LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 1 of 13

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1 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 1 of FindArticles > Ecology > Sept, 1998 > Article > Print friendly Nest-site selection: microhabitat variation and its effects on the survival of turtle embryos Dawn S. Wilson INTRODUCTION Nest-site selection can be defined as the placement of eggs by females at sites that differ from random sites within a delimited area. Such behavior has been well documented in egg-laying amphibians, reptiles, and birds and may function as a means of protecting the embryos from predation pressures and/or environmental extremes (Joern and Jackson 1981, Becker and Erdelen 1982, Petranka 1990, Burger 1993). Schwarzkopf and Brooks (1987) hypothesized that the selected sites offer a greater chance of survival to the developing embryos than the nonselected sites; therefore, natural selection should favor the evolution of nest-site selection. Within reptiles, researchers have found that many species place their eggs at sites that differ from random (e.g., Malaclemys terrapin [Burger and Montevecchi 1975], Pituophis melanoleucus [Burger and Zappalorti 1986], Amblyrhynchus cristatus [Rauch 1988], Tropidurus spp. [Burger 1993]). The microhabitat surrounding the nest site has been shown to influence the thermal environment experienced by developing embryos of reptiles with temperature-dependent sex determination, and therefore the resulting sex ratio of the offspring (Bull and Vogt 1979, Wilhoft et al. 1983, Janzen 1994). Field incubation environments also have been shown to influence the future growth and survivorship of hatchlings exiting the nest cavity (Burger 1976a, Leshem and Dmi'el 1986, Cagle et al. 1993). No investigator, however, has tested whether survivorship to hatching of embryos oviposited at these nonrandom (selected) sites is higher than survivorship of embryos oviposited at random sites. Because many species that lay eggs exhibit postovipositional care of embryos (Shine 1988), teasing apart the benefits of postovipositional care (e.g., nest guarding, egg attendance, thermoregulation) for the developing offspring from the benefits of nest-site selection is difficult in these species. Postovipositional care is rare or absent in turtles. Female turtles walk to a terrestrial nesting site, deposit their eggs under some type of substrate, and leave their offspring to face the abiotic challenges associated with the specific microhabitat surrounding the nest site. Turtles, therefore, make good model organisms with which to test the hypothesized selective advantage of nest-site selection. Variables typically measured by researchers in studies of nest-site selection by aquatic turtles include distance from shoreline, elevation above the water level, slope of land, and density of overstory vegetation. Distance from the shoreline and elevation above the water level are variables most often measured in studies of beach- and sandbar-nesting species and relate to the likelihood of the nest flooding when water levels are high (Burger and Montevecchi 1975, Plummer 1976, Cox and Marion 1978, Ehrenfeld 1979). Slope of land and overstory density are variables most often associated with the incubation temperature of the eggs (Legler 1954, Schwarzkopf and Brooks 1987, Plummer et al. 1994). Vegetational cover immediately surrounding the nest site has been investigated for its role in predicting sex ratios of hatchling turtles (Janzen 1994); however, less attention has been given to its possible effects on embryo survival.

