Download Chapter 14: Terrapin Conservation: Mitigating Habitat Loss, Road

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Chapter 14: Terrapin Conservation: Mitigating Habitat Loss, Road Mortality, and Subsidized Predators
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John C. Maerz1, Richard A. Seigel2, and Brian A. Crawford1
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Introduction
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D. B. Warnell School of Forestry and Natural Resources, University of Georgia, Athens, GA 30602.
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Department of Biological Sciences, Towson University, Towson, MD 21252.
The majority of animals have complex life cycles that require periodic migration to
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complementary habitats. As a result, the management of such species can be challenging because it
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requires assessing and targeting interventions toward multiple threats concurrently. In a previous
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chapter in this volume, Chambers and Maerz (in review) address the specific impacts and management
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of terrapin bycatch in commercial and recreational crab pots. While bycatch impacts on terrapin
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populations are well-documented throughout the species range, a suite of terrestrial factors also
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interact to impact terrapin populations such that bycatch management needs to be included as a part of
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a more comprehensive terrestrial-aquatic management strategy (Hart 2005, Crawford et al. 2014a).
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In this chapter, we address the major terrestrial management issues for terrapins, which include
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road mortality during nesting migrations, nest depredation by mesopredators, and vegetation effects on
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nest microclimate and depredation. We first summarize the terrestrial habits of terrapins and their
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importance relative to aquatic life stages. We note that terrapins spend very little time in terrestrial
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environments, yet the terrestrial phases of their lives appear to present more numerous and influential
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threats to population growth. Next we review current knowledge on each major terrestrial threat to
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terrapins, and we discuss interactions between threats and opportunities for complementary
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management options. We stress that failure to account for impacts at all life stages may often render
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management activities targeted at one or a subset of stages ineffective, and we discuss how
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complementary terrestrial management creates flexibility and opportunities for compensatory actions
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when certain threats cannot be fully remediated.
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Terrapin Life Cycles, Demographic Rates, and Terrestrial Habits
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Juvenile and adult terrapins primarily live in aquatic environments, with terrestrial habits limited to brief
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annual migrations of females onto land to nest, and hatchlings dispersing from terrestrial nests to
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aquatic habitats. Terrestrial movements of juvenile and adult male terrapins are believed to be rare, but
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individuals have occasionally been encountered (<2% of observations) during road surveys (Szerlag and
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McRobert 2006, Crawford 2011). Terrapins show similar general nesting behavior throughout the
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species range, though patterns can vary geographically associated with changes in coastal environments
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and movement of the species into more inland brackish environments (Roosenburg 1994). Generally,
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females nest from late spring through mid summer and make multiple nesting migrations within a single
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breeding season often failing to nest during a migration. Diel nesting patterns may vary geographically,
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potentially in relation to predation risk. Several studies show daylight nesting of terrapins concentrated
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around the diurnal high tide (Fig. 1; Burger and Montevecchi 1975, Zimmerman 1992, Goodwin 1994,
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Butler et al. 2006, Szerlag and McRobert 2006, Crawford et al. 2014b). Nesting during the high tide may
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reduce the time and distance female terrapins must travel, and may be related to higher survival among
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nests laid above the high tide line. Daytime nesting also occurs in the late morning through mid
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afternoon in localities where tidal influences are absent (Seigel 1980). However, approximately half of
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females nest at night in Sandy Neck Massachusetts (Auger and Giovannone 1979) and females nest
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primarily at night along the Patuxent River in Maryland (Roosenburg 1994). The terrestrial portions of
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nesting routes are generally short (<50 m), but can be as long as 1600 m in Massachusetts (Auger and
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Giovannone 1979). Females typically nest a few meters above the spring high tide (Burger and
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Montevecchi 1975, Butler et al. 2004) and generally in sandy soils, and females have been reported
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nesting in a variety of vegetation habitats including areas of bare sand, exposed and vegetated dunes,
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short or tall dense grasses, and dense shrubs. Attributes of sandy soils that may be important in nesting
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habitat selection include access, thermal and moisture conditions, soil composition and texture,
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disturbance, and predation risk (Burger and Montevecchi 1975, Goodwin 1994, Roosenburg 1994,
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Feinberg and Burke 2003, Ner 2003, Scholz 2006, Hackney 2010, Grosse et al. in review). Nesting
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duration is generally short (15 – 120 min) with the majority of time allocated to nest site selection
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(Roosenburg 1994). Females will often frequently abandon nesting, often in response to disturbance by
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predators or humans.
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Recommended location for Figure 1
Because terrapin hatching success and sex ratio are dependent on nest incubation temperatures
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and other factors affected by topography and vegetation structure, one expects female terrapins to
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show fidelity to natal nest sites or local, interannual nest site selectivity fidelity. Sheridan (2010) used
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mark-recapture and genetic markers to show natal nest site fidelity among some female terrapins, and
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other studies show nest site fidelity within and among years (Goodwin 1994, Crawford 2011). Crawford
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(2011) reports capturing 50% of nesting female terrapins within 50 m of their capture location the
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previous nesting season, and 80% of females were captured within 200m of their capture location the
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previous nesting season. Roosenburg (1996) used egg size data to infer that females are more selective
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about nest sites when they have larger eggs; however, nest site fidelity and selectivity may vary
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geographically (Roosenburg 1994). Mean incubation time varies with latitude and microhabitat, ranging
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from as short as 66-69 days in central and northern Florida (Seigel 1980, Butler et al. 2004) to 74 days in
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New Jersey and 77 days in New York (Scholz 2006). However, local factors such as the presence of
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vegetation that shades nests can slow development and create greater local variation incubation time
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than is seen over wide latitudes (Goodwin 1994, Wneck 2010).
