we note that terrapin density along the Downing Musgrove Causeway to Jekyll Island, which is a known location of high annual female terrapin road mortality, ...
A Report to Georgia Department of Natural Resources on:
Relationship Between Diamondback Terrapin Abundance and Road and Crabbing Pressures Along Coastal Georgia
Conducted and prepared by Dr. John C. Maerz and Mr. Andrew M. Grosse Daniel B. Warnell School of Forestry and Natural Resources The University of Georgia Athens, GA 30602
The information presented in this report is the product of the principle investigator and student investigator listed on the title page. The principle investigator reserves full rights to the publication of the information presented. This report is offered to the Georgia Department of Natural Resources to provide a full reporting of our research findings and fulfill the final obligation of this funding contract with Georgia Department of Natural Resources.
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Acknowledgments We thank Kerry Holcomb, Daniel van Dijk, Justin Nowakowski, Natalie Hyslop, Jack Maerz, Robert Maerz, Mark Dodd, Mike Harris, Erica Kemler, Terry Norton, Summer Teal-Simpson, Jordan Gray, Matt McKinney, Alan Grosse, Rachel Grosse, Peggy Grosse, Robert Horan, George Pirie, Kristin Felton, David Osborne, Taylor Sauls, Joe Milanovich, Jayna DeVore, Vanessa Kinney, Andrew Ferreira, Andrew Durso, Matt Erickson, Sean Sterrett, Kristen Cecala, Andy Davis, Janice Denney, Anna McKee, Victor Long, LeighAnne Harden, Megan Heidenreich, James Moore, Charlie Stoudenmire, Keith Deane, Serena Newman, and Sylvan Cox for their assistance in the field. This document was improved by comments from Kristen Cecala, Joe Milanovich, Sean Sterrett and Jayna DeVore. Funding for this project was provided by a State Wildlife Grant to JCM from the Georgia Department of Natural Resources, Coastal Resources Division. Additionally, all research protocols were approved by the Institutional Animal Care and Use Committee at the University of Georgia under AUP # A2007-10031.
Collaborators Dr. Kurt Buhlmann (Savannah River Ecology Lab, University of Georgia), Dr. Jeb Byers (Odum School of Ecology, University of Georgia), Mr. Brian Crawford (D. B. Warnell School of Forestry and Natural Resources, University of Georgia), Dr. Michael Dorcas (Department of Biology, Davidson College), Dr. Jeff Hepinstall (D. B. Warnell School of Forestry and Natural Resources, University of Georgia), Ms. Michelle Kaylor (Georgia Sea Turtle Center), Dr. Terry Norton (Georgia Sea Turtle Center), and Dr. Tracey Tuberville (Savannah River Ecology Lab, University of Georgia).
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Project Summary Human harvest of natural resources from natural areas and increased development and use of exurban natural habitats for recreational use are major management challenges for the conservation of wildlife. Understanding how activities contribute to the current and future status of wildlife is critical in developing effective, long-term management strategies. In Georgia, the diamondback terrapin (Malaclemys terrapin) is listed as a “high-priority” species for conservation efforts within coastal habitats. Factors identified in Georgia’s State Wildlife Action Plan (SWAP) as potentially contributing to M. terrapin population declines include habitat conversion, fragmentation of populations, competition and predation from non-native invasive species, and vehicle-induced road mortality. Though not mentioned explicitly within Georgia’s SWAP, bycatch in commercial and recreational crab pots is a well-documented cause of terrapin population declines in other portions of the species’ range. Although both crabbing and vehicle-induced mortality may affect terrapin population declines, the two processes are likely to have different effects on the size and sex ratio of M. terrapin populations. The objectives of this research were to assess the independent and potentially additive or interactive effects of road and crabbing pressures on the abundance and population structure of M. terrapin populations on Georgia’s coast. Between 2007 and 2008, we conducted single-year mark-recapture estimates for 29 tidal creeks chosen using a stratified random selection of creeks with known proximity to high densities of roads or high numbers of commercial crab pots. We estimated that terrapins currently occupy 88% of Georgia’s tidal creeks, with a mean density of 151 terrapins/km (95% confidence interval on density = 62-240). This density was comparable to current densities reported for Kiawah Island, SC. We found a clear pattern of declining terrapin abundance associated with commercial crabbing activity; however, we found no measurable relationship between terrapin abundance and road density or proximity. The latter result may reflect both limits of the study design and the fact that Georgia’s coast is still relatively undeveloped with regards to the density of busy roads. Design limitations included difficulty of generating relevant metrics of road pressures, and selecting sites at random with regard to knowledge of terrapin road mortality. For example, we note that terrapin density along the Downing Musgrove Causeway to Jekyll Island, which is a known location of high annual female terrapin road mortality, was below the median lower quartile among non-crabbing creeks. Therefore, we caution that while we find no measurable relationship between terrapin abundance and road density or proximity for coastal Georgia, high traffic roads may be having local effects on terrapin populations. Diamondback terrapins are state listed as an S3 (rare or uncommon) species in Georgia. Our conclusion is that terrapins in Georgia are relatively widespread and at least moderately abundant with some areas of notably high densities. Georgia has the opportunity to act to preserve its robust terrapin populations and alleviate the negative effects of human activities on its stressed populations. In its pending revision to its State Wildlife Action Plan, we recommend commercial crabbing be explicitly identified as a potential factor affecting the status of terrapins in Georgia. Because commercial crabbing is an important industry to the communities of coastal Georgia, we make several recommendations to reduce the impact of this industry on terrapin populations. First, require all commercial crab pots to have a bycatch reduction device (BRD) or restrict the placement of crab pots in shallow waters between April and June if those pots do not have
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BRDs. Establish and enforce a maximum soak time for active crab pots, and clean up ghost pots from shallow tidal creeks. Designate select areas with currently high densities of terrapins as areas of high conservation value for terrapins, and regulate activities such as commercial crabbing or fishing within those areas to maintain their conservation value. We do recommend further monitoring of the local effects of vehicle mortality on terrapin populations along Georgia’s causeways where high numbers of terrapin mortalities are well documented. Identification of effective management strategies for reducing vehicle mortality in those areas will be an important area for immediate research. Finally, we recommend that a long-term monitoring program be developed; however, additional work on a less resource-intensive approach is still needed. We feel that the use of head count surveys is insufficient as a monitoring approach, but we provide evidence that the use of parasite surveys may provide a rapid assessment tool for estimating terrapin population sizes among a large number of sites.
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Table of Contents Acknowledgements
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Project Summary
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Introduction Need
1
Study species
3
Approach Study site selection
4
Terrapin sampling and abundance estimation
6
Statistical analyses
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Results Terrapin occupancy and abundance
8
Crabbing and road associations with density
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Head counts and population estimation
11
Discussion Key findings
11
Management recommendations
14
Supplemental and future research Road mortality on causeways
17
Terrapin parasites as population indicators
20
Terrapin trophic and high-marsh ecology
22
Products, Deliverables, and Broader Impacts
26
Literature cited
28
Appendix A
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Introduction Need Natural habitat loss and degradation is the primary cause of wildlife population declines and species loss in the continental United States (Diamond, 1984; Venier and Fahrig, 1996; Mitchell and Klemens, 2000; Guthery et al., 2001). Human harvest of natural resources from natural areas can impact non-resource species. Further, growing urban populations place significant pressures on exurban natural habitats through increased land use and development for recreational use (Thompson and Jones, 1999). Understanding how human activities contribute to the current and future status of wildlife is critical in developing effective, long-term management strategies. With the harvest of marine resources and the development of coastal areas for recreation, a number of animal species that depend on coastal habitats are of increasing conservation concern. Species such as the diamondback terrapin (Malaclemys terrapin), an estuarine specialist, have experienced declines throughout their range (Seigel and Gibbons, 1995; Dorcas et al., 2007). Anthropogenic activities in coastal ecosystems, such as commercial and recreational crab harvesting, vehicle-induced road mortality, and habitat loss have been repeatedly identified as threats to M. terrapin populations (Seigel and Gibbons, 1995; Wood, 1997; Roosenburg, 2004). In parts of the coastal southeastern U.S. that remain relatively underdeveloped, terrapin populations appear relatively abundant; therefore, there remains the opportunity to study human impacts on M. terrapin populations and intervene before populations decline as they have elsewhere in the species’ range. In Georgia, M. terrapin is listed as a “high-priority” species for conservation efforts within coastal habitats (Georgia Department of Natural Resources, 2005). Factors identified in Georgia’s State Wildlife Action Plan (aka, Comprehensive Wildlife Conservation Strategy) as potentially contributing to M. terrapin population declines in Georgia include habitat conversion, fragmentation of populations, competition and predation from non-native invasive species, and vehicle-induced road mortality (Georgia Department of Natural Resources, 2005). In coastal areas, roads are often constructed on elevated land through or adjacent to marshes, and the vegetation along roads is kept back by maintenance such that roadsides create attractive nesting areas for terrapins (Szerlag-Egger and McRobert, 2007). In other, more developed coastal regions within the species’ range, intense road mortality of terrapins is well documented (Seigel and Gibbons, 1995). In recent years within Georgia, high numbers of female terrapins were documented as killed along some causeways leading to Georgia’s barrier islands (Fig. 1). While it is hard to imagine, in light of extensive information on turtle life histories, that documented levels of road mortality are not affecting terrapin populations, there has never been a published scientific study linking road mortality to terrapin population declines within Georgia or the larger species’ range. By contrast, bycatch in commercial-grade crab pots (Fig. 1) is a well-documented source of terrapin mortality in other parts of the species’ range and has been linked to local and regional declines in terrapin abundance (Roosenburg et al., 1997; Hoyle and Gibbons, 2000; Roosenburg and Green, 2000; Dorcas et al., 2007). Although both crabbing and vehicle-induced mortality may affect terrapin population declines, the two processes are likely to have different effects on
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Figure 1. Left panel: adult female diamaondback terrapin with shell fracture from vehicle strike on the DowningMusgrove Causeway to Jekyll Island, GA. Right panel: 96 dead diamondback terrapins recovered from a commercial crab pot in a Georgia tidal creek. The pot was marked by a commercial buoy, but was sunk in deep in the mud and had significant accumulation of benthic organisms indicating it was neglected.
