S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 478 2013 SOUTHEASTERN NATURALIST 12(3):478–491 Mammalian Depredation of Artificial Alligator Snapping Turtle (Macrochelys temminckii) Nests in North Louisiana Samuel R. Holcomb1,2,* and John L. Carr1 Abstract - Nest depredation is a major source of mortality in many turtle populations. Although turtle life histories may have evolved with relatively high levels of nest depredation, present-day levels may be negatively impacting populations that are already declining. This degree of depredation may be problematic for species such as Macrochelys temminckii (Alligator Snapping Turtle), which has relatively low reproductive output for a large turtle, yet little is known about depredation of M. temminckii nests. We constructed 90 artificial M. temminckii nests in 2008 and 2009 at Black Bayou Lake National Wildlife Refuge in Louisiana to identify nest predators and elucidate patterns of nest depredation. All artificial nests were depredated, with Procyon lotor (Raccoon), and Dasypus novemcinctus (Nine-banded Armadillo) being the two most common nest predators. Other predators included Lontra canadensis (Northern River Otter), Didelphis virginiana (Virginia Opossum), and Lynx rufus (Bobcat). Nest depredation is a major threat to Alligator Snapping Turtles at this site and may be limiting recruitment in this population. Introduction Mortality rates during the egg stage are quite high for many chelonians, with nest depredation often being the primary source of mortality (Hamilton et al. 2002, Iverson 1991). Certain aspects of turtle reproduction and nesting behavior may have evolved to mitigate depredation risk, such as masking nesting activity by nesting on or after days with rainfall events (Bowen and Janzen 2005, Burke et al. 1994), as well as the production of multiple clutches of eggs (Hamilton et al. 2002, Jackson 1988). Thus, nest predators may have had an important role in shaping turtle life histories and populations (Hamilton et al. 2002, Wilbur and Morin 1988), and relatively high levels of nest depredation were likely common historically. The high nest mortality typical of turtle life histories was historically offset by significantly higher survival rates at later stages in the life cycle, which include high survival rates of the long-lived adults (Iverson 1991). However, many turtle populations currently face stress from anthropogenic factors such as habitat fragmentation and degradation (Gerlach 2008, Rizkalla and Swihart 2006, Saumure and Bider 1998), road mortality (Aresco 2005, Ashley and Robinson 1996, Gibbs and Shriver 2002), commercial collection (Ceballos and Fitzgerald 2004, Cheung and Dudgeon 2006, Schlaepfer et al. 2005), climate change (Chaloupka et al. 2008, Janzen 1994), and egg poaching (Tomillo et al. 2008). Additionally, populations of some nest predators have prospered due to habitat fragmentation, the provision of supplemental food 1Department of Biology and Museum of Natural History, University of Louisiana at Monroe, Monroe, LA 71209. 2Louisiana Department of Wildlife and Fisheries, PO Box 98000, Baton Rouge, LA 70898. *Corresponding author - Samsw1@aol.com. 479 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 sources, and mesopredator release resulting from the extirpation of large carnivores (Mitchell and Klemens 2000, Oehler and Litvaitis 1996, Prugh et al. 2009). Therefore, levels of nest depredation may be elevated due to increased population density of predators, potentially representing an additive source of mortality for already stressed populations. The threat presented by increased levels of nest depredation may be most severe for species with delayed sexual maturity and relatively low annual reproductive output, such as Macrochelys temminckii Troost (Alligator Snapping Turtle), which produces a single clutch of 30–35 eggs per year and reaches sexual maturity at 15–21 years of age (Ewert and Jackson 1994, Reed et al. 2002, Tucker and Sloan 1997, Woosley 2005). The Alligator Snapping Turtle is more strongly aquatic and secretive than most sympatric species, and is considered a species of conservation concern throughout its range (Buhlmann and Gibbons 1997). Although habitat loss and human exploitation are widely seen as the primary threats to this species (Reed et al. 2002, Sloan and Lovich 1995), a lack of data on many aspects of its life history and ecology hinders effective conservation. A valuable technique for investigating nest depredation and depredation rates is the use of artificial nests (King et al. 1999). Experiments using artificial nests have been particularly popular among ornithologists for answering numerous questions related to ecology, evolution, and land management (Major et al. 1999). Due to the difficulty