2 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 2 of 13 In this paper, I show how microhabitat characteristics of nest sites directly influence offspring survival of the freshwater turtle, Kinosternon baurii, in central Florida. Specifically, I tested two null hypotheses: (1) no differences exist between microhabitat characteristics at nest sites and random sites within the study area, and (2) no differences exist between rates of survival of embryos at nest sites and random sites. MATERIALS AND METHODS Study animal The striped mud turtle, Kinosternon baurii, is a small aquatic turtle that ranges throughout the southeastern United States and occupies a variety of freshwater habitats (Lamb and Lovich 1990). Mature females average 99 mm carapace length (CL) and may oviposit several clutches of one to six elliptical, brittle-shelled eggs from September to June (Iverson 1979). Because the development of embryos of K. baurii can be arrested over winter (embryonic diapause), striped mud turtle eggs may remain in the nest cavity for as long as 1 yr before completion of development (Ewert 1991, Ewert and Wilson 1996). The particular site where a female deposits her eggs may therefore have a profound effect on the development and subsequent survival of her offspring. Study area I conducted my research at the Ecological Research Area (Eco Area) of the University of South Florida (USF), Hillsborough County, Florida from September 1990 to September The Eco Area is a 200-ha tract of land composed predominantly of a riverine hardwood swamp forest ("wetland") bordering an isolated patch of xeric sandhill ("upland"). Gravid striped mud turtles exit the wetland and walk onto the upland to nest. Ground cover of the upland is composed of grasses (e.g., Aristida spp., Andropogon spp.) and a wide variety of herbaceous species with occasional open patches of bare ground. The overstory is dominated by turkey oak (Quercus laevis) and longleaf pine (Pinus palustris). Soils of the upland are well-drained yellow sand deposits of the Lakeland series (Mushinsky 1985). The upland portion of the Eco Area is subdivided into experimental plots that have been subjected to prescribed fires of varying frequencies (Mushinsky 1985). Potential nesting areas for striped mud turtles range from plots that have not been burned for [greater than]25 yr to plots that are burned annually. I restricted my study to plots with burn frequencies of 1, 2, 5, and 7 yr. Because the 1- and 2-yr and the 5- and 7-yr plots were similar in vegetation characteristics (percent ground and canopy cover), I combined these pairs of plots for analysis, and refer to them as "low canopy" (1- and 2-yr) and "medium canopy" (5- and 7-yr) plots. Sampling I intercepted gravid females as they traveled from the wetland to their upland nesting site with a 1490 m long drift fence that separated [approximately]80-90% of the upland from the wetland. The drift fence was made of 40 cm wide PVC siding buried 5 cm into the ground and supported by wooden stakes every 3-4 m. I buried 149 pitfall traps (11.3-L buckets) level to the ground every 10 m along both sides of the fence. Pitfall traps were numbered consecutively from 1 to 149 on each side of the fence (total 298 traps), allowing me to record capture locations for each female trapped at the drift fence. Because the nests of K. baurii often are cryptic and thus difficult to locate, I found it necessary to track females to their nest sites. I captured females in the early morning hours and brought them

3 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 3 of 13 back to the USF laboratory where each individual was fitted with a thread-bobbin tracking device which I attached to the rear of the carapace (Wilson 1994). Turtles equipped with thread bobbins were released within a few hours of capture on the upland side of the fence, near their original site of capture. I attached the free end of the thread-bobbin to vegetation, which allowed the thread to unwind as the turtle walked through the upland in search of a nest site. Late in the afternoon of the same day, I returned to the study area, followed the thread line, and marked the path walked by each turtle. I marked each nest that I found with a flag placed 1 m north of the center of the nest. I followed a random sample of females and observed their behavior while on the sandhill. I found that the majority of females tracked to their nest sites dug several false nests and spent time searching for a suitable nest site; therefore, I believe that handling of females prior to nesting did not adversely effect their nesting behavior. Microhabitat variables To test the null hypothesis that no differences existed between microhabitat characteristics at nest and random sites, I compared the distributions of microhabitat characteristics that I measured at each nest site to those measured at random sites. I located random sites by positioning myself on the firelane that ran beside each study plot and paced random distances across the plot until I had reached the other side, marking each randomly located site with a flag. I spaced my starting points on the firelane evenly apart (every 10 m) so that my sampling of random points would include the majority of the microhabitats present on each plot. Between 30 and 40 random sites were located on each plot, dependent on size of plot. I measured the vegetation structure (ground cover) immediately surrounding each nest and random site. I centered a one meter square grid on each site and visually estimated the percentage of bare ground, herbaceous plants, woody plants, and leaf litter that covered the area within the grid. I measured the distance to, and height of, the closest vegetation (herbaceous or woody). I obtained core samples of soil from a subsample of nest and random sites, directly adjacent to each site (so as not to disturb the nest) to determine soil water content. Core samples were taken to a depth of 5 cm, the average nest depth of striped mud turtles at this study site (Wilson, unpublished data). Because the amount