest mounds are open, elevated formations 372 with predator-excluder boxes that have been used to attract semi-aquatic turtles to nest inside the 373 boxes and protect eggs (Buhlmann and Osborn 2011). The Georgia Sea Turtle Center is currently testing 374 a hybrid barrier at one hot spot on the Downing-Musgrove Causeway using Tenax fencing that leads to a 375 series of nest boxes spanning 21 m of protected roadside habitat (Figure 5A & B). Grosse et al. (in 376 review) reported high raccoon predation on the Jekyll Island causeway nest mounds despite the 377 presence of a predator exclusion cage, and high nest temperatures that approached conditions that can 378 result in deformities or death of embryos. Nonetheless, surviving nests on nest mounds produced 100% 379 female hatchlings. Adjustments to better exclude predators (e.g., electrified wires) and the use of 16 380 sparse vegetation to stabilize mounds and provide some nest shading are currently being evaluated. 381 While more monitoring is needed to measure the mortality of adults and eggs in nest boxes, terrapins 382 are voluntarily nesting in the boxes and fewer adults have been struck on the road adjacent to the nest 383 box barrier installation (GSTC; unpubl. data). 384 Hot moments of terrapin terrestrial activity and mortality also create opportunities for targeted 385 management actions that can address the more spatially diffuse aspects of terrapin mortality on roads. 386 Studies of terrapins and other turtles have identified broad hot moments (May through July) associated 387 with species’ nesting seasons when frequent overland movements occur (Wood 1997, Szerlag and 388 McRobert 2006, Beaudry et al. 2010, Cureton and Deaton 2012) and in some cases, identified narrower 389 peaks (< 20 days) skewed toward the beginning of terrapin nesting seasons (Burger and Montevecchi 390 1975, Feinberg and Burke 2003, Crawford et al. 2014b). These coarser temporal hot moments allow for 391 management strategies such as the use of seasonal signage or public awareness campaigns to alert 392 drivers to the possibility of terrapin activity on roads. However, acclimation to static signage can limit 393 the effectiveness of alerting motorists to wildlife activity along roads (Sullivan et al. 2004). More 394 localized hot moments permit more dynamic interventions to alter driver behavior. For example, at 395 many sites terrapin nesting is highly correlated with tide amplitude and time to the daytime high tide, 396 and tide schedules are known well in advance. This creates a situation analogous to a school zone and 397 therefore the opportunity for more targeted motorist alerts. In 2012, the Georgia Sea Turtle Center, 398 University of Georgia, and Georgia Department of Transportation installed two flashing warning signs 399 (similar to school zone signage) programmed to the local tide schedule that alert drivers on the 400 Downing-Musgrove Causeway to Jekyll Island, GA during the 3hr windows when terrapins are most likely 401 to be active on the causeway (Fig. 3D). These are the first devices of their kind to target turtles, but their 402 efficacy in reducing road mortality is yet to be determined. 17 403 Ultimately, all matters of predator, vegetation and road management are linked under the 404 broader and increasing problem of declining availability of suitable nesting habitat. There have already 405 been significant losses of natural shore line across the terrapin’s range, and efforts to limit coastal 406 erosion are likely to result in increased area of bulk heading and dredge fill (Roosenburg 1994, Wneck 407 2010, Winters 2013). There is an relatively urgent need for agencies and local stakeholders to identify 408 and protect remaining nesting sites for terrapins. With nesting concentrated into fewer areas, those 409 areas will need active vegetation management to maintain high nest temperatures to maximize nest 410 survival and increase the production of female hatchlings. Vegetation management to prevent the 411 encroachment of shrubs or trees would also complement other measures to reduce nest predation by 412 subsidized mammalian predators. 413 414 Conclusions 415 Like many species with complex life cycles, the conservation of terrapins requires assessing and 416 targeting interventions toward multiple, concurrent threats in both aquatic and terrestrial habitats. 