The Influence of Maternal Size on the Eggs and Hatchlings of Loggerhead Sea Turtles
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1 SOUTHEASTERN Southeastern Naturalist NATURALIST Vol. 13(X): , No. X The Influence of Maternal Size on the Eggs and Hatchlings of Loggerhead Sea Turtles Anne Marie LeBlanc 1,*, David C. Rostal 1, K. Kristina Drake 1, Kristina L. Williams 2, Michael G. Frick 3, John Robinette 4, and Debra E. Barnard-Keinath 4 Abstract - Our study examined variation in and correlation of reproductive traits for a population of Caretta caretta (Loggerhead Sea Turtle) nesting in Georgia and compared the results with those of other studies. We assessed variability in reproductive traits (i.e., maternal length, clutch size, egg diameter, egg mass, hatchling length, and hatchling mass) on the population level and individual level. At the population level, we investigated interannual and intraseasonal variation of these traits for 810 Loggerhead Sea Turtle nests in Georgia, on Wassaw National Wildlife Refuge (NWR) and Blackbeard Island NWR during and , respectively. As the nesting season progressed, we observed a decrease in clutch size, mean egg diameter, mean egg mass per clutch, mean hatchling length per clutch, and mean hatchling mass per clutch. Further, we measured all previously mentioned traits on a subset of the female turtles encountered on the beach (n = 24) and used these data to examine the variability of the traits on the individual level. Generalized linear modeling using this more refined individual-level data set indicated that 55% of the variability in clutch size was explained by a combination of maternal length (47%) and hatchling length (8%). This model suggested that clutch size was positively related with maternal length (t = 4.79) and negatively related with hatchling length (t = -1.90). Greater maternal length resulted in larger clutch size, but not larger egg size; thus, egg size was relatively constant irrespective of maternal length. These results support optimal egg-size theory, indicating a trade-off between clutch size and hatchling size to produce the optimum maternal investment per offspring. Introduction Caretta caretta L. (Loggerhead Sea Turtle) is a circumtropical species (Bolten 2003, Dodd 1988), and its presence in multiple marine environments provides a model to investigate geographic differences in reproductive characteristics (Tiwari and Bjorndal 2000, Van Buskirk and Crowder 1994). Previous research has suggested that the reproductive ecology of Loggerhead Sea Turtles varies among geographic nesting assemblages as a result of behavioral, morphological, physiological, or dietary differences among widely separated populations (reviewed by Broderick et al. 2003, Stokes et al. 2006). However, whether such differences exist 1 Department of Biology, Georgia Southern University, PO Box 8042, Statesboro, GA Caretta Research Project, PO Box 9841, Savannah, GA Archie Carr Center for Sea Turtle Research, Department of Biology, University of Florida, Gainesville, FL US Fish and Wildlife Service, Savannah Coastal Office-Wassaw and Tybee National Wildlife Refuges, 1000 Business Center Drive, Suite 10, Savannah, GA * Corresponding author - annemarielbeich@gmail.com. Manuscript Editor: Ray Carthy and Glen Mittelhauser 1
2 within the same population is unknown due to the difficulty in intercepting individual turtles for every nesting event within a season (Schroeder et al. 2003). Optimal egg-size theory predicts that, in a given environment, there is an optimal amount of maternal investment per offspring that results in the maximum level of maternal fitness apart from maternal body size (Smith and Fretwell 1974). This theory leads to a maternal energy trade-off between clutch size and offspring size, regardless of maternal body size, resulting in optimum maternal fitness (Smith and Fretwell 1974). However, physical constraints have also been reported to affect egg size. For example, the relationship between egg size and clutch size reported in two freshwater turtle species did not conform to optimal egg-size theory because the pelvic-aperture width limited maximum egg size (Congdon and Gibbons 1987). The optimal egg-size theory assumes that increased energy expenditure per individual will result in larger offspring with increased fitness, and that maternal reproductive capacity is limited, either due to space or available energy resources (Smith and Fretwell 1974). Optimal egg-size theory predicts that allocation to individual offspring occurs relatively evenly within clutches (Wilkinson and Gibbons 2005). Previous studies have surmised that reproductive variation should manifest in clutch size (Rollinson and Brooks 2008), and numerous studies have examined reproductive variation in freshwater turtles (Congdon and Gibbons 1987, Congdon and van Loben Sels 1993, Congdon et al. 1994, Janzen et al. 2009). We examined variation in and correlation of