of soil organics and soil texture may influence the ability of the soil to retain water, I also measured these two variables at both nest and random sites. To determine water content and organic content of each sample, I weighed soil samples, dried them at 60 [degrees] C for 24 h, reweighed them, combusted them in a muffle furnace at 550 [degrees] C for 5 h, and reweighed them. I measured soil water content at two different times of year: during winter, when the soil was relatively dry, and again during spring, when the soil was relatively wet. Using the Bouyoucos soil texture method (Bouyoucos 1962), I analyzed soil samples for percent composition of sand, silt, and clay particles. Experimental design To test the null hypothesis that no differences existed between survivorship of embryos at nest sites and random sites, I conducted a field experiment comparing embryonic development and survivorship between these two types of sites. From September through November 1994, I brought 75 gravid females that I had captured at the drift fence into the laboratory and placed each of them in a 20-L plastic bucket containing [approximately]10 cm of moist sand obtained from the study site. I injected the females with oxytocin to induce egg laying (Ewert 1979). Most females laid eggs within 3-4 h in the moist sand. I weighed and measured all eggs and placed them temporarily in moist vermiculite. Because striped mud turtles lay an average of three eggs (Iverson 1979), I grouped eggs into three-egg experimental clutches by randomly selecting eggs from the collection of 210 eggs until all eggs had been used, subject to the constraint that no clutch contained [greater

4 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 4 of 13 than]1 egg from the same female. I constructed experimental nests in the field by burying the threeegg clutches 5 cm deep at sites located in both low and medium canopy plots. Results of the nest placement part of my study indicated that females preferred to deposit eggs at sites close to, or underneath, clumps of grass or other herbaceous plants and not in areas of open, bare ground. I therefore placed experimental nests in one of two treatments: sites located 1-5 cm from ground cover ("covered") and sites located 3050 cm from ground cover ("open"). Covered sites had been used previously by a nesting female during the first 3 yr of the study, and open sites were located at randomly chosen sites in close proximity to previously used nest sites. Soil at covered sites retained no signs of previous nest contents or structure. My sample sizes were as follows: low canopy plots (12 covered and 19 open nest sites) and medium canopy plots (22 covered and 17 open nest sites). Because I found during the first two years of my study that natural rates of predation on nests were high, and my main interest was in comparing embryo survival between the two treatments, I protected nests from predators by enclosing them in wire cages. Nest cages ([approximately]30 cm height x 15 cm radius) consisted of hardware cloth formed into cylinders and closed at the bottom. Hardware cloth tops were attached to each cage with wire. Because nests located in both covered and open sites were enclosed with cages, I made the assumption that if the wire cages had any effect on the environment immediately surrounding the nest, the effect was the same for both treatments. To determine survivorship of embryos in the experimental nests, I periodically monitored embryonic development by "candling" the eggs in the field. To candle the eggs, I illuminated the egg contents using a small penlight while I sat in a mini darkroom constructed of large, black plastic bags. I recorded the date that the embryo broke embryonic diapause (resumed development) and the condition of each embryo. Eggs of Kinosternon baurii, like all other turtle eggs, are laid in a late gastrula stage (Ewert 1985); however, the embryos of K. baurii remain in this stage until developmental arrest is terminated by an external stimulus (i.e., winter chilling, Ewert 1991). I considered the embryo to have broken out of the gastrula stage and resumed development when I observed an elongation of the primitive plate. I recorded the condition of the embryo by observing the subsequent embryonic development using the staging of Yntema (1968). I considered an embryo dead when the air bubble inside the shell moved about freely within the egg. Eggs were opened to confirm death (I was 100% correct). Survivorship for each nest was scored as percent hatching (defined as pipping of the eggshell; Ewert 1979) of the total number of embryos in the nest (100, 66, 33, or 0%). Because striped mud turtles dig relatively shallow nests, I hypothesized that if differences in survival of embryos between the covered and open sites existed, then differences may be attributable to differences in nest temperatures. I measured soil temperatures in a small study plot at the Eco Area from 1 January 1994 to 15 August I buried temperature probes that were attached to a data logger (Campbell Scientific) at average nest depth at 12 sites (six covered and six open). Temperature data from mid-may to August were inadvertently lost and replacement temperature data were collected using portable data loggers (Hobo-Temps, Onset Computer, Pocasset, Massachusetts, USA) placed in two covered (C1, C2) and two open (O1, O2) nest sites in a medium canopy plot during Temperature readings were recorded at 30-min intervals. Temperature data were used solely for comparisons of soil temperatures between covered and open sites. My choice of the two experimental types of nest sites (covered vs. open) reflects differences that I observed in the microhabitat surrounding the nest and not overstory density. Because low and medium canopy plots have different burn histories, overstory density above the nest sites may also contribute to temperature differences between the two treatments. Therefore, I measured the overstory density above both covered and open nest sites in each plot using a spherical densiometer (Janzen 1994).

