Study Site

Our study site was a 6.69-km beach in Indian River County, Florida (Fig. 1). Nesting season for loggerhead sea turtles in this area begins in May and extends through August, with peak nesting occurring in June and July. Alternately, nesting season for green turtles begins in June and ends in September, with peak nesting occurring in July and August. We have been monitoring nesting and hatching activity on this beach since 2003. The initial surveyed area of the sample beach was 2.14 km from 2004 to 2006 and was later increased to 6.69 km in 2007. For the years 2007–2014, a paired t-test was used on the hatching success values from the 2.14-km beach and the 4.55-km beach to assess whether there was a significant difference between annual means. There was not (t = 1.116, df = 7, p = 0.301), and we chose to use reproductive success data from the total beach area surveyed each year, 2004–2014. This study site was composed of a mosaic of features also found at other sea turtle nesting beaches around Florida. The beach had considerable human development behind the primary dune including family homes, multistory buildings, public parks, and a resort, as well as stretches of undeveloped land. The beach also has received varied engineering responses to beach erosion, including seawall construction and beach/dune sand placement, as well as no overt management for erosion. Human use of the beach varied, from low usage near undeveloped dune and condominiums unoccupied during the summer, to high usage at a beach resort adjacent to a public park.

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Sampling Methods

To select a spatially and temporally representative sample of nests on our study site, we marked every nth loggerhead and green turtle nest encountered during daily morning nesting surveys. The integer for n was chosen to provide a relatively constant number of marked nests each sample year. This method is specified in guidelines used throughout Florida (FWC 2007) as a systematic way to select a representative sample of nests allowing seasonal, annual, and spatial comparisons of hatchling production. Where n = 1, every nest was marked, where n = 2, every other nest was marked, and so on.

During our nesting surveys, egg clutch locations were identified by evidence in the sand left by the nesting sea turtle (Witherington et al. 2009). For a selected sample nest, the clutch was marked by measuring its distance to a set of identifying stakes, which served to triangulate the clutch location at the time of nest excavation (e.g., after incubation). In high-traffic areas of the beach, all nests were marked for monitoring and use in educational programs. Where the nest-marking scheme (nth nest scheme) differed between beach areas within a single year, such as between high-traffic areas and the rest of the study beach, we weighted the data so that the representation of nests was even over the entire study site. Our focus was on loggerhead and green turtle nests. Although leatherback turtles (Dermochelys coriacea) do nest within our study site, the nesting density was too low to draw meaningful conclusions about their reproductive success.

We made comparisons of hatching and emergence success between our study site and a composite sample of 16 other Florida beaches that were surveyed 2002–2012 (henceforth, the Florida data; Brost et al. 2015). The Florida data were collected using the same standardized protocol used in our study.

Nest Counts and Monitoring

Nests (buried egg clutches) were marked during 7-d/wk nesting surveys from April through October of each year, in accordance with the standards set forth by FWC. The species was determined by appearance of the crawl (track and nest sign; Witherington and Witherington 2015). Each surveyor received standardized crawl-identification training offered by FWC to all nesting beach surveyors in Florida, in addition to 2 wks of hands-on training with experienced project surveyors. Verification of species included consultation within the program group and examination of hatchlings. Evidence from the latter suggests that the species error rate is less than 1%.

Each nth nest encountered on a daily nesting survey was selected as a sample nest and marked. The clutch in each marked nest was located by hand digging down into the nest mound. Digging was limited to test holes in the nest mound to locate soft sand above the clutch, and to sufficient excavation to touch the top egg. After recording measurements from two markers in the dune to the nest indicating the exact location of the clutch, the surveyor reburied the clutch without disturbing the remainder of the eggs. Only nests in which the clutch was located the morning after oviposition were included in our sample. Nests were not protected using a screen or mesh cover to exclude predators. Surveyors monitored sample nests daily throughout incubation, noting disturbances such as mammalian predation events and wash-overs (i.e., nests that had been covered by wave wash). Despite high-density nesting, our surveyors were able to associate disturbance events with particular marked nests because all such nest areas were denoted with stakes; the clutch located in the center. In accordance with the FWC Marine Turtle Conservation Guidelines (2007), nest contents were inventoried 72 hrs following signs of hatchling emergence or on the 70th day of incubation if signs of emergence were not observed. Contents of each inventoried sample nest were categorized as eggs that were live pipped, dead pipped, empty shell (constituting > 50% of the shell), whole, or damaged, and hatchlings in the nest were recorded as either live or dead (Miller 1999). The empty shells represented hatchlings that escaped from the egg. Presence of fungi and bacterial staining or other unusual characteristics were also noted by beach monitors during excavation.