of locating natural nests of some turtles, this technique has also proved valuable in investigating depredation of turtle nests (e.g., Marchand et al. 2002, Wilhoft et al. 1979). As the purpose of artificial nest studies is to make inferences about depredation of natural nests, such studies are only valid if predators respond to artificial nests similarly to natural nests; primary concerns during artificial nest construction include mimicking the physical characteristics of natural nests and avoiding the deposition of human scent (King et al. 1999, Major and Kendall 1996). With careful consideration of artificial nest construction, turtle-nest predators perceive artificial nests as actual nests (Burke et al. 2005, Hamilton et al. 2002). There is little known concerning predators of Alligator Snapping Turtle nests, or the effects of nest depredation on Alligator Snapping Turtle populations. Redmond (1979) and Ewert et al. (2006) identified Procyon lotor L. (Raccoon) as a predator of Alligator Snapping Turtle nests in Georgia and Florida, but provided little additional information and mentioned no other nest predators. To address this knowledge gap, we investigated Alligator Snapping Turtle nest depredation in northern Louisiana in 2008 and 2009. We typically found only 10–12 nests at our site each year. Thus, by using artificial nests we were able to experiment with a larger number of nests than if we had used natural nests. Additionally, we were able to study nest depredation without exposing natural nests to predators, a decided advantage when working with a species of conservation concern. Field-Site Description This study was conducted at Black Bayou Lake National Wildlife Refuge (NWR), which is located approximately 8 km north of the city of Monroe, in S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 480 Ouachita Parish, LA. Field-work was conducted entirely on the western portion of the refuge near a railroad causeway on the west side of the lake. This causeway has been identified as a primary nesting area for Alligator Snapping Turtles at the refuge (Woosley 2005), as has a wooded peninsula near the south end of the causeway transect. Two 1-km transects were established for conducting nesting surveys (Holcomb and Carr 2011, Woosley 2005) and were also used for the artificial nest experiments; one located along the causeway and the other located on the peninsula. The railroad causeway transect consisted of the railway on top of a straight, elevated roadbed of fill dirt with water approximately 5–10 m from the rails on both sides at usual water levels. The elevated roadbed is covered in ballast (rocks) and the water–land margin has a fringe of trees and shrubs of variable height. The peninsula transect consisted of a mown trail approximately 3 m wide that was separated from the lake by a strip of bottomland hardwood forest on one side and bordered by a reforested cotton field on the other side. Both transects were characterized by frequent human disturbance (i.e., mowing, railroad maintenance operations) and high observed levels of turtle nest depredation. Methods Field methods Artificial nests were constructed along both nesting transects following the 2008 and 2009 Alligator Snapping Turtle nesting seasons, but while other turtles (emydids and Apalone spinifera Lesueur [Spiny Softshell]) were still nesting. Fifteen artificial nests were constructed along each transect between 21 May and 2 July 2008. Thirty artificial nests were constructed along each transect between 5 June and 10 July 2009. Artificial nests were situated along transects in locations similar (in terms of ground cover and proximity to water) to those of naturally laid Alligator Snapping Turtle nests at this site (Holcomb and Carr 2011, Woosley 2005). Artificial nests were constructed by using a hand shovel to excavate 22-cmdeep cavities with widths of ≈15 cm x 19 cm, the mean dimensions of natural nests at the site (Woosley 2005). Once the nest cavity was constructed, 6 medium-sized chicken eggs were placed in the cavity, providing a total egg mass similar to a small clutch of average-sized Alligator Snapping Turtle eggs (Woosley 2005), and the cavity was refilled with the soil resulting from excavation. Soil was then mounded on top of the nest and contoured to mimic the appearance of a freshly laid natural Alligator Snapping Turtle nest, with disturbed soil covering an area of ≈30 by 40 cm and up to 10–12 cm high (Fig. 1). This size and configuration of disturbed soil is unique to Alligator Snapping Turtles at the site, and very different from Spiny Softshell and emydid nests. Disposable gloves were worn throughout the nest construction process to minimize the amount of human scent deposited. The date and time of construction were