Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 572 2014 SOUTHEASTERN NATURALIST 13(3):572–586 Dispersal Behavior of Diamond-backed Terrapin Post-hatchlings Andrew T. Coleman1,4,*, Thane Wibbels1, Ken Marion1, Taylor Roberge1, David Nelson2, and John Dindo3 Abstract - Post-emergence dispersal behavior of hatchling turtles has been investigated in several species, and a variety of species-specific orientation patterns have been reported. In the current study, we examined the orientation and dispersal behavior of hatchling, post-hatchling, and yearling Malaclemys terrapin pileata (Mississippi Diamond-backed Terrapin) by utilizing an orientation arena on two natural nesting beaches. Each age group displayed strong orientation and dispersal towards high-marsh vegetation instead of open water. The results suggest an innate behavior in young Diamond-backed Terrapins in which they orient from open beach areas toward vegetated marsh areas. The results also stress the importance of having healthy marsh habitat adjacent to nesting areas to provide critical habitat for these vulnerable life-history stages of Diamond-backed Terrapins. Introduction Orientation behavior of hatchlings has been investigated in several turtle species, most notably in sea turtles. Salmon et al. (1992, 1995) and Lohmann et al. (1997) reviewed previous research on this topic and summarized that sea turtle hatchlings primarily utilize visual cues to guide them from the nest to the open water. Hatchlings collect these cues within their “cone of acceptance”, which is a visual field with a wide horizontal angle and a narrow vertical angle. They display orientation to the brightest direction, and due to the narrow vertical angle within their “cone of acceptance”, the light closest to the horizon, which is usually moonlight reflecting on the water, has the greatest influence. Additionally, hatchling sea turtles tend to orient away from high silhouettes on the horizon, such as dunes or vegetation bordering the beach (Lohmann et al. 1997, Salmon et al. 1992). Unfortunately, artificial lighting that is located near the nesting beach can be brighter than natural light, thus resulting in hatchlings orienting away from open water and travelling inland (Salmon et al. 1995). More recent research has shown that olfactory (Fuentes-Farias et al. 2011) and magnetic cues (Fuentes-Farias et al. 2011, Stapput and Wiltschko 2005) in addition to visual cues are used by sea turtle hatchlings in their movements to the water after emergence. Orientation behavior of freshwater turtle hatchlings has been examined in a variety of studies, but the results do not reveal a succinct pattern as with sea turtle species. Anderson (1958) observed hatchlings of Apalone mutica Lesueur (Smooth 1Department of Biology, University of Alabama at Birmingham, Birmingham, AL 35294. 2Department of Biology, University of South Alabama, Mobile, AL 36688. 3Dauphin Island Sea Lab, Dauphin Island, AL 36528. 4Current address - Institute for Marine Mammal Studies, Gulfport, MS 39503. *Corresponding author - acoleman@imms.org. Manuscript Editor: John Placyk Southeastern Naturalist 573 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 Softshell), Graptemys oculifera Baur (Ringed Map Turtle), and Graptemys pulchra Baur (Alabama Map Turtle) display negative orientation to tall, dark forms, a strategy similar to sea turtles. But although it was noted that hatchlings of these species venture from their nests to the water after sunset, they do not utilize light reflected off the water in their dispersal (Anderson 1958). Standing et al. (1997) and McNeil et al. (2000) found that Emydoidea blandingii Holbrook (Blanding’s Turtle) hatchlings from a population in Nova Scotia do not seek water after emergence despite the seemingly strong selective pressures favoring entering the water. Visual cues appear to be utilized by hatchlings even though silhouettes of nearby vegetation along with slope and open horizon are not important cues (Standing et al. 1997). The hatchlings’ movements showed some evidence of “cover seeking” behavior (McNeil et al. 2000), and their movements were more direct under vegetative cover (Standing et al. 1997). However, some hatchlings exhibited a diverse array of orientation behaviors after emergence, which was proposed as an adaptive “bet-hedging” strategy in which different responses to various environmental stimuli in a dynamic habitat presumably better ensure higher overall survival rates for the population (McNeil et al. 2000, Standing et al. 1997). Tuttle and Carroll (2005) observed similar scattered dispersal in Glyptemys insculpta LeConte (Wood Turtle) hatchlings, and they suggested that in addition to visual cues, olfactory and auditory cues along with positive geotaxis appear to influence hatchling orientation. Pappas et al. (2009) studied a population of Blanding’s Turtles that nest a long distance from their resident wetlands. The authors observed similar orientation behavior to that of Standing et al. (1997) and McNeil et