the size and sex ratio of M. terrapin populations. Vehicle-induced mortality is known to disproportionately affect female turtles because they emerge onto high ground such as near roads to nest (Gibbs and Shriver, 2002; Steen and Gibbs, 2005; Szerlag and McRobert, 2006); so it is postulated that turtle populations impacted by vehicle mortality should be increasingly male biased. On the other hand, Roosenburg et al. (1997) demonstrated that bycatch in crab pots is biased toward male and juvenile terrapins because mature female terrapins are generally too large to enter crab pots. If crabbing activities are affecting terrapin populations, then those populations should be increasingly female biased and have a greater proportion of larger turtles (Szerlag and McRobert, 2006; Dorcas et al., 2007). For example, despite suspicions that increasing residential densities were leading to high vehicular-mortality rates among female terrapins on Kiawah Island, SC, Dorcas et al. (2007) report that the steady population declines of terrapins around Kiawah Island were associated with the populations becoming progressively female biased and larger in body size. This pattern is consistent with crab-pot mortality as the driver of population change. Despite evidence of the effects of commercial and recreational crabbing as drivers of terrapin population declines, crabbing activities are not explicitly identified by Georgia’s State Wildlife Action Plan as a potential factor affecting terrapin conservation status in Georgia. The objectives of this research were to assess the independent and potentially additive or interactive effects of road and crabbing pressures on the abundance and population structure of M. terrapin populations on Georgia’s coast. Specifically, we tested the hypotheses that 1) M. terrapin density has a negative relationship with road density or proximity and crabbing activity, 2) terrapin sex ratio (male:female) is positively related to road density or proximity and negatively related to crabbing activity. We also provide evidence of human-driven evolutionary changes in terrapin growth rates. In addition, this research addressed potential methods for longterm monitoring of terrapin populations including estimates of effort needed to determine 2
whether terrapins occupy a creek, the efficacy of head counting as a measure of abundance, and the potential to use local parasite densities to estimate terrapin abundance. Finally, this project facilitated new lines of research and conservation action including (1) the identification of potential areas of high-conservation value for terrapins in Georgia, (2) assessment of patterns of road mortality along the Downing-Musgrove Causeway to Jekyll Island, and (3) patterns of prey use among terrapins that indicates a higher reliance on feeding “terrestrially” within the high marsh than was previously suspected.
Study Species Malaclemys terrapin is the only strictly estuarine species of emydid turtle found in North America (Ernst et al., 1994). Seven sub-species inhabit the brackish tidal zones from Cape Cod, Massachusetts south around the Florida peninsula and west around the Gulf of Mexico to Texas (Fig. 2; Ernst et al., 1994). The Carolina terrapin, M. t. centrata, is the species found in Georgia’s brackish tidal marshes (Fig. 2). The subspecies is sexually dimorphic with adult females growing significantly larger than adult males (Ernst et al., 1994). Terrapin beak morphology is adapted to crushing hard-bodied prey, and they are reported to prey on a range of estuarine fauna including mud and periwinkle snails, fiddler crabs, and blue crabs. It is assumed that terrapins spend much of their time in the water during low tide and feed on prey in the water or in the high marsh during high tide. In Georgia, terrapins breed in April, and females generally nest from mid-May through mid-July.
Figure 1. Range of seven sub-species of diamondback terrapin. A) Malaclemys terrapin terrapin B.) M. t. centrata C.) M. t. Tequesta D.) M. t. rhizopararum E.) M. t. macrospilota F.) M. t. pileata G.) M. t. littoralis. (source: Hart 2005)
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Approach Site Selection Study sites were chosen using a stratified random design. We categorized 138 creeks of an appropriate size to seine according to two factors: road density and number of crab pots (Fig. 2). Road density was determined using existing GIS data to measure kilometers of road within 0.5 km on each side of tidal creeks and standardized to a density measurement (km/km2). Georeferenced crabbing activity from 2003 to 2006 (time period for which state records are available) was obtained from the Georgia Department of Natural Resources, Coastal Resources Division (Brunswick, GA). Based on observed distributions among all creeks, we considered high road densities >2.00 km of roads within 500 m of each creek, and high crabbing activity > 0.5 crab pots/km of creek. Each of 138 creeks was placed into one of four “treatments” based on their corresponding road density and crabbing pressure: high roads-no crabbing, high roadscrabbing, low roads-crabbing, and low roads-no crabbing. We then ranked creeks within each category by a randomly assigned number, and then visited potential creeks in rank order and vetted them based on accessibility and safety criteria (e.g., we excluded creeks that required boating in the open ocean to access the creek) until six tidal creeks from each of the four classes were identified. During sampling, if we failed to capture a terrapin during the first two sampling periods, we considered terrapins absent from the site, and we added the next randomly selected site within the same class to our study sites. In addition, we sampled a creek parallel to the Downing Musgrove Causeway to Jekyll Island at the request of Georgia Department of Natural Resources. The Downing-Musgrove Causeway did not have any record of commercial crabbing between 2003 and 2006, and we did not observe crabbing activity during our study; however, the road is a known hotspot for adult female terrapin mortality (>250 nesting females annually; Holcomb et al. unpublished data). Ultimately, we sampled 29 tidal creeks distributed evenly across the Georgia coast (Fig. 2). Because existing GIS road density layers included all paved surfaces in Georgia (e.g. driveways, subdivisions, parking lots), and were therefore not necessarily indicative of vehicular pressure, we additionally measured the distance (km) to the closest ‘relevant’ road from each creek. Specifically, we examined each creek using digital photographs and used our best judgment as to the closest road that could sustain traffic (i.e. higher traffic volume streets, and not driveways or subdivision roads). We took into account barriers, such as sea walls, that may influence the ability of terrapins to access a road (Fig. 3). Once we determined the nearest relevant road, we classified all sites as being proximate (within 1.2 km of a road) or distant (> 2.3 km from the nearest road). We also attempted to generate traffic volume data for our relevant roads; however, AADT (annual average daily traffic) data were not available for many of our roads, and AADT may not reflect seasonally relevant measures such as high traffic volumes on causeways to barrier island beaches during the peak periods of terrapin nesting.
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Figure 2. All potential study sites (hollow rectangles) and actual study sites (solid black rectangles) overlaid on road density (km road per 0.75 km2) and crab pot density (pots per km) between 2003-2006.
We verified our measure of crab pot density with direct counts of crab pots during our sampling. We used actual crab pot numbers in our analyses, and based on observed patterns of crabbing activity, further refined crabbing classifications to no crabbing, low crabbing (1-2 pots per creek; only one creek had two pots), and high crabbing (three or more pots per creek).
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Figure 3. Examples of determination of distance to nearest relevant road (represented by the dotted line) for two study creeks in coastal Georgia, taking into account potential barriers (sea wall) and low traffic roads.
Terrapin sampling and abundance estimation We used individual mark-recapture to estimate terrapin density. We seined each creek, using two 10 m, 2.54 cm mesh seines with a bag following the methods of Dorcas et al. (2007) (Fig. 4). We did not use trammel nets during this study. Seining began each day immediately prior to low tide, and seines were pulled from the start of each sampling area and continued until we reached the end of the creek, occasionally pulling the seines onto the mud bank to remove captured M. terrapin and bycatch. Depending on width and depth of creeks, seines were either pulled in tandem or side-by-side to maximize the area sampled. Each creek was seined up and back during each visit. Each creek was seined at low tide every 20 days between April 1st and June 30th, for a total of five mark-recapture periods per creek. This time period is the most effective for capturing terrapins in the study region (Gibbons et al., 2001). Following capture, all turtles were sexed based on position of the cloaca on the tail and head allometry, measured (carapace length, plastron length, shell width and depth), weighed (g), ‘aged’ by counting scute rings (Sexton, 1959), and uniquely marked using marginal scute notches (Cagle, 1939).
Figure 4. Seining for diamondback terrapins in a Georgia tidal creek at low tide.