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Hatchlings may emerge from nests in the late summer, fall or the following spring, when they
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appear to disperse into high marsh environments. Burger (1976) reports that hatchling terrapins in New
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Jersey move quickly into grassy vegetation and downslope, which would be consistent with rapid
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dispersal bias from elevated nesting areas into marsh vegetation. However, Muldoon and Burke (2012)
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report that hatchlings emerging in fall in New York tended to move up in elevation rather than down
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until spring when the behavior reversed. They also report finding hatchlings on land up to nine months
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after emergence from the nest, which may indicate prolonged terrestrial habits by some individuals or in
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some environments. Once in the high marsh, hatchlings appear to avoid open water and tend to stay
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close to vegetation, often burrowing in areas of dense rack (Lovich et al. 1991). Laboratory studies
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suggest that hatchling and juvenile terrapins may also use the high marsh and terrestrial habitats to
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reduce osmotic stress that can inhibit growth (Dunson 1985, Kinneary 2008, Holliday et al. 2009).
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The demographic rates associated with the terrapin life cycle are typical of most turtles
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including other members of the Emydidae (Heppell 1998, Ernst and Lovich 2009). We have provided a
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list of stage-specific estimates of terrapin demographic rates and the associated context from across the
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species range in Table 1. Generally, terrapin life history is characterized by high annual adult survival,
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and potentially low but highly variable egg survival, and slow growth and low survival from hatching to
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adulthood. Females generally mature between 6 and 8 years though some smaller subspecies may
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mature at 4 years, and females lay 1-3 clutches of 5 to 15 eggs per annum. Hatchling sex ratio is
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environmentally determined, and incubation temperature and egg size can have significant positive
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effects on juvenile growth and maturation rates (Roosenburg and Place 1995, Roosenburg and Kelley
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1996). There are few estimates of adult annual survival despite the existence of several multi-year
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population studies across the species range (e.g., Mitro 2003, Dorcas et al. 2007). Mitro (2003)
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estimated adult annual survival between 0.94-0.96, which is consistent with estimates of adult annual
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survival for freshwater emydids (Heppell 1998). There are few direct measures or indirect estimates of
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hatchling or juvenile annual survival [aptly referred to as the missing years]. Mitro (2003) estimated
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juvenile annual survival between 0.446 and 0.565, which is lower than estimates for other emydids
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(Heppell 1998); however, Mitro (2003) did not distinguish hatchling from juvenile survival. As with other
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species, hatchling survival is likely to be lower than juvenile annual survival (Heppell 1998). Draud and
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Zimnavoda (2004) documented 33% mortality of hatchling terrapins over a 29 day period, though this
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resulted from predation by introduced Norway rats. Crawford et al. (2014a) estimated annual hatchling
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survival was ~25%, which is consistent with rates estimated for other emydids (Heppell 1998).
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With such limited data on most terrapin demographic rates, there is little opportunity to
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evaluate geographic variation for most terrapin demographic rates. We do know that terrapin clutch size
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increases significantly with latitude with a small concurrent increase in mean age at maturity from 6 to 8
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years (Table 1). One would expect higher adult or nest survival rates to accompany delayed maturity.
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Nest or egg survival rates to hatching are highly variable among sites and years such that there are no
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clear geographic trends in variation. Rather, variation in nest and egg survival is governed by local
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conditions such as nest and predator abundance and vegetation (Table 1).
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All turtle life stages influence population growth and viability, but population growth is not
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equally sensitive to variation in all demographic rates and all demographic rates are not equally variable
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or amenable to management (de Kroon et al. 2000). Like other turtles (Heppell 1998, Enneson and
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Litzgus 2008), terrapin population growth is most sensitive to variation in adult female survival, followed
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by juvenile and hatchling survival, and finally female fecundity (Mitro 2003, Crawford et al. 2014a).
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Models of terrapin population growth are consistent with other species that indicate 3-5% additive
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reductions in female survival are sufficient to cause population declines (Crawford et al. 2014a). Though
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terrapin population growth is least sensitive to nest or egg survival (Mitro 2003, Crawford et al. 2014a),
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nest or egg survival is naturally and anthropogenically highly variable (Table 1). When one factors in
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that terrapins have temperature dependent sex determination, which creates a potential for sex-specific
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nest or egg survival rates, and the existing knowledge about factors that affect nest survival and sex
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ratios of hatchlings, the nest life stage is more valuable as a management target than is reflected by its
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elasticity.
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Terrestrial Threats to Terrapin Populations
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Though terrapins spend a relatively brief portion of their lives in terrestrial habitats, a suite of terrestrial
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threats can have a disproportionately large effect on terrapin populations. Terrapins are confronted
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with modified access and alterations to nesting habitats, nesting females can experience high mortality
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rates along coastal roads, and subsidized predators can increase both adult and egg mortality. Arguably
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the two largest terrestrial threats, and the two for which there is the greatest amount of research, are
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vehicle strikes on coastal roads and high nest depredation from subsidized mammalian predators.