reproductive traits for a population of Loggerhead Sea Turtles nesting in Georgia and compared our results with those of other studies. We investigated reproductive traits (maternal length, clutch size, egg diameter, egg mass, hatchling length, and hatchling mass) from Loggerhead Sea Turtles nesting north of Florida a population currently in decline and for which information regarding their reproductive ecology is lacking (TEWG 2000). We investigated these reproductive traits at the population level and at the individual level to determine from an evolutionary perspective which of them was being selected for. We also tested optimal egg-size theory and predicted that we would find a trade-off between clutch size and hatchling size. Field-Site Description We conducted this study on two barrier islands: Wassaw National Wildlife Refuge (WI), off the coast of Richmond Hill, GA (31 87'N, 80 97'W), and Blackbeard Island National Wildlife Refuge (BBI), off the coast of Valona, GA (31 30'N, 81 12'W). Female Loggerhead Sea Turtles use both of these barrier islands for egg deposition from mid-may until early August, and eggs hatch from late June until early October (Williams and Frick 2000). Both islands experience high daily tidal fluctuations (sometimes >2.4 m), and are largely composed of Holocene deposits derived from adjacent riverine systems and the continental shelf (Johnson et al. 1974). Historically, the highest nesting density of Loggerhead Sea Turtles on the Georgia coast occurred on BBI, where Loggerhead Sea Turtle nest-protection programs have been in place since 1965 (Dodd and MacKinnon 2003). WI is among the few islands along the Georgia coast experiencing an increase in Loggerhead Sea 2
3 Turtle nesting activity since monitoring and nest protection began in 1973 (Dodd and MacKinnon 2003). Methods Population-level data We conducted nightly patrols on WI ( ) and BBI ( ) throughout the nesting season. We tagged, measured, and monitored nesting females for return nesting events. We identified individual females using an inconel front-flipper tag [MANUFACTURER, LOCATION] and a subcutaneous passive integrated transponder (PIT) tag [MANUFACTURER, LOCATION] in the front right flipper. For each nesting female, we recorded the curved carapace length (CCL) from nuchal notch to the tip of the posterior marginal. We relocated nests that were deposited in areas with a high probability (>80%) of seawater inundation to higher parts of the beach to prevent nest loss, according to United States Fish and Wildlife Service (USFWS) protocol on WI and BBI (as discussed in National Marine Fisheries Service and USFWS 2008). Relocation occurred within 6 hours after egg deposition to reduce the possibility of movementinduced mortality (Limpus et al. 1979). As a predator deterrent, we covered all nests with wire screens for the duration of their incubation. Tuttle and Rostal (2010) found that relocated and in situ nest temperatures were not significantly different and thus, we combined data from relocated and in situ nests for our analyses. We measured clutch sizes for all relocated nests (n = 582) when they were transferred to their new locations. Maximum egg width and egg mass were measured from a subset of 20 eggs per clutch for many of the relocated nests (n = 203 and n = 37 nests, respectively); all eggs were brushed free of sand prior to measurement using dial calipers or a digital scale. We determined clutch sizes for nests that were left in situ (n = 228) by counting the number of eggshells left in the nest chamber after hatchling emergence; any eggshell that constituted >50% of an egg was counted (Broderick et al. 2003, Dodd and Mackinnon 2003). Following hatching, a subset of 20 hatchlings (n = 82 nests) was brushed free of sand and measured using dial calipers. We measured the straight carapace length (SCL) from the nuchal notch to the supracaudal notch for each hatchling. Hatchlings were also weighed using a Pesola spring scale in 2000 and a digital scale from 2001 to Individual-level data For a subset (n = 24) of the nesting female Loggerhead Sea Turtles encountered, we measured all variables (maternal length, clutch size, egg diameter, egg mass, hatchling length, and hatchling mass) for the same nest. We used this data set in further analyses to examine individual variation of reproductive variables, as described below. Data analysis Population-level data. We report averages as means (± SE). For all tests, we defined significance as α We tested the assumptions of normal distribution 3