al. (2000), with the majority of Blanding’s hatchlings dispersing towards dark horizons, which correlate with riparian habitats. However, they doubted the “bet-hedging” strategy because the hatchlings migrating away from wetlands would most likely not be able to overcome the increased risks of predation or desiccation. They noted that Blanding’s hatchlings that initially oriented away from dark horizons modified their direction when new environmental cues arose (Pappas et al. 2009). In contrast to hatchling Blanding’s turtles, hatchlings of Chelydra serpentina L. (Snapping Turtle) and Chrysemys picta belli Gray (Western Painted Turtle) orient to open areas, mostly near open horizons (Congdon et al. 2011). The authors postulated that females of these species nest in close proximity to wetlands to reduce the number of open horizons available to emerging hatchlings. This strategy could help ensure that the nearest open horizon is associated with a neighboring wetland. Furthermore, Congdon et al. (2011) argued that a common reproductive ecology scenario for nesting freshwater turtle species is to nest close to water with hatchling orientation toward nearby open horizons. Several studies have investigated various factors that could affect survival probabilities of freshwater turtle hatchlings upon emergence from nests. These factors include body size (Janzen et al. 2000, Tucker 2000), nest-site characteristics (Kolbe and Janzen 2001), water loss (Kolbe and Janzen 2002), and exposure to predation (Janzen et al. 2007). Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 574 We examined the orientation behavior of Malaclemys terrapin pileata Wied- Neuwied (Mississippi Diamond-backed Terrapin; hereafter Terrapin) hatchlings, post-hatchlings, and yearlings on two natural nesting beaches. Terrapins exclusively inhabit brackish water environments of salt marshes, bays, and estuaries along the Atlantic and Gulf of Mexico coasts (Carr 1952). Although the ecology of adult Terrapins has been carefully studied (mostly in Atlantic Coast populations [Ernst and Lovich, 2009]), Seigel and Gibbons (1995) listed juvenile Terrapin ecology as a topic that was lacking clear insight. Pilter (1985) reported observing juvenile Terrapins under marsh vegetation, and Lovich et al. (1991) observed hatchlings released in water swim directly to land and venture to tidal wrack located at the high-tide line. Additionally, Butler et al. (2004) observed 160 out of 172 hatchlings’ discernible tracks leading directly to marsh vegetation. Thus, upper salt marsh habitat may serve as a critical refuge in the life cycle of Terrapins. However, this proposed dispersal to upper salt marsh habitats can be perilous. Numerous organisms prey on Terrapin nests and hatchlings, including Procyon lotor L. (Raccoon; Feinburg and Burke 2003, Muldoon and Burke 2012), Corvus ossifragus Wilson (Fish Crow; Butler et al. 2004), Corvus brachyrhyncos Brehm (American Crow; Butler et al. 2004), Ocypode quadrata Fabricius (Ghost Crab; Butler et al. 2004), Rattus norvegicus Berkenhout (Norway Rat; Draud et al. 2004, Muldoon and Burke 2012), and even roots of Ammophila breviligulata Fernald (American Beachgrass; Lazell and Auger 1981). To investigate potential dispersal cues in the current study, Terrapins were able to choose between migrating to the open water in the bay or toward salt marsh vegetation. Their choices were analyzed to evaluate the importance of the surrounding environments to the post-emergence orientation of Terrapins. Materials and Methods The Alabama population of Terrapins has experienced a significant historical decline (Coleman 2011, Nelson and Marion 2004), so a head-start program was initiated to address unsustainable levels of nest predation (Coleman 2011). We obtained Terrapin eggs from nesting females captured in pitfall traps on the nesting beach surrounding Cedar Point Marsh. This site is located north of Dauphin Island along the Gulf Coast of Alabama. We palpated captured females to determine if they were gravid. If so, they were given a safe dose of oxytocin, which stimulates egg laying as described by Ewert and Legler (1978). Terrapins display temperature- dependent sex determination (Roosenburg and Kelley 1996), and eggs were incubated at a constant temperature of either 26 °C (male-producing temperature) or 31 °C (female-producing temperature) in the animal facility located at the University of Alabama at Birmingham (UAB). The majority of eggs were incubated at 31 °C to increase the number of females in the population to theoretically quicken the pace of recovery (Shaver and Wibbels 2007). UAB animal-facility rooms did not have access to sunlight and were kept at 24–26 ºC. We separated eggs and hatchlings by clutch and fed hatchlings daily to satiation. Obtaining these hatchlings provided opportunities to research various aspects of Terrapin biology, such as this study; however, the main purpose of the project was the eventual release of Southeastern Naturalist 575 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 