THE RISK OF HATCHLING LOSS TO NEARSHORE PREDATORS AT A HIGH-
DENSITY LOGGERHEAD NESTING BEACH IN SOUTHEAST FLORIDA.
by
Kelly R. Stewart
A Thesis Submitted to the Faculty of
The Charles E. Schmidt College of Science
In Partial Fulfillment of the Requirements for the Degree of
Master of Science
Florida Atlantic University
Boca Raton, Florida
August 2001
i
Copyright by Kelly R. Stewart
ii
iii ABSTRACT
Author: Kelly R. Stewart
Title: The risk of hatchling loss to nearshore predators at a
high-density loggerhead nesting beach in southeast
Florida.
Institution: Florida Atlantic University
Thesis Advisor: Dr. J. Wyneken
Degree: Master of Science
Year: 2001
It has been recognized that mortality is high for juvenile stages of long-
lived vertebrates such as sea turtles, however few studies have quantified
mortality rates. The objective of this study was to assess the relative risk
that hatchlings face in their first few minutes in the water, at the
commencement of their offshore migration from a natural high-density
nesting beach (Juno/Jupiter, FL). I followed 217 hatchlings at night by
kayak, as they left the beach and documented the proportion surviving the
initial 15 minutes in the water. Of these, 206 survived for an empirical
survival rate of 95%. Tarpon were the most common predator observed.
This survival rate is much higher than that previously observed at a
hatchery (72%); this may be due to temporal and spatial variation in nest
location at the natural beach. Juno and Jupiter beaches are therefore
highly productive sea turtle rookeries.
iv TABLE OF CONTENTS
List of Tables…………………………………………………….. vi
List of Figures …………………………………………………… vii
Introduction …………………………………………………… 1
Materials and Methods ……………………………………… 5
Results ……………………………………………………….. 12
Discussion ……………………………………………………. 17
Appendix 1 ……………………………………………………… 29
Appendix 2 …………………………………………………….. 31
Appendix 3 ……………………………………………………… 35
Literature Cited …………………………………………………. 36
v LIST OF TABLES
Table 1. A summary of site descriptions. Bottom topography, distance from the Juno pier, Jupiter Inlet, and abundance of fish species is indicated for each site …………………………………………………………………. 8
Table 2. A summary of predatory fish caught, dates, site type, and stomach contents ………………………………………………………………………. 11
Table 3. A summary of predation events on hatchling loggerhead turtles. Water depth, and the hatchling’s last known compass heading were recorded upon being taken by fish. Hatchlings were taken at reef sites, but when they were taken, they had already crossed the reef and were over sand bottom ………………………………………………………………………. 12
Table 4. Orientation of hatchlings migrating from sites along Juno/Jupiter beaches during the summer of 2000. Sample size (n) for each site is given. R-vector is a measure of dispersion………………………………………….. 13
Table 5. A summary of catch-per-unit-effort (for predatory fish only) for each month of the study. Catch-per-unit-effort is in units of fish per hour ……….. 22
Table 6. Comparison of hatchery sites (Hillsboro hatchery) and natural high-density nesting beach sites (Juno and Jupiter beaches). * The effective density was ~6000 nests/km, however the actual length of the hatchery was only 0.1 km, and represented a nest density an order of magnitude higher than the natural site………………………………………………… 24
vi LIST OF FIGURES
Figure 1. Location of the study site in Palm Beach County, Florida, USA. Six sampling sites are indicated by labels at right of the shoreline map of Palm Beach County. Three site-types were identified; sand, reef, and transitional categories were based on bottom substrate ………………………….. 6
Figure 2. A tracing of hatchling tracks as they left the beach and migrated to deeper water. The line at left represents the shoreline, and the terminal point of each hatchling track is the point where they were released from their tether. This particular set of tracks was taken from data that were recorded at a transitional site-type Other site-types had similar track lines. The average heading that hatchlings took on this offshore migration was 77.8°……… 14
Figure 3. Percentage of hatchling turtles surviving the first 15 minutes of offshore migration, at each site-type during the hatchling season of 2000……….. 15
Figure 4. Percentage of hatchling turtles surviving the first 15 minutes of offshore migration, across the hatchling season of 2000…………………………… 16
vii Introduction
Sea turtles, like other long-lived vertebrates are iteroparous (Heppell et al. 1999).