recorded, and location was determined using a handheld GPS receiver. After construction was complete, a Wildview™ XTREME 2, 2.0 megapixel Digital Scouting Camera was positioned so that any predator excavating the nest would activate the motion sensor and be photographed. All photographs were date- and time-stamped, and stored on Secure 481 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 Digital (SD) cards, which were retrieved following depredation. Nests were checked daily, and batteries and SD cards were replaced as needed. Data analysis All images were examined and any predator photographed was identified. If a potential predator was photographed and the nest was subsequently depredated (i.e., when next checked), the assumption was that the predator photographed was responsible, even when the depredation event itself was not captured in the photo. For nests that were visited by more than one predator species, the first predator photographed was considered to be responsible for depredation. The exact time of all predator visits was noted, along with the number of individuals involved. The interval between the visits of different species, or between visits by the same species, was calculated. Two images of the same species were considered separate visits when an interval of at least 1 hour had elapsed between photos. It was not possible to determine if subsequent visits by the same species represented the same or different individuals. The interval between construction and depredation was determined for each nest where the exact time of depredation was known. For nests where the exact time of depredation was not known, the nest was placed into one of the following categories: <24 hours survival, <48 hours survival, <72 hours survival, and Figure 1. Freshly laid natural Alligator Snapping Turtle nest at Black Bayou Lake NWR, showing the characteristic disturbance (Photograph © S.R. Holcomb). S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 482 >72 hours survival, which was possible due to the daily nest checks described previously. We calculated average survival time for artificial nests for 2008 and 2009, as well as for the two years combined, and by predator species. Due to a few apparent outliers, the modal survival time for the two-year study was also determined. Finally, daily survival rates for artificial nests were calculated for the first 4 days following construction using the Kaplan-Meier method (Krebs 2000). This method allows a staggered entry of nests into the study and provides a finite survival rate easily converted to percentages (Krebs 1999). Results All 90 artificial nests constructed during this study were depredated, but the depredation event was not recorded photographically at every nest. Images of predators (Fig. 2) were obtained at 9 of 30 nests (30.0%) in 2008, and at 42 of 60 nests (70.0%) in 2009, yielding an overall success rate of 56.7% (51 of 90 nests). During the first year, we had more camera failures due to batteries being drained while photographing non-target subjects, such as trains passing on the railroad causeway, than we had the second year. Multiple predator species were recorded at 16 nests (31.4%), and multiple visits to the same nest by the same species were recorded at 21 nests (41.2%) (Table 1). In total, we recorded multiple visits (i.e., at least two) by predators at 49.0% (25/51) of nests. Figure 2. Nest camera photographs of predators depredating artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR: A) Raccoons, B) Nine-banded Armadillo, C) Virginia Opossum, D) Northern River Otters. 483 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 The Raccoon was the most common predator, documented at 43 of 51 nests. At 41 nests, the Raccoon was the first predator photographed, and it was documented simultaneously with Dasypus novemcinctus L. (Nine-Banded Armadillo) once. A Raccoon also visited a single nest that had already been depredated by a Ninebanded Armadillo. Overall, Raccoons were determined to be responsible for 82.4% of documented artificial nest depredation events. There were 21 instances where Raccoons re-visited a nest, with some nests being visited as many as 4 times (Table 1). For 5 artificial nests depredated by Raccoons, multiple individuals were involved; a pair of Raccoons depredated 3 nests, and 2 nests were depredated by a group of 3 animals (Fig. 2A). The second-most common predator was the Nine-banded Armadillo (Fig. 2B), which was the first predator documented at 6 nests, and which visited 11 nests that had previously been visited by the Raccoon. Therefore, 11.8% of documented depredation events were attributed to the Nine-banded Armadillo. There were no documented revisits by the Nine-banded Armadillo, and only one occurrence of 2 