the captive-reared Terrapins into Cedar Point Marsh after they had grown to approximately 200–300 g, usually at about one year of age. We created open-orientation arenas on the nesting beach surrounding Cedar Point Marsh (CPM) and on another nesting beach at Airport Marsh (AM), which is located behind Dauphin Island, AL (Fig. 1). The nesting beach surrounding CPM has a north–south orientation, whereas the AM nesting location runs east–west. Given the narrow width of nesting beaches at CPM and AM, arenas had a diameter of 6 m and consisted of 12 open “gates” delineated by short PVC pipes inserted into the ground (Fig. 2). PVC pipes were evenly spaced around the circumference of the circular arenas (at 30° intervals relative to the center) to mark the 12 “gates”. Gate 1 always faced Due North (0°). We performed orientation trials only at CPM in 2008, at both CPM and AM in 2009, only at AM in 2010, and only at CPM in 2012. It was not logistically possible to utilize naturally emergent hatchlings because the shell-hash substrate of CPM beach made it unsuitable to predictably find in situ nests. Terrapins were transported from UAB to the nesting beaches and held prior to their trials in a cooler to prevent access to natural orientation cues (e.g., natural light, olfaction, slope, open horizons). After their tests, the Terrapins were placed back in the cooler and transported back to UAB. We tested three age groups of Terrapins: hatchlings, post-hatchlings, and yearlings. Hatchlings were classified as turtles within one week after pipping (Table 1). We waited until the yolk sac of hatchlings had been absorbed within the plastron before trialing. Post-hatchlings were classified as turtles that were between one to eight weeks of age (McCauley and Bjorndal 1999). Yearlings were turtles that hatched and were trialed the previous nesting season and were approximately one year of age when retrialed. We tested Terrapins individually per trial and placed them under an opaque releasing device in the center of the arena for two minutes before starting. An observer, in a cryptic location outside the arena, remotely removed the releasing device via a string. The open arena allowed Terrapins to encounter multiple potential orientation cues. Terrapins were allowed to crawl in the arena for up to 10 minutes or until they travelled through one of the gates. We noted the gate the Terrapin passed through, along with the time taken to exit the arena and any notable orientation behavior. Trials were conducted between mid-morning to mid-afternoon hours (0900–1600). Table 1. Sample sizes of Diamond-backed Terrapin groups tested in orientation arena by location and year. Year Location Terrapin age group n 2008 Cedar Point Marsh Post-hatchlings 60 2009 Cedar Point Marsh Post-hatchlings 55 Yearlings 23 2009 Airport Marsh Post-hatchlings 4 Yearlings 23 2010 Airport Marsh Post-hatchlings 41 2012 Cedar Point Marsh Hatchlings 39 Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 576 Figure 1. Google Earth© image of orientation arenas location on nesting beach at Cedar Point Marsh (top) and Airport Marsh (bottom). Arena drawn to scale, and due north and scale are indicated. Southeastern Naturalist 577 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 We performed chi-square goodness-of-fit analyses on each dataset to determine if preference for orientation-arena gates was non-random among the test subjects. We also performed Rayleigh z tests on each dataset to determine the uniformity of and the mean direction of dispersal. First, we examined the overall orientation behavior of Terrapins, regardless of age group, by year. Next, we examined if yearlings that had been exposed to orientation cues at a previous year’s trial display different dispersal than naïve hatchlings and post-hatchlings. Third, we investigated any potential effects of incubation temperature on orientation and dispersal. Incubation temperature has been found to influence turtle hatchling performance in sea turtles (Burgess et al. 2006, Mickelson and Downie 2010) and freshwater turtles (Booth et al. 2004, Freedberg et al. 2004). All analyses were separated by location. For the incubation-temperature analysis, we only utilized the Terrapins’ initial trial, so no yearlings were included; Airport Marsh results were also not analyzed because of the low number of post-hatchlings incubated at 26 ºC that were initially tested at this location. Finally, we performed a one-way ANOVA on the exit times (i.e., time required to travel from the center of arena and pass through a gate) of Terrapins separated by age groups and incubation temperature. We transformed the exit-time data with natural logs to approximate normality. We completed all statistical analyses in Microsoft© Excel. Figure 2. Diagram of open orientation arena used on both Cedar Point and Airport marshes. The arena was composed of twelve “gates” that were delimited by PVC pipes positioned evenly around the circumference of the arena at intervals of 30° angles relative to the center. Gate 1 always faced due north (0°). Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 578 Results Overall orientation and dispersal behavior In total, we performed 245 individual trials utilizing orientation arenas at CPM and AM, and 208 trials resulted in hatchlings, post-hatchlings, and yearlings exiting the arena in the allotted 10 min. Terrapins displayed a significant orientation preference at CPM and dispersed in the direction of marsh vegetation (Fig. 3, Table 2). The 2009 trials at AM indicated significant orientation preference and non-uniform dispersal (Fig. 4), but the 2010 trials at AM did not. The mean angle for the 2009 trials was 199.1°, which was facing marsh vegetation. The average exit time for Terrapins that made it out of the arena in under the allotted 10 min was 281.92 s ± 17.86 95% CI. Effect of orientation experience Experienced yearlings and naïve hatchlings and post-hatchlings displayed significant orientation at CPM (Table 3). The dispersal of all three groups was in the direction of marsh vegetation. At AM, neither group displayed a significant gate preference. However, yearlings did display non-uniform dispersal toward marsh vegetation. Significant differences were detected between age groups in the exit Figure 3. Results from 2008 trials examining orientation behavior of Diamond-backed Terrapin post-hatchlings on a natural nesting beach surrounding Cedar Point Marsh. Seven post-hatchlings of the 60 released did not exit the arena in the allotted 10 minutes. Posthatchlings showed a significant preference for gates facing marsh vegetation (χ2 = 162.20, df = 11, P < 0.001). Their dispersal was not uniformly distributed (Rayleigh’s z41.75, P < 0.001), and the mean angle was 50.78° as denoted by the arrow. Southeastern Naturalist 579 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 times (F = 46.26; df = 2,155; P < 0.0001) at CPM. Yearlings (mean = 118.42 s ± 24.82 95% CI) displayed the fastest exit times, followed by post-hatchlings (mean = 306.72 s ± 24.09 95% CI) and hatchlings (mean = 332.43 s ± 38.42 95% CI). Significant differences (F = 12.95, df = 1,45, P = 0.0008) were also detected between yearlings (mean = 185.58 s ± 43.73 95% CI) and post-hatchlings (mean = 299.20 s ± 41.02 95% CI) at AM. Effect of incubation temperature We detected no differences in orientation between Terrapins incubated at 26 °C and 31 °C at CPM (Table 4). Both groups displayed significant dispersal toward Table 2. Results of chi-square goodness-of-fit analyses examining dispersal preferences of Diamondbacked Terrapins as well as results of Rayleigh’s z analyses examining the uniformity of dispersal and mean angle of direction. Each chi-square analysis had 11 degrees of freedom. Asterisk denotes levels of significance at α level of 0.05. Mean Year Location n χ2 χ2 0.05,11 P z z0.05,n P angle (°) 2008 Cedar Point Marsh 53 162.20* 19.68 <0.001 41.75* 2.982 < 0.001 50.78 2009 Cedar Point Marsh 70 265.81* 19.68 <0.001 53.58* 2.985 < 0.001 53.77 2009 Airport Marsh 21 20.71* 19.68 <0.05 8.65* 2.960 <0.001 199.10 2010 Airport Marsh 28 17.45 19.68 >0.05 1.49 2.969 >0.05 107.37 2012 Cedar Point Marsh 36 57.33* 19.68 <0.001 12.65* 2.975 <0.001 18.67 Figure 4. Results from 2009 trials examining orientation behavior of Diamond-backed Terrapin post-hatchlings and yearlings on a natural nesting beach surrounding Airport Marsh. Six individuals of the 27 released did not leave the orientation arena in the allotted 10 min. A significant preference for exiting gates facing marsh vegetation was observed (χ2 = 20.71, df = 11, P < 0.05). Their dispersal was not uniformly distributed (Rayleigh’s z8.65, P < 0.001), and the mean angle was 199.1° as denoted by the arrow. Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 580 marsh vegetation. We also observed no significant difference in exit times (F = 0.22, df = 1,137, P = 0.64) between the incubation temperature groups at CPM. Terrapins incubated at 26 ºC displayed slightly faster exit times (mean = 309.04 s ± 36.24 95% CI) than those incubated at 31 ºC (mean = 315.46 s ± 24.84 95% CI). Orientation behaviors We observed certain orientation behaviors among the age groups throughout the study. Terrapins would extend their heads and would often turn their bodies in a complete circle before making any directional movements. Once movement was initiated, it was often intermittent, with individuals periodically stopping to perform another “orientation circle” with heads extended before continuing with their movements. Finally, of the 37 trials in which Terrapins did not exit the arena in the allotted time, 20 of these trials resulted in individuals burying themselves into the beach substrate instead of dispersing. Discussion This study is the first to utilize a constructed arena on a natural nesting beach to quantitatively assess dispersal preferences of Diamond-backed Terrapins. Terrapins showed significant preference for dispersing toward marsh vegetation rather than open water. This result is in