Females with large body size produce numerous small offspring in several
clutches. These characteristics indicate that, over time, evolutionary pressures have selected for a life history strategy in which investment in individual offspring is minimal and survival of young is generally very low. Many authors have recognized that mortality prior to maturation is probably extremely high in sea turtles (Stancyk 1982; Richardson and Richardson 1982; Heppell et al. 1996).
Egg loss and nest predation are well documented (Stancyk 1982; Witzell and
Banner 1980; Gyuris 1994). Since sea turtles have high fecundity, some laying approximately 200-600 eggs per season (Hirth 1980; Van Buskirk and Crowder
1994; Miller 1997), it is estimated that perhaps one in 10,000 hatchlings will survive to maturity (Frazer 1986).
Marine turtles are logistically difficult to study in the ocean and, as a result, very few baseline data exist to describe vital rates of the aquatic stages. While much important information has been gathered on the nesting beach about the reproductive cycles, fecundity, and parameters that impact nest success of sea turtles, disproportionately little is known about life in the water.
Life for hatchling sea turtles is inherently risky. Besides being very small, hatchlings have few defense mechanisms against predators. Some of the threats to reaching adulthood include predation during the earliest life stages,
1 e.g. as hatchlings crawling from the nest to the ocean, swimming in nearshore waters, and as pelagic-stage juveniles. Other sources of mortality include: incidental capture in fishing gear; ingestion of foreign materials such as tar and plastics; collisions with boats; and in some places, harvesting of eggs, subadults and adults (Lutcavage et al. 1997).
Baseline population sizes (e.g. hatchling, juvenile, adult), recruitment levels, and mortality/survival values are described by estimates or arithmetically derived guesses and limited empirical data (Crouse et al. 1987; Heppell 1998; Heppell et al. 1999). In addition, very few studies have attempted to quantify and partition mortality at various life stages. To date, no demographic baselines have been established for the pelagic stage. The pelagic stage of loggerheads may last for
6.5-11.5 years (Bjorndal et al. 2000), and begins when hatchlings enter the water after having traversed the beach from the nest.
Hatchlings typically emerge at night. Along Florida’s east coast, most hatchlings enter the water between the hours of 1930 and 0630, with peak emergences occurring from 2300 - 0000 h (Witherington et al. 1990). Several investigators suggested that this pattern of nocturnal hatchling emergence is both a predator avoidance mechanism as well as a behavior reflecting the hatchlings’ limits in thermal tolerance (Mrosovsky 1968; Lohmann et al. 1997). Hatchlings usually emerge en masse, orientate seaward, crawl vigorously down the beach and then proceed offshore, distancing themselves from the beach and its perils. Offshore
2 migration (after Dingle 1996) is characterized by hyperactive, oriented swimming
(frenzy), which lasts about 24 hours (Salmon and Wyneken 1987), followed by less vigorous oriented swimming (post-frenzy) until turtles reach cover provided by flotsam such as Sargassum (Witham 1980; Carr 1986). The frenzy is believed to rapidly distance hatchlings from predator-rich nearshore waters
(Salmon and Wyneken 1987).
In one study of hatchling survival focusing on the early pelagic stage, Gyuris
(1994) estimated that most of the first year mortality of green turtles could be attributed to aquatic predation within the first hour after entering the ocean off
Australian beaches at the Great Barrier Reef. Gyuris (1994) followed 1740 hatchlings offshore over 3 seasons and found that predation rates in the water ranged between 0-85%, with a mean predation rate of 31%. Witherington and
Salmon (1992) found that aquatic predators took 6.8% (5 of 74) of loggerhead hatchlings during daytime and nighttime swimming trials in turbid waters off the east-central coast of Florida. Most other studies simply reported predation or documented predators. Caldwell (1959), Witham (1974) and Fletemeyer (1978) reported seeing predation on loggerhead and green turtle hatchlings in Florida waters. Booth and Peters (1972) documented green turtle hatchlings in
Australian waters being taken by crabs, black-tipped sharks and other species of fish. None of these studies attempted a quantification of the hatchling survival rate in the water.