4 and equal variances prior to performing analysis of variance (ANOVA) and linear regressions. If the assumption of a normal distribution was not met, we employed the nonparametric Spearman s signed ranks test. We calculated hatching success as the number of hatched eggs divided by the total clutch size. If multiple clutches were observed for a single female, we averaged the reproductive metrics measured and used the means in our analyses. For nests where the female could not be identified, we assigned a unique identifier so that each unknown was treated as a unique individual. For turtles that had multiple nest-times per year, each individual nesting female s length, clutch sizes, egg sizes, and hatchling sizes were averaged so that unequal weighting would not occur. We used an ANOVA to test for differences in mean maternal length, mean clutch size, mean egg diameter, mean hatchling length, hatch success, and the date of oviposition among years. We employed a t-test to examine differences in the dates of oviposition between the two islands surveyed. Combining the data from both islands studied, the relationship among the date of oviposition and mean clutch size, mean egg mass, mean hatchling length, mean hatchling mass, and mean hatch success was analyzed using parametric linear regression or, if necessary, nonparametric Spearman s signed ranks. We analyzed the relationship between the date of oviposition and mean egg diameter for each island using nonparametric Spearman s signed ranks. For these analyses, the data were sorted by date of oviposition, and the daily mean for each measurement was used for analyses to prevent unequal weighting. To determine if there were any differences between the whole population data set and its subset describing individual variation, we used t-tests to detect differences in maternal CCL, clutch size, mean egg diameter, mean hatchling length, hatch success, and the Julian date of oviposition. Individual-level data. We examined variation of the same reproductive traits on the individual level. Analyses were performed on a subset of turtles (n = 24) from the 2003 nesting season on BBI for which we measured all variables (maternal length, clutch size, egg diameter, egg mass, hatchling length, and hatchling mass) for the same female/clutch. If multiple clutches were observed for a particular female, only data from the first observed nest were used for these analyses. We divided nesting events into early (Julian date of oviposition on or before day 171) and late season (Julian date of oviposition after day 171) categories. The data were analyzed using generalized linear modeling (Proc GLMSELECT, SAS v. 9.2; SAS Institute, Inc., Cary, NC) where the final model selection was determined by Schwarz bayesian information-criterion (SBC) statistics (Judge et al. 1985, Schwarz 1978, and described in SAS version 9.2). We tested 2 models with this dataset. The first model evaluated the impacts of multiple variables (e.g., season [early vs. late], maternal size, egg diameter, egg mass, hatchling length, and hatchling mass) upon clutch size. The second model evaluated the impacts of the same variables on hatchling length. We used JMP statistical software package version (2012, SAS), SYSTAT version 11, or SAS version 9.2 for all analyses. 4
5 Results Population-level data We tracked 301 nests on WI ( ) and 509 nests on BBI ( ), and measured reproductive traits on each (Table 1). We found no significant difference among years for maternal CCL (F 3, 345 = 1.481, P = 0.219), mean egg diameter per clutch (F 3, 130 = 2.307, P = 0.080), mean hatchling length per clutch (F 3, 62 = 0.645, P = 0.589), or hatch success (F 3, 445 = 0.644, P = 0.587). However, we did find a significant difference in annual clutch size (F 3, 433 = 2.628, P = 0.050), with 2003 clutches (mean clutch size = 119 eggs) significantly larger than 2001 and 2002 clutches (mean clutch size = 112 eggs for both years). We did not find any geographic variation in any of the measured reproductive traits, except egg diameter, where BBI egg diameter was significantly larger than WI egg diameter (t 1, 79 = , P = 0.011). We combined data from all years and both study sites for subsequent analyses unless otherwise noted. We observed 1 6 six nests per year for individual nesting females. For this population-level data set, the number of repeat samples per individual per year, as well as the data for all years and both islands sampled is provided in Table 1. For the 4-year study, the dates of oviposition ranged from 4 May to 19 August, with the median date falling on 20 June. We found no significant difference in the dates of oviposition between BBI and WI (t = , df = 628; P = 0.436) or among years sampled (F 3, 805 = 2.214, P = 0.085). We then examined each of the variables for seasonal variation. As date of oviposition increased, there was a decrease in clutch size (n = 94, R s 2 = ; P < 0.001), mean egg mass (df = 1, 20; R 2 = 0.253, P = 0.017), mean hatchling length (df = 1, 46; R 2 = 0.111; P = 0.021), and mean hatchling mass (df = 1, 19; R 2 = 0.256; P = 0.019). As Table 1. Summary data for the population-level and individual-level subsets used in this study. Population-level data was collected on Blackbeard Island (BBI; ) and Wassaw Island (WI; ). For each year ( ), each individual nesting female s length (CCL), clutch sizes, egg sizes (egg diameter data are separated by island), and hatchling sizes were averaged so that unequal weighting would not occur; the number of repeat samples per individual per year (n) are provided. Individual-level data were collected on BBI (2003); data are from individual nests (n = 24) laid throughout the duration of the study. Egg and hatchling sizes are expressed as means of each clutch measured. For each data set, the mean (± SE) and sample size (n) are provided for each variable measured. Population Number of repeat samples Individual level per individual per year level mean ± SE (n) mean ± SE (n) Date of oviposition ± 0.7 (809) na na na na na na ± 3.4 (24) Maternal length (cm) ± 0.3 (349) ± 1.1 (24) Clutch size ± 1.2 (437) ± 3.8 (24) Egg diameter (mm) BBI 41.8 ± 0.2 (84) ± 0.2 (24) WI 41.0 ± 0.3 (50) Egg mass (g) 39.1 ± 0.6 (30) ± 0.6 (24) Hatchling length (mm) 44.3 ± 0.2 (66) ± 0.2 (24) Hatchling mass (g) 18.7 ± 0.3 (28) ± 0.3 (24) 5
6 date of oviposition increased, there was a decrease in egg diameter on BBI (n = 64, R s 2 = ; P = 0.002) and on WI (n = 44, R s 2 = ; P = 0.005). Individual-level data We found no significant differences between the population-level data set and individual variation subset (Table 1) when comparing maternal length (t = 0.519, df = 25; P = 0.608), clutch size (t = , df = 26; P = 0.313), mean egg diameter (t = , df = 37; P = 0.371), mean hatchling length (t = 0.705, df = 51; P = 0.484), hatch success (t = , df = 26; P = 0.063), and Julian date of oviposition (t = , df = 25; P = 0.611). Because our analyses detected significant seasonal differences for the variables measured for the population-level data set, we examined variation of the same reproductive traits on the individual level using two generalized linear models to determine which of these traits varied the least and thus was being selected for, from an evolutionary perspective. The first model indicated that 54.8% of the variability in clutch size was explained by a combination of maternal size (47.0%; positive relation, t = 4.79) and hatchling length (7.7%; negative relation, t = -1.90). The second model indicated that 62.0% (positive relation, t = 5.99) of the variability in hatchling length was explained by hatchling mass. Discussion Overall, the values for the reproductive parameters we measured in this study were within the range of those measured for other studies conducted in the same location and around the world (for comparison to other studies see Table 2 and Supplemental File 1 [available online at suppl-files/s13-3-s975-leblanc-s1, and, for BioOne subscribers, at org/ /s975.s1.]; Baptistotte et al. 2003, Broderick et al. 2003, Dodd 1988, Table 2: Summary of Loggerhead Sea Turtle measurements from other studies conducted worldwide; (detailed data provided in Supplemental File 1,Tables 1 6 [available online at us/senaonline/suppl-files/s13-1-s975-leblanc-s1, and, for BioOne subscribers, at org/ /s975.s1]): range of mean maternal length (CCL), clutch size, egg diameter, egg mass, hatchling length (SCL), and hatchling mass. Sample size (n) provided for the range s minimum and maximum study. Only mean samples with n 10 were used; ranges were excluded. For comparison, population-level data from this study are shown for each individual nesting female s length (CCL), clutch sizes, egg sizes (egg diameter data are separated by island), and hatchling sizes. This study (population level) mean ± SE (n) 6 Range of mean measurements worldwide, (n) Maternal length, CCL (cm) ± 0.3 (349) 71.9 (11) (25) Clutch size ± 1.2 (437) 70.4 (128) 149 (26) Egg diameter (mm) Blackbeard Island 41.8 ± 0.2 (84) (23) 49.9 (260) Wassaw Island 41.0 ± 0.3 (50) Egg mass (g) 39.1 ± 0.6 (30) 20.3 (500) 42.0 (4840) Hatchling length (mm) 44.3 ± 0.2 (66) 40.0 (221) 45.8 (60) Hatchling mass (g) 18.7 ± 0.3 (28) 18.7 (28) 22.0 (58)
7 Ehrhart 1979, Ehrhart and Yoder 1978, Frazer and Richardson 1985a, Godley et al. 2001, Kamezaki 2003, Margaritoulis et al. 2003, Stoneburner 1980, Van Buskirk and Crowder 1994). The data are also comparable to historical data from that have been collected on WI as part of a long-term monitoring project (Williams and Frick 2000), and thus these morphological parameters have not varied over time. Seasonal variation We found significant seasonal variation in reproductive traits for Loggerhead Sea Turtles nesting in Georgia. In this study, mean values for all measured clutch, egg, and hatchling variables decreased later in the nesting season (i.e., as date of oviposition increased). Late-season clutch size decreases have also been reported in other freshwater turtles and sea turtles (reviewed by Wilkinson and Gibbons 2005). Wilkinson and Gibbons (2005) also reported a seasonal egg-size decrease in a freshwater turtle; however, the clutch-size decrease was only apparent in the last clutch. Seasonal variation in these traits may be due to reduced reproductive investment