stark contrast to the orientation preferences of sea turtles, which rely on visual cues (Lohmann et al. 1997; Salmon et al. 1992, 1995) along with possible olfactory and magnetic cues (Fuentes-Farias et al. 2011) to orient away from dark silhouettes and toward open horizons of the sea. It was Table 4. Results of chi-square goodness-of-fit and Rayleigh’s z analyses comparing dispersal behavior between post-hatchlings incubated at 26 °C and post-hatchlings incubated at 31 °C on the natural nesting beach surrounding Cedar Point Marsh. Asterisks denote levels of significance at α level of 0.05. Temperature n χ2 χ2 0.05,11 P z z0.05,n P Mean angle (°) 26 °C 49 93.36* 19.68 <0.0001 29.74 2.981 <0.001 31.06 31 °C 105 264.83* 19.68 <0.0001 57.37 2.988 <0.001 41.96 Table 3. Results of chi-square goodness-of-fit and Rayleigh’s z analyses comparing dispersal behavior among yearlings, naïve post-hatchlings, and hatchlings on the natural nesting beach surrounding Cedar Point Marsh and between yearlings and naïve post-hatchlings at Airport Marsh. Asterisks denote levels of significance at α level of 0.05. Mean Location/exposure n χ2 χ2 0.05,11 P z z0.05,n P angle (°) Cedar Point Marsh Yearlings 19 79.06* 19.68 < 0.001 16.97* 2.956 <0.001 41.80 Post-hatchlings 104 317.39* 19.68 < 0.001 78.14* 2.988 <0.001 42.73 Hatchlings 36 57.33* 19.68 < 0.001 12.65* 2.975 <0.001 18.67 Airport Marsh Yearlings 19 17.04 19.68 >0.05 6.94* 2.956 <0.001 200.66 Post-hatchlings 30 16.4 19.68 >0.05 1.64 2.971 >0.05 118.45 Southeastern Naturalist 581 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 also different from other freshwater turtle species that were documented to disperse away from dark silhouettes (Anderson 1958) or toward open horizons (Congdon et al. 2011). Congdon et al. (2011) hypothesized that, for freshwater turtles, the most common strategy is for females to nest near water and hatchlings to orient toward the nearest open horizon. As stated above, this tendency was not observed with the Alabama population of Diamond-backed Terrapins examined in this study. Terrapins displayed a significant preference for orienting toward marsh vegetation instead of open water. Hatchling Blanding’s Turtles also disperse toward dark horizons, which are associated with riparian habitats (Pappas et al. 2009), but these hatchlings traveled much farther to reach their desired wetlands (average distance 589 m; Congdon et al. 2011) than Terrapins do to reach high marsh vegetation at our sites. Similar to other turtle species, visual cues seemed to be the primary cues used by Terrapins in their movements. They would often perform “orientation circles” with extended heads before moving directionally, thus consistent with the hypothesis that they were scanning the entire field of view for visual orientation cues. Burger (1976) observed similar behavior with Terrapin hatchlings raising their heads and looking around. In her study, hatchlings emerged between 0700 and 1900, with most between 1200 and 1700. When the hatchlings emerged from nests on flat areas, tracks were observed in random directions; however, they crawled down the gradient from nests laid on slopes (Burger 1976). Results indicated that hatchlings would move down inclines in different compass orientations, although individuals chose moving to vegetation regardless of incline (Burger 1976). Visual cues were suggested to be vital for hatchling orientation in Kinosternon flavescens Agassiz (Yellow Mud Turtles; Iverson et al. 2009) and Wood Turtles (Tuttle and Carroll 2005), as they have been for Blanding’s Turtles (Pappas et al. 2009, 2013), Western Painted Turtles (Congdon et al. 2011), and Snapping Turtles (Congdon et al. 2011, Pappas et al. 2013). After displacement from their normal post-emergence migration to wetlands, Yellow Mud Turtle hatchlings nonrandomly re-oriented toward the direction of the wetland destination. The authors suggested that reflected light intensity may have been a major visual cue for the hatchlings (Iverson et al. 2009); however, Congdon et al. (2011) suggested that positive geotaxis or open-horizon orientation were more probable cues for the turtle hatchlings in their study. Wood Turtle hatchlings exhibited saltatory searches with “stop and go” movements (Tuttle and Carroll 2005). Similar saltatory movements were observed frequently in the current study. Other cues could have influenced the Terrapin movements in our study. The arenas were constructed in relatively flat areas, so the influence of positive geotaxis was not examined in this study. As observed by Burger (1976), compass direction did not affect hatchling migration in the current study. The arena at CPM had a N–S orientation, whereas the arena at AM had a E–W orientation. However, the results obtained from AM were not as clear as those from CPM. A greater diversity in the location of vegetation surrounding the AM arena may have confounded the orientation behavior given the strong preference for beach vegetation observed by Burger Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 