3 It is well documented that coastal land use in Florida has degraded nesting
habitats in many areas, and may be responsible for the spatial distribution of
turtle nesting beaches that we now see (Salmon et al. 2000). For example in
southeast Florida, habitat alteration has perhaps artificially concentrated nesting
in areas that are physically most acceptable to nesting sea turtles – those
beaches adjacent to appropriate oceanographic features (currents for dispersal,
sufficient water temperature, etc.), having sufficient sand, being relatively unlit,
and having tall landward silhouettes. Very high nest densities (400-600
nests/km) are found at just a few sites along the eastern coast of Florida
(Witherington and Meylan 2001). Spatial concentration of nests may make the
risk even greater for hatchlings leaving these beaches and migrating offshore. At
hatcheries, very dense nest concentrations and therefore, high hatchling
densities, may attract high numbers of aquatic predators (Wyneken et al. 2000).
In a study of survival of hatchlings migrating offshore, risks to hatchlings were an order of magnitude higher in waters adjacent to hatcheries, compared to nearby natural low-density sites (Wyneken 2000). Predatory fish and squid congregated in the nearshore waters in front of the high density nesting beaches (Wyneken et al. 2000).
Quantification of mortality for different life stages is important to our understanding of basic life history characteristics of loggerhead sea turtles. A firm understanding of life history characteristics is critical to managers charged with formulating and implementing recovery plans for threatened and
4 endangered species. Empirical data become the baseline against which to
measure future trends. Baselines established now enable us to track how
populations change over time.
The objective of this study was to assess the relative risk that hatchlings face in
their first few minutes in the water, at the commencement of their offshore migration. In conducting this study, I addressed the following questions. (1) On a natural, high-density nesting beach, how many hatchlings entering the water survive the initial phase of the offshore migration? (2) Does this risk of mortality vary across the hatchling season (July-September)? (3) Does the risk to hatchlings leaving beaches with heavy reef structure or vertical complexity differ from that associated with locations having a simple sand bottom? (4) How does this risk compare to survival rates observed at hatchery sites in Florida? (5) What is the total production of hatchlings from this site?
Materials and Methods
Study Sites and Nest Locations
Juno Beach and Jupiter Island, both in Palm Beach County, Florida, USA (26°
90’ N, 80° 05’ W; Figure 1) were chosen as the study sites because in both locations, turtles nest in large numbers (400-600 nests/km/year). All hatchlings at both sites emerge from natural nests, and then swim offshore over sand, rock reef, or transitional bottom substrates on their way to deeper water.
5 26° 90’ N
Lat. N
Long. Palm Beach County 80° 05’ W
Figure 1. Location of the study site in Palm Beach County, Florida, USA. Six sampling sites are indicated by labels at right of the shoreline map of Palm Beach County. Three site-types were identified; sand, reef, and transitional categories were based on bottom substrate.
Initial assessment of the entire beach was conducted by fixed-wing aircraft to
obtain an overall view of bottom substrates. Substrate types included: (1) sand -
no rock or hard-bottom existed with few fish, (2) transitional - sand dominated
with rocky outcroppings and groupings, rock not extensive, but with more fish
6 (defined by both abundance and species) than sand sites, and (3) reef - rock
dominated, sand rarely visible, extensive vertical complexity with complex fish
assemblages. Sampling sites (defined by Florida Index Nesting Beach 100 m
zones; FMRI 2001) were then assessed along 15 km of shoreline by visual in-
water surveys to confirm topography and complete basic site mapping. Each site
was classified as simple sand, complex (rocky, reef, or vegetated) or transitional
(at sites where bottom structure is dynamic due to abundant sand transport).
Transect surveys to map and qualitatively survey the fish fauna were conducted by two people for 30 minutes, out to a depth of 6 meters for each site. Any fish species seen were recorded on slates, and the number and relative abundance of each fish species was recorded (Table 1).
Six sites were chosen for the project (Figure 1), and random sampling of these sites was conducted over the course of the season. The 6 sites were categorized into 3 site-types based on bottom substrate as described above.
Early in the nesting season (May – July) on morning surveys, 43 natural nests located on Juno’s beaches were marked with stakes. Nests were monitored daily to document any perturbations (overwash or predation) and to determine when nests were ready to emerge. Turtles were collected from these marked nests on the night they were due to emerge. At the conclusion of the season, I
evaluated the success of marked nests; and calculated hatch and emergence
rates to incorporate into a production estimate for the beach. This estimate of
7 Table 1. A summary of site descriptions. Bottom topography, distance from the Juno pier, Jupiter Inlet, and abundance of fish species is indicated for each site.