5 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 5 of 13 RESULTS Nest placement Tracking females with thread bobbins, I located 62 nest sites in the Eco Area. I measured microhabitat characteristics at 42 nest and 120 random sites in the low canopy plots and at 20 nest and 95 random sites in the medium canopy plots. Females placed their eggs at sites that differed in vegetation structure from random sites. I found no difference in percent herbaceous vegetation, percent woody vegetation, percent litter, or vegetation height between nest and random sites. However, for both low canopy (LC) and medium canopy (MC) plots, nest sites differed from random sites in distance from closest vegetation [Mann-Whitney U test] ([ILLUSTRATION FOR FIGURE 1 OMITTED]; LC: U = 3708, P [less than] 0.001; MC: U = 1366, P [less than] 0.01) and in percent bare ground ([ILLUSTRATION FOR FIGURE 2 OMITTED]; LC: U = 2935, P = 0.05; MC: U = 1478, P [less than] 0.01). In other words, females apparently were selecting sites that were close to vegetation (covered sites) and avoiding sites far from vegetation (open sites). Water content of the soil was significantly higher at nest sites than at random sites, both during the winter (Kruskal-Wallis one-tailed test: H = 14.6, n = 24 soil samples (12 at nest sites and 12 at random sites), P [less than] 0.001) and spring (H = 9.1, n = 30 soil samples (15 at each site type), P [less than] 0.003) sampling periods. No differences were found in organic composition (H = 0.001, n = 30 soil samples, P = 1.0), or in soil texture (all samples were composed of 97-99% sand with [less than]1% each of silt and clay) of soil samples taken at nest and random sites. Embryo development and survivorship Eggs of striped mud turtles are laid in the fall, remain in embryonic diapause throughout the winter months, and continue embryonic development when temperatures increase in the spring (Ewert and Wilson 1996). Eggs in nests located at open sites broke embryonic diapause and resumed development earlier in the spring than did those at covered sites ([ILLUSTRATION FOR FIGURE 3 OMITTED]; G = 32.73, df = 6, P [less than] 0.001). Because embryos located at open sites resumed development 1-2 mo earlier than embryos located at covered sites, and rates of development have been shown to be temperature dependent (Packard and Packard 1988), embryos at open sites should have completed their incubation period and hatched sooner than embryos at covered sites. Indeed, surviving embryos at open sites hatched from early August to late August, whereas surviving embryos at covered sites hatched from late August to late September. Nest survivorship was independent of plot (LC and MC) for both covered (G = 2.67, df = 3, P [greater than] 0.3) and open (G = 6.46, df = 3, P [greater than] 0.05) nest sites. Combining all plots, nest survivorship was not independent of treatment ([ILLUSTRATION FOR FIGURE 4 OMITTED]; G = 23.96, df = 3, P [less than] 0.001), nor was nest survivorship independent of treatment within plots (LC plots: G = 17.52, df = 3, P [less than] 0.001; MC plots: G = 12.65, df = 3, P [less than] 0.01). Embryo survivorship, therefore, was higher at nests located close to vegetation than at nests located far from vegetation, in both low and medium canopy plots. Minimum soil temperatures at nest depth were not significantly different between covered and open sites ([ILLUSTRATION FOR FIGURE 5A OMITTED]; Mann-Whitney U test: U = 723, P = 0.34); however, maximum soil temperatures differed significantly between types of sites ([ILLUSTRATION FOR FIGURE 5B OMITTED]; U = 1061, P [less than] 0.001). Maximum soil temperatures at open sites averaged 6.6 [+ or -] 2.3 [degrees] C (mean [+ or -] 1 SD; range = 2 [degrees] -11 [degrees] C) higher than those at covered sites. Because the majority of embryos that died did so during the months of June and July, I present more detailed descriptions of soil