582 (1976). In contrast, the orientation arena we used at CPM was on a beach with very sparse vegetation due to overwashing from several tropical storms and hurricanes during recent years. Iverson et al. (2009) detected evidence for compass orientation in Yellow Mud Turtle yearlings. Displaced yearlings non-randomly re-oriented in the same direction as they were traveling when captured. Although the mechanism for setting the compass could not be concluded, the authors hypothesized that the compass for hatchlings was set in their initial wetland migration (Iverson et al. 2009). Pappas et al. (2009) suggested a sun compass was utilized by displaced experienced hatchlings that persisted on their initial direction even if it was in the opposite direction of their desired target. We did not detect any influence of experience on orientation direction at CPM, with all age groups distinctly choosing marsh vegetation. Olfactory and auditory cues could also have influence on Wood Turtle hatchlings (Tuttle and Carroll 2005). Neither of these possibilities was explored in the present study, but it could be argued that the relatively small distance that Terrapin hatchlings disperse after emergence compared to other turtle species, such as Blanding’s Turtles, may not require the use of multiple cues. It should not be surprising that the Terrapin burying behavior was observed. Terrapins emerge during daylight hours, with the highest emergence occurring during the hottest portion of the day (Burger 1976). Desiccation has been shown to be a powerful influence on turtle hatchling migrations (Kolbe and Janzen 2002). Dead hatchlings that apparently succumbed to overheating have been found at CPM (A.T. Coleman, UAB, Birmingham, AL, pers. observ.). Thus, burying themselves into the substrate appears to be an alternative strategy to direct movement to marsh vegetation. We did not wait to investigate whether Terrapins that buried themselves later completed their migration when ambient temperatures decreased. However, this strategy could increase their chances of falling prey to nocturnal predators. Although it was not logistically possible to utilize naturally emergent hatchlings, we do not expect our results to significantly deviate from that of naturally emerging hatchlings. First, previous studies with hatchling Terrapins have revealed similar orientation behaviors and dispersal (Burger 1976, Lovich et al. 1991, Muldoon and Burke 2012). Second, hatchlings and post-hatchlings used in the current study had not been exposed to any natural orientation cues associated with a nesting beach prior to their experimental trials. And as stated above, each age group (hatchling, post-hatchling, and yearling) displayed significant orientation towards marsh vegetation. However, the negative relationship between age and exit times indicated that size could influence movement rates and thus migration success in Terrapin hatchlings, which has been observed in other species (Janzen et al. 2000). Similar to experience, incubation temperature did not appear to affect Terrapin orientation, although incubation temperature has been shown to influence posthatchling growth (Roosenburg and Kelley 1996). The current findings highlight how a turtle’s ecology and nesting environment may influence the evolution of orientation mechanisms. The widths of the nesting beaches at CPM and AM, which are adjacent to marsh habitats, are approximately Southeastern Naturalist 583 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 10–15 m, similar to other Terrapin nesting sites in Florida (Butler et al. 2004), Maryland (Roosenburg et al. 2003), and New York (Draud et al. 2004). However, Terrapins in a Rhode Island population travelled much farther to nest (>500 m; Goodwin 1994). Therefore, different populations of Terrapins may display different dispersal behaviors or rely on different cues based on their unique ecology and nesting environments. For instance, in a population of Terrapins inhabiting Jamaica Bay, NY, a lower proportion of hatchlings was found to disperse to upland marsh habitats than would be expected based on our results (even though the majority [55–64%] of captured hatchlings were moving in the direction of marsh habitats; Muldoon and Burke 2012). A study in Jamaica Bay designed similar to ours would provide further insight to the cues used by Terrapin hatchlings from this New York population. Overall, our results revealed a very robust and innate orientation toward marsh vegetation in Terrapin hatchlings, post-hatchlings, and yearlings, and they agree with other published observations (Butler et al. 2004, Pilter 1985) and studies (Burger 1976, Draud et al. 2004, Lovich et al. 1991) concerning Terrapin habitat use post-emergence. The results of the current study also stress the importance of ample higher marsh habitat with associated tidal wrack and debris adjacent to Terrapin nesting beaches. This habitat could provide the necessary refuge and resources to individuals of this vulnerable