Distance Distance % % # Fish Total # of from pier from inlet Sand Rock species fish Sand 1 2,800 m 8,600 m 100 0 0 0 Sand 2 2,600 m 3,200 m 100 0 3 ~ 10 Transitional 1 3,550 m 9,350 m 90 10 6 ~ 30 Transitional 2 600 m 5,500 m 80 20 18 ~ 40-50 Reef 1 7,300 m 1,500 m 10 90 17 ~ 50-75 Reef 2 8,100 m 2,300 m 5 95 21 ~ 75-100
productivity (recruitment to the pelagic stage) was calculated using emergence success, total number of nests for the study area, and survival rate in nearshore waters.
Mortality, Survivorship, and Predator Identification
Several complementary techniques were used to document hatchling sea turtle mortality and assess the inherent risks of particular sites. These included: (1) following hatchlings offshore to quantify mortality or successful migration from the nearshore, (2) surveys of predatory fish during the season, and (3) visual identification of predators, (when possible) as hatchlings were taken.
Assessing Mortality Rates and Risk
Turtles were followed offshore according to the randomly scheduled site order beginning on July 5, 2000 and ending on September 27, 2000, and when weather and wave conditions would allow. A total of 217 hatchlings were followed as they swam away from the 6 sites at Juno/Jupiter, over 22 nights of sampling. A total of 74 hatchlings were followed at reef and transitional bottom
8 substrate sites, and 69 hatchlings were followed from sand bottom sites. On each night of sampling, I attempted to follow 10 hatchlings as weather would allow. Due to varying weather conditions, the number of turtles followed each night ranged from 5 to 14.
Ten loggerhead turtle hatchlings, which were ready to emerge, were taken from the top of a marked nest near the designated site in the afternoon and placed in a dark Styrofoam® cooler. They were held at ambient temperatures (24-28 ºC) until their release that night. Hatchlings were followed individually as they migrated offshore. This work was done at night using kayaks. Each hatchling was tethered by a smooth light cotton thread, 150 cm in length, and attached to a streamlined balsa wood float (Witherington and Salmon 1992) so that it could be tracked offshore. The wood was whittled into a hull, and painted flat black. It contained on its top surface an embedded, green cold-chemical glow stick that was visible only from above the water. The balsa wood hull was not attacked by fish when it was towed offshore without a hatchling tethered to it. The weight of the float in water was negligible (1.9 g in air). Using these floats slowed the progress of a hatchling, but not significantly (Witherington and Salmon 1992).
Each hatchling, once fitted, was allowed to crawl down the beach, enter the water, and begin swimming. Each turtle was followed by kayak at a distance of
5-20 m to avoid disturbing it or drawing attention to the hatchlings and float.
Every 3 minutes, the hatchling’s position was recorded from 5 m behind the
9 hatchling, using a hand-held GPS unit (Garmin Models 12 and 38, range of
accuracy = 15-30 m). The turtle’s heading was also recorded at this time. If the
hatchling had not been taken by a predator after 15 minutes, it was recaptured
and freed to continue its migration. On occasions when the hatchling was taken
by a predator, I was able to identify the predator species if it jumped out of the
water during hatchling capture, or if it took the hatchling close enough to me that
I could see it in the clear water. Often, following the predation event, the float
and tether were recovered with the line cut and the hatchling gone.
Six times during the season, once at each site, a number (20-100) of untethered
hatchlings were released along with the tethered individual to see if predation
increased when there were more hatchlings in the water at the same time.
Angling (Hook and Line Captures)
Angling at the 6 sites was conducted over the course of 5 months (June through
October). Angling for predators was conducted on 36 nights during the hatchling
season (Appendix 1A). The choice of site each evening was based on where we
had followed hatchlings the previous night. Angling (surfcasting) began at 2000
h ± 1h and continued for 3h. Frozen and live scaled sardines, (Harengula
jaguana), squid (Loligo spp.), cut fish (Mugil cephalus), pennaid shrimp, and mole crabs (Emerita talpoida), were used for bait. Dead turtles were not used as bait to avoid biasing the stomach content analysis. When a fish was caught, the time of capture was recorded. The line was quickly returned to the water and
10 fishing resumed. I recorded the length of time each line was in the water and this
was converted to an estimate of effort (Appendix 1A). Fish had been previously
classified as predatory or non-predatory based on mouth size, gape size, and
presence or absence of teeth. Predatory fish are defined as opportunistic
feeders, with mouth morphologies (teeth and/or a gape) large enough to take a
hatchling or part thereof. Non-predatory fish were released immediately back
into the water. Predatory fish were anesthetized by immersion in ice water, killed
by decapitation and the stomach contents were examined and recorded (Table
2). At least two fishing lines were used per night.