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However, the variety of terrestrial threats that have been identified to date indicates that threats that
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are localized or have small effects are part of a larger cumulative set of terrestrial threats to terrapin
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populations. In many cases, terrestrial threats are likely spatially correlated and interact across multiple
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life stages with dramatic negative consequences to terrapin populations.
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Alterations to Nesting Habitats – Though not initially identified among the pressing threats to
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sustaining terrapin populations, intensifying coastal land use and associated changes in land cover are
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emerging as an important factor influencing local and regional terrapin abundance. For example, Wneck
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(2010) and Winters (2013) report that 38% of the shoreline of Barnegat Bay, NJ has been altered in
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manners detrimental to terrapin nesting habitat. We know of only one study that has examined the
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effects of terrestrial land use on terrapin populations at a large spatial extent. Isdell et al. (2013) found
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that terrestrial land use, notably agricultural land use, adjacent to marsh habitat was strongly negatively
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correlated with terrapin occupancy within the Chesapeake Bay. How agricultural practices affect
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terrapin populations is unknown, but may be related to effects on nesting habitats through soil
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disturbance and dense planting of vegetation.
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The bulk of our knowledge about anthropogenic impacts on nesting habitats is limited to
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estimates of local effects on terrapin behavior or nest success. Roosenburg (1991) highlighted that
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increasing coastal development results in the loss of intact shoreline and the common practice of
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constructing bulkheads to stabilize shorelines. Bulkheads can block terrapin access to proximate,
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preferred nesting sites, which can increase female nesting migration distances, cause females to nest in
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suboptimal habitats, or concentrate nests into smaller areas (Roosenburg 1994). Winters (2013) used
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telemetry to measure the effects of bulkheading on terrapin nesting in Barnegat Bay, New Jersey. She
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found that bulkheads could increase total travel distance up to 500%. When displacing females
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concentrates nests in areas, this can lead to higher nest predation rates (Roosenburg and Place 1995). In
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addition, manmade structures can shade terrapin nesting areas, resulting in longer development times
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and increased male-biased hatchling sex ratios (Wneck 2010).
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Coastal development practices that alter soils may also be detrimental to terrapin nesting
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(Wneck 2010). Terrapins evolved to nest in sandy soils, which have properties such as large particle
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sizes that improve gas diffusion and lower water potential that can reduce hydric constraints on
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developing embryos (Roosenburg 1994, Wneck 2010). The common practice of dredging of bays to
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clear shipping channels, fill uplands, and construct causeways can negatively impact remaining terrapin
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nesting habitats. In highly developed coastal areas, dredge fill areas and causeways may be the only
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terrapin nesting habitat available (Wood and Herlands 1997, Wneck 2010). Dredge soils contain high
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concentrations of organic solids, fine sediments, and salts that would increase gas exchange and hydric
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constraints on terrapin eggs (Wneck 2010). Wneck (2010) demonstrated that terrapin embryos are
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incapable of developing in fresh dredge soil because the high salt content causes embryos to desiccate.
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After one year, terrapin embryos could develop in aged dredge, but egg survival was still reduced
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relative to natural sandy soils.
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Increasing coastal development also leads to shifts in vegetation that directly affect terrapin
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nesting success and interact with subsidized predators to affect nest survival. Terrapins prefer to nest in
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areas of patchy, short vegetation, where nests develop faster and tend to produce a higher proportion
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of female hatchlings (Burger and Montevecchi 1975, Goodwin 1994, Roosenburg 1994, Feinberg and
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Burke 2003, Ner 2003, Scholz 2006, Hackney 2010, Grosse et al. in review). The dense planting of dune
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grasses to control erosion or dense areas of invasive plants can increase terrapin nest failure
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(Roosenburg 1991, Wneck 2010). Some plant roots will infiltrate and kill terrapin eggs (Lazell and Auger
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1981), and dense grasses can reduce soil moisture potential, resulting in higher egg failure rates. Dense
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herbaceous cover or the succession or deliberate planting of trees and shrubs can also reduce terrapin
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nest survival and skew hatchling sex ratios. Dense vegetation shades nests, resulting in longer
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development times, higher egg mortality, and male biased hatchling sex ratios (Wneck 2010).
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Vegetation cover may also interact with predator abundance to affect terrapin nest success.
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Roosenburg and Place (1995) found that shaded nests in dense grass had higher survival rates but
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produced almost 100% male hatchlings. Burger (1977) reports high mammalian depredation of terrapin
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nests in wooded, shrub and edge habitats, and Hackney (2010) found that terrapin nests in shrub or
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edge habitats closer to marshes had a higher probability of being depredated compared to nests in open
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sandy areas farther from the marsh. Grosse et al. (in review) demonstrated experimentally that shaded
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nests in shrub habitats had lower survival rates as a result of higher depredation by raccoons, and
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surviving nests in shaded shrub habitats produced 100% male hatchlings. In contrast, open, grassy
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habitats had the highest nest survival rates and produced 100% female hatchlings (Grosse et al. in
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review). Collectively, these studies show that altered terrestrial vegetation can influence nest survival
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and hatchling sex ratios, and that increasing shrub or tree cover may interact with increases in
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subsidized mammalian predators to increase nest mortality.
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Subsidized Terrestrial Predators –Mortality of terrapins on land, particularly nest and hatchling
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mortality, is clearly related to subsidized predator abundance. Known terrestrial predators of adult
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terrapins are raccoons and foxes, while terrestrial nest and hatchling predators include ghost crabs,
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grackles, crows, foxes, raccoons, armadillos, introduced Norwegian rats and red imported fire ants.