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During 2008, we opportunistically conducted 17 head counts prior to seining for terrapins. When possible, a minimum of three technicians drove the length of the site, at low tide, just prior to seining, and counted the number of M. terrapin heads observed. This process was repeated for the return trip. After surveying the length of the site both up and back, all three technicians recorded the number of M. terrapin heads counted, representing the overall average for that transect. Immediately following, each creek was seined and the total number of M. terrapin captured by seining was compared to the total number of heads counted from the boat. We used a modified approach to estimate terrapin abundance for each study creek. We recognize that capture probabilities are not a species-level attribute, and that when estimating population abundance at multiple sites, it is ideal to estimate terrapin capture probabilities for each study site (MacKenzie and Kendall, 2002; Mazzerolle et al. 2007). However, because we failed to recapture terrapins of one or both sexes in creeks with few individuals, it was not possible for us to estimate sex-specific capture probabilities for terrapins for all study creeks. Therefore, we proceeded with the assumption that terrapin behavior with regard to capture and recapture probabilities were similar among creeks. We pooled all data into two data sets, one for males and one for females, and then we used each data set to estimate capture and recapture probabilities for each sex. We used Program CAPTURE (White and Burnham 1999) to determine the most appropriate model for measuring sex-specific terrapin capture probabilities. We used sex-specific capture probabilities and the mean number of each sex captured over the five sampling periods to generate male and female closed-population abundance estimates for each creek. We summed these estimates to generate a total density and sex ratio for each creek.
Statistical Analysis We conducted two sets of analyses to test our hypotheses. First, we used ANOVA to test the hypotheses that terrapin density was negatively related to crabbing activity and proximity to a road. We used road proximity (proximate or distant) and crabbing activity (none, low or high) as fixed factors. We used the same model to test the hypotheses that the terrapin male:female sex ratio was positively related to road density or proximity and negatively related to crabbing activity. We also used generalized linear models combined with model selection (Akaike’s Information Criterion, AIC) to examine specific linear relationships among crabbing, road density and proximity measures to terrapin densities and sex ratios. In addition to providing additional tests of hypotheses, linear models may be useful for management purposes in relating specific habitat measures to terrapin population metrics. Density estimates were square-root transformed to meet the assumption of homogeneity of variance, and we used a log10 (ratio + 1) transformation for sex ratio analyses. To determine whether terrapin size distributions differed as among creeks with different crabbing pressures, we used a one-way ANOVA on the percentage of M. terrapin less than 107 mm plastron length among creeks with different crabbing activity classifications. All analyses were conducted in STATISTICA v8.0 (StatSoft, Inc., Tulsa, OK).
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Results Terrapin occupancy and abundance Ground confirmation of crabbing efforts within coastal tidal creeks revealed that GA DNR records for crabbing efforts within our study creeks were biased low. We found commercial crabbing in eight of 29 sites (28%) where there are no records of crabbing activity between 20032006. Four of those eight sites had at least three commercial pots within the ~ 1 km of shallow tidal creek sampled. We assume this simply reflects that not all possible tidal creeks in GA were monitored for crab pots; however, we note that all sites we sampled with records of crab pots between 2003-2006 still had active commercial crab pots in 2007 or 2008. In five visits to each of 15 pre-selected tidal creeks during the summer of 2007, 977 M. terrapin were captured, consisting of 783 individuals. Similarly, in five visits to 14 pre-selected tidal creeks during the summer of 2008, 1028 M. terrapin were captured, consisting of 764 individuals. In total, during both sampling periods (2007 = April 1st to June 24th and 2008 = April 1st to June 26th), 2,005 M. terrapin were captured, consisting of 1,547 individuals. Appendix A contains a complete summary of numbers of terrapins captured by creek as well as descriptions of the locations of each creek. The mean number of M. terrapin captured in each visit was 12 (range = 0-175, SD = 22.7, n = 153). Overall, captures were male biased, with 77% males and 23% females. Over the course of this study, we observed 87 terrapin road mortalities, 99% of which were nesting females. We also observed 153 terrapins, equal to nearly10% of all live terrapins observed among study creeks, drowned in crab pots within study creeks. Males made up 83% of drowned terrapins, and the mean plastron length of drowned terrapins was 107 mm (median = 102 mm, 25% - 75% quartiles = 97-110 mm). We estimated that between April and June, 87.7% of tidal creeks in Georgia are occupied at low tide by M. terrapin. Mean terrapin density among our 29 study creeks was 151 terrapins/km (95% confidence interval on mean density = 62-240); however, the distribution of terrapin densities was significantly leptokurtic, right skewed. Median terrapin density was 65 terrapins/km (lower – upper quartiles = 39-149 terrapins/km). We identified two relatively proximate sites (Sites 97 and 98, Appendix A) within the large shallow estuary west of Sea Isle, GA where terrapin density estimates were far greater, 735-1040 terrapins/km, than anywhere else we sampled along the Georgia coast. Site 93 west of Saint Simons Island, GA also had a relatively dense terrapin population (510 terrapins/km). All other sites had densities less than 300 terrapins/km. With an estimated occupancy of 87.7% of creeks, an average estimated density of 151 terrapins/km (95% confidence interval on density = 62-240), and our initial 135 potential tidal creeks representing 760 km of tidal creek, we estimate that there are ~92,000 subadult and adult terrapins along coastal Georgia (95% confidence interval 38,000-146,000). Note, this estimate is highly qualified (see Key Findings Discussion below).
Crabbing and road associations with density Terrapin density declined significantly with increasing crabbing activity (MS = 417.045, F1,25 = 9.425, P = 0.005, Fig. 5), but was not explained by proximity to a road (MS = 7.568, F1,25 =
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0.171, P = 0.683). There was no measurable interaction between crabbing activity and road proximity (MS = 2.230, F1,25 = 0.050, P = 0.824, Fig. 3). Sex ratio was not measurably related to crabbing activity (MS = 0.082, F1,25 = 1.164, P = 0.219, Fig. 4), road proximity (MS = 0.135, F1,25 = 2.667, P = 0.118), or an interaction between the two factors (MS = 0.110, F1,25 = 2.180, P = 0.155).
Figure 5. Mean terrapin density (upper panel) and sex ratio (lower panel) as a function of crabbing activity and proximity to a road. Density values are square-root transformed, and sex ratio values are log10(ratio + 1) transformed. Error bars represent ± 1 SE.
The best model (based on AIC) included the single factor of number of crab pots in the creek. This model was statistically significant and showed a negative relationship between the number of crab pots and terrapin density (Likelihood ratio Chi-square = 9.060, df = 1, P = 0.003). The model including both number of crab pots and distance to the nearest road was within two AIC of the top model and also significant (Likelihood ratio Chi-square = 9.244, df = 2, P = 0.010); however, only the number of crab pots was identified as a significant factor in that model (Wald statistic = 5.625, P = 0.018, Fig. 6). Distance to the nearest road was not a significant factor (Wald statistic = 0.152, P = 0.696). The best model for predicting sex ratio only included crab pot number; however, that model was generally indistinguishable from other models and was not statistically significant (Likelihood ratio Chi-square = 1.823, df = 1, P = 0.177). The model that included both crab pot number and distance to nearest road was not significant (Likelihood ratio Chi-square = 2.499, df = 2, P = 0.287), and neither crab pot number (Wald statistic = 2.073, P = 0.150) nor distance to nearest road (Wald statistic = 0.683, P = 0.409) was significant within the model (Fig. 6). Finally, the percentage of terrapins that were less than 107 mm plastron length tended to vary between creeks with and without crabbing activity (MS = 556.05, F2,21 = 2.816, P = 0.083, Fig. 7). It is clear (Fig. 7) that the mean percentage of terrapins below 107 mm plastron length is lower among creeks with crabbing activity, though it does differ between creeks with high or low crabbing activity. When crabbing activity classes are combined, the difference in mean percentage of terrapins below 107 mm plastron length between creeks with and without crabbing activity is statistically significant (MS = 1110.23, F2,21 = 5.887, P = 0.023).
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Figure 6. Multiple linear regression relationships between the number of crab pots in a creek and the distance to the nearest relevant road and terrapin density (upper panel) or sex ratio (lower panel). The model for terrapin density was significant (Likelihood ratio Chi-square = 9.244, df = 2, P = 0.010) with only the number of crab pots as a significant factor (Wald statistic = 5.625, P = 0.018). The model for sex ratio was not significant (Likelihood ratio Chi-square = 2.499, df = 2, P = 0.287). Plane represents multiple linear regression.
Figure 7. Mean (± 1 SE) percent of M. terrapin captured that were smaller than 107 mm plastron length as a function of crabbing activity level within the creek (107 mm represents the mean plastron length for terrapins found dead in crab pots). When crabbing activity classes are combined, the difference in mean percentage of terrapins below 107 mm plastron length between creeks with and without crabbing activity is statistically significant (MS = 1110.23, F2,21 = 5.887, P = 0.023).