Hatching and Emergence Success

We calculated hatching and emergence success values from sample nests marked during 2004–2014. Our sample included inventories of 2,543 loggerhead nests, constituting 34.4% of all loggerhead nests deposited during the study period and 972 green turtle nests, constituting 44.7% of all green turtle nests deposited during the study period. For loggerheads and green turtles, respectively, 5.7% and 13.0% of all marked nests were excluded from calculations after their clutches were searched for but not found by the surveyor and were not recorded as being washed-out. These nests lost their marking stakes attributable to vandalism or may have had errors in measurements describing their distance from remaining stakes. Although surveyors may have been unable to find some of these nests because the eggs were washed away, it is likely that most of these nests excluded from our analysis had fates similar to the nests that we did not exclude.

In sample nests that we inventoried, clutch size was recorded as the number of unhatched eggs and egg shells at excavation. Hatching success (HS) was calculated using the formula HS = S/C_i where S is the number of empty shells and C_i is the observed clutch size. Emergence success (ES) was calculated using the formula ES =  (S – R)/C_i, where the additional variable (R) accounts for the number of hatchlings remaining in the nest upon excavation (Miller 1999). We calculated mean hatching and emergence success values for our study site including washed-out nests that had 0% hatching and emergence success. Determinations of nest wash-outs were made using multiple lines of evidence, including sand erosion to clutch depth and repeated attempts to locate eggs at the marked location. Nests where marking stakes were lost were not used in the analysis. Additionally, to further understand the impact of storms, we calculated monthly mean total precipitation (millimeters) at the nearest weather station with a full time series for the study period available (Vero Beach 4 SE FL US, approximately 7.13 km from the southern boundary of the study site) from data obtained from National Oceanic and Atmospheric Administration (NOAA) National Centers for Environmental Information.

Mammalian Predation

We compiled records of mammalian nest predation events over the entire study period, 2004–2014. Because nonmammalian predators (e.g., crabs, insects) left less conspicuous evidence, we did not analyze their predation because of reduced detectability. Thus, the total predation rates we report should be considered minimum predation at our study site. Sample nests with complete predation (all eggs destroyed) were recorded as having 0% success. Nests experiencing partial predation by mammals were assigned a proxy value for both hatching and emergence success following procedures defined by Brost et al. (2015), where these authors examined depredated nests of known clutch size. For loggerhead turtles, proxy values of 36.7% and 35.7% were used for hatching and emergence success, respectively; and, for green turtles, proxy values of 36.8% and 25.8% were used for hatching and emergence success, respectively (Brost et al. 2015).

Sea State Correlations

Wave-height data from the closest NOAA weather buoy to our study site (41009, 20 NM east of Cape Canaveral, FL) were used to determine a correlation between local wave height during each sample nest's incubation and the hatching success of the nest. Data resolution of the buoy was 30-min intervals. We selected a value corresponding to 1200 hrs to represent wave height for each day during the course of incubation, if there were missing data for that time, we selected 1230 or 1300 hrs. There were additional periods of missing wave data, which we accounted for by using data from the second closest buoy to our study site (41010, 120 NM East of Cape Canaveral, FL). We ran a linear regression on compiled wave-height records from the 2 buoys during periods corresponding to the year before and the year after the periods of missing data from buoy 41009 (2003–2006 for 2004 and 2011–2013 for 2012). We used the linear regression equation (2011/2013, r² = 0.6731 and 2003–2005, r² = 0.7512) to predict wave height at the near-shore buoy (41009) when data from this buoy were missing. Wave-height data from 5 September through 18 October 2004 and the entire season in 2012 were extrapolated using this technique. Note that we did not vary wave sampling throughout the locally semidiurnal tidal cycle. Although it is likely that wave height had a greater effect on beach erosion and nest mortality during higher tides, the offset between daily sampling and tidal periodicity meant that our sampling was not biased relative to tides.