available for allocation in later clutches as maternal body fat reserves are depleted (Wilkinson and Gibbons 2005). The decrease in egg size later in the season may be related to reduced reproductive maternal investment or it could be related to the different environmental conditions experienced by eggs developing later in the season (e.g., colder mean temperatures, increased temperature variability, altered hydric environment; Wilkinson and Gibbons 2005). For the latter, this may be an adaptive explanation for temporal variation in optimal egg size (Rollinson and Brooks 2008). Drake (2001), who also worked at our study sites, found via ultrasound that there was little variation in yolk size across the season for multiple females, and that most variation in Loggerhead Sea Turtle egg size was the result of albumin deposited in the oviduct. Wallace et al. (2006) found that Dermochelys coriacea (Vandelli) (Leatherback) hatchling size was most correlated to yolk size and not the amount of albumin, which created the most variation in egg size. Seasonal variation has also been shown to affect growth rates in hatchling Loggerhead Sea Turtles, thus potentially enhancing survivability for faster-growing hatchlings from the earlier portion of the nesting season (Stokes et al. 2006). Relationships between reproductive parameters Our results support the optimal egg-size theory presented by Smith and Fretwell (1974). In this study, clutch size increased with increasing maternal length, which is expected since this has been observed in most sea and freshwater turtle species (e.g., for review see Rollinson and Brooks 2008, Tiwari and Bjorndal 2000). This trend has also been reported for Loggerhead Sea Turtles nesting in Greece (Hays and Speakman 1991), Cyprus (Broderick et al. 2003), and throughout the Mediterranean (Broderick and Godley 1996, reviewed by Margaritoulis et al. 2003), as well as for Leatherbacks nesting in Costa Rica (Price et al. 2004) and some freshwater turtle species (Wilkinson and Gibbons 2005). Larger female marine turtles can physically hold more eggs than smaller females (Broderick et al. 2003). Even though body size 7
8 may restrict clutch size due to turtles rigid body cavities, larger females still might produce small clutches due to resource limitation or other constraints (Gibbons et al. 1982). We found that 47% of the variation in clutch size was explained by maternal length, with larger females producing larger clutches than smaller females; 53% of the variation in clutch size was due to unknown factors. Similar trends have been reported in Georgia (Frazer and Richardson 1985a, b), Florida (Ehrhart 1995), Greece (Hays and Speakman 1991), Cyprus (Broderick et al. 2003), and Brazil (Baptistotte et al. 2003, Tiwari and Bjorndal 2000). In fact, positive correlations between these reproductive parameters (e.g., clutch size and egg size) and maternal body size have been reported for many turtle species (Bjorndal and Carr 1989, Hays et al. 1993, reviewed by Wilkinson and Gibbons 2005). Caldwell (1959) found a negative relationship between maternal length and egg diameter, but we found a positive linear relationship between maternal size and egg diameter. Using our model, egg size did not contribute a significant amount of variation to clutch size, indicating that this trait is conserved among Loggerhead Sea Turtles. In our study, the majority of the variability in clutch size was due to maternal size and hatchling size. Rollinson and Brooks (2008) reported that within individuals, clutch size varied more than mean egg mass across years. Indeed, many studies have found no relationship between egg size and maternal body size; examples include Hays and Speakman (1991) for Loggerhead Sea Turtles, Broderick et al. (2003) for Loggerhead Sea Turtles and Chelonia mydas L. (Green Sea Turtles), and Wilkinson and Gibbons (2005) reviewed studies on many species of freshwater turtles. The egg measurements we obtained were similar to those reported for other Loggerhead Sea Turtle populations around the world, suggesting that this trait may have significant evolutionary and physiological implications (i.e., egg size is under strong selection pressure). Tiwari and Bjorndal (2000) found that egg size decreased with increasing latitude when looking at turtles in the Atlantic and the Mediterranean. However, we observed the same range in egg size reported by Tiwari and Bjorndal (2000) throughout one season for turtles on BBI and WI. In fact, a cautionary note for researchers may be to maintain consistency in the time of season when the eggs are measured (i.e., sample early, mid-, or late season or sample the entire season) so that seasonal variation is not a factor when making statistical comparisons. A long-term study conducted by Rollinson and Brooks (2008) provides some support to the claim that a positive correlation between egg mass and maternal body size may exist in small-bodied turtles because of maternal physical constraints on egg size coupled with selection towards an optimum value (Congdon and Gibbons 1987, Smith and Fretwell 1974). Rollinson and Brooks (2008) hypothesized that egg size increases with female body size until females are large enough to produce eggs of an optimal size (reviewed by Rollinson and Brooks 2008), as found in our study with Loggerhead Sea Turtles. In this study, hatchling length explained 7.74% of the variability in clutch size, second to maternal size. Hatchling size increased with increasing maternal length but was negatively correlated with clutch size, indicating the trade-off between clutch size and hatchling size. A positive correlation between maternal size and 8