6 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 6 of 13 temperatures during those two months. I used 32 [degrees] C as a potential thermal maximum for striped mud turtle embryos because laboratory experiments have shown that turtle eggs incubated at this temperature result in high rates of embryo mortality in some turtle species (Ewert 1979). I used 36 [degrees] C as a potential thermal extreme because embryos of some turtle species have been shown to withstand only brief periods at or above this temperature (Ewert 1979). Daily soil temperatures [TABULAR DATA FOR TABLE 1 OMITTED] at open sites were either [greater than or equal to]32 [degrees] C or [greater than or equal to]36 [degrees] C more often than those at covered sites during these two months (Table 1). In July, when soil temperatures were the highest, covered sites were at [greater than or equal to]32 [degrees] C an average of 5.5 h/d and at [greater than or equal to]36 [degrees] C an average of 1 h/d, whereas soil temperatures at open sites were at [greater than or equal to]32 [degrees] C an average of 7.2 h/d and at [greater than or equal to]36 [degrees] C an average of 4 h/d (Table 1). Although the low and medium canopy plots had different burn histories, overstory density did not differ between low and medium canopy plots for both covered and open nest sites combined (Kruskal-Wallis one-tailed test: H = 0.31, df = 1, P = 0.58). Combining all plots, I found that nests located at covered sites had higher overstory density than those located at open sites (H = 4.24, df = 1, P = 0.04). Within plots, however, this relationship was true only for nests located in the low canopy plots (H = 5.01, df = 1, P = 0.03) and not the medium canopy plots (H = 1.55, df = 1, P = 0.21). Because both low and medium canopy plots were burned periodically, overstory density was low throughout these plots and probably had less influence on nest temperatures, and hence survival, than did ground vegetation. DISCUSSION Flemming et al. (1992) found geographical variation in nest site selection by Piping Plovers and suggested that different selective forces (e.g., camouflage from predators, protection from wind) could possibly play a role in choice of nest site characteristics by plovers throughout their range. Gauthier and Thomas (1993) suggested that cliff swallows selected sites that minimized their time investment in nest construction, thereby decreasing their energy cost. Most investigators studying nest site selection have taken a comparative approach and have focused on determining whether differences exist between nest and random sites in order to assess habitat needs of reproducing organisms (e.g., Petranka 1990, Blakesley et al. 1992). An experimental approach, however, provides more definitive information about the possible fitness consequences of habitat selection (e.g., Kam et al. 1996), which aids researchers in making informative decisions concerning habitat management (Buchanan et al. 1995). I combined both a comparative and an experimental approach to assess microhabitat choices of nesting striped mud turtles and to determine whether these choices provided a selective advantage to the developing embryos. On an upland sandhill in central Florida, female striped mud turtles laid their eggs at sites that differed from random. Females routinely placed their nests close to clumps of grass or other vegetation and avoided open sunny sites. In contrast, most turtle species studied have been shown to deposit their eggs in open areas of little ground cover and full exposure to the sun (e.g., Chelydra [Petokas and Alexander 1980], Chrysemys [Schwarzkopf and Brooks 1987], Apalone [Plummer et al. 1994]). This difference in nest placement between striped mud turtles and other species studied may be attributed to the fact that most research on nest-site selection by turtles has been carried out on medium- to large-sized turtle species. Female striped mud turtles mature at a small body size ( mm CL [Wilson, unpublished data]) and represent the small end of the body size continuum for turtle species. In comparison, medium to large turtle species mature at body sizes ranging from 122 to 216 mm CL for Chrysemys picta (Iverson and Smith 1993), mm plastron length (PL) for Apalone mutica (Plummer 1977) and mm CL for Chelydra serpentina (Congdon et al. 1987).