Table 2. A summary of predatory fish caught, dates, site type, and stomach contents.
Site Stomach Date Type Species contents 7/12/00 sand Carcharhinus brevipinna brown liquid, not possible to identify 7/13/00 trans Caranx crysos brown liquid, digested material 8/14/00 reef Lutjanus griseus Empty 8/14/00 reef Centropomus undecimalis empty, stomach lavage only 8/17/00 trans Anisotremus surinamensis green liquid 8/21/00 reef Haemulon parrai Empty 8/25/00 trans Arius felis Fish scales, vertebrae, small bones 8/25/00 trans Arius felis 4 loggerhead hatchlings, fish flesh 9/1/00 reef Caranx hippos Empty 9/11/00 trans Arius felis Digested fish, brown material 9/18/00 trans Elops saurus Empty 9/26/00 sand Arius felis turtle eggs and scutes, mullet 10/06/00 sand Caranx crysos Empty
Statistical Analysis
Using power analysis and sample size estimation, I determined that a minimum
sample size of 96 turtles followed offshore would be needed to accurately assess
survival at this beach, for six sites (+/- 10%, α = 0.05 Appendix 2; Box et al.
1978). Statistical analyses of hatchling survival by site type, by season, and by
11 comparing survival at hatchery and natural beaches, were performed using chi- square analysis (Steel and Torrie 1980). Analysis of hatchling orientation while swimming offshore was performed using circular statistics (Zar 1986).
Results
A total of 217 loggerhead hatchlings were followed as they migrated from nearshore waters to deeper waters (average 4.5 m) offshore. Aquatic predators took 11 hatchlings during trials. Of these, tarpon took 4, a carcharhinid shark took one and 6 hatchlings were taken by unidentified predators (Appendix 3).
Over the entire study area, an average of 95% of the hatchlings survived.
Because the minimum sample size required to assess survival was 96, and I followed 217 turtles, the power of my survival estimation is high (0.96). For each hatchling that was taken by a predator, the time of disappearance, depth of water and bottom topographical features at the predation site, as well as the turtles’ final headings were also recorded (Table 3).
Table 3. A summary of predation events on hatchling loggerhead turtles. Water depth and the hatchling’s last known compass heading were recorded upon being taken by fish. Hatchlings were taken at reef sites, but when they were taken, they had already crossed the reef and were over sand bottom.
Date Taken Depth of Water Bottom Substrate Final Heading 7/11/2000 7 m sand 73° 7/13/2000 4 m sand 60° 7/13/2000 4 m sand 73° 8/1/2000 5 m sand 105° 8/11/2000 2.5 m rock 85° 8/31/2000 6 m sand 84° 9/15/2000 4 m sand 76° 9/15/2000 4 m sand 80° 9/23/2000 ~5 m sand 70° 9/23/2000 ~5 m sand 88° 9/23/2000 ~5 m sand 61°
12 Hatchlings swam on an average heading of 77.8º (ENE) offshore (Table 4). They
did not display any avoidance behavior (tuck, dive, etc.) or other evidence that
they detected predators (Witherington and Salmon 1992; Wyneken and Salmon
1997), but swam in an almost direct route offshore (Figure 2). Swimming slowed
only when the hatchlings surfaced to breathe.
Table 4. Orientation of hatchlings migrating from sites along Juno/Jupiter beaches during the summer of 2000. Sample size (n) for each site is given. R-vector is a measure of dispersion.
Site Type n Orientation (°) R-vector * Sand 1 38 73 .98 Sand 2 23 72 .99 Transitional 1 10 73 .99 Transitional 2 56 80 .96 Reef 1 45 84 .97 Reef 2 29 77 .96 All sites 201 77 .96
* All samples show significant orientation by a Rayleigh test (p < 0.001).