We examined the relationship between wave height and hatching success by developing Spearman Rank Order Correlations (bivariate) between hatching success for each species and both 1) mean wave height during incubation, and 2) highest wave height during incubation. In a third analysis, we determined the number of days each nest spent with 2 m or higher waves recorded at buoy 41009. We ran an additional Spearman Rank Order Correlation (bivariate) between these high-wave-height days and hatching success. Tropical cyclone events were also examined relative to the number of nests washed-out attributable to storm erosion. We expected tropical cyclones to influence the phenology of reproductive success. To examine this question, we determined the relationship between the seasonality of incubation period and hatching success with a Spearman Rank Order Correlation.

Representative Reproductive Success

Measures of hatching and emergence success for our study site varied within and between years such that individual years and periods within seasons were often unrepresentative of long-term rates. Mean annual emergence success ranged 41.6%–80.6% for loggerheads and 10.2%–84.1% for green turtles. These ranges represent years in which hatching and emergence success was low for both species (Figs. 2 and 5), highlighting the importance of multiple sampling years to generate these vital rates. Annual hatching and emergence success rates for loggerhead nests in our study site were higher than each of the annual rates published as a composite from 16 Florida beaches during the same period (Brost et al. 2015) (Fig. 5). Our study site showed higher reproductive success for green turtle nests in 56% of the years when the studies overlapped (Brost et al. 2015).

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Mean hatching and emergence success for loggerhead nests at our study site were higher than mean rates in each of the representative studies (at nesting beaches in Florida and Turkey; Table 5). These mean rates for green turtle nests on our beach were in the middle range of values reported from Florida, the Galapagos (Ecuador), Mozambique, Turkey, and Brazil (Table 5). We reason that these rates represent varied conditions that affect hatchling production. However, the sample size is small in terms of global beach locations where published reproductive success data are representative and include multiple years. The criteria we used for our comparisons selected published data that 1) were reported as hatching success values, 2) had minimal sampling bias, 3) were representative of the reported beach over an entire nesting season, 4) were from sample nests that did not receive manipulation or biased treatment, and 5) included all nest fates (e.g., depredated and washed-out nests were not omitted). Although we observe that our loggerhead and green turtle reproductive success rates were in the middle to high end of the range we found, we use caution in light of the small sample size for our comparisons. One difference in comparisons between species may be that there are more comparable data from widely distributed green turtle nesting beaches, with a sample that includes more high-success and low-success beaches.

Table 5. Representative reproductive success of loggerhead and green turtle nests measured in studies with comparable methods (see “Methods” in text) to the current study (Indian River County, FL).

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The moderate to high sea turtle reproductive success at our beach occurred under some conditions that are conventionally thought of to create threats to nest survivorship. These conditions include anthropogenic erosion responses such as armoring and periodic fill placement and recreational beach use as a result of residential development, public parks, and a major beach resort. What may moderate effects from these potential threats is an extensive conservation program undertaken across the study site and sampling period.

The conservation program at our study site has provided an enhanced vigilance for early signs of nest predation problems. At the resort and in many of the residential areas within our study site, trash that would subsidize nest predator populations is carefully managed. Studies with low representative estimates of reproductive success typically cite predation rates that may explain this mortality. The highest reported estimates for green turtle reproductive rates we found came from small, island beaches with little or no mammalian nest predation (Bellini et al. 2012; Anastácio et al. 2014).