individuals at the same nest. Only 3 artificial nest depredation events were attributed to a predator species other than the Raccoon or the Nine-banded Armadillo, with 3 different species implicated. Didelphis virginiana Kerr (Virginia Opposum) was the first predator documented at one nest, and an opposum visited another nest after a Raccoon (Fig. 2C). Lynx rufus Schreber (Bobcat) was the first predator photographed at one nest, and 2 nests that had previously been visited by the Raccoon were visited by Bobcats. The last predator species documented was Lontra canadensis Schreber (Northern River Otter), which was responsible for the depredation of a single nest (2 individuals present, Fig. 2D). Artificial nests were depredated heavily during the first 24 hours following construction, with 77 of the 90 (85.6%) artificial nests failing to survive beyond 24 h (Fig. 3). Of the remaining 13 nests, 8 were destroyed within the first 48 h, leaving only 5 nests (5.6%) that survived more than 48 h. The average survival time of artificial nests was slightly more than 19 h, and the modal survival time was 13 h. The interval to depredation was shorter, on average, for nests depredated by the Nine-banded Armadillo, compared to nests depredated by the Raccoon (Table 2). The Kaplan Meier survival estimate for the first day following construction was 14.44%, and by day 4 was 1.11% (Table 3). Diel timing of depredation events was determined from the photographs obtained of nest predators for 51 of the 90 artificial nests. Most nest depredation occurred between sunset and sunrise (73.0%). The Raccoon was the only predator Table 1. Mean and range of intervals (h) to initial and subsequent visits to artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR by the Raccoon. n = number of nests. To 1st visit 1st visit–2nd visit 2nd visit–3rd visit 3rd visit–4th visit n 21 21 8 3 Mean 16.7 15.5 12.9 14.5 Range 4.3–88.0 1.4–94.8 1.2–26.1 3.6–32.2 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 484 documented to destroy nests diurnally (31.0% of all Raccoon depredation), except for one instance of Nine-banded Armadillo depredation that occurred shortly before sunset (Fig. 4). Figure 3. Survival times of artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR in 2008 and 2009 for which the interval to depredation is known, grouped into 6-hour classes. Nests for which the interval to depredation was estimated have been added to the appropriate 24-hour block. Table 2. Average survival time of artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR in hours (h) for 2008, 2009, both years combined, and for each predator species, and modal survival time of artificial nests for the two years of the study. n = number of nests used for the average or modal survival time calculation. Time (h) n Average survival time 2008 18.6 9 2009 19.2 42 2-year total 19.1 51 Raccoon 18.4 42 Nine-banded Armadillo 12.7 6 Virginia Opossum 12.6 1 Bobcat 91.8 1 River Otter 21.5 1 Modal survival time 2-year total 13.0 51 485 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 Discussion The 100% depredation rate on artificial nests during this study is consistent with depredation rates on natural nests at Black Bayou Lake NWR (J.L. Carr, pers. observ.), as well as multiple studies of Chelydra serpentina L. (Snapping Turtle) nest depredation. For example, annual depredation levels occasionally reached 100% for a Snapping Turtle population in Michigan (Congdon et al. 1987), and a New York population experienced a one-year depredation rate of 94.4% (Petokas and Alexander 1980). This similarity to other studies extends to the timing of nest destruction; almost 86% of all artificial nests constructed Table 3. Daily survival estimates for days 1–4 after nest construction for artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR. Survival rates were calculated using the Kaplan- Meier method in Ecological Methodology (Krebs 2000). Day Survival rate (%) Standard error 95% Confidence interval (%) 1 14.44 0.037 7.18–21.71 2 5.56 0.024 0.08–10.29 3 3.34 0.019 0.00–7.04 4 1.11 0.011 0.00–3.27 Figure 4. Diel timing of depredation of artificial Alligator Snapping Turtle nests at Black Bayou Lake NWR for 2008 and 2009, with each nest placed into 1 of 24 one-hour blocks, with mean sunrise and sunset indicated. S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 486 during this study were depredated within the first 24 hours, and less than 6% survived beyond 48 hours, consistent with observed depredation patterns on Snapping Turtle nests (Congdon et al. 2000, Petokas and Alexander 1980, Wirsing et al. 2012). However, this finding differs from Florida observations suggesting that predators seldom depredated Alligator Snapping Turtle nests until several days after oviposition (Ewert and Jackson 1994). The depredation rate on our artificial nests might have been slightly lower had the experiment been conducted earlier in the nesting season, as nest predators may improve their efficiency at locating nests throughout the nesting season (Engeman et al. 2005), though others have found that earlier nests are more prone to depredation (Kolbe and Janzen 2002). We consider it unlikely that beginning our artificial nest experiments earlier in the nesting season would have had an appreciable effect on depredation rates, as natural nests laid earlier appear to be just as prone to depredation as later nests at this site (J.L. Carr, pers.observ.). The primary Alligator Snapping Turtle nesting areas at Black Bayou Lake NWR are highly linear habitats and represent ecological edges, both factors that may increase nest depredation (Kolbe and Janzen 2002, Major et al. 1999, Temple 1987, Wirsing et al. 2012), and represent what have been referred to as “predator travel corridors” (Wirsing et al. 2012). Additionally, the railroad causeway transect provides very narrow strips of nesting habitat situated between the railroad tracks and the water’s edge, greatly reducing the area that nest predators must search. This situation may result in an increased rate of nest depredation (Andersson and Wiklund 1978, Marchand et al. 2002), although it is not predicted that “incidental” predator species will exhibit a density-dependent pattern of depredation (Wirsing et al. 2012). The results of our artificial nest experiments are consistent with the observation that high nest-depredation rates are not related to olfactory or visual cues associated with a nesting female turtle’s presence (Hamilton et al. 2002, Wilhoft et al. 1979). Interestingly, in an Illinois study, nests with greater soil disturbance, such as those of Snapping Turtles, were more likely to be depredated than nests of species exhibiting less disturbed soil, such as Chrysemys picta Schneider (Painted Turtle; Strickland et al. 2010). Similarly, the Snapping Turtle, the species with the larger and more obvious soil disturbance, had nests depredated at a significantly higher rate than Painted Turtles in Ontario, Canada (Wirsing et al. 2012). This finding suggests Alligator Snapping Turtle nests are at higher risk relative to most sympatric species given the large soil disturbance that is characteristic of their nests (Woosley 2005). The Raccoon was the primary predator species in this study, as in many studies on turtle nest depredation (e.g., Butler et al. 2004, Marchand and Litvaitis 2004, Mitchell and Klemens 2000, Stancyk 1982, Tuberville and Burke 1994, Wirsing et al. 2012). Nine-banded Armadillos were found to be an important nest predator in this study, though of minor importance compared to the Raccoon. Drennen et al. (1989) were among the first to report the Nine-banded Armadillo as a predator of turtle nests in North America, although armadillos were previously known as a 487 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 major nest predator of Trachemys venusta Gray (Meso-American slider) in Panama (Moll and Legler 1971). Although Nine-banded Armadillos consume intact eggs, they also likely act as secondary predators on nests that have already been partially depredated, perhaps because they are attracted by partially eaten eggs and invertebrates (Drennen et al. 1989). This explanation seems consistent with 11 instances in this study where the Nine-banded Armadillo was documented at nests that had already been depredated by Raccoons. However, Nine-Banded Armadillos acted as primary predators of 6 Gopherus polyphemus Daudin (Gopher Tortoise) nests in Georgia (Smith et al. 2012). The Nine-banded Armadillo may be becoming more important as a nest predator of North American turtles following significant range expansion over the last century (Smith and Doughty 1984). Virginia Opossums have previously been identified as predators of Snapping Turtle nests (Hamilton 1940) and Emydoidea blandingii Holbrook (Blanding’s Turtle) nests (Congdon et al. 2000). Both the Bobcat and the Northern River Otter have rarely been identified as predators of turtle nests. For example, Vogt and Bull (1984) reported a single emydid nest taken by a River Otter, and Bobcats were implicated in the depredation of 3 Caretta caretta L. (Loggerhead Sea Turtle) nests (Martin et al. 2005) and a single artificial Graptemys ouachitensis ouachitensis Cagle (Ouachita Map Turtle) nest (Rosenzweig 2003). The greatest threat to recruitment in this population of Alligator Snapping Turtles is mammalian nest depredation. This threat is demonstrated by the depredation of all 90 artificial nests constructed during this study, as well as the short mean interval to depredation. Black