9 offspring size (even within a population) has also been reported by Fox and Czesak 2000 ( reviewed by Roff 1992) and Rollinson and Brooks (2008), while others have found no correlation (reviewed by Rollinson and Brooks 2008). In our study, over half of the variability in hatchling length was explained by hatchling mass. Positive correlations between egg size and hatchling size have been reported in numerous species, including several species of freshwater turtles (reviewed by Wilkinson and Gibbons 2005, Rollinson and Brooks 2008). Ecological, evolutionary, and physiological implications In summary, the nesting biology of Loggerhead Sea Turtles on WI and BBI in Georgia, is similar in many ways to that previously described for Loggerhead Sea Turtles in the southeastern US. Over half of the variability we saw in Loggerhead Sea Turtle clutch size was attributable to maternal length and hatchling length, while the other half of the variation was not explained in our models. In general, larger females produce larger clutches up to a point, but there also seems to be a trade-off between clutch size and hatchling size in this Loggerhead Sea Turtle population. We found that egg size did not contribute significantly to clutch-size determination. Therefore, it is conserved among females, and a certain size of egg is being selected. The results of this study agree with the findings of Wallace et al. (2007), who surmised that larger clutch sizes, rather than bigger eggs, are produced due to the high mortality at early life stages. There is further support for this theory in the results of modeling by Mazaris et al. (2005) to assess sea turtle population viability, which concluded that producing many hatchlings could make up for mortality in other life stages. However, increasing juvenile survivorship does not offset the loss of adults in turtle populations; adults represent the most important and critical life stage for conservation (Congdon et al. 1993, 1994). The results of many studies suggest that larger hatchlings may have increased fitness (Froese and Burghardt 1974, Janzen et al. 2000, Miller et al. 1987), especially in a resource-poor environment (Noriyuki et al. 2010); however, Congdon et al. (1999) was not able to detect any benefit of increased hatchling size. Rollinson and Brooks (2008) offered the hypothesis that larger females have more energy to allocate to reproduction and more space in which to hold their clutch. Larger females also dig deeper nests to hold larger clutches, thus their hatchlings must have greater energy reserves (i.e., better fitness) to emerge from a deeper nest cavity. Future research should focus on whether energy allocation per egg differs between smaller and larger Loggerhead Sea Turtles and if this translates into actual benefits in terms of maternal or hatchling fitness. Acknowledgments We thank the Caretta Research Project on Wassaw NWR and the USFWS Loggerhead Sea Turtle Program on Blackbeard Island NWR for providing personnel, equipment, and funding to conduct this project. We also thank David Veljacic, Robert Cail, Peter Range, Karen Pacheco, Darryl Woodard, Scott Gilge, Mark Dodd, and Adam Mackinnon, as well as USFWS interns (Alison Brady, Laura Csoboth, Neil McIntosh, and Jake Tuttle), and 9
10 Caretta Research Project volunteers. Logistical support was provided by Georgia Southern University, Statesboro, GA; USFWS; Georgia Department of Natural Resources, Atlanta, GA; and The University of Alabama at Birmingham. In addition, we thank Thane Wibbels and Susan Jewell for their review of this manuscript as well as Jessica Stephen and Nick Farmer for statistical assistance. Permits were provided by the Georgia Department of Natural Resources (29-WMB-02112), USFWS ( ; ), and Georgia Southern University IACUC. Additional funding was provided by Georgia Southern University Competitive Research Grants and Academic Excellence Award. Literature Cited Baptistotte, C., J.C.A Thomé, and K.A. Bjorndal Reproductive biology and conservation status of the Loggerhead Sea Turtle (Caretta caretta) in Espírito Santo State, Brazil. Chelonian Conservation and Biology 4(3): Bjorndal, K.A., and A. Carr Variation in clutch size and egg size in the Green