Predatory attacks came without apparent warning, and the hatchling and the float
apparatus submerged immediately. The glowing float was sometimes observed
underwater, moving at rates of speed faster than any hatchling was previously
seen swimming. Often the float and thread bobbed to the surface shortly after
the attack and was recovered, missing only the hatchling. On 3 occasions, the
predator (tarpon) was observed leaping out of the water, after having taken a
hatchling.
In this study I followed only one hatchling swimming at a time. On the six nights
when hatchlings were followed as part of a group, no predation was noted, for
13 Atlantic Ocean
Juno Beach
Figure 2. A tracing of hatchling tracks as they left the beach and migrated to deeper water. The line at left represents the shoreline, and the terminal point of each hatchling track is the point where they were released from their tether. This particular set of tracks was taken from data that were recorded at a transitional site-type. Other site-types had similar track lines. The average heading that hatchlings took on this offshore migration was 77.8°.
either the tethered hatchling, or the untethered turtles that I was able to track. All hatchlings were observed swimming offshore at or near the surface.
Survival by site type
There were no significant differences in hatchling survival between pairs of sites or among rock sites, transitional sites and sandy sites. Survival was 97.3%
(72/74) at transitional sites, 95.7% (66/69) at sand sites, and 91.9% (68/74) at rock reef sites (Figure 3). Since there were no significant differences found
14 100 95 90 85 80 75 70 65 60
Percentage Surviving Percentage 55 50 Reef Sand Transition Site-type
Figure 3. Percentage of hatchling turtles surviving the first 15 minutes of offshore migration, at each site-type during the hatchling season of 2000.
among sites, data were pooled and an average survival rate of 95% was used for subsequent calculations (Appendix 2).
Seasonal survival
There were no significant differences in survival across the hatchling season
(comparisons among study months). Interestingly, chi-square tests showed no significant difference in hatchling survival among study months (p=0.058), survival in September ranked lower (87.5%) than during the preceding 2 months
(July and August; survival 96.1% and 97% respectively; Figure 4).
15 100 95 90 85 80 75 70 65 60 55 50 July August September Month
Figure 4. Percentage of hatchling turtles surviving the first 15 minutes of offshore migration, across the hatchling season of 2000.
Predators
All fish caught while angling or seen while snorkeling at each site are listed in
Appendix 1B. The most commonly caught species were gray snapper (Lutjanus griseus), ladyfish (Elops saurus), blue runner (Caranx crysos), bluefish
(Pomatomus saltatrix), and catfish (Arius felis). Of the predatory fish caught, only one individual catfish (A. felis) had eaten 4 loggerhead hatchlings (Table 2).
Based on angling studies and snorkeling surveys, predatory fish appeared to be more abundant at rock reef sites, although quantitative measures were not used that would have allowed me to test this statistically.
16 Hatchling survival (95%) at Juno and Jupiter beaches was significantly greater than hatchling survival (72%) at the hatchery site (Χ2 = 35.9, df = 1; p < 0.001).
Productivity
The emergence success for hatchlings at the study site was 86.5 hatchlings per nest. The total number of nests for the season was 7,200. Using the survival rate of 95% and multiplying it by emergence success and total number of nests, I calculated that 590,000 hatchlings survived the initial part of the offshore swim (in this case 0.25 km beyond this beach) and presumably recruited to the pelagic.
Discussion
Sea turtles face many obstacles to reaching adulthood (Stancyk 1982;
Richardson and Richardson 1982; Heppell et al. 1996), but very few studies have attempted to quantify mortality associated with the earliest stages of a sea turtle’s life (exceptions: Gyuris 1994; Witherington and Salmon 1992). The objective of my study was to assess the relative risk a hatchling faces during its first few minutes in the water, (commencement of migration) at a natural beach. This survival estimate provides an important basis for future comparison with similar beaches, as well as with managed ‘hatchery’ beaches. As well, the estimate of mortality in nearshore waters that is derived from this study has implications, which are far-reaching and may be important when applied in models and in building recovery plans for species in Atlantic waters. Presumably the first hour of a hatchlings life is the most treacherous. Fifteen minutes was the time interval
17 chosen to follow the hatchlings in this study because this amount of time allowed the hatchlings to cross the nearshore reef line and to get out into deep water, where survival should increase due to decreased threats of predation from fish, and due to increased protection while in the pelagic habitat (hatchlings are cryptic in sargassum). Wyneken et al. (2000) found that predation after 15 minutes of swimming by hatchlings leaving nearshore waters was minimal.