Bayou Lake NWR is a semi-urban refuge with large populations of mesopredators and no higher-order predators to exert top-down control. Therefore, if nest predator populations are to be reduced, it will have to be through active management. Control of nest predators has been a strategy often employed in conservation of sea turtles and has been successful at reducing nest depredation; for example, depredation rates decreased from 95% to less than 10% following the implementation of integrated predator monitoring and control on Jupiter Island in Florida (Engeman et al. 2003, Engeman et al. 2005). The inclusion of monitoring in predator control efforts is essential, as removal of one predator species from a site can have unintended consequences (Barton and Roth 2007, Ratnaswamy and Warren 1998) that could make predator control counterproductive. Predator control efforts should be undertaken as part of a long-term strategy, as one-time-only predator control efforts may decrease nest losses to predators in the short term, with depredation rates rising again after a few years (Christiansen and Gallaway 1984). Although predator exclusion can be effective under certain circumstances (Smith et al. 2012), it is not a viable solution for this population of Alligator Snapping Turtles. Specifically, it would not be logistically feasible to fence off large areas of nesting habitat (e.g., Smith et al. 2012), and protecting individual nests is too labor intensive to be a long-term solution. If losses of Alligator Snapping Turtle nests to vertebrate nest predators can be reduced to nominal levels at Black Bayou Lake NWR, recruitment of hatchlings into the population could be significantly increased. As the situation currently S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 488 stands, and assuming our results are representative of what occurs around the lake periphery, there is little reason to believe that any meaningful level of natural recruitment is occurring in this population. Acknowledgments This research was performed under Louisiana state scientific collecting permits LNGP-08-043 and LNHP-09-059 and US Fish and Wildlife Service Special Use Permits 42651-08-04 and 42651-09-03. Funding was provided by the Louisiana Department of Wildlife and Fisheries and the US Fish and Wildlife Service, Division of Federal Aid, through State Wildlife Grant T-57. We would like to thank the staff of Black Bayou Lake NWR for their cooperation. Mitch Ray, Lisa Brown, and Matt Pardue provided assistance with field-work. Lisa Brown and David Steen provided helpful comments on the manuscript. Literature Cited Andersson, M., and C.G. Wiklund. 1978. Clumping versus spacing out: Experiments on nest predation in Fieldfares (Turdus pilaris). Animal Behaviour 26:1207–1212. Aresco, M.J. 2005. The effect of sex-specific terrestrial movements and roads on the sex ratio of freshwater turtles. Biological Conservation 123:37–44. Ashley, E.P., and J.T. Robinson. 1996. Road mortality of amphibians, reptiles and other wildlife on the Long Point Causeway, Lake Erie, Ontario. Canadian Field-Naturalist 110:403–412. Barton, B.T., and J.D. Roth. 2007. Raccoon removal on sea turtle nesting beaches. Journal of Wildlife Management 71:1234–1237. Bowen, K.D., and F.J. Janzen. 2005. Rainfall and depredation of nests of the Painted Turtle, Chrysemys picta. Journal of Herpetology 39:649–652. Buhlmann, K.A., and J.W. Gibbons. 1997. Imperiled aquatic reptiles of the southeastern United States: Historical review and current conservation status. Pp. 201–232, In G.W. Benz, and D.E. Collins (Eds.). Aquatic Fauna in Peril: The Southeastern Perspective. Lenz Design and Communications, Decatur, GA. 554 pp. Burke, R.L., C.M. Schneider, and M.T. Dolinger. 2005. Cues used by Raccoons to find turtle nests: Effects of flags, human scent, and Diamond-Backed Terrapin sign. Journal of Herpetology 39:312–315. Burke, V.J., J.W. Gibbons, and J.L. Greene. 1994. Prolonged nesting forays by Common Mud Turtles (Kinosternon subrubrum). American Midland Naturalist 131:190–195. Butler, J.A., C. Broadhurst, M. Green, and Z. Mullin. 2004. Nesting, nest predation, and hatchling emergence of the Carolina Diamondback Terrapin, Malaclemys terrapin centrata, in northeastern Florida. American Midland Naturalist 152:145–155. Ceballos, C.P., and L.A. Fitzgerald. 2004. The trade in native and exotic turtles in Texas. Wildlife Society Bulletin 32:881–891. Chaloupka, M., N. Kamezaki, and C. Limpus. 2008. Is climate change affecting the population dynamics of the endangered Pacific Loggerhead sea turtle? Journal of Experimental Marine Biology and Ecology 356:136–143. Cheung, S.M., and D. Dudgeon. 2006. Quantifying the Asian turtle crisis: Market surveys in southern China, 2000–2003. Aquatic Conservation: Marine and Freshwater Ecosystems 16:751–770. Christiansen, J.L., and B.J. Gallaway. 