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Many studies report anecdotal predation on adult female terrapins by raccoons, but detailed reports of
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such occurrences are uncommon (Figure 2). Seigel (1980) and Feinberg and Burke (2003) documented a
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relatively high number of adult female terrapins killed by raccoons over two year periods in Florida and
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New York respectively, which indicates that adult mortality could be high during nesting migrations in
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areas where human activities subsidize predators. Burger and Montevecchi (1975) and Roosenburg
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(1994) suggest that high mammalian predation risk may be a selective pressure promoting diurnal
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nesting habits by female terrapins.
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The available literature also indicates that terrapin nest and juvenile survival rates can be high in
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areas with few predators, but can be extremely low in areas of high natural or introduced predator
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density (Table 1). Numerous studies show raccoon predation is the biggest determinant of terrapin nest
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success, and in many studies of sites with high raccoon densities throughout the species’ range,
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raccoon’s routinely depredate as much as 95% of nests (Feinberg and Burke 2003, Butler et al. 2006).
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Several studies note that mammalian depredation of nests generally occurs within 48 hours of nesting
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(Burger 1977, Roosenburg 1991, Goodwin 1994, Munscher et al. 2012, Crawford et al. 2014a), and as
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mentioned previously, nests in shrubby or wooded habitats may be more vulnerable to mammalian
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predators . Several studies also document that predators are significant sources of mortality for
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hatchlings in the nest and after emergence (Feinberg and Burke 2003, Butler et al. 2006). A study in
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Oyster Bay Harbor, New York documented that introduced rats depredated 67% of terrapin hatchlings
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within 30 days of emerging from nests (Draud and Zimnavoda 2004).
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Roads - Roads have become a pervasive fixture on most landscapes with conservation
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implications for many species. In the Eastern and Gulf Coasts of the United States respectively, 60 to
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80% of areas are within 400 m of a road (Riitters et al. 2003) and are experiencing the fastest annual
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increases in traffic density (Baird 2009). In the case of terrapins and other turtle species, models predict
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road mortality to cause substantial declines of turtle populations on a regional scale (Fahrig et al. 1995,
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Gibbs and Shriver 2002, Andrews et al. 2008, Litvaitis and Tash 2008, Langen et al. 2009, Beaudry et al.
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2010).
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Roads can affect terrapin populations through the permanent loss of habitat, increased
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mortality from vehicle strikes, and by creating a barrier to movement that restricts movements of
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individuals between terrestrial and aquatic habitats (for reviews of road impacts on various taxa see
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Forman and Alexander 1998, Trombulak and Frissell 2000, Andrews et al. 2008, Fahrig and Rytwinski
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2009). In general, turtles use complex habitat networks for migrating, mate-searching, nesting, and
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hibernating that often bring them across roadways (Gibbs and Shriver 2002, Aresco 2005, Brennessel
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2006, Beaudry et al. 2008, Langen et al. 2009). Road mortality is particularly high among terrapins
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because they are slow moving, do not avoid roads, and cannot flee from oncoming cars (Gibbs and
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Shriver 2002, van Langevelde and Jaarsma 2004, Fahrig and Rytwinski 2009). Moreover, because turtle
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road mortality is generally related to movements for breeding and nesting (Wood and Herlands 1997,
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Gibbs and Shriver 2002, Beaudry et al. 2010), it disproportionately affects mature females (Steen et al.
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2006, Grosse et al. 2011, Crawford et al. 2014a). Among studies that have monitored terrapin activity
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on roads, > 98% of individuals impacted were adult females (Wood and Herlands 1997, Hoden and Able
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2003, Szerlag and McRobert 2006, Crawford et al. 2014b). Since turtle populations are strongly governed
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by high adult female survival, even minor additive road mortality can lead to rapid population decline.
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Despite documentation of high numbers of terrapins killed on roads throughout the species
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range, there are relatively few studies that evaluated the local or regional impacts of roads on terrapins
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or factors that cause terrapin mortality on roads to vary. At the regional scale, Grosse et al. (2011)
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conducted a statewide assessment of the relationship between commercial crabbing and roads on
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terrapin abundance in Georgia, and found that proximity to roads did not correlate with terrapin
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abundance or sex ratio statewide. However, they did find that terrapin abundance was notably low on
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causeways that bisect marshes to barrier islands. Wood and Herlands (1997) reported high numbers of
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terrapins killed on roads annually along causeways that bisect marshes en route to densely populated
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beaches in New Jersey. Crawford et al. (2014a) directly estimated adult female terrapin mortality on the
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9-km Downing-Musgrove Causeway to Jekyll Island, Georgia and found that mean annual adult female
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mortality from vehicle collisions during nesting migrations was 11%, and ranged annually over a three
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year period between 4.4% and 16.4%. They estimated that even the lowest annual additive mortality of
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4.4% from vehicle collisions was sufficient to cause the terrapin population to decline, and consistent
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with the high rate of female mortality, they estimated that terrapin populations in the creeks adjacent
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to the causeway had greater than a 4:1 male biased sex ratio. Similarly, Avissar (2006) reported that the
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sex ratio of the terrapin population along the Garden State Parkway in New Jersey, where terrapin road
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mortality is frequent, has increased from 0.61 to 5.7 between 1989 and 2003, and mean terrapin
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carapace length declined over the same 14 year time period consistent with a loss of older adult
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females.