417 Terrapins exhibit a life history typical of most aquatic turtles, which involves relatively little time in 418 terrestrial environments. Nonetheless, the terrestrial phases of terrapin lives present more numerous 419 and influential threats to sustaining populations. Currently nest predation and road mortality are the 420 two largest known, widespread threats to terrapin populations, but these threats are related to lesser 421 appreciated threats to terrapin conservation such as soil modification and degradation, the planting of 422 dense vegetation for erosion control, and the planting or encroachment of shrubs and trees around 423 marshes. The correlated nature of threats can interact to impact terrapin populations, but also creates 424 opportunities for complementary management strategies such as marrying predator control with 425 vegetation management. 18 426 New quantitative approaches to evaluating threats and management options show early 427 potential to improve terrapin conservation. Efforts to identify spatial and temporal patterns of threats 428 such as hot spots and hot moments of terrapin activity on roads can facilitate targeted management to 429 maximize the efficiency of interventions. Models and experiments are improving the effectiveness of 430 management options, and the development of a greater suite of management tools will aide tailoring of 431 management plans to local situations. However, the quality of models and, therefore, their ability to 432 inform at scales relevant to management depend on rigorous data on population demographic rates and 433 per capita effects of various threats. Despite widespread attention and significant research on terrapins, 434 there is little knowledge of geographic or temporal variation of terrapin demographic rates. Such 435 information would enable more precise estimates of local impacts, and our knowledge of juvenile 436 terrapin ecology is insufficient to identify management needs or opportunities for this life stage. Finally, 437 the majority of research to date addresses threats at relatively local scales. There have been insufficient 438 numbers of studies that estimate the impacts of threats at larger scales (e.g., Grosse et al. 2011, Isdell 439 2013). Such information is important for determining whether threats that have conspicuous local 440 effects are of similar importance across larger spatial scales, determining whether the importance of 441 threats vary geographically in relation to changes in species ecology or human activities, and identifying 442 potentially larger scale factors that threaten a species across its range (e.g., agricultural impacts on 443 terrapins; Isdell 2013). 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Pages 21-27 in Proceedings: Conservation, Restoration, and Management of 612 Tortoises and Turtles—An International Conference. New York Turtle and Tortoise Society. 613 Zimmerman, T. D. 1992. Latitudinal Reproductive Variation of the Salt Marsh Turtle, the Diamondback 614 Terrapin (Malaclemys terrapin). University of Charleston, Charleston, South Carolina. 26 615 616 27 617 Table 1. Stage-specific estimates of Diamondback terrapin survival and reproductive rates in the presence and absence of identified threats. 618 Estimate or Stage parameter Nest survival change in estimate State Identified threat Comment Source 0.828 FL none Following raccoon removal Munscher et al. 2012 0.552-0.853 NJ none Open, loamy soils with no dredge materials Wneck 2010 0.626-0.721 NY none Open, grassy habitat, predator exclusion devices used Scholz 2006 0.060-0.700 MD Raccoon predation Artificial nests. Survival varied among beaches and years. Roosenburg and Place 1995 0.078 NY Raccoon predation Feinberg and Burke 2003 0.083-0.161 MD Raccoon predation Roosenburg 1991 0.128 RI Raccoon predation Goodwin 1994 0.135-0.181 FL Raccoon predation 5-18% of nests were lost to storm inundation. Butler et al. 2004 0.156 GA Raccoon predation Simulated nests with chicken eggs; shrub vegetation Grosse et al. in review 28 Hatchling annual survival 0.233 FL Raccoon predation Cessation of raccoon removal Munscher et al. 2012 0.250-0.840 NJ Raccoon predation Reported higher predation, specifically by mammals, in area of higher tree and shrub cover Burger 1977 0.340 NJ Raccoon predation 0.381 GA Raccoon predation Estimate from monitored nests Crawford et al. 2014 0.475-0.491 FL Raccoon predation Estimate from monitored nests only Munscher et al. 2012 0.548 GA Raccoon predation Simulated nests with chicken eggs; open grassy vegetation Grosse et al. in review 0.674 NY Raccoon predation An additional 14.7% of eggs in surviving nests failed to hatch. Ner 2003 0.000 – 0.594 NJ Dredge soils Egg fail to develop in fresh dredge soils. Attributed to high salt concentrations in dredge soils. Survival increases one year post dredge. Wneck 2010 0.111-0.634 NJ Shade Shaded, loamy soils with no dredge materials Wneck 2010 0.253 GA none Estimated from population model with other known demographic rates. Crawford et al. 2014 Burger 1976 29 Juvenile annual survival Adult annual female survival Mean clutch size Estimated from population model with other known demographic rates. Included hatchling year in juvenile survival estimate. 