1984. Raccoon removal, nesting success, and hatchling emergence in Iowa turtles, with special reference to Kinosternon flavescens (Kinosternidae). Southwestern Naturalist 29:343–348. 489 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 Congdon, J.D., G.L. Breitenbach, R.C. van Loben Sels, and D.W. Tinkle. 1987. Reproduction and nesting ecology of Snapping Turtles (Chelydra serpentina) in southeastern Michigan. Herpetologica 43:39–54 Congdon, J.D., R.D. Nagle, O.M. Kinney, M. Osentoski, H.W. Avery, R.C. van Loben Sels, and D.W. Tinkle. 2000. Nesting ecology and embryo mortality: Implications for hatchling success and demography of Blanding’s Turtles (Emydoidea blandingii). Chelonian Conservation and Biology 3:569–579. Drennen, D., D. Cooley, and J.E. Devore. 1989. Armadillo predation on Loggerhead Turtle eggs at two national wildlife refuges in Florida, USA. Marine Turtle Newsletter 45:7–8 Engeman, R.M., R.E. Martin, B. Constantin, R. Noel, and J. Woolard. 2003. Monitoring predators to optimize their management for marine turtle nest protection. Biological Conservation 113:171–178. Engeman, R.M., R.E. Martin, H.T. Smith, J. Woolard, C.K. Crady, S.A. Shwiff, B. Constantin, M. Stahl, and J. Griner. 2005. Dramatic reduction in predation on marine turtle nests through improved predator monitoring and management. Oryx 39:318–326. Ewert, M.A., and D.R. Jackson. 1994. Nesting ecology of the Alligator Snapping Turtle (Macroclemys temminckii) along the lower Apalachicola River, Florida. Florida Game and Fresh Water Fish Commission's Nongame Wildlife Program, Tallahassee, FL. Report NG89-020. 45 pp. Ewert, M.A., D.R. Jackson, and P.E. Moler. 2006. Macrochelys temminckii—Alligator Snapping Turtle. Pp. 58–71, In P.A. Meylan (Ed.). Biology and Conservation of Florida Turtles. Chelonian Research Monographs 3. Chelonian Research Foundation, Lunenberg, MA. 376 pp. Gerlach, J. 2008. Fragmentation and demography as causes of population decline in Seychelles freshwater turtles (genus Pelusios). Chelonian Conservation and Biology 7:78–87. Gibbs, J.P., and W.G. Shriver. 2002. Estimating the effects of road mortality on turtle populations. Conservation Biology 16:1647–1652. Hamilton, A.M., A.H. Freedman, and R. Franz. 2002. Effects of deer feeders, habitat and sensory cues on predation rates on artificial turtle nests. American Midland Naturalist 147:123–134. Hamilton, W.J. 1940. Observations on the reproductive behavior of the Snapping Turtle. Copeia 1940:124–126. Holcomb, S.R., and J.L. Carr. 2011. Hatchling emergence from naturally incubated Alligator Snapping Turtle (Macrochelys temminckii) nests in northern Louisiana. Chelonian Conservation and Biology 10:222–227. Iverson, J.B. 1991. Patterns of survivorship in turtles (Order Testudines). Canadian Journal of Zoology 69:385–391. Jackson, D.R. 1988. Reproductive strategies of sympatric freshwater emydid turtles in northern peninsular Florida. Bulletin of the Florida Museum, Biological Sciences 33:115–158 Janzen, F.J. 1994. Climate-change and temperature-dependent sex determination in reptiles. Proceedings of the National Academy of Sciences 91:7487–7490. King, D.I., R.M. DeGraaf, C.R. Griffin, and T.J. Maier. 1999. Do predation rates on artificial nests accurately reflect predation rates on natural bird nests? Journal of Field Ornithology 70:257–262. Kolbe, J.J., and F.J. Janzen. 2002. Spatial and temporal dynamics of turtle nest predation: Edge effects. Oikos 99:538–544. S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 490 Krebs, C.J. 1999. Ecological Methodology, 2nd Edition. Benjamin/Cummings, Menlo Park, CA. 620 pp. Krebs, C.J. 2000. Programs for Ecological Methodology [computer program]. Version 5.2. East Setauket, NY. Major, R.E., and C.E. Kendal. 1996. The contribution of artificial nest experiments to understanding avian reproductive success: A review of methods and conclusions. Ibis 138:298–307. Major, R.E., F.J. Christie, G. Gowing, and T.J. Ivison. 1999. Elevated rates of predation on artificial nests in linear strips of habitat. Journal of Field Ornithology 70:351–364. Marchand, M.N., and J.A. Litvaitis. 2004. Effects of landscape composition, habitat features, and nest distribution on predation rates of simulated turtle nests. Biological Conservation 117:243–251. Marchand, M.N., J.A. Litvaitis, T.J. Maier, and R.M. DeGraaf. 2002. Use of artificial nests to investigate predation on freshwater turtle nests. Wildlife Society Bulletin 30:1092–1098. Martin, R.E., R.M. Engeman, H.T. Smith, C.K. Crady, M. Stahl, and B. Constantin. 2005. Cheloniidae (Marine Turtle) nest predation by Bobcats. Herpetological Review 36:56–57. Mitchell, J.C., and M.W. Klemens. 