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Recommended location for Figure 3
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Causeways constructed through marshes create a significant “ecological trap” for females
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terrapins (Schlaepfer et al. 2002). With increasing coastal development, elevated causeways through
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the marsh become the only available nesting habitat for terrapins. Female terrapins are naturally
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attracted to nest in open, elevated habitat in proximity to the marsh (Szerlag and McRobert 2006), and
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it is often the case that portions of the causeway most proximate to the road are mowed to maintain
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short vegetation (Figure 3), while areas more proximate to the marsh may be planted or overgrown with
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shrubs. This makes the most attractive parts of causeways for nesting those that are immediately
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adjacent to the road (Wood and Herlands 1997, Crawford et al. 2014b). Traffic volumes on coastal roads
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peak between May and August (Baird 2009), which overlaps with the terrapin nesting season
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throughout the range of the species (Seigel 1980, Zimmerman 1992, Wood and Herlands 1997, Feinberg
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and Burke 2003, Crawford et al. 2014b), and because female terrapins often nest proximate to the
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diurnal high tide, they are likely to be active on roads during the day when traffic volume is highest. It is
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under these conditions that we observe the highest numbers of terrapin-vehicle collisions. For example,
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in New Jersey, Hoden and Able (2003) documented 450 terrapins killed on 8 km of Great Bay Boulevard
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near Tuckerton between 1999 and 2002, and Wood and Herlands (1997) documented 4,020 terrapins
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killed on 28 km causeways to the Cape May Peninsula between 1989 and 1995. Between 2009 and
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2013, Crawford et al. (2014b) documented 757 female terrapins killed along 9 km of the Downing-
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Musgrove Causeway to Jekyll Island, Georgia.
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At finer spatial scales, terrapin mortality along a road can be spatially and temporally diffuse or
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clustered. Areas of concentrated activity or mortality on roads are known as threat hot spots, and
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periods of concentrated activity are known as threat hot moments (Beaudry et al. 2008, Beaudry et al.
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2010). Crawford et al. (2014b) found that 30% of terrapins road mortalities occurred over a 2-year
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period were distributed among three hot spots representing only 0.8 km (9%) of the 9-km causeway to
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Jekyll Island, Georgia (Figure 4A). These hotspots were spatially stable across years, likely reflecting high
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interannual nest site fidelity among females at that site. Crawford et al. (2014b) found no clear
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relationship between terrapin road mortality and proximity to the tidal creek or shrub or grass cover
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above the high marsh; however, they did find a positive relationship between road mortality and high
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marsh vegetation. Female terrapins nested more frequently along the roads proximate to areas of well-
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vegetated high marsh. The use of more densely vegetated high marsh during nesting migrations may be
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related to minimizing exposure to high summer temperatures or predators. Crawford et al. (2014b) also
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demonstrated that terrapin occurrences on roads are more concentrated in the earlier part of the
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nesting season and 52% of terrapin road mortality is concentrated within a 3-hr window around the
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diurnal high tide when females generally prefer to nest (Figure 4B). By integrating information on the
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spatial and temporal predictability of terrapin activity, there is the potential to development
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management strategies to target high terrapin vehicle mortality on coastal causeways.
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Integrated Management of Terrestrial Threats
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Multiple factors often contribute to wildlife population declines such that management activities that
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focus on single threats may compromise the ability of any management effort to stabilize or recover
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declining populations. Ultimately, conservation efforts for declining species like the terrapin should
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identify, integrate, and find management solutions for multiple terrestrial threats as part of a holistic
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framework if management is to be successful (Heppell et al. 1996). Evidence from a range of sites
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indicates that road mortality and nest mortality from subsidized and introduced predators are
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independently, sufficiently high such that intervening in one threat without addressing the other is
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unlikely to stabilize or recover terrapin populations. Moreover, the issues of roads, predators, and
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vegetation changes are interrelated such that their management can and should be coordinated. Below
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we highlight those interconnections as management opportunities.
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Without question, directly targeting subsidized predatory mammals such as raccoons around
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important terrapin nesting areas would have a large positive effect on terrapin recruitment and
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population recovery. Multiple studies across the species’ range show raccoon and other mammal
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predation in the largest current determinant of terrapin nest survival. Crawford et al. (2014) modeled
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the joint impacts of road mortality and mammalian nest depredation on terrapin population growth and
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found that even complete elimination of road mortality would not stabilize or recover the terrapin
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population without a concurrent reduction in nest predation. Nest predation rates in their model were
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notably lower than those reported in other studies, indicating that predator management must be a
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required element of any terrapin management plan. However, we note that mammalian predator
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control can be a sensitive issue, and we caution that a failure to consider public reaction to mammal
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control may result in a general lack of support for terrapin conservation. Nonlethal predator controls
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can be effective for protecting small numbers of known nests, and Mitro (2003) modeled the benefit of
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protecting a proportion of terrapin nests and found that protecting as few as 5% of nests was sufficient
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to increase fecundity by 47% and significantly increase the population growth rate. In some cases,
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nonlethal predator exclusion can be integrated to improve other management actions such as barriers
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or manmade nesting that function primarily to prevent road mortality (discussed further below).
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However, predator excluders do not always work (Grosse et al. in review), they can require considerable
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investments of personnel time, and the effect is lost if nest protection interventions are stopped. In
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these regards, nest protection may not be an effective long-term solution for population management.