The average hatchling survival in the water at the beginning of the offshore migration, for hatchlings leaving Juno and Jupiter beaches, was 95%. This is the first time hatchling mortality has been quantified for nearshore waters, adjacent to a natural high-density nesting beach. Of the 217 hatchlings followed, 95%
(206) survived. This is an empirically accurate estimate, because of the high power associated with the analysis (0.96). I can therefore use this value with confidence as the initial survival rate in the water for hatchlings migrating away from Juno and Jupiter beaches for the summer of 2000.
Based upon my observations while on the water and those of other investigators
(Frick 1976), my presence on the water had little or no effect on either hatchling or fish behavior (Helfman, personal communication). Hatchlings were taken when they were close to the kayaks (<5 m) or when the boats were at maximum distance (>20 m) from the turtles. Because of these observations and the large sample size of this study over the course of the season, I am confident that my presence had no measurable effect on hatchling survival.
18 Survival by site type
There was no significant difference in hatchling survival among sites; the average
survival rate (95%) was used for the entire study area (Figure 3). Although not
significant, hatchling survival was lower at the reef sites when compared to the
sandy and transitional sites. Based upon other studies of predation (Gyuris
1994; Witherington and Salmon 1992), I expected to see a higher level of
predation at reef sites, since site complexity and structure provide habitat for
more species of fish.
At Juno and Jupiter beaches, nesting density is fairly consistent at approximately
600 nests/km/year. Loggerhead sea turtles deposit their nests with temporal
variation - nesting 2-7 times per season (Hirth 1980; Van Buskirk and Crowder
1994), and nesting approximately every 4 years in Florida (Turtle Expert Working
Group 2000). Nests are also deposited with spatial variation - successive
clutches are laid at least 0-5 km apart depending on the locale (Miller 1997).
This behavior allows turtles to distribute reproductive effort over time and space,
and helps to ensure that in a highly dynamic and temporally unstable
environment such as a beach, chances are minimal that all clutches could be lost
(Miller 1997). High nest density on a natural beach, combined with spatial and
temporal variation of nesting, may have contributed to the observation that there
was no significant difference seen in survival rates for hatchlings at the three site
types.
19 Prey species have several strategies or tactics for avoiding predators. These include escape through sheer numbers; also known as the dilution effect (or confusion effect; Goodenough et al. 2001), by unpredictability in space or across time, by size, or through crypsis (Goodenough et al. 2001) and escape by a variety of other specialized defense mechanisms (McNaughton and Wolf 1979).
Sea turtle hatchlings cannot escape by size as they are ~5 cm long, they are somewhat conspicuous in shallow waters, and are relatively defenseless at this early age. Therefore, large numbers of hatchlings entering the water at the same time may swamp predators close to shore. This strategy is a viable one, as predators typically cannot respond to all hatchlings at once and some therefore, escape. The timing of hatchling emergences from a high-density nesting beach, being spatially and temporally unpredictable may well reduce losses. In effect, having many nests on the beach, with several spatially distant nests emerging each evening, means that several hundred hatchlings will leave the beach and swim offshore, but they will not be in a predictable location. While a group of hatchlings entering the water together may attract the attention of some predators, on average, an individual in a group usually has a better chance of survival than it might if it was swimming by itself (Vine 1973).
While hatchlings enter the water nightly, they are not spatially predictable so resident fish may utilize them opportunistically but probably are not actively looking for hatchlings or responding to them in the same way they would with a
20 resident school of baitfish (e.g. a bait run of mullet). As well, predatory reef fish, which tend to be ambush predators, especially at twilight (Helfman 1993), can become confused when several prey items appear all at once in a tight group
(Goodenough et al. 2001), because they are not able to choose which target to attack. Non-resident or wide-ranging cruising species, such as tarpon (Megalops atlanticus) and bluefish (Pomatomus saltatrix), rely on visual cues to locate schools of prey, and may be able to take advantage of high prey densities.
Aquatic predators that are resident adjacent to a natural high-density nesting beach may, on average see or encounter more loggerhead hatchlings than at less densely nested sites, but loggerhead hatchlings are not temporally as abundant as