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Head counts and population estimation Average number of M. terrapin heads counted by three observers over two passes ranged from 0 to 46 turtles. We observed 0 heads on two occasions in creeks where terrapins were detected by seining and for which terrapin abundance was estimated, with estimated terrapin abundance of 22 and 42 terrapins/creek. Among all 17 head-count observations, we found that there was a strong correlation between the average number of M. terrapin heads counted by three observers over two passes and the number of terrapins captured by seining on that visit (Number of M. terrapin caught = 2.862 + 1.645* average heads counted; r = 0.939, P < 0.001), and estimated M. terrapin density from the five mark-recapture samples (n = 17, r = 0.891, P = 20 terrapin heads observed in creeks with estimated densities above 700 terrapins/km. The remainder of observations averaging less than 10 heads counted were in creeks with 75% over a period of 16 years, and resulted in a shift in population structure to larger, older individuals in the population. In our study, the overwhelming majority of crab pots in creeks associated with lower abundances of terrapins were commercial crab pots. Similarly, in the upper Chesapeake Bay, Roosenburg et al. (1997) estimated that 15%-78% terrapins in shallow tidal creeks are removed by commercial crabbing annually. In its State Wildlife Action Plan, Georgia identified road mortality as a significant factor impacting the conservation of diamondback terrapins in coastal Georgia. Our study showed no measureable relationship with road density or the distance to the nearest relevant road and current patterns of terrapin abundance among tidal creeks along the Georgia coast. Georgia has a relatively rural coastal region with several barrier islands with little or no vehicle traffic. Sixteen (55%) of the 29 randomly selected sites we studied were located more than 2.3 km from a biologically relevant road. This contrasts sharply with patterns throughout the United States where 50% of land lies within 0.38 km of a road (Riitters and Wickham 2003). Riitters and Wickham (2003) identified coastal regions including the southeastern United States as vulnerable to the impacts of roads because 60-80% of the land lies within 0.38 km of a road; however, that may not accurately reflect road proximity to estuarine habitats. Further, most of Georgia’s coastal roads sustain low levels of traffic. Therefore, it is possible that density and traffic volume near Georgia’s coastal estuaries is not yet sufficient to currently affect terrapin abundance across the Georgia coast. We caution that where high traffic roads come in close proximity to marshes, road mortality may be a significant factor affecting local terrapin abundance. It is widely accepted that turtle populations cannot sustain significant increases in adult female mortality (Heppell 1998). There is ample evidence of adult female terrapin mortality on coastal roads that bisect or closely parallel marshes. For example, in seven years in southern New Jersey, over 4,000 terrapins were killed when attempting to cross the Garden State Parkway of the Cape May Peninsula (Wood and Herlands 1997). Within Georgia, 405 nesting female terrapin mortalities were reported on the Tybee Island causeway between 2005 and 2007 (J. Gray, unpublished data), and 442 terrapin mortalities (99% nesting females) were documented on the Jekyll Island causeway between 2007 and 2008 (T. Norton, unpublished data). Our study included three creeks within 30 m of a high traffic road including one along the Tybee Island causeway and one along the Jekyll Island
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causeway. Terrapin density estimates in all three creeks were below the median value among all sites. We believe it is likely that road mortality is having localized effects along causeways in coastal Georgia. We also must acknowledge that several factors may have limited our ability to measure any general impact of roads on terrapin populations. The amount of roads in proximity to creeks can include many driveways and low traffic streets in dense residential areas that pose little risk of vehicle mortality to turtles. This is the case for the two most dense terrapin populations we documented. Although these sites were among the highest for road density, the area is highly residential and most of the area that constituted roads posed no realistic risk to terrapins. Determining the distance to the most relevant road requires a subjective criteria as to whether a road is biologically relevant, in most cases without any information about whether female terrapins nest near that road. Further, we used straight-line distances from creeks to roads. We do not know whether terrapins make straight-line, over-marsh migrations to nest sites, or whether they swim along creeks until they near nesting areas. So, straight-line distances may not reflect actual migration distance. Finally, other studies show that traffic volume and speed play a large role in how roads effect wildlife populations (Rosen and Lowe, 1994; Fahrig et al., 1995; Forman, 2000; Trombulak and Frissell, 2000). AADT data was not available for the majority of our study sites, and for others the available data reflect an annual average. Because many of the roads are used to reach coastal beaches, traffic volume is likely high during the summer and low during the remaining nine months. Terrapins nest from mid-May through mid-July, which coincides with peak traffic volumes. Measures of traffic levels during this period might provide a better metric for evaluating road impacts on terrapin populations. Contrary to expectation, we failed to find evidence that road density or proximity or crabbing effort was associated with variation in terrapin sex ratio. Because females migrate out of the water to nest, road mortality has been consistently documented to be higher among adult female turtles (Gibbs and Shriver, 2002; Gibbs and Steen, 2005; Szerlag and McRobert 2006). Consequently, turtle populations in areas of high road density or greater road proximity are often more male biased than populations in areas that are more distant from or have fewer roads (Steen et al. 2006). Our own observations on terrapin road mortality showed vehicular mortality was biased toward adult female terrapins; however, we found no correlation between road density or proximity and terrapin sex ratios. Tucker et al. (2001) suggest that females may have a slightly lower natural survival rate due to their increased vulnerability during nesting migrations (i.e. high risk of boat strikes, predators). Therefore, vehicular mortality may be replacing other natural or anthropogenic sources of mortality and not lead to a measurably large shift in terrapin population sex ratio. The absence of an effect on sex ratio may also be further evidence that terrapin road mortality rates are not yet sufficient in coastal Georgia to have affected terrapin abundance or sex ratio. Finally, other factors that affect sex-specific mortality or “births” may be compensating for road mortality effects on terrapin sex ratio. We did not find road proximity or density interacted with crabbing activity to affect sex ratio, indicating the lack of road effects was not a product of compensatory mortality by male terrapins in crab pots. Terrapins do exhibit temperature-dependent sex determination (Roosenburg and Kelley 1996), and features of roads such as less vegetation by roadsides might result in warming nest temperatures and the biased production of females.
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Management Recommendations Diamondback terrapins are state listed as an S3 (rare or uncommon) species in Georgia. Our research suggests that terrapins occupy a large proportion of shallow tidal creeks in Georgia, with densities comparable to some creeks monitored long-term in South Carolina. That said, current densities in those South Carolina tidal creeks are known to have declined by 50% since the late 1980s (Dorcas et al. 2007), and our results suggest that the same human activities negatively affecting terrapin populations in other parts of its range, particularly commercial crab fisheries, are affecting terrapin abundance along Georgia’s coast. Our conclusion is that terrapins in Georgia are relatively widespread and at least moderately abundant with some areas of notably high densities, such that Georgia has the opportunity to act to preserve its robust terrapin populations and alleviate the negative effects of human activities on other populations. Georgia is in a position to avoid the common pitfall of waiting to manage a species before its population status within the state becomes critical. Though evidence for the negative effects of crabbing on terrapin populations is documented and generally known within the wildlife management community, crabbing is not explicitly identified as a potential factor affecting the conservation of terrapins in Georgia. Our study suggests that crabbing is a significant factor influencing the abundance of the species along coastal Georgia. Commercial crabbing is an important industry to the communities of coastal Georgia, so effective management must find suitable ways to minimize the impact of this industry on terrapin populations. We know some of the factors that determine whether a particular crab pot poses a significant risk to terrapins. When wire crab pots were introduced to commercial crab fisheries in the 1930s, early testing demonstrated significant numbers of terrapins captured in pots placed in shallow waters from April through June (Davis 1942). This time period coincides with peak activity of terrapins in the water in shallow tidal creeks. In South Carolina, Bishop (1983) reports 93% of terrapins caught in commercial crabbing gear were caught in shallow creeks during April, May and June and primarily in wire pots. Bishop (1983) also found that “peeler pots” [standard wire crab traps using live male blue crabs as bait to capture molting “soft shell” female crabs] captured higher numbers of adult terrapins than wire pots baited with fish. Hart (2005) noted that pots placed in shallow waters close to shore in April and May capture more terrapins, and she raised concern that peeler pots, which tend be fished in shallow waters in the spring may present a particular risk to terrapins. Our observations are consistent with those reported in earlier studies. The crab pots that we observed killing large numbers of terrapins were generally located far up in shallow tidal creeks that were only accessible by boat at high tide and were more likely to be neglected as evidenced by the growth of epibenthos and partial burial (Fig. 1). Restriction on where crab pots may be placed, at least between April and June, could significantly reduce terrapin mortality. We also concur with other studies that conclude that crab pots that are over-soaked, neglected, abandoned, or lost pose the greatest risk to terrapin populations. Currently, Georgia has no regulation limiting soak times for commercial crab pots (Code of Georgia, 2009). When wire crab pots are checked daily, only 10% of captured terrapins drown (Bishop, 1983; Roosenburg et al. 1997). The proportion of terrapins found dead in crab pots increases to 40% if pots are checked every 1-2 days (Hart, 2005), and we found nearly 100% mortality in pots
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visibly neglected for long periods of time. Therefore, a defined and enforced short soak time for crab pots could reduce the bycatch mortality of terrapins by up to 90% and should be a regulatory priority in GA. Furthermore, efforts to clean up abandoned or lost pots, and education and enforcement about the responsible recreational use of commercial crab pots would be meritorious conservation actions. Georgia could require bycatch reduction devices (BRDs) on commercial crab pots, particularly those fished in shallow waters, as another mechanism to reduce terrapin mortality rates due to crabbing. We are aware of 12 studies published in peer-reviewed journals, theses or the gray literature addressing the effectiveness of BRDs on reduction of terrapin capture rates and on blue crab capture numbers and sizes (see Hart 2005 for most recent review). Generally, all these studies tested rectangular wire or plastic frames placed across the larger circular openings of standard commercial wire crab pots. BRD dimensions range from 4-5 cm X 8-12 cm. Nearly all studies found a reduction of terrapin capture numbers in crab pots modified with BRDs. A few studies reported minor reductions in blue crab size or numbers for the smallest BRDs, of 4-4.5 cm narrowest dimension; however, these reductions were relatively negligible and not consistently observed. Further, several studies using slightly larger BRDs report increased numbers of crabs in modified pots; however, these larger BRD pots occasionally still capture terrapins. Hart (2005) modeled the potential effect of BRD reductions for small BRDs that may reduce blue crab harvest and large BRDs that still capture smaller terrapins but have no negative effect on blue crab catch. Those estimates suggest that small BRDs could increase terrapin population growth rates () by 18-22% and large BRDs could increase population growth rates by 11-13%. Finally, Georgia could designate areas of high conservation value for terrapins. We identified several areas such as the marshes west of Sea Island, GA and Saint Simons Island, GA where terrapin densities are in excess of 500 terrapins per kilometer (Fig. 8). These areas are relatively shallow with limited boat access, and are used primarily for recreational fishing and kayaking. We were told that occasionally there are oyster and bait harvests in those estuaries, but we did not observe this during our study. The uplands are well-developed residential areas, which may limit the potential for high-volume road traffic around nesting areas. Because such areas have high densities of terrapins, are currently free of crabbing activity, and have little road build-out potential, regulation of other harvest activities in these estuaries could maintain their conservation value.