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Road mortality is the other known major terrestrial threat for which management solutions will
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be essential to recover terrapin populations, particularly in marshes adjacent to coastal causeways. The
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identification of hot spots and hot moments of movements by terrapins across roads creates
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opportunities for targeted management actions to address terrapin road mortality. Barriers (e.g., Fig
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5A) that prevent animals from crossing roads are effective at reducing wildlife-vehicle collisions when
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placed at previously-observed hot spots (Clevenger et al. 2001, Aresco 2005). For example, researchers
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at the Wetlands Institute in New Jersey installed short barrier fences in 2004, composed of silt fencing,
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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). Studies examining the regional impacts of threats are also important in
444
identifying the role of state and federal agencies and regulations in terrapin management as opposed to
445
threats that may require more localized attention.
446
447
Literature Cited
448
19
449
450
451
452
453
454
455
456
457
458
459
460
461
462
463
464
465
466
467
468
469
470
471
472
Andrews, K. M., J. W. Gibbons, D. M. Jochimsen, J. Mitchell, and R. Jung Brown. 2008. Ecological effects
of roads on amphibians and reptiles: a literature review. Herpetological Conservation 3:121-143.
Aresco, M. J. 2005. Mitigation measures to reduce highway mortality of turtles and other herpetofauna
at a north Florida lake. Journal of Wildlife Management 69:549-560.
Auger, P. J., and P. Giovannone. 1979. On the fringe of existence: Diamondback terrapins and Sandy
Neck. Cape. The Cape Naturalist 8:44-58.
Avissar, N. G. 2006. Changes in population structure of diamondback terrapins (Malaclemys terrapin
terrapin) in a previously surveyed creek in southern New Jersey. Journal Information 5.
Baird, R. C. 2009. Coastal urbanization: the challenge of management lag. Management of
Environmental Quality: An International Journal 20:371-382.
Beaudry, F., P. G. deMaynadier, and M. L. Hunter, Jr. 2008. Identifying road mortality threat at multiple
spatial scales for semi-aquatic turtles. Biological Conservation 141:2550-2563.
Beaudry, F., P. G. deMaynadier, and M. L. Hunter, Jr. 2010. Identifying hot moments in road-mortality
risk for freshwater turtles. Journal of Wildlife Management 74:152-159.
Brennessel, B. 2006. Diamonds in the Marsh: A Natural History of the Diamondback Terrapin. University
Press of New England, Hanover and London.
Buhlmann, K. A., and C. P. Osborn. 2011. Use of an artificial nesting mound by wood turtles (Glyptemys
insculpta): a tool for turtle conservation. Northeastern Naturalist 18:315-334.
Burger, J. 1976. Behavior of hatchling diamondback terrapins (Malaclemys terrapin) in the field. Copeia
1976:742-748.
Burger, J. 1977. Determinants of hatching success in diamondback terrapin, Malaclemys terrapin. The
American Midland Naturalist 97:444-464.
Burger, J., and W. A. Montevecchi. 1975. Nest site selection in the terrapin Malaclemys terrapin. Copeia
1975:113-119.
20
473
Butler, J. A., C. Broadhurst, M. Green, and Z. Mullin. 2004. Nesting, nest predation and hatchling
474
emergence of the Carolina diamondback terrapin, Malaclemys terrapin centrata, in
475
northwestern Florida. The American Midland Naturalist 152:145-155.
476
477
478
Butler, J. A., R. A. Seigel, and B. K. Mealey. 2006. Malaclemys terrapin - Diamondback terrapin. Pages
279-295 in P. A. Meylan, editor. Biology and Conservation of Florica Turtles.
Chambers, R. M., and J. C. Maerz. in review. Terrapin bycatch in the blue crab fishery.in W. Roosenburg
479
and V. S. Kennedy, editors. Ecology and Conservation of the Diamondback Terrapin. Johns
480
Hopkins University Press, Baltimore, MD.
481
482
483
Clevenger, A. P., B. Chruszcz, and K. E. Gunson. 2001. Highway mitigation fencing reduces wildlifevehicle collisions. Wildlife Society Bulletin 29:646-653.
Crawford, B. A. 2011. Mortality and management: Assessing diamondback terrapins (Malaclemys
484
terrapin) on the Jekyll Island Causeway. Masters Thesis. University of Georgia, Athens.
485
Crawford, B. A., J. C. Maerz, N. P. Nibbelink, K. A. Buhlmann, and T. M. Norton. 2014a. Estimating the
486
consequences of multiple threats and management strategies for semi-aquatic turtles. Journal
487
of Animal Ecology provisionally accepted.
488
489
490
491
492
493
494
Crawford, B. A., J. C. Maerz, N. P. Nibbelink, K. A. Buhlmann, and T. M. Norton. 2014b. Hot spots and hot
moments of diamondback terrapin road-crossing activity. Journal of Animal Ecology accepted.
Cureton, J. C., and R. Deaton. 2012. Hot moments and hot spots: identifying factors explaining temporal
and spatial variation in turtle road mortality. Journal of Wildlife Management 76:1047-1052.
de Kroon, H., J. van Groenendael, and J. Ehrle'n. 2000. Elasticities: A review of methods and model
limitations. Ecology 81:607-617.