7 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 7 of 13 Because most turtles generally dig flask-shaped nests with their hind legs, large turtle species have the capacity to dig relatively deeper nests than small turtle species (Ehrenfeld 1979). Nest depth is correlated with nest temperature, and the amplitude of the temperature cycle in the nest decreases with increasing depth; consequently, shallower nests reach higher daily temperatures for longer periods of time than deeper nests (Burger 1976b, Ewert 1979, Packard and Packard 1988, Thompson 1988, Congdon and Gibbons 1990). Relatively large turtle species should, therefore, place their nests in microhabitats that have little surrounding vegetative cover, so that the eggs can reach the appropriate incubation temperature for complete embryonic development (Congdon et al. 1987, Butler and Hull 1996). For instance, Burger (1976b) found that nest depth influenced the survivorship of eggs of Malaclemys terrapin buried at open, sunny nest sites; all eggs survived at a mean depth of 18.2 cm, whereas no eggs survived at a mean depth of 12.5 cm. On the other hand, small turtle species should place their relatively shallow nests near vegetative cover to protect the embryos from environmental extremes. Female Pseudemydura umbrina ( mm CL) have been shown to place their shallow nests close to grass tussocks (Kuchling 1993), and female Kinosternon subrubrum ( mm CL; Mahmoud 1967) have been shown to nest in thick vegetation (Bodie et al. 1996). Females selected sites at which the water content of the soil was greater than that of soil sampled from random sites. Water content, however, has been shown not to be as useful a measurement as water potential in studies concerning the effects of water exchange between the nesting substrate and turtle eggs (Packard and Packard 1988). Water potential, which is a measure of the energy required to move water between the soil and the egg, is a better predictor of the availability of soil moisture to the developing embryo (Tracy 1982). Kinosternids, however, have rigid-shelled eggs, and laboratory experiments have shown that the well-developed calcareous layer surrounding the egg contents prevents the loss or uptake of large amounts of water from the environment (Packard et al. 1982, Tracy 1982). Also, hatching success and hatchling growth in this type of egg appear unaffected by differing levels of soil hydration (Packard et al. 1979, 1981). Because water content describes how much water is actually present in the soil, a nesting female searching for a nest site may be able to physically assess water content of the soil and use this information as an indicator of the potential quality of the site in terms of other microhabitat variables. Survivorship of embryos at selected sites (near vegetation) was significantly higher than that of embryos at nonselected sites (away from vegetation). Although I cannot rule out the effects of water on embryo survival, I believe that the observed difference in survivorship between the two treatments was a direct result of the maximum temperatures imposed on developing embryos inside the nest cavity. Soil at open sites, devoid of vegetative cover, reached higher daily temperatures and maintained these higher temperatures for longer periods of time than soil at sites close to vegetative cover. The temperature at which turtle embryos cease development and die differs among turtle species. It appears, however, from laboratory experiments, that incubation at a constant temperature [greater than or equal to]32 [degrees] C can result in high rates of embryonic death for some species (Yntema 1978, Ewert 1979). When incubated in the laboratory at a constant temperature, embryos of two species of soft-shell turtles suffered high mortality at temperatures of 33 [degrees] C and 34 [degrees] C, and died at temperatures of 36 [degrees] C and 37 [degrees] C (Choo and Chou 1987, Plummer et al. 1994), and embryos of Chelydra serpentina died at temperatures [greater than]32.5 [degrees] C (Yntema 1978). In the field, however, nest temperatures are not constant, but fluctuate with an amplitude that depends upon the nest depth and microhabitat surrounding the nest site (Congdon and Gibbons 1990). Nests of several species of turtles have been shown to reach temperatures well above 33 [degrees] C (Burger 1976b, Ewert 1979, Alho and Padua 1982, Georges 1992). Laboratory evidence suggests that, although critical temperatures exist at which survival of turtle embryos is much