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Figure 8. Estimated terrapin density (terrapins per km) at study sites along coastal Georgia. Crab pot density (pots per km) is provided for reference.
Without prior estimates of terrapin abundance, we cannot know whether populations in Georgia are stable, have increased or declined. This illustrates the need to establish regular monitoring of terrapin populations. Harden et al. (2009) propose that head counts would work as a less resource-intensive method for tracking the relative abundance of terrapins. They report a positive relationship (r = 0.733) between the numbers of heads counted at low tide compared to the number captured by seining. Harden et al. (2009) could not provide an analysis of whether head counts corresponded well with estimated terrapin abundance. We used 17 sampling
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occasions in 2008 to evaluate the potential for using head counts to estimate terrapin capture numbers and estimated abundance. We found a stronger correlation between numbers of heads counted at low tide and numbers of terrapins captured in seines, and a positive correlation between head counts and estimated terrapin abundance; however, the results of Harden et al. (2009) and our analysis were heavily influenced by a small number of observations where large numbers of heads were counted in dense creeks. When we restricted our analysis to tidal creeks with < 200 terrapins/km, which represents >75% of the tidal creeks we studied in Georgia, then we failed to find a statistically significant correlation between terrapin head count and the number captured by seining, and the relationship between head count and estimated terrapin density was still statistically significant but relatively weak. Therefore, it is our opinion that head counts will be inadequate for monitoring terrapin population size among the majority of sites in coastal Georgia. An additional limitation on the utility of head counts is the need to conduct head count surveys at low tide. Harden et al. (2009) found significantly more terrapins were observed during head counts at low tide, and we observed similar patterns. During high tide, terrapins appear to disperse into the high marsh (personal observations). The need to conduct head counts at low tide limits the times when surveys can occur and limits boat access to many shallow creeks where terrapin abundances can be high. As an alternative to head counts, we suggest the potential to use the prevalence of a specialized terrapin parasite that occurs as external cysts on mud snails as a more effective means for monitoring terrapin abundance (see section on Supplemental and Future Research below).
Supplemental and Future Research Road mortality on causeways As we pointed out earlier, while we found no measurable relationships between road density or proximity and terrapin density among Georgia’s tidal creeks, there is ample evidence of terrapin mortality on coastal roads that bisect or closely parallel marshes. As an example, we noted that volunteer efforts at the Georgia Sea Turtle Center documented 442 adult terrapin mortalities (99% nesting females) on the Downing-Musgrove Causeway between 2007 and 2008 (T. Norton, unpublished data), and we estimated terrapin density in one creek adjacent to the DowningMusgrove Causeway was 63 terrapins/km, which is well below the median of 149 terrapins/km among all non-crabbing creeks, and around the 25% lower quartile of 63.4 terrapins/km among non-crabbing creeks. It is widely accepted that turtle populations cannot sustain high rates of adult female mortality (Heppell, 1998); so it is likely that road mortality is having localized effects in coastal areas including along causeways within Georgia. In collaboration with the Georgia Sea Turtle Center (Dr. Terry Norton, Ms. Michelle Kaylor, and Mr. Kerry Holcomb) and Savannah River Ecology Lab (Dr. Kurt Buhlmann, Dr. Tracey Tuberville, and Mr. Brian Crawford), we established a study to estimate the temporal and spatial patterns of terrapin mortality along the Downing-Musgrove Causeway, and to evaluate the use of man-made nesting habitats to reduce vehicle mortality. With funds partially supplied by this SWG, we monitored daily activity and mortality of terrapins on the causeway from late April through mid July 2009. We documented 295 adult female terrapins emerging onto the causeway, 165 of which were killed or injured (9 were rehabilitated and released) and 130 of
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which were captured alive, marked, and released. Though terrapins nest twice, we only recaptured (alive or dead) 11 turtles returning to the causeway. We found a strong pattern of terrapin emergence onto the causeway centered on the diurnal high tide (Fig. 9). Fifty-five percent of female terrapins were observed on the causeway between one hour before and two hours past the projected high tide (according to county tide charts). Seventy-three percent of female terrapins were observed on the causeway between two hours prior to and three hours after the projected diurnal high tide. We find these results encouraging as they show we can predict peak times when female terrapins are likely to be active on the causeway. These results should lead to more targeted management actions to reduce vehicle-related mortality on the causeway.
Figure 9. Number and cumulative percentage of female terrapins observed in 2009 on the Downing-Musgrove Causeway to Jekyll Island as a function of time relative to diurnal high tide as reported by county-level tide charts. Dark grey panel depicts three-hour window from one-hour before to two hours after predicted high tide when 55% of female terrapins were observed on the causeway. Lighter grey panel depicts five-hour window from two hours before to three hours after predicted high tide when 73% of female terrapins were observed on the causeway.
We are currently analyzing spatial patterns of mortality to identify whether particular areas of the causeway are hotspots of vehicle mortality: we are focusing on windbreak vegetation as a potential predictor of why terrapins cross the causeway in search of nesting habitat. In April 2009 we assisted the Georgia Sea Turtle Center in the construction of 12 manmade nest mounds along the causeway. Each mound is ~ 8 X 16 feet at the base with a 4 X 8 ft predator exclusion cage at the top (Fig. 10). We did observe some voluntary nesting activity on mounds in 2009, and we translocated eggs from females that nested too low in the marsh or in areas of high nest depredation to mounds. We are still determining how to evaluate the effectiveness of mounds at attracting female terrapins to nest and whether they will sufficiently deter road mortality.
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Figure 10. Upper panel: man-made nest mound with predator exclusion cage positioned in gap in windbreak along the Downing-Musgrove Causeway to Jekyll Island. Lower left panel: view of man-made nest mound from marsh showing proximity of causeway. Lower right panel: female diamondback terrapin positioned to crawl under access gap at base of predator exclusion cage on man-made nest mound.
Future research efforts (2010-2011) will focus on mark-recapture estimates of population sizes of terrapins in additional creeks parallel to the causeway and on radio-telemetry of adult females moving between the tidal creeks and nesting habitats. First, marking large numbers of 19
females prior to the first nesting event and tracking a subset of females will allow us to accurately estimate individual vehicle mortality rates for diamondback terrapins. This information can then be used to estimate the impact of vehicles on terrapin population growth (which we presume is negative) and model whether various levels of reduced vehicle mortality will be sufficient to stabilize populations or allow them to grow. Second, mark-recapture efforts work will serve as the initial phase of a long-term monitoring of sub populations along the causeway so we can evaluate the effects of vehicle mortality and any management interventions on terrapin population growth.
Terrapin parasites as population indicators As was noted earlier in our discussion of using head counts to monitor terrapin populations, a common challenge of monitoring animal populations in estuaries, particularly vertebrate populations, is the logistical and resource demands required to generate reasonable estimates of abundance. A novel and exciting approach is to use the prevalence of specialized parasites in intermediate hosts to track the composition and abundance of vertebrate populations. Briefly, many specialized parasites of vertebrates such as trematodes have a life stage within an intermediate host. In the ultimate vertebrate host, the parasites reproduce and are shed in the animal’s feces into the environment where they infect an intermediate host such as a snail. The parasite takes over the snail’s reproductive system, churning out large numbers of cercaria that often infect a secondary host such as a fish. The ultimate hosts consume the secondary hosts, thereby completing the parasites life cycle. Because the loss or decline of the secondary or ultimate host would disrupt this cycle, the prevalence of the parasite in the intermediate host is predicted to reflect the abundance of the secondary or ultimate host. Dr. Jeb Byers, Associate Professor in the University of Georgia’s Odum School of Ecology, has demonstrated the applicability of this concept by showing that prevalence of various trematode parasites in mud snails (Ilyanassa obsoleta) could predict the composition and abundance of marine fish assemblages in New Hampshire estuaries. Among the suite of parasitic trematodes that occur in mud snails is Pleurogonious malaclemys, which as the name implies infects diamondback terrapins. This trematode is somewhat unique in that rather than producing free-swimming larval cercaria that infect a secondary host, P. malaclemys cercaria settle on hard substrates such as the shells of other mud snails where they form metacercarial cysts (Fig. 11). This allows the parasite to be consumed by terrapins, which specialize on hardbodied estuarine prey such as crabs and snails.