life-history stage (Lovich et al. 1991, Muldoon and Burke 2012, Pilter 1985). Therefore, the presence of these habitats is critical for the success of hatchling survival and eventual recruitment into the adult population. Unfortunately, loss of marsh habitat is rampant throughout coastal ecosystems (Bertness et al. 2004), and this loss represents a major threat to the future viability of Diamond-backed Terrapin populations (Butler et al. 2006, Roosenburg 1991). Acknowledgments This project had approval from University of Alabama at Birmingham’s Institution for Animal Care and Use Committee under APN# 110309342. Funding for this project was provided for the Alabama Center for Estuarine Studies, the Alabama Department for Conservation and Natural Resources through a State Wildlife Grant, and UAB’s Department of Biology. Logistical support was provided by UAB’s Department of Biology and Dauphin Island Sea Lab. Numerous UAB undergraduate students in the Wibbels’ lab supplied great care to the Terrapin hatchlings. J. Pitchford and two anonymous reviewers provided a muchappreciated review of the manuscript. Literature Cited Anderson, P.K. 1958. The photic responses and water-approach behavior of hatchling turtles. Copeia 1958(3):211–215. Bertness, M., B.R. Silliman, and R. Jefferies. 2004. Salt marshes under siege. American Scientist 92(1):54–61. Booth, D.T., E. Burgess, J. McCosker, and J.M. Lanyon. 2004. The influence of incubation temperature on post-hatching fitness characteristics of turtles. International Congress Series 1275:226–233. Burger, J. 1976. Behavior of hatchling Diamondback Terrapin (Malaclemys terrapin) in the field. Copeia 1976(4):742–748. Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 584 Burgess, E.A., D.T. Booth, and J.M. Lanyon. 2006. Swimming performance of hatchling Green Turtles is affected by incubation temperature. Coral Reefs 25(3):341–349. Butler, J.A., C. Broadhurst, M. Green, and Z. Mullin. 2004. Nesting, nest, predation, hatchling emergence of the Carolina Diamondback Terrapin, Malaclemys terrapin centrata, in Northeastern Florida. American Midland Naturalist 152(1):145–155. Butler, J.A., G.L. Heinrich, and R.A. Seigel. 2006. Third workshop on the ecology, status, and conservation of Diamondback Terrapins (Malaclemys terrapin): Results and recommendations. Chelonian Conservation and Biology 5(2):331–334. Carr, A. 1952. Handbook of Turtles. Cornell University Press, Ithaca, NY. 542 pp. Coleman, A.T. 2011. Biology and conservation of Diamondback Terrapins (Malaclemys terrapin pileata) in Alabama. Ph.D. Dissertation. University of Alabama at Birmingham, Birmingham, AL. 221 pp. Congdon, J.D., M. Pappas, B. Brecke, and J. Capps. 2011. Conservation implications of naïve hatchling Snapping Turtles (Chelydra serpentina) and Painted Turtles (Chrysemys picta belli) dispersing from experimental nests. Chelonian Conservation and Biology 10(1):42–53. Draud, M., M. Bossert, and S. Zimnavoda. 2004. Predation on hatchling and juvenile Diamondback Terrapins (Malaclemys terrapin) by the Norway Rat (Rattus norvegicus). Journal of Herpetology 38(3):467–470. Ernst, C.H., and J.E. Lovich. 2009. Turtles of the United States and Canada. Johns Hopkins University Press, Baltimore, MD. 840 pp. Ewert, M.A., and J.M. Legler. 1978. Hormonal induction of oviposition in turtles. Herpetologica 34(3):314–318. Feinburg, J.A., and R.L. Burke. 2003. Nesting ecology and predation of Diamondback Terrapins, Malaclemys terrapin, at Gateway National Recreation Area, New York. Journal of Herpetology 37(3):517–526. Freedberg, S., A.L. Stumpf, M.A. Ewert, and C.E. Nelson. 2004. Developmental environment has long-lasting effects on behavioural performance in two turtles with environmental sex determination. Evolutionary Ecology Research 6:739–747. Fuentes-Farias, A.L., G. Gutiérrez-Ospina, E.M. Herrera, V. Camarena-Ramírez, G. Ochoa- Tovar, J. Mendoza-Torreblanca, A. Báez-Saldaña, R. Martínez-Méndez, J. Urrutia- Fucugauchi, and M.L.G. Zepeda. 2011. Marine turtle hatchlings use multiple sensory cues to orient their crawling towards the sea: Biological and conservation policy implications. Advances in Bioscience and Biotechnology 2:47–51. Goodwin, C.C. 1994. Aspects of nesting ecology of the Diamondback Terrapin (Malaclemys terrapin) in Rhode Island. M.S. Thesis. University of Rhode Island, Kingston, RI. 92 pp. Iverson, J.B., R.L. Prosser, and E.N. Dalton. 2009. Orientation in juveniles of a semiaquatic turtle, Kinosternon flavescens. Herpetologica 65(3):237–245. Janzen, F.J., J.K. Tucker, and G.L. Paukstis. 2000. Experimental analysis of an early lifehistory stage: Selection on size of hatchling turtles. Ecology 81(8):2290–2304. Janzen, F. J., J.K. Tucker, and G.L. Paukstis. 2007. Experimental analysis of an early lifehistory stage: Direct or indirect selection on body size of hatchling turtles? Functional Ecology 21(1):162–170. Kolbe, J.J., and F.J. Janzen. 2001. The influence of propagule size and maternal nest-site selection on survival and behavior of neonate turtles. Functional Ecology 15(6):772–781. Kolbe, J.J., and F.J. Janzen. 