Turtle nesting population at Tortuguero, Costa Rica. Herpetologica 45(2): Bolten, A.B The Loggerhead Sea Turtle: A most excellent fishe. Pp. 1 3, In A.B. Bolten and B.E. Witherington (Eds.). Loggerhead Sea Turtles. Smithsonian Books, Washington, DC. 352 pp. Broderick, A.C., and B.J. Godley Population and nesting ecology of the Green Turtle, Chelonia mydas, and the Loggerhead turtle, Caretta caretta, in northern Cyprus. Zoology in the Middle East 13: Broderick, A.C., F. Glen, B.J. Godley, and G.C. Hays Variation in reproductive output of marine turtles. Journal of Experimental Marine Biology and Ecology 288: Caldwell, D.K The Loggerhead Turtles of Cape Romain, South Carolina (abridged and annotated manuscript of W.P. Baldwin, Jr., and J.P. Loftin, Jr.). Bulletin of the Florida State Museum of Biological Sciences 4: Congdon, J.D., and J.W. Gibbons Morphological constraint on egg size: A challenge to optimal egg-size theory? Proceedings of the National Academy of Sciences USA 84(12): Congdon, J.D., and R.C. van Loben Sels Relationships of reproductive traits and body size with attainment of sexual maturity and age in Blanding s Turtles (Emydoidea blandingi). Journal of Evolutionary Biology 6(4): Congdon, J.D., A.E. Dunham, and R.C. van Loben Sels Delayed sexual maturity and demographics of Blanding s Turtles (Emydoidea blandingii): Implications for conservation and management of long-lived organisms. Conservation Biology 7(4): Congdon, J.D., A.E. Dunham, R.C. van Loben Sels Demographics of Common Snapping Turtles (Chelydra serpentina): Implications for conservation and management of long-lived organisms. Integrative and Comparative Biology 34(3): Congdon, J.D., R.D. Nagle, A.E. Dunham, C.W. Beck. O.M. Kinney, and S.R. Yeomans The relationship of body size to survivorship of hatchling Snapping Turtles (Chelydra serpentina): An evaluation of the bigger is better hypothesis. Oecologia 121: Dodd, C.K., Jr Synopsis of the biological data on the Loggerhead Sea Turtle, Caretta caretta (L.). US Department of the Interior Fish and Wildlife Service Biological Report 88 (14): Dodd, M.G., and A.H. Mackinnon Loggerhead Turtle (Caretta caretta) nesting in Georgia, Annual report submitted to US Fish and Wildlife Service for grant E-5-3 Coastal Endangered Species Management. [PROVIDE LOCATION] 46 pp. 10
11 Drake, K.K Reproductive parameters of nesting Caretta caretta on Georgia s barrier islands. M.Sc. Thesis. Georgia Southern University, Statesboro, GA. 110 pp. Ehrhart, L.M Reproductive characteristics and management potential of the sea turtle rookery at Canaveral National Seashore, Florida. Pp , In R.M. Linn (Ed.). Proceedings of the First Conference on Scientific Research in the National Parks, New Orleans, LA November Transactions and Proceedings Series-National Park Service, No. 5. National Park Service, US Government Printing Office, Washington, DC. Ehrhart, L.M A review of sea turtle reproduction. Pp , In K.A. Bjorndal (Ed.). Biology and Conservation of Sea Turtles. Revised edition. Smithsonian Institution Press, Washington, DC. 615 pp. Ehrhart, L.M., and R.G. Yoder Marine turtles of Merritt Island National Wildlife Refuge, Kennedy Space Center, Florida. Pp , In G.E. Henderson (Ed.). Proceedings of the Florida and Interregional Conference on Sea Turtles, July 1976, Jensen Beach, FL. Florida Marine Research Publications No. 33. [PROVIDE LOCATION] 66 pp. Fox, C.W., and M.E. Czesak Evolutionary ecology of progeny size in arthropods. Annual Review of Entomology 45: Frazer, N.B., and J.I. Richardson. 1985a. Annual variation in clutch size for Loggerhead Turtles, Caretta caretta, nesting at Little Cumberland Island, Georgia, USA. Herpetologica 41: Frazer, N.B., and J.I. Richardson. 1985b. Seasonal variation in clutch size for Loggerhead Turtles, Caretta caretta, nesting at Little Cumberland Island, Georgia, USA. Copeia 4: Froese, A.D., and G.M. Burghardt Food competition in captive juvenile Snapping Turtles, Chelydra serpentine. Animal Behavior 22: Gibbons J.W., J.L. Greene, and K.K. Patterson Variation in reproductive characteristics of aquatic turtles. Copeia 1982: Godley, B.J., A.C. Broderick, J.R. Downie, F. Glen, J.D. Houghton, I., Kirkwood, S. Reece, and G.C. Hays Thermal conditions in nests of Loggerhead Turtles: Further evidence suggesting female skewed sex ratios of hatchling production in the Mediterranean. Journal of Experimental Marine Biology and Ecology 263: Hays, G.C., and J.R. Speakman Reproductive investment and optimum clutch size of Loggerhead Sea Turtles (Caretta caretta). Journal of Animal Ecology 60: Hays, G.C., C.R. Adams, and J.R. Speakman Reproductive investment by Green Turtles nesting on Ascension Island. Canadian Journal of Zoology 7: Janzen, F.J., and D.A. Warner Parent offspring conflict and selection on egg size in turtles. Journal of Evolutionary Biology 22(11): Janzen, F.J., J.K. Tucker, and G.L. Paukstis Experimental analysis of an early lifehistory stage: Selection on size of hatchling turtles. Ecology 81: Johnson, A.S., H.O. Hillestad, S.F. Shanholtzer, and G.F. Shanholtzer An ecological survey of the coastal region of Georgia. US Department of the Interior, National Park Service Scientific Monograph Series No pp. Judge, G.G., W.E. Griffiths, R.C. Hill, H. Lutkepohl, and T.C. Lee The Theory and Practice of Econometrics, Second Edition. John Wiley and Sons, Inc., New York, NY. 793 pp. Kamezaki, N What is a Loggerhead Turtle? The morphological perspective. Pp , In A.B. Bolten and B.E. Witherington (Eds.). Loggerhead Sea Turtles. Smithsonian Institution Press, Washington, DC. 319 pp. 11