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Figure 11. Right panel: close-up of mud snail (Ilyanassa obsoleta) operculum with Pleurogonious malaclemys metacercarial cysts (indicated by arrows). Right panel: close-up (20X) of Pleurogonious malaclemys metacercarial cyst from a mud snail collected in a Georgia tidal creek.
Between August and October 2008, we sampled mud snails in 12 of the 29 creeks where we had conducted mark-recapture estimates of terrapin abundance. At each site, we collected 100 + mud snails evenly as they occurred along a 100 m section of creek we had sampled earlier for terrapins. Mud snails were placed into plastic containers containing creek water and transported to shore where they were placed in mesh bags and stored moist in fresh water. Later the same day, snail samples were shipped overnight for analysis at the University of New Hampshire. Snails were examined intact under a dissecting scope, and the number of metacercarial cysts on each snail was counted. Each snail was then placed in an individual container with water for 24 h, and then water samples were examined under a microscope to determine whether the snail had shed larval cercaria. This would indicate whether the snail’s gonads were infected by the parasite, or whether the snail simply had metacercaria outside its shell that it acquired from other infected snails. Finally, snails were dissected to confirm whether their gonads were infected.
Figure 12. Correlation between the proportion of mud snails (Ilyanassa obsoleta) with external Pleurogonious malaclemys metacercarial cysts and the density of diamondback terrapins (Malaclemys terrapin) estimated from mark-recapture during five seining events between April and June among 12 shallow tidal creeks along coastal Georgia.
We found a significant positive relationship between the prevalence of metacercarial cysts on mud snails and the estimated density of terrapins in the creek (N = 12, r = 0.663; Fig. 21
12). Forty-four percent of the variation in mud snail parasite prevalence was explained by terrapin density, which undoubtedly stems from the fact that the trematode must use the terrapin as its definitive host to complete its life cycle; thus, cyst and final host abundance are tightly coupled. Anecdotally, we add that we failed to detect P. malaclemys in tidal creeks where we determined terrapins were absent. We emphasize that the level of correlation reported here, although already strong, is conservative. We are completing multivariate modeling to incorporate other potential environmental influences on trematode abundance such as temperature and salinity. We expect these analyses will likely further enhance our ability to predict terrapin abundance at tidal creek sites throughout Georgia. Unlike head counts, which appear to provide strong predictive power of terrapin abundance when extreme values from a few dense sites are included but provide poor resolution among low density sites, the trematode cyst relationship is relatively consistent across narrower ranges of terrapin densities. We find the correlation of trematode cysts and terrapin abundance particularly exciting, and suggest that trematode cyst prevalence on mud snails may be a more effective tool for rapid estimation and monitoring of terrapin abundance among a large number of sites. Further research could improve the value of trematode measures to predict terrapin abundance by understanding the mechanistic regulation of the parasite dynamics between turtle and snail populations. We believe this would be a fruitful area for future research investment.
Terrapin trophic and high-marsh ecology During the course of our mark-recapture study, we initiated a diet study of terrapins with Mr. Matt Erickson, an undergraduate at the time in the University of Georgia’s Warnell School of Forestry and Natural Resources. Consistent with reports throughout the literature, we observed that terrapin abundance in tidal creeks declined at high tide, later in the summer (after June), and that females had lower capture probabilities in tidal creeks compared to males and sub-adult females. We speculated that terrapins were moving into the higher marsh during high tide and later in the season to forage, and that fecal and stable isotope analyses would confirm the prevalence of high-marsh fauna in terrapin diets. Diet studies are an important part of natural history research because they can help identify an organism’s key resources, which provide information on habitat use and its functional role in the ecosystem. This is particularly useful for animals that are secretive or difficult to study, as is the case for terrapins. Terrapins have been documented consuming numerous species, both in captivity and in their natural environment. Food items recorded for wild terrapins include periwinkle snails (Littorina irrorata), salt marsh snails (Melampus bidentatus), fiddler crabs (Gelasimus spp., Uca spp.), marine annelids (Nereis irratabilis), mussels (Mytilus edulis), clams (Anomalocardia cuneimens), Atlantic silverside (Menidia menidia), and plant material, including Sargassum spp. and unidentified grass fragments (Bishop, 1983; Ernst and Barbour, 1972; Hay, 1892; Hurd et al., 1979; Middaugh, 1981). Further, in a study using only male terrapins, Davenport et al. reported a feeding strategy called “cropping” in which adults would approach medium-sized blue crabs (Callinectes sapidus) from the side or rear and take rear legs without killing the crabs (Davenport et al. 1992). Tucker et al. (1995) examined fecal samples from wild-caught terrapins in South Carolina and found periwinkle snails constituted 76-79% of their diet by volume. The remainder was made up of mud fiddler crabs (Uca pugnax), heavy marsh crabs (Sesarma 22
reticulatum), blue crabs (C. sapidus), barnacles (Balanus spp.), and clams (Polynesoda caroliniana). Tucker et al. (1995) also investigated food resource partitioning among three size classes and found small terrapins (head width < 20mm) specialized on small periwinkle snails (< 10mm), with large periwinkle snails (> 10mm), and clams being less important. Medium-sized terrapins (head width 20-30mm) also consumed mostly small periwinkle snails, but increased their consumption of large periwinkle snails, blue crabs, and fiddler crabs. Large terrapins (head width > 30mm) had even broader diets, including small and large periwinkle snails, blue crabs, mud crabs, and fiddler crabs. Due to the absence of mud snails (Ilyanassa obsoleta), which are abundant and more accessible to terrapins than periwinkle snails, Tucker et al. (1997) hypothesized that mud snails may not be suitable prey for terrapins. They tested the shell strength of mud snails in comparison with periwinkle snails, fiddler crabs, and blue crabs and found that the average shell strength of mud snails was twice that of periwinkle snails, three times that of fiddler crabs, and 1.3 times that of blue crabs. Tucker et al. (1997) suggest that it may be more efficient for terrapins to prey on periwinkle snails than small mud snails for the same handling effort. The conclusion that terrapins do not feed on mud snails is contradicted by the existence of the trematode parasite Pleurogonious malaclemys, which is a specialist parasite of terrapins that infects mud snails and encysts on their shells to be transmitted to terrapins through consumption. Further, we observed that captive terrapins, including small juveniles, will readily prey upon mud snails (personal observations). The differences in terrapin diets among studies likely reflect methodological differences. Traditional fecal-sample examination depends on the presence of hard, identifiable parts in samples. This approach may underrepresent the importance of softer-bodied prey in terrapin diets. It’s difficult to quantify the types and number of soft-bodied prey consumed without direct observation since the soft tissues are easily digestible and not typically found in feces. One method to identify the types of soft-bodied animals eaten is by analyzing terrapin tissues for stable isotopes, which is a more contemporary approach to studying diets and food web structure (Post 2002). Stable isotopes can be used to identify important prey because of different patterns of heavy isotope enrichment across trophic levels. Generally, 13C is used to identify likely food resources because 13C generally shifts < 1 ‰; therefore, predators tend to have a similar 13C as their prey (Gannes et al. 1997, 1998; Post 2002). 15N tends to shift more from prey to predator such that predators generally have a 15N 2-4 ‰ above their prey. We used traditional fecal sample analysis merged with stable isotope analysis to estimate terrapin diets in shallow tidal creeks along the Georgia coast and to determine whether diets shift as a function of turtle sex, size, and as a result of injury. In 2008, 69 terrapins collected during seining for population estimates were randomly chosen to sample feces. Upon capture, turtles were rinsed with creek water to remove most sediment and debris, and then placed in plastic bins with a small amount of creek water. Turtles were held in small, plastic bins for 30-45 min and allowed to defecate. The contents of the bins were then filtered, placed individually in labeled plastic bags, and frozen for storage. Prior to analyses, sediment and fine debris was removed by rinsing in a fine strainer. Strained samples were dried in an oven at 60˚C to a constant mass, and dry masses were recorded. We separated each sample into crab parts, snail parts, vegetation, and unidentifiable shell fragments, and each category was weighed. All intact snail opercula, crab leg segments, and chelipeds were counted and measured. All length measurements were taken
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using a digital vernier caliper (Mitutoyo). Items found through fecal analysis were classified to the lowest taxonomic resolution possible. To estimate the size of crabs and snails eaten, numerous reference specimens were collected. Reference crabs were weighed and measured for carapace length, width, leg segment length, and cheliped length. Reference snails were weighed and measured for shell length (apexspire) and operculum length. When intact chelipeds were present in samples, mass of that prey item was estimated based on linear regression of crab body mass to cheliped length. When intact opercula were present, mass of that prey item was estimated based on linear (for mud snails) or exponential (for periwinkles) regression of snail mass to opercula length. Fourteen terrapins held for fecal collection were randomly selected for stable isotope analysis. Claws were chosen as the tissue because clipping nails was a minimally invasive procedure, and avian and reptile claws have been shown to be moderate time scale diet integrators (Bearhop et al., 2003). To supplement turtle claw data, claws, tails, and hand lobes (soft tissue clipped from foot) were donated from 10 female terrapins freshly killed by vehicles along the Downing-Musgrove Causeway to Jekyll Island. Clipped nails, tails, and hand lobes were placed in labeled vials and frozen for storage. We opportunistically collected replicate samples of potential prey of terrapins while seining creeks and by targeted collections with high marsh zones. In total we collected multiple individuals of 16 potential prey species. All terrapin and potential prey samples for isotopic analysis were dried at 60°C to a constant mass, then milled to a fine powder. Milled samples were dried again at 60°C, and then analyzed at the Odum School of Ecology Stable Isotope Laboratory at the University of Georgia using continuous-flow isotope-ratio mass spectrometry (Thermo-Finnigan Delta V Isotope Ratio Mass Spectrometer (Bremen, Germany) coupled to a Carlo Erba CHN Combustion Analyzer via Thermo-Finnigan Conflo III Interface (Milan, Italy)). Stable isotope results are reported relative to PDB belemnite for 13C and relative to atmospheric N2 for 15N. Of the 69 terrapins held for fecal collection, 49 produced feces. One hundred percent of crab fragments were identified as Uca spp. Snail fragments were identified as periwinkle snails, mud snails, and salt-marsh snails (Melampus bidentatus). All sex and size classes of terrapins had similar proportions of crab (~40%-45%) and snail (~26%-30%) parts in their feces. Periwinkle snails were found in 87% of fecal samples and mud snails were found in 20% of fecal samples. Interestingly, both species were found together in only 7% of fecal samples, suggesting that a terrapin that fed on mud snails had limited access to periwinkle snails. When mud snails were present in the fecal sample, they were abundant (Mean = 82, SD = 77) compared to periwinkles (Mean = 9, SD = 13). Adult males (83%) and sub-adult females (17%) accounted for all fecal samples with mud snails. Ten of the 24 terrapins used for isotopic analysis were sampled using hand lobes and tails, as well as claws to determine how claw signatures correlated to signatures of other tissues. Average values for claws were similar to hand lobe and tail values. Both 15N and 13C values of terrapin claws were strongly correlated with tail and hand lobe tissues (Fig. 13). However, claws tended to be slightly depleted in both elements compared to the softer tissues (Fig. 13).