0.446-0.565 RI Mitro 2003 0.952 RI 0.908 MD -0.099 to -0.448 MD Bycatch Roosenburg and Kendall, pers. comm.; Roosenburg et al. 1997 -0.060 to -0.110 SC Bycatch Hoyle and Gibbons 2000 -0.099 to -0.448 MD Bycatch -0.088 NJ Road mortality Szerlag and McRobert 2006 -0.044 to -0.164 GA Road mortality Crawford et al. 2014 16 RI 13 MD Mitro 2003 Roosenburg and Kendall, pers. comm. Goodwin 1994 Roosenburg 1991 30 Mean clutch frequency per year 12-13 NY Estimated from protected nests. Ner 2003 12 MA Zimmerman 1992 11 NY Feinberg and Burke 2003 10 NJ Montevecchi and Burger 1975 7 VA Reid 1955 7 SC Zimmerman 1992 7 FL Seigel 1979, 1980 1-2 RI Godwin 1994 >=2 NY Feinberg and Burke 2003 1-3 MD Roosenburg 1991 619 620 31 621 622 623 Figure 1. (A) Proportion of nesting female terrapins observed as a function of proximity to the daytime high tide for three sites across the Atlantic 624 portion of the species’ range. The figure was based on data reported by Goodwin (1994), Burger and Montevecchi (1975), and Crawford et al. 625 (2014b). (B) Adult female diamondback terrapin nesting in short, patchy vegetation near Jekyll Island, Georgia. The shrub layer in the 626 background marks the high marsh boundary (source: B. A. Crawford). 627 32 628 629 630 Figure 2. Adult female terrapin killed by raccoon while attempted to nest after sunset. The raccoon also dug up and ate the eggs she had 631 deposited. Jekyll Island, Georgia. Source: J. C. Maerz 632 33 633 634 635 636 637 638 639 Figure 3. Adult female terrapins nesting on (A) Great Bay Boulevard causeway near Tuckerton, New Jersey and (B) the Downing-Musgrove Causeway to Jekyll Island, Georgia. In addition to the causeways representing elevated area above and immediately proximate to the marsh, we draw attention to the shrub and tree lines most proximate to the marsh line in contrast to shorter maintained vegetation adjacent to the road edge. Photo sources: (A) G. Sakowicz, (B) B. A. Crawford, and (C) J. C. Maerz. 34 640 641 642 643 644 Figure 4. Spatial and temporal patterns of adult female terrapin activity over two years on the Downing-Musgrove Causeway to Jekyll Island, 645 Georgia. (A) 29.2% of females were observed within the 3 hot spots spanning 803 m (9.2%) of the causeway’s total length, and 51.9% of females 646 were observed within all hot and warm spots spanning 1859 m (21.3%) of the causeway. Note also the three hot spots are in an area where 647 there is extensive unvegetated high marsh (tan shading) but the specific locations of the hot spots are proximate to local points where vegetated 35 648 high marsh (green shading) extends up to the causeway. (B) The probability a terrapin occurs on the causeway in relation to time within the 649 nesting season and proximity to the daytime high tide. Note that within the first third of the nesting season the probability that a terrapin was 650 on the causeway within 1 hour of the daytime high tide was 0.80. This probability declined as the nesting season progressed and with increasing 651 time from the daytime high tide. Sources: (A) is modified from results available in Crawford et al. (2014b). (B) is reproduced from Crawford et al. 652 (2014b). 653 36 654 655 656 37 657 Figure A. Management interventions to address terrestrial threats to diamondback terrapins on the Downing-Musgrove Causeway to Jekyll 658 Island, Georgia. (A) Tynex barrier fence blocking nesting female terrapins from accessing the causeway. Note the barrier directs turtles to a 659 manmade nest mound covered with a predator exclusion box [also pictured in (B)]. (B) Mandmade nest mound with predator exclusion box on 660 the causeway. (C) Flashing sign alerting motorists during periods when the probability of turtles emergin on the road is highest. This sign is 661 programmed using tide calendars for the island and the relationships between nesting season and daytime high tide using described in Crawford 662 et al. (2014b) [see Figure 4B this chapter]. (D) Removal of overgrown wax myrtle and trees along the marsh line to create more optimal nesting 663 habitat proximate to marsh and farthest from the causeway. The vegetation removal reduces nest depredation rates and increases the 664 production of female hatchlings. Photo sources: (A) B. A. Crawford, (B) J. C. Maerz, (C) B. A. Crawford, and (D) Florida Times Union 38