Dorcas, M. E., J. D. Wilson, and J. W. Gibbons. 2007. Crab trapping causes population decline and
495
demographic changes in diamondback terrapin over two decades. Biological Conservation
496
137:334-340.
21
497
Draud, M., and S. Zimnavoda. 2004. Predation on hatchling and juvenile diamondback terrapins
498
(Malaclemys terrapin) by the Norway rat (Rattus norvegicus). Journal of Herpetology 38:467-
499
470.
500
Dunson, W. A. 1985. Effect of water salinity and food salt content on growth and sodium efflux of
501
hatchling diamondback terrapins (Malaclemys). Physiological Zoology 58:736-747.
502
Enneson, J. J., and J. D. Litzgus. 2008. Using long-term data and a stage-classified matrix to assess
503
conservation strategies for an endangered turtle (Clemmys guttata). Biological Conservation
504
141:1560-1568.
505
506
507
508
509
510
511
Ernst, C. H., and J. E. Lovich. 2009. Turtles of the United States and Canada. 2nd edition. The Johns
Hopkins University Press, Baltimore, Maryland.
Fahrig, L., J. H. Pedlar, S. E. Pope, P. D. Taylor, and J. F. Wegner. 1995. Effect of road traffic on amphibian
density. Biological Conservation 73:177-182.
Fahrig, L., and T. Rytwinski. 2009. Effects of roads on animal abundance: an empirical review and
synthesis. Ecology and Society 14:21.
Feinberg, J. A., and R. L. Burke. 2003. Nesting ecology and predation of diamondback terrapins,
512
Malaclemys terrapin, at Gateway National Recreation Area, New York. Journal of Herpetology
513
37:517-526.
514
515
516
517
518
519
Forman, R. T. T., and L. E. Alexander. 1998. Roads and their major ecological effects. Annual Review of
Ecology and Systematics 29:207-231.
Gibbs, J. P., and W. G. Shriver. 2002. Estimating the effects of road mortality on turtle populations.
Conservation Biology 16:1647-1652.
Goodwin, C. C. 1994. Aspects of Nesting Ecology of the Diamondback Terrapin (Malaclemys terrapin) in
Rhode Island. Masters. University of Rhode Island.
22
520
Grosse, A. M., K. A. Buhlmann, J. C. Maerz, B. A. Crawford, T. M. Norton, M. Kaylor, S. Diltz, S. Nelson, A.
521
Hupp, R. Thomas, and T. D. Tuberville. in review. Effects of vegetation and artifical habitat
522
management on the nesting success and sex ratios of Carolina diamondback terrapins
523
(Malaclemys terrapin). Herpetological Conservation and Biology.
524
Grosse, A. M., J. C. Maerz, J. Hepinstall-Cymerman, and M. E. Dorcas. 2011. Effects of roads and crabbing
525
pressures on diamondback terrapin populations in coastal Georgia. The Journal of Wildlife
526
Management 75:762-770.
527
528
529
Hackney, A. D. 2010. Conservation Biology of the Diamondback Terrapin in North America: Policy Status,
Nest Predation, and Managing Island Populations. Masters. Clemson University.
Hart, K. M. 2005. Population Biology of Diamondback Terrapins (Malaclemys terrapin): Defining and
530
Reducing Threats Across their Geographic Range. Ph.D. Dissertation. Duke University, Durham,
531
NC.
532
533
534
535
536
Heppell, S. S. 1998. Application of life-history theory and population model analysis to turtle
conservation. Copeia 1998:367-375.
Heppell, S. S., L. B. Crowder, and D. T. Crouse. 1996. Models to evaluate headstarting as a management
tool for long-lived turtles. Ecological Applications 6:556-565.
Hoden, R., and K. Able. 2003. Habitat use and road mortality of diamondback terrapins (Malaclemys
537
terrapin) in the Jacques Cousteau National Estuarine Research Reserve at Mullica River - Greay
538
Bay in southern New Jersey.
539
540
541
542
Holliday, D. K., A. A. Elskus, and W. Roosenburg. 2009. Impacts of multiple stressors on growth and
metabolic rate of Malaclemys terrapin. Environmental Toxicology and Chemistry 28:338-345.
Isdell, R. 2013. Geospatial analysis of anthropogenic impacts on diamondback terrapins in the lower
Chesapeake Bay. Masters thesis. The College of William and Mary.
23
543
Kinneary, J. J. 2008. Observations on terrestrial feeding behavior and growth in diamondback terrapin
544
(Malaclemys) and snapping turtle (Chelydra) hatchlings. Chelonian Conservation and Biology
545
7:118-119.
546
Langen, T. A., K. M. Ogden, and L. L. Schwarting. 2009. Predicting hot spots of herpetofauna road
547
mortality along highway networks. Journal of Wildlife Management 73:104-114.
548
549
550
551
Lazell, J. D. J., and P. J. Auger. 1981. Predation on diamondback terrapin (Malaclemys terrapin) eggs by
dunegrass (Ammophila breviligiulata). Copeia 1981:723-724.
Litvaitis, J. A., and J. P. Tash. 2008. An approach toward understanding wildlife-vehicle collisions.
Environmental Management 42:688-697.
552
Lovich, J. E., A. D. Tucker, D. E. Kling, J. W. Gibbons, and T. D. Zimmerman. 1991. Behavior of hatchling
553
diamondback terrapins (Malaclemys terrapin) released in a South Carolina salt marsh.