2002. Experimental analysis of an early life-history stage: Water loss and migrating hatchling turtles. Copeia 2002(1):220–226. Southeastern Naturalist 585 A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 Lazell, J.D. Jr., and P.J. Auger. 1981. Predation on Diamondback Terrapin (Malaclemys terrapin) eggs by Dunegrass (Ammophila breviligulata). Copeia 1981(3):723–724. Lohmann, K.J., B.E. Witherington, C.M. F. Lohmann, and M. Salmon. 1997. Orientation, navigation, and natal beach homing in sea turtles. Pp. 107–136, In P. Lutz and J. Musick (Eds.). The Biology of Sea Turtles. CRC Press Boca Raton, FL. 432 pp. Lovich, J.E., A.D. Tucker, D.E. Kling, J.W. Gibbons, and T.D. Zimmerman. 1991. Hatchling behavior of Diamondback Terrapins (Malaclemys terrapin) released in a South Carolina salt marsh. Herpetological 22(3):81–83. McCauley, S.J., and K.A. Bjorndal. 1999. Conservation implications of dietary dilution from debris ingestion: Sublethal effects in post-hatchling loggerhead sea turtles. Conservation Biology 13(4):925–929. McNeil, J.A., T.B. Herman, and K.L. Standing. 2000. Movement of hatchling Blanding’s turtles (Emydoidea blandingii) in Nova Scotia in response to proximity to open water: A manipulative experiment. Chelonian Conservation and Biology 3(4):611–617. Mickelson, L.E., and J.R. Downie. 2010. Influence of incubation temperature on morphology and locomotion performance of Leatherback (Dermochelys coriacea) hatchlings. Canadian Journal of Zoology 88(4):359–368. Muldoon, K.A., and R.A. Burke. 2012. Movements, overwintering, and mortality of hatchling Diamond-backed Terrapins (Malaclemys terrapin) at Jamaica Bay, New York. Canadian Journal of Zoology 90(5):651–662. Nelson, D.H., and K.R. Marion. 2004. Mississippi Diamondback Terrapin. Pp. 52–53 In R.E. Mirarchi, M.A. Bailey, T.M. Haggerty, and T.L. Best (Eds.). Alabama Wildlife, Volume Three: Imperiled Amphibians, Reptiles, Birds, and Mammals. University of Alabama Press, Tuscaloosa, AL. 228 pp. Pappas, M.J., J.D. Congdon, B.J. Brecke, and J.D. Capps. 2009. Orientation and dispersal of hatchling Blanding’s Turtles (Emydoidea blandingii) from experimental nests. Canadian Journal of Zoology 87(9):755–766. Pappas, M.J., J.D. Congdon, B.J. Brecke, and S. Freedberg. 2013. Orientation of freshwater hatchling Blanding’s (Emydoidea blandigii) and Snapping Turtles (Chelydra serpentina) dispersing from experimental nests in agricultural fields. Herpetological Conservation and Biology 8(2):385–399. Pilter, R. 1985. Malaclemys terrapin terrapin (Northern Diamondback Terrapin) behavior. Herpertological Review 16(3):82. Roosenburg, W.M. 1991. The Diamondback Terrapin: Habitat requirements, population dynamics, and opportunities for conservation. Pp. 227–234, In A. Chaney and J.A. Mihursky (Eds.). New Perspectives in the Chesapeake System: A Research and Management and Partnership. Proceedings of a Conference. Chesapeake Research Consortium Publication No 137. Solomons, MD. 718 pp. 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(2):198–204. Roosenburg, W.M., P.E. Allman, and B.J. Fruh. 2003. Diamondback Terrapin nesting on the Poplar Island Environmental Restoration Project. In Proceedings of the 13th Biennial Coastal Zone Conference, Baltimore, MD. US NOAA/CS/20322-CD. Salmon, M., J. Wyneken, E. Fritz, and M. Lucas. 1992. Seafinding by hatchlings sea turtles: Role of brightness, silhouette, and beach slope as orientation cues. Behavior 122(1–2):56–77. Southeastern Naturalist A.T. Coleman, T. Wibbels, K. Marion, T. Roberge, D. Nelson, and J. Dindo 2014 Vol. 13, No. 3 586 Salmon, M., M.G. Tolbert, D.P. Painter, M. Goff, and R. Reiners. 1995. Behavior of Loggerhead Sea Turtles on an urban beach. II. Hatchling orientation. Journal of Herpetology 29(4):568–576. Seigel, R.A., and J.W. Gibbons. 1995. Workshop on the ecology, status, and management of the Diamondback Terrapin (Malaclemys terrapin). Savannah River Ecology Laboratory, 2 August 1994: Final results and recommendations. Chelonian Conservation and Biology 1(3):241–243. Shaver, D.J., and T. Wibbels. 2007. Head-starting the Kemp’s Ridley Sea Turtle. Pp. 297– 323, In P. Plotkin (Ed.). Biology and Conservation of Ridley Sea Turtles. Johns Hopkins University Press Baltimore, MD. 356 pp. Standing, K.L., T.B. Herman, D.D. Hurlburt, and I.P. Morrison. 1997. Post-emergence behavior of neonates in a northern peripheral population of Blanding’s Turtle, Emydoidea blandingii, in Nova Scotia. Canadian Journal of Zoology 75(9):1387–1395. Stapput, K., and W. Wiltschko. 2005. The sea-finding behavior of hatchling Olive Ridley Sea Turtles, Lepidochelys olivacea, at the beach of San Miguel (Costa Rica). Naturwissenschaften 92(5):250–253. Tucker, J.K. 2000. Body size and migration of hatchling turtles: Inter- and intraspecific comparisons. Journal of Herpetology 34(4):541–546. Tuttle, S.E., and D.M. Carroll. 2005. Movements and behavior of hatchling Wood Turtles (Glyptemys insculpta). Northeastern Naturalist 12(3):331–348.