2000. Primary and secondary effects of habitat alteration. Pp. 5–32, In M.W. Klemens (Ed.). Turtle Conservation. Smithsonian Institution Press, Washington, DC. 334 pp. Moll, E.O., and J.M. Legler. 1971. The life history of a Neotropical slider turtle, Pseudemys scripta (Schoepff), in Panama. Bulletin of the Los Angeles County Museum of Natural History, Science 11:1–102. Oehler, J.D., and J.A. Litvaitis. 1996. The role of spatial scale in understanding responses of medium-sized carnivores to forest fragmentation. Canadian Journal of Zoology 74:2070–2079. Petokas, P.J., and M.M. Alexander. 1980. The nesting of Chelydra serpentina in northern New York. Journal of Herpetology 14:239–244. Prugh, L.R., C.J. Stoner, C.W. Epps, W.T. Bean, W.J. Ripple, A.S. Laliberte, and J.S. Brashares. 2009. The rise of the mesopredator. BioScience 59:779–791. Ratnaswamy, M.J., and R.J. Warren. 1998. Removing Raccoons to protect sea turtle nests: Are there implications for ecosystem management? Wildlife Society Bulletin 26:846–850. Redmond, A. 1979. Observations on the Alligator Snapping Turtle. Bulletin of the Georgia Herpetological Society 5:5–6. Reed, R.N., J. Congdon, and J.W. Gibbons. 2002. The Alligator Snapping Turtle (Macrochelys [Macroclemys] temminckii): A review of ecology, life history, and conservation, with demographic analyses of the sustainability of take from wild populations. Aiken, SC: Savannah River Ecology Laboratory. 14 pp. Rizkalla, C.E., and R.K. Swihart. 2006. Community structure and differential responses of aquatic turtles to agriculturally induced habitat fragmentation. Landscape Ecology 21:1361–1375 Rosenzweig, A. 2003. The reproductive ecology and life history of Graptemys ouachitensis (Testudines: Emydidae) in the Red River of Louisiana. M.Sc. Thesis. University of Louisiana at Monroe, Monroe, LA. 95 pp. Saumure, R.A., and J.R. Bider. 1998. Impact of agricultural development on a population of Wood Turtles (Clemmys insculpta) in southern Quebec, Canada. Chelonian Conservation and Biology 3:37–45. 491 S.R. Holcomb and J.L. Carr 2013 Southeastern Naturalist Vol. 12, No. 3 Schlaepfer, M.A., C. Hoover, and C.K. Dodd, Jr. 2005. Challenges in evaluating the impact of the trade in amphibians and reptiles on wild populations. BioScience 55:256–264. Sloan, K., and Lovich, J.E. 1995. Exploitation of the Alligator Snapping Turtle, Macroclemys temminckii, in Louisiana: A case study. Chelonian Conservation and Biology 1:221–222. Smith, L.L., and R.W. Doughty. 1984. The Amazing Armadillo: Geography of a Folk Critter. University of Texas Press, Austin, TX. 134 pp. Smith, L.L., D.A. Steen, L.M. Conner, and J.C. Rutledge. 2012. Effects of predator exclusion on nest and hatchling survival in the Gopher Tortoise. Journal of Wildlife Management 77:352–358. Stancyk, S.E. 1982. Non-human predators of sea turtles and their control. Pp. 139–152, In K.A. Bjorndal (Ed.). Biology and Conservation of Sea Turtles. Smithsonian Institution Press, Washington, DC. 583 pp. Strickland, J., P. Colbert, and F.J. Janzen. 2010. Experimental analysis of effects of markers and habitat structure on predation of turtle nests. Journal of Herpetology 44:467–470. Temple, S.A. 1987. Predation on turtle nests increases near ecological edges. Copeia 1987:250–252. Tomillo, P.S., V.S. Saba, R. Piedra, F.V. Paladino, and J.R. Spotila. 2008. Effects of illegal harvest of eggs on the population decline of Leatherback Turtles in Las Baulas Marine National Park, Costa Rica. Conservation Biology 22:1216–1224. Tuberville, T.D, and V.J. Burke. 1994. Do flag markers attract turtle nest predators? Journal of Herpetology 28:514–516. Tucker, A.D, and K.N. Sloan. 1997. Growth and reproductive estimates from Alligator Snapping Turtles, Macroclemys temminckii, taken by commercial harvest in Louisiana. Chelonian Conservation and Biology 2:587–592. Vogt, R.C., and J.J. Bull. 1984. Ecology of hatchling sex ratio in map turtles. Ecology 65:582–587. Wilbur, H.M., and P.J. Morin. 1988. Life history evolution in turtles. Pp. 387–439, In C. Gans, and R.B. Huey (Eds.). Biology of the Reptilia. Volume 16, Ecology B: Defense and Life History. Alan R. Liss, Inc., New York, NY. 659 pp. Wilhoft, D.C., M.G. Del Baglivo, and M.D. Del Baglivo. 1979. Observations on mammalian predation of Snapping Turtle nests (Reptilia, Testudines, Chelydridae). Journal of Herpetology 13:435–438. Wirsing, A. J., J.R. Phillips, M.E. Obbard, and D.L. Murray. 2012. Incidental nest predation in freshwater turtles: Inter-and intraspecific differences in vulnerability are explained by relative crypsis. Oecologia 168:977–988. Woosley, L.B. 2005. Population structure and reproduction of Alligator Snapping Turtles, Macrochelys temminckii, at Black Bayou Lake National Wildlife Refuge. M.Sc. Thesis. University of Louisiana at Monroe, Monroe, LA. 59 pp.