12 Limpus, C.J., V. Baker, and J.D. Miller Movement-induced mortality of Loggerhead eggs. Herpetologica 35: Margaritoulis, D., R. Argano, I. Baran, F. Bentivegna, M.N. Bradai, J.A. Camiñas, P. Casale, G. De Metrio, A. Demetropoulos, G. Gerosa, B.J. Godley, D.A. Haddoud, J. Houghton, L. Laurent, and B. Lazar Loggerhead Turtles in the Mediterranean Sea: Present knowledge and conservation perspectives. Pp , In A.B. Bolten and B.E. Witherington (Eds.). Loggerhead Sea Turtles. Smithsonian Books, Washington, DC. 352 pp. Mazaris, A.D., O. Fiksen, and Y.G. Matsinos Using an individual-based model for assessment of sea turtle population viability. Population Ecology 47: Miller, K., G.C. Packard, and M.J. Packard Hydric conditions during incubation influence locomotive performance of hatchling Snapping Turtles. Journal of Experimental Biology 127: National Marine Fisheries Service and US Fish and Wildlife Service Recovery plan for the northwest Atlantic population of Loggerhead Sea Turtle (Caretta caretta), Second Revision. National Marine Fisheries Service, Silver Spring, MD. 325 pp. Noriyuki, S., S. Kishi, and T. Nishada Seasonal variation of egg size and shape in Ypthima multistriata (Lepidoptera: Satyridae) in relation to maternal body size as a morphological constraint. Annals of Entomological Society of America 103(4): Price, E.R., B.P. Wallace, R.D. Reina, J.R. Spotila, F.V. Paladino, R. Piedra, and E. Vélez Size, growth, and reproductive output of adult female Leatherback Turtles, Dermochelys coriacea. Endangered Species Research 5:1 8. Roff, D.A The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York, NY. 535 pp. Rollinson, N., and R.J. Brooks Optimal offspring provisioning when egg size is constrained : A case study with the Painted Turtle, Chrysemys picta. Oikos 117: Schroeder, B.A., A.M. Foley, and D.A. Bagley Nesting patterns, reproductive migrations, and adult foraging areas of Loggerhead Turtles. Pp , In A.B. Bolten and B.E. Witherington (Eds.). Loggerhead Sea Turtles. Smithsonian Books, Washington, DC. 352 pp. Schwarz, G Estimating the dimension of a model. Annals of Statistics 6: Smith, C.C., and S.D. Fretwell The optimal balance between size and number of offspring. American Naturalist 108(962): Stokes, L., J. Wyneken, L.B. Crowder, and J. Marsh The influence of temporal and spatial origin on size and early growth rates in captive Loggerhead Sea Turtles (Caretta caretta) in the United States. Herpetological Conservation and Biology 1(2): Stoneburner, D.L Body depth: An indicator of morphological variation among nesting groups of adult Loggerhead Sea Turtles (Caretta caretta). Journal of Herpetology 14: Tiwari, M., and K.A. Bjorndal Variation in morphology and reproduction in the Loggerheads, Caretta caretta, nesting in the United States, Brazil, and Greece. Herpetologica 56(3): Turtle Expert Working Group (TEWG) Assessment update for the Kemp s Ridley and Loggerhead Sea Turtle populations in the western North Atlantic. NOAA Technical Memorandum NMFS-SEFSC-444. US Department of Commerce, National Marine Fisheries Service, Southeast Fisheries Science Center, Miami, FL. 115 pp. Tuttle, J., and D. Rostal Effects of nest relocation on nest temperature and embryonic development of Loggerhead Sea Turtles (Caretta caretta). Chelonian Conservation and Biology 9(1):
13 Van Buskirk, J., and L.B. Crowder Life-history variation in marine turtles. Copeia Wallace, B.P., P.R. Sotherland, P.S. Tomillo, S.S. Bouchard, R.D. Reina, J.R. Spotila, and F.V. Paladino Egg components, egg size, and hatchling size in Leatherback Turtles. Comparative Biochemistry and Physiology (Part A) 145: Wallace, B.P., P.R. Sotherland, P.S. Tomillo, R.D. Reina, J.R. Spotila, and F.V. Paladino Maternal investment in reproduction and its consequences in Leatherback Turtles. Oecologia 152 (1): Wilkinson, L.R., and J.W. Gibbons Patterns of reproductive allocation: Clutch and egg-size variation in three freshwater turtles. Copeia 4: Williams, K.L., and M.G. Frick Results from the long-term monitoring of nesting Loggerhead Sea Turtles (Caretta caretta) on Wassaw Island, Georgia: NOAA Technical Memorandum NMFS-SEFSC-446. US Department of Commerce, National Marine Fisheries Service, Southeast Fisheries Science Center, Miami, FL. 32 pp. 13
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