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Therefore, we would expect terrapin claw samples to be slightly less enriched in 15N (~1.52.50/00) compared to other tissues (2-3.50/00).
Figure 13. Correlations between claw and and tail and hand lobe tissue concentrations of 13C and 15N for 10 adult female diamondback terrapins. Black lines show 1:1 relationship, and red lines show linear correlation.
Isotopic signatures of 13C and 15N for all species are plotted in Figure 14. Terrapins had 13C values similar to smooth chord grass (Spartina alterniflora) suggesting they derive the most of their energy from the high-marsh food web and not marine sources within the estuary. This is consistent with our fecal analysis, which indicated the majority of terrapin prey were periwinkle snails and mud and sand fiddler crabs. However, there was an ontogenetic shift in stable isotope values with sub-adult female and male terrapins values between mud snails, which occur primarily on the mud flats within the marine zones of the estuary and high-marsh prey that occur within the Spartina. This is also consistent with the fecal analysis, which only found mud snails in male and sub-adult female terrapin feces, and our mark-recapture analysis, which showed that males and sub-adult females have a higher capture probability in the water at low tide than adult females. Consistent with previous studies using only fecal samples, we found that terrapins consumed primarily fiddler crabs and periwinkle snails. Stable isotope data generally confirm this since only snail species and fiddler crab species have the appropriate isotopic signatures to be terrapin prey and occur in terrapin fecal samples. Together, our stable isotope and fecal analysis suggest a strong reliance on high-marsh prey by terrapins, and a shift toward greater utilization of high-marsh fauna as prey by nesting adult female terrapins. These results counter some reports or characterizations of terrapins as obligate aquatic foragers. Mud and fiddler crabs and periwinkle snails tend to remain out of the water within the high marsh, migrating with the tide line or up vegetation stalks. They remain active under water only in a few centimeters of depth. The prevalence of these organisms in terrapin diets is more consistent with terrestrial feeding. Further, we feel the indication of an increasing reliance on high-marsh fauna indicates that nesting size female terrapins may spend more time in the high marsh, perhaps reflecting conservative movements between subsequent nesting events. This is consistent with seining data that shows lower capture probabilities for large females in tidal creeks during low tide (Grosse et al. unpublished data). If this hypothesis is correct, we may be underestimating the importance of the high-marsh habitats for adult female terrapins. Classically, it is thought that the high
25
marsh is important for very young terrapins. Shifts in terrapin habitat use and diet imply that the influence of terrapins on marsh ecosystems may differ with age structure or sex ratio of the population.
Figure 13. Stable isotope biplot of 13C and 15N values for diamondback terrapins (red symbols) and their potential prey items. Prey items with solid blue labels are species that both stable isotope and fecal sample analysis indicate are the most common prey in terrapin diets. Solid green labels are species that stable isotope and fecal analyses indicate are occasional prey in terrapin diets. Open blue symbols depict prey reported to be important for terrapins, but for which stable isotope and fecal analyses indicate are not consumed or are an insignificant resource for terrapins. Open green symbols are prey for which stable isotope data cannot exclude them from terrapin diets, but for which there is no fecal evidence that the species is consumed. Grey symbols are species that stable isotope and fecal analyses indicate are not consumed or are an insignificant resource for terrapins. The dashed lines bracket the range of 13C values we observed for Spartina alterniflora. Note that most terrapins, particularly adult females, have 13C values near to or fully contained within the S. alterniflora food web and directly above mud fiddler crabs, sand fiddler crabs, and periwinkle snails, which were the major constituents observed in fecal samples; however, sub-adult females and males are shifted from adult females between mud snails and mud fiddler crabs, sand fiddler crabs, and periwinkle snails.
Products, Deliverables, and Broader Impacts 1. Created GIS database of road densities and crabbing records for all coastal Georgia tidal creeks. 2. Generated mark-recapture data set for 29 shallow tidal creeks across coastal Georgia. 3. Collaborated with Dr. Terry Norton (Jekyll Island Sea Turtle Center) to collect blood samples from terrapins at multiple sites along coastal Georgia for a broader health assessment.
26
4. Established three additional lines of research and management beyond those defined in the original scope of work: Study of hot spots and hot moments of vehicle related terrapin mortality along the Downing Musgrove Causeway to Jekyll Island. Includes generation of population estimates of vehicle mortality rates for modeling impacts of vehicle mortality on population growth, and the evaluation of habitat management and potential use of man-made nesting habitat as conservation tool. Identification and measurement of potential to use trematode parasite prevalence on mud snails and as a low-cost, rapid assessment technique for estimating terrapin density among tidal creeks. Initiated studies of foraging and high-marsh ecology of terrapins that may better inform habitat use and needs for the species. 5. Participated in public outreach at 5th annual Nest Fest (Jekyll Island, GA) 6. Research was featured in: South Magazine, 2007 University of Georgia Research Magazine, Fall 2008 DNR Nongame e-news letter, 2008 7. Presented results of this study at 8 regional, national and international venues representing various constituencies of the academic and conservation fields. th 4 Symposium on the Ecology, Status, and Conservation of the Diamondback Terrapin in Millersville, MD Daniel B. Warnell School of Forestry and Natural Resources Graduate Student Symposium in Athens, GA Southeast Regional Diamondback Terrapin Working Group Meeting in Charleston, SC Southeastern Partners in Amphibian and Reptile Conservation Annual Meeting in Athens, GA Diamondback Terrapin Road Mortality Workshop at Jekyll Island, GA Joint Meeting of Ichthyologists and Herpetologists in Montreal, Canada
University of Georgia Herpetological Society Meeting in Athens, GA Ecological Society of America Annual Meeting, Albuquerque, NM 8. Generated one masters thesis (Andrew Michael Grosse, M.Sc. 2009. D. B. Warnell School of Forestry and Natural Resources, the Universrity of Georgia, Athens, GA), one senior thesis (Matthew Erickson, BNR. 2009. D. B. Warnell School of Forestry and Natural Resources, Universrity of Georgia, Athens, GA), and facilitated the start of a second masters thesis (Brian Crawford, M.Sc. in progress. D. B. Warnell School of Forestry and Natural Resources, the Universrity of Georgia, Athens, GA) to address vehicle mortality on the Downing-Musgrove Causeway. 9. Generated one publication with three additional manuscripts to be submitted by September 2009. Grosse, A. M., J. D. van Dijk, K. L. Holcomb, and J. C. Maerz. 2009. Diamondback terrapin mortality in crab pots in a Georgia tidal marsh. Chelonian Conservation and Biology 8:98-100.
27
Grosse, A. M., J. C. Maerz, J. A. Hepinstall-Cymerman, and M. E. Dorcas. Associations between road and crabbing pressures and diamondback terrapin abundance in Coastal Georgia. Journal of Widlife Management: in review. Grosse, A. M. and J. C. Maerz. Increased growth-rates among diamondback terrapins associated with commercial crabbing. Manuscripted prepared, journal to be determined. M. Erickson, J. C. Maerz, and A. M. Grosse. Diet analysis of diamondback terrapins along the Georgia coast. Manuscript in prep for Southeastern Naturalist.