Predation Effects on Mortality

Mammalian predation was not a major cause of nest mortality in our study (Table 3). The low influence of egg predators is not common in sea turtle nesting habitats adjacent to human development. Urban expansion brings additional food resources for generalist scavengers/predators and spans temporal gaps between peaks in natural food abundance (Prange et al. 2004). As a result, many predator populations subsidized by human development have contributed to increased predation rates on sea turtle nests (Engeman et al. 2006). We hypothesize that the low mammalian predation rates we observed reflect low predator abundance, possibly attributable to the efficient management of food waste at the nearby resorts and private properties. Low nest predation has had an important influence on hatchling production. The mean rate of mammalian nest predation within the study period for our site was 1.3%. By comparison, an analysis of the Florida data by Brost et al. (2015) showed that mammalian predators (mostly raccoons, but including coyotes, Canis latrans) reduced emergence success from 73% to 34% in loggerhead nests and from 67% to 35% in green turtle nests (relative to nests with no mortality factors reported). On many beaches, mammalian predation is a dominating sea turtle nest mortality factor, with up to 97% of nests partially or completely destroyed (Talbert et al. 1980; Hopkins and Murphy 1981; Schroeder 1981; Kurz et al. 2012).

Our study may indicate the upper range of hatching and emergence success for beaches that have fully addressed nest-predation problems. Nest-predation management is known to reduce predation and increase reproductive success. A study by Engeman et al. (2005) showed a reduced predation rate from 95% to 9.4%, with a large increase in hatchling production. Predation management can take many forms. We propose that the conservation efforts undertaken at our study site to educate visitors about reducing human subsidies of nest predators (managing trash, not feeding wildlife) are an effective way to address the threat from predators.

Storm and Sea-State Effects on Mortality

Storm erosion had a large effect on nest mortality in our study (Fig. 3). Tropical cyclones resulted in increased wash-overs, wash-outs, and accretion/erosion events at the nest, effects that have been directly attributed to egg mortality (Martin 1996). For loggerhead nests in our study, 2004, 2008, 2010, and 2011 had the largest number of wash-outs and nearly all of these wash-outs resulted from named meteorologic events (hurricanes and tropical storms). For green turtle nests, 2004, 2008, 2010–2012 had the largest number of wash-outs and nearly all of these wash-outs resulted from named storms. The increased wash-outs in green turtle nests in 2012 were largely caused by Hurricane Sandy, which made landfall in late October. The annual nesting period for green turtles in Florida extends well beyond when loggerheads stop nesting (Brost et al. 2015), thus resulting in a temporal overlay of the typical green turtle nest incubation period and the Florida hurricane season.

We compared differences in the vulnerability of loggerhead and green turtle nests to storm erosion. The peak number of incubating loggerhead nests each year occurred in July (91.8% of nests incubated in this month), which was a month earlier than the August peak in green turtle incubation (88.4% of nests incubated in this month). This difference affected nest mortality, with the percentage of washed-out nests for both species increasing dramatically from August forward (Fig. 3). Green turtle nests were most vulnerable to complete wash-outs from storm events, a conclusion also made in a study by Dewald and Pike (2014).

We found individual storms to have large effects on nest mortality. Major storms are well known to shift large volumes of beach sand, with both excessive accretion and erosion that suffocates nests, drowns them, and washes them away (Milton et al. 1994). In the current study in 2004, 100% of the nests incubating during the landfalls of Hurricanes Frances and Jeanne (storms striking in close succession) were completely washed-out. The storms resulted in 25 m of horizontal beach loss within portions of our study site.

The seasonality of hatching success we measured (Fig. 2) corroborated the pronounced effects from late-season storms we observed. For each species, the peak in hatching success (represented by curves on Fig. 2 for each species) was near the beginning of the nesting season for each species, between the first nesting of the season and the peak in total incubating nests. Hatching success was lowest for the last third of the season when storm effects were most frequent (Fig. 3). In addition to reduced hatching success as a result of increased erosion and accretion, major meteorologic events are generally associated with large volumes of rainfall, which may have adverse effects on embryonic development (Ragotzkie 1959). Mean precipitation over the study period was highest during the last third of the nesting season for both species, indicating that a combination of high wave wash and increased rainfall may lead to decreased hatching success (Table 2). We hypothesize that selective pressure from storm-induced nest mortality is a principal driver shaping the nesting phenology of loggerheads and green turtles in Florida. Sea turtles commonly show a distinctly peaked nesting season with the number of new nests diminishing in the stormy season (Pike and Stiner 2007; Fuentes et al. 2011; Bourjea et al. 2015).