554
Herpetological Review 22:81-83.
555
556
Mitro, M. G. 2003. Demography and viability analyses of a diamondback terrapin population. Canadian
Journal of Zoology 81:716-726.
557
Muldoon, K. A., and R. L. Burke. 2012. Movements, overwintering, and mortality of hatchling Diamond-
558
backed Terrapins (Malaclemys terrapin) at Jamaica Bay, New York. Canadian Journal of Zoology
559
90:651-662.
560
Munscher, E. C., E. H. Kuhns, C. A. Cox, and J. A. Butler. 2012. Decreased nest mortality for the Carolina
561
diamondback terrapin (Malaclemys terrapin centrata) following removal of racoons (Procyon
562
lotor) from a nesting beach in northeastern Florida. Herpetological Conservation and Biology
563
7:176-184.
564
Ner, S. E. 2003. Distribution and Predation of Diamondback Terrapin Nests at Six Upland Islands of
565
Jamaica Bay Unit and Sandy Hook Unit, Gateway National Recreation Area. Masters. Hofstra
566
University.
24
567
568
569
Riitters, K. H., J. D. Wickham, R. V. O'Neill, K. B. Jones, E. R. Smith, J. W. Coulston, T. G. Wade, and J. H.
Smith. 2003. Fragmentation of continental United States forests. Ecosystems 5:815-822.
Roosenburg, W. 1991. The diamondback terrapin: Population dynamics, habitat requirements, and
570
opportunities for conservation. Pages 227-234 in New Perspectives in the Chesapeake System: A
571
Research and Management Partnership. Chesapeake Research Consortium, Baltimore,
572
Maryland.
573
574
575
576
577
Roosenburg, W. M. 1994. Nesting habitat requirements of the diamondback terrapin: A geographic
comparison. Wetland Journal 6:8-11.
Roosenburg, W. M., and K. C. Kelley. 1996. The effect of egg size and incubation temperature on growth
in the turtle, Malaclemys terrapin. Journal of Herpetology 30:198-204.
Roosenburg, W. M., and A. R. Place. 1995. Nest predation and hatchling sex ratio in the diamondback
578
terrapin: implications for management and conservation. Pages 65-70 in Toward a Sustainable
579
Coastal Watershed: The Chesapeake Bay Experiment. Chesapeake Research Consortium,
580
Norfolk, VA.
581
582
583
584
585
586
587
588
589
590
Roosenburg, W. W. 1996. Maternal condition and nest site choice: An alternative for the maintenance of
environmental sex determination. American Zoologist 36:157-168.
Schlaepfer, M. A., M. C. Runge, and P. W. Sherman. 2002. Ecological and evolutionary traps. Trends in
Ecology and Evolution 17:474-480.
Scholz, A. L. 2006. Impacts of Nest Site Choice and Nest Characteristics on Hatchling Success in the
Diamondback Terrapins of Jamaica Bay, New York. Masters. Hofstra University, Hempstead, NY.
Seigel, R. A. 1980. Nesting habits of diamondback terrapins (Malaclemys terrapin) on the Atlantic coast
of Florida. Transactions of the Kansas Academy of Sciences 83:239-246.
Sheridan, C. M. 2010. Mating System and Dispersal Patterns in the Diamondback Terrapin (Malaclemys
terrapin). Drexel University, Philadelphia, Pennsylvania.
25
591
Steen, D. A., M. J. Aresco, S. G. Beilke, B. W. Compton, E. P. Congdon, C. K. Dodd, Jr., H. Forrester, J. W.
592
Gibbons, J. L. Greene, T. A. Langen, M. J. Oldham, D. N. Oxier, R. A. Saumure, F. W. Schueler, J.
593
M. Sleeman, L. L. Smith, J. K. Tucker, and J. P. Gibbs. 2006. Relative vulnerability of female
594
turtles to road mortality. Animal Conservation 9:269-273.
595
596
597
598
599
600
601
602
603
604
605
Szerlag, S., and S. P. McRobert. 2006. Road occurrence and mortalithy of the northern diamondback
terrapin. Applied Herpetology 3:27-37.
Trombulak, S. C., and C. A. Frissell. 2000. Review of ecological effects of roads on terrestrial and aquatic
communities. Conservation Biology 14:18-30.
van Langevelde, F., and C. F. Jaarsma. 2004. Using traffic flow theory to model traffic mortality in
mammals. Landscape Ecology 19:898-907.
Winters, J. 2013. The effects of bulkheading on diamondback terrapin nesting in Barnegat Bay, NJ.
Doctoral dissertation. Drexel University, Philadelphia, Pennsylvania.
Wneck, J. P. 2010. Anthropogenic Impacts on the Reproductive Ecology of the Diamondback Terrapin,
Malaclemys terrapin. Doctoral disseration. Drexel University, Philadelphia, Pennsylvania.
Wood, R., and R. Herlands. 1997. Turtles and tires: the impact of roadkills on northern diamondback
606
terrapin, Malaclemys terrapin terrapin, populations on the Cape May Peninsula, southern New
607
Jersey, USA. Pages 46-53 in J. Van Abbema, editor. Conservation, Restoration, and Management
608
of Tortoises and Turtles - An International Conference. New York Turtle and Tortoise Society,
609
New York.
610
Wood, R. C. 1997. The impact of commerical crab traps on northern diamondback terrapins, Malaclemys
611
terrapin terrapin. 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