8 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 8 of 13 reduced, brief periods well above these critical values are tolerated by many species (Yntema 1978, Ewert 1979). In my study, some eggs incubated in open sites produced viable hatchlings. Although I did not observe any shell abnormalities in these hatchlings, I do not know what effects high incubation temperatures may have on the future fitness of these hatchlings. It has been shown that the incubation environment may have long-term effects on hatchling growth and survivorship (e.g., Gutzke et al. 1987). McKnight and Gutzke (1993) found that intermediate temperatures yielded hatchlings that grew faster when compared to hatchlings from eggs incubated at thermal extremes. Rapid growth in posthatching turtles may significantly increase their chances of survival by increasing their ability to escape predation and/or their ability to compete with siblings for food (Froese and Burghardt 1974, Janzen 1993). CONCLUSIONS Although limited, our current knowledge concerning nest placement by turtles in the terrestrial habitat largely comes from studies on turtles of relatively large body size. In general, larger turtle species place their eggs in open areas to maximize exposure of the nest to the sun, whereas smaller turtle species need the protection provided by vegetative cover for proper embryonic development of their eggs. In areas of little aboveground vegetation, however, small turtle species may need to adopt a different strategy. For example, female yellow mud turtles (Kinosternon flavescens, mm at maturity; Iverson 1990, Iverson 1991a) from the Nebraska sandhills construct nests in habitats devoid of canopy cover and with little ground vegetation (J. B. Iverson, personal communication). Female yellow mud turtles dig head first into the sandy soil, and at a depth of [approximately]13 cm, turn around and begin to construct their nest cavity with their hind legs. These relatively small females subsequently deposit their eggs at an average depth of 20 cm below the soil surface. In contrast, female striped mud turtles at my study site deposited eggs in shallow nests under the protective cover of abundant ground vegetation. In a review of annual survivorship of turtles, Iverson (1991b) found that mortality was inversely related to age; annual rates of survival for the egg and hatchling stages were significantly lower than those of later life history stages. We already know that turtle eggs are prone to high rates of predation (Iverson 1991b, Wilbur and Morin 1988); therefore, it is especially important in these times of continued habitat destruction and alteration that we know more about the impact of abiotic factors on embryo survival. Aquatic turtles not only use upland habitats for nesting, but also for winter hibernation, summer estivation, and movement from unsuitable aquatic habitats (Gibbons 1986, Buhlmann 1995). based on movement data, Burke and Gibbons (1995) made recommendations about the amount of upland that should be protected around a wetland for aquatic turtles to reproduce successfully. Although it is important to know how much upland to protect, we must also have a basic understanding of the quality of upland habitat needed for reproduction and how the structure of that habitat may contribute to offspring survival. ACKNOWLEDGMENTS I thank the members of my dissertation committee, Drs. Henry Mushinsky, Earl McCoy, John Lawrence, Peter Meylan, and Peter Stiling, for their advice and support throughout the course of this research. I thank the herpetology group at USF for their help in drift fence construction. Earlier drafts of this paper were improved by comments from Earl McCoy, Henry Mushinsky, and C. Richard Tracy. Statistical advice was provided by Earl McCoy, Kevin Jansen, and Brad Robbins. Partial funding for this research was provided by grants from Chelonian Research Foundation, Theodore Roosevelt Memorial Fund, and Tampa Federation of Garden Club Circles. LITERATURE CITED

9 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and its... Page 9 of 13 Alho, C. J. R., and L. F. M. Padua Reproductive parameters and nesting behavior of the Amazon turtle Podocnemis expansa (Testudinata: Pelomedusidae) in Brazil. Canadian Journal of Zoology 60: Becker, P. H., and M. Erdelen Vegetation surrounding herring gull (Larus argentatus) nests in relation to wind direction. Journal of Ornithology 123: Blakesley, J. A., A. B. Franklin, and R. J. Gutierrez Spotted Owl roost and nest site selection in northwestern California. Journal of Wildlife Management 56: Bodie, J. R., K. R. Smith, and V. J. Burke A comparison of diel nest temperatures and nest site selection for two sympatric species of freshwater turtle American Midland Naturalist 136: Bouyoucos, G. J Hydrometer method improved for making particle size analysis of soil. Agronomy Journal 54: Buchanan, J. B., L. L. Irwin, and E. L. McCutchen Within-stand nest site selection by spotted owls in the eastern Washington cascades. Journal of Wildlife Management 59: Buhlmann, K. A Habitat use, terrestrial movements, and conservation of the turtle, Deirochelys reticularia in Virginia. Journal of Herpetology 29: Bull, J. J., and R. C. Vogt Temperature-dependent sex determination in turtles. Science 206: Burger, J. 1976a. Behavior of hatchling diamondback terrapins (Malaclemys terrapin) in the field. Copeia 1976: b. Temperature relationships in nests of the northern diamondback terrapin, Malaclemys terrapin terrapin. Herpetologica 32: Colony and nest site selection in lava lizards Tropidurus spp. in the Galapagos Islands. Copeia 1993: Burger, J., and W. A. Montevecchi Nest site selection in the terrapin Malaclemys terrapin. Copeia 1975: Burger, J., and R. T. Zappalorti Nest site selection by pine snakes, Pituophis melanoleucus, in the New Jersey pine barrens. Copeia 1986: Burke, V. J., and J. W. Gibbons Terrestrial buffer zones and wetland conservation: a case study of freshwater turtles in a carolina bay. Conservation Biology 9: Butler, J. A., and T. W. Hull Reproduction of the tortoise, Gopherus polyphemus, in northeastern Florida. Journal of Herpetology 30: Cagle, K. D., G. C. Packard, K. Miller, and M. J. Packard Effects of the microclimate in natural nests on development of embryonic painted turtles, Chrysemys picta. Functional Ecology 7: Choo, B. L., and L. M. Chou Effect of temperature on the incubation period and hatchability

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12 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and... Page 12 of 13 attention to responses of Cnemidophorus sexlineatus. Herpetologica 41: Packard, G. C., and M. J. Packard The physiological ecology of reptilian eggs and embryos. Pages in C. Gans. and R. B. Huey, editors. Biology of the Reptilia. Volume 16. Ecology B. Defense and life history. Alan R. Liss, New York, New York, USA. Packard, G. C., T. L. Taigen, T. J. Boardman, M. J. Packard, and C. R. Tracy Changes in mass of softshell turtle (Trionyx spiniferus) eggs incubated on substrates differing in water potential. Herpetologica 35: Packard, G. C., T. L. Taigen, M. J. Packard, and T. J. Boardman Changes in mass of eggs of softshell turtles (Trionyx spiniferus) incubated under hydric conditions simulating those of natural nests. Journal of Zoology 193: Packard, M. J., G. C. Packard, and T. J. Boardman Structure of eggshells and water relations of reptilian eggs. Herpetologica 38: Petokas, P. J., and M. M. Alexander The nesting of Chelydra serpentina in northern New York. Journal of Herpetology 14: Petranka, J. W Observations on nest site selection, nest desertion, and embryonic survival in marbled salamanders. Journal of Herpetology 24: Plummer, M. V Some aspects of the nesting success in the turtle, Trionyx muticus. Herpetologica 32: Reproduction and growth in the turtle Trionyx muticus. Copeia 1977: Plummer, M. V., C. E. Shadrix, and R. C. Cox Thermal limits of incubation in embryos of softshell turtles (Apalone mutica). Chelonian Conservation Biology 1: Rauch, N Competition of marine iguana females (Amblyrhynchus cristatus) for egg-laying sites. Behaviour 107: Schwarzkopf, L., and R. J. Brooks Nest-site selection and offspring sex ratio in painted turtles, Chrysemys picta. Copeia 1987: Shine, R Parental care in reptiles. Pages in C. Gans and R. B. Huey, editors. Biology of the Reptilia. Volume 16. Ecology B. Defense and life history. Alan R. Liss, New York, New York, USA. Thompson, M. B Nest temperatures in the pleurodiran turtle, Emydura macquarii. Copeia 1988: Tracy, C. R Biophysical modeling in reptilian physiology and ecology. Pages in C. Gans and F. H. Pough, editors. Biology of the Reptilia. Volume 12. Academic Press, London, UK. Wilbur, H. M., and P. J. Morin Life history evolution in turtles. Pages in C. Gans and R. B. Huey, editors. Biology of the Reptilia. Volume 16. Ecology B. Defense and life history. Alan R. Liss, New York, New York, USA.

13 LookSmart's FindArticles - Ecology: Nest-site selection: microhabitat variation and... Page 13 of 13 Wilhoft, D. C., E. Hotaling, and P. Frances Effects of temperature on sex determination in embryos of the snapping turtle, Chelydra serpentina. Journal of Herpetology 17: Wilson, D. S Tracking small animals with thread bobbins. Herpetological Review 25: Yntema, C. L A series of stages in the embryonic development of Chelydra serpentina. Journal of Morphology 125: Incubation times for eggs of the turtle Chelydra serpentina (Testudines: Chelydridae) at various temperatures. Herpetologica 34: COPYRIGHT 1998 Ecological Society of America COPYRIGHT 2000 Gale Group