One key, storm-related effect we identified as determining nest mortality was wave height. In our analyses, mean wave height and highest wave height during incubation and duration of > 2-m waves, each was negatively correlated with hatching success. Large waves that break near the beach suspend sand that is carried away by the longshore current running parallel to the beach, causing erosion that can extend into the dune (McLachlan and Brown 2010). Other factors influence beach-sand dynamics, but wave energy and the extent and duration of storm tides have been shown to be principal factors. For example, Zhang et al. (2001) found that a combination of wave energy, storm tide, storm duration, and topography of the beach had the most significant impacts on beach erosion.

Unmeasured Mortality Factors

We recognize other unmeasured factors that may have had important effects on sea turtle reproductive success. High groundwater from extensive rainfall has been known to affect incubating sea turtle eggs (Ragotzkie 1959; Kraemer and Bell 1980).

In the sands of densely nested beaches, microbes and fungi are known to cause egg mortality. At Ostional Beach, Costa Rica, hatching success of olive ridley (Lepidochelys olivacea) nests was negatively correlated with fungal abundance, and high microbial activity was also shown to reduce hatching success (Bézy et al. 2015). High abundance in microbial and fungal communities within sands of arribada (mass-nesting-arrival) beaches like Ostional are thought to benefit from the contents of broken eggs. The egg contents are either from sea turtles digging into other sea turtles' nests or from eggs damaged by predators. High-density nesting beaches for green turtles are also affected by these density-dependent factors affecting nest survivorship (Tiwari et al. 2006). Within nests on our study site, we commonly found the presence of fungi and bacterial staining in unhatched eggs found during excavation.

Substrate characteristics, such as sand grain size and organic matter content, can affect the rate of diffusion of gases and elements into and out of the nest cavity, which is vital for proper embryonic development. For example, Mortimer (1990) found sand grain size to be positively correlated with mortality in green turtle clutches incubating within the dry sands of Ascension Island. Elsewhere, fine-grained quartz sands have been shown to inhibit drainage of rainwater through nest cavities, causing eggs to drown (Kraemer and Bell 1980). On our study site, variation in nesting substrate was brought about by periodic and spatially variable placement of artificial fill material (frequently from inland-mined sediment). Because our rates of reproductive success were relatively high, it is tempting to conclude that effects from this artificial fill were minimal. However, we hypothesize that these effects could be complex, and indirect, to include changes in nest-site choice that would make nests vulnerable to lower-beach erosion.

A key unmeasured mortality factor in our study was predation of eggs by ghost crabs (Ocypode quadrata). We frequently recorded evidence of ghost crab predation in unhatched eggs within inventoried nests, but we did not have confidence in the false negatives associated with this predation assessment. As eggs were not counted immediately after oviposition in the current study, it was difficult to determine the number of eggs that may have been stolen by ghost crabs. Many of the eggs we recorded as “damaged” could have been from ghost crabs. Although these sea turtle egg predators are considered to be important (Brost et al. 2015), unbiased rates describing ghost crab contribution to egg mortality will require careful assessments of detectability. We believe that rates of ghost crab predation in our study site are lower than published rates of ghost crab predation on other less inhabited beaches because reduced human presence on isolated beaches is a factor that favors a high ghost crab abundance (Marco et al. 2015).

Target Reproductive Success Rates for Managed Beaches

Resource managers tasked with protecting sea turtle nests must be able to identify when diminishing returns result from conservation actions (Murdoch et al. 2007). To have high returns on sea turtle reproductive success given investment in nest-protection actions, one should understand what fraction of nest mortality factors is mitigable. Whereas factors such as storm erosion, substrate pathogens, and other stochastic events are often large scale and impossible to guard against, factors like mammalian predation and human disturbance are often able to be reduced with wise management practices.

We hypothesize that the sea turtle reproductive rates for our study site, measured over a long time series and within an area of spatially variable land use, represent targets for nesting beach management. The conservation outreach undertaken during our study was designed to address threats from mortality factors like human disturbance and predation by subsidized predators. Our study was not designed as an experiment to test for these conservation benefits, but we do note that nest mortality from predation and human disturbance was extremely low. Thus, we hypothesize that the reproductive rates we measured provide an achievable target where these threats can be managed under an active conservation program.