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Harden, L. A., S. E. Pittman, J. W. Gibbons, and M. E. Dorcas. 2009. Development of a rapid-assessment technique for diamondback terrapin (Malaclemys terrapin) populations using head-count surveys. Applied Herpetology 6:237-245. Hart, K. M. 2005. Population biology of diamondback terrapins (Malaclemys terrapin): Defining and reducing threats across their geographic range. Ph.D. Dissertation. Duke University. Hay, O. P. 1892. Some Observations on the turtles of the genus Malaclemys. Proc. U.S. Nat. Mus. 15:379-384. Heppell, S. S. 1998. Application of life-history theory and population model analysis to turtle conservation. Copeia 1998;367-375. Hoyle, M. E., and J. W. Gibbons. 2000. Use of a marked population of diamondback terrapins (Malaclemys terrapin) to determine impacts of recreational crab pots. Chelonian Conservation and Biology 3:735-737. Hurd, L. E., G. W. Smedes, and T. A. Dean. 1979. An Ecological study of a natural population of diamondback terrapins (Malaclemys terrapin) in a Delaware Salt Marsh. Estuaries 2:28-33. Mazerolle, M. J., L. L. Bailey, W. L. Kendall, J. A. Royle, S. J. Converse, and J. D. Nichols. 2007. Making great leaps forward: Accounting for detectability in herpetological field studies. Journal of Herpetology 41:672-689. MacKenzie, D. I., and W. L. Kendall. 2002. How should detection probability be incorporated into estimates of relative abundance? Ecology 83:2387-2393. Middaugh, D. P. 1981. Reproductive Ecology and Spawning Periodicity of the Atlantic Silverside, Menidia menidia (Pisces: Antherinidae). Copeia 1981:766-776. Mitchell, J. C., Klemens, M. W. 2000. Primary and secondary effects of habitat alteration. In: Klemens, M. W. (Ed), Turtle Conservation. Smithsonian Institution Press, Washington and London, USA, pp. 5-32. Post, D. M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703-718. Riitters, K. H., and J. D. Wickham. 2003. How far to the nearest road? Frontiers in ecology and the environment 1:125-129. Rosen, P. C., and C. H. Lowe. 1994. Highway mortality of snakes in the Sonoran desert of southern Arizona. Biological Conservation 68: 143-148. Roosenburg, W. M., 2004. The impact of crab pot fisheries on terrapin (Malaclemys terrapin) populations: Where are we and where do we need to go? In: Swarth, C., Roosenburg, W. M., Kiviat, E. (Eds.), Conservation and Ecology of Turtles of the Mid-Atlantic Region: A Symposium, Salt Lake City, UT, pp. 23-30. Roosenburg, W. M., W. Cresko, M. Modesitte, and M.B. Robbins. 1997. Diamondback terrapin (Malaclemys terrapin) mortality in crab pots. Conservation Biology 11:1166-1172. Roosenburg, W. M., and J. P. Green. 2000. Impact of a bycatch reduction device on diamondback terrapin and blue crab capture in crab pots. Ecological Applications 10: 882-889. 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. 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, 27-37. Sexton, O. J. 1959. A method of estimating the age of painted turtles for use in demographic studies. Ecology 40, 716-718. Steen, D. A., M. J. Aresco, S. G. Beilke, B. W. Compton, E. P. Condon, C. K. Dodd Jr., H. Forrester, J. W. Gibbons, J. L. Greene, G. Johnson, T. A. Langen, M. J. Oldham, D. N. Oxier, R. A. Saumure, F. W. Schuler, J. M. Sleeman, L. L. Smith, J. K. Tucker, and J. P. Gibbs. 2006. Relative vulnerability of female turtles to road mortality. Animal Conservation 9:269-273. Szerlag-Egger, S., and S. P. McRobert. 2007. Northern diamondback terrapin occurrence, movement, and nesting activity along a salt marsh access road. Chelonian Conservation and Biology 6: 295-301. Szerlag, S., and S. P. McRobert. 2006. Road occurrence and mortality of the northern diamondback terrapin. Applied Herpetology 3:27-37. Thompson, K., and A. Jones. 1999. Human population density and prediction of local plant extinction in Britain. Conservation Biology 13:185-189. Trombulak, S. C., and C. A. Frissell. 2000. Review of ecological effects of roads on terrestrial and aquatic communities. Conservation Biology 14, 18-30. Tucker, A. D., N. N. Fitzsimmons and J. W. Gibbons. 1995. Resource Partitioning by the Estuarine Turtle Malaclemys terrapin: Trophic, Spatial, and Temporal Foraging Constraints. Herpetologica 51:167-181.
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Tucker, A. D., J. W. Gibbons, and J. L .Greene. 2001. Estimates of adult survival and migration of diamondback terrapins: conservation insight from local extirpation within a metapopulation. Canadian Journal of Zoology 79:2199-2209. Tucker, A. D., S. R. Yeomans and J. W. Gibbons. 1997. Shell Strength of Mud Snails (Ilyanassa obsolete) May Deter Foraging by Diamondback Terrapins (Malaclemys terrapin). American Midland Naturalist 138:224-229. Venier, L., and L. Fahrig. 1996. Habitat availability causes the species abundance-distribution relationship. Oikos 76: 564-570. White, G.C., and K. P. Burnham. 1999. Program MARK: Survival estimation from populations of marked animals. Bird Study 46:120-138. Wood, R. C. 1997. The impact of commercial crab traps on northern diamondback terrapins, Malaclemys terrapin terrapin. In: Van Abbema, J. (Ed.), Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles--An International Conference. New York Turtle and Tortoise Society, New York, USA. Pp. 21-27. Wood, R. C., and R. Herlands. 1997. Turtles and tires: The impact of road kills on northern diamondback terrapin, Malaclemys terrapin terrapin, populations on the Cape May Peninsula, southern New Jersey, USA. In: Van Abbema, J. (Ed.), Proceedings: Conservation, Restoration, and Management of Tortoises and Turtles--An International Conference, Purchase, NY, pp. 46-53.
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APPENDICES APPENDIX A. Summary data including latitude/longitude for each tidal creek, total captures by sex and corresponding Mean Plastron Length (PL), Standard Deviation (SD) and Range. Creek
Coordinates
Total Males
Mean PL
SD
Range
Total Females
Mean PL
SD
Range
4
32° 0'36.51"N
80°56'26.56"W
40
105.8
4.95
92-116
7
149.5
26.54
98-167
6
31°59'32.79"N
80°56'22.74"W
47
103.9
4.01
94-112
8
143.6
16.74
117-166
7
32° 2'37.88"N
80°57'53.74"W
21
95.7
5.10
85-103
11
136.7
26.69
94-169
9
32° 2'32.93"N
80°59'15.15"W
36
99.2
6.83
83-116
4
112.3
31.49
87-157
11
32° 1'9.96"N
81° 1'7.53"W
17
99.9
5.16
90-108
4
127.4
34.91
95-170
12
32° 0'55.05"N
81° 0'47.85"W
14
104.4
4.45
98-111
4
167.0
8.12
159-174
13
32° 0'35.91"N
81° 1'9.39"W
0
16
31°57'7.26"N
81° 5'2.61"W
5
105.2
2.28
103-108
3
170.3
3.06
167-173
21
31°50'33.16"N
81° 8'46.23"W
8
104.6
6.86
90-111
4
150.5
45.56
89-187
37
31°47'47.84"N
81°17'3.51"W
16
102.8
5.10
96-116
6
133.6
29.23
95-161
39
31°46'24.38"N
81°15'56.15"W
19
103.3
5.69
92-116
6
157.7
6.62
148-166
45
31°42'49.11"N
81°13'53.50"W
6
109.1
7.63
100-117
0
48
31°40'43.16"N
81°18'35.80"W
0
52
31°33'40.62"N
81°13'1.93"W
24
105.2
4.25
97-113
144.2
34.89
88-182
54
31°37'33.39"N
81°14'57.29"W
0
60
31°29'31.86"N
81°20'13.30"W
20
159.5
7.78
154-165
64
31°28'52.50"N
81°16'24.98"W
0
0
0 8 0 104.7
7.58
90-115
2 0
66
31°28'6.61"N
81°18'2.70"W
15
105.4
6.69
90-119
5
144.2
20.02
119-165
70
31°27'9.46"N
81°19'44.15"W
23
106.1
7.42
91-120
2
154.0
9.90
147-161
91
31°13'34.07"N
81°24'57.00"W
37
103.5
6.83
86-113
6
144.5
28.77
95-170
93
31°11'46.44"N
81°25'45.29"W
163
98.7
5.99
83-114
41
122.6
23.45
86-179
97
31°11'16.78"N
81°21'0.61"W
156
101.1
8.36
82-176
40
142.0
22.12
101-175
98
31°10'31.27"N
81°22'9.07"W
223
97.3
5.34
72-111
103
135.1
22.61
82-166
100
31°10'33.01"N
81°26'36.56"W
42
99.5
7.12
81-115
21
136.6
28.39
95-190
102
31°10'4.86"N
81°27'2.36"W
10
104.1
4.98
97-111
8
145.8
27.87
106-172
109
31° 7'5.27"N
81°26'40.16"W
116
98.2
5.65
86-115
36
120.3
23.62
86-157
122
30°58'0.52"N
81°27'5.89"W
66
106.1
6.50
89-119
11
148.7
24.65
111-184
123
30°54'40.69"N
81°29'32.54"W
14
104.8
4.56
98-113
7
136.6
24.09
107-166
JC
31° 3'51.64"N
81°27'11.89"W
22
99.6
5.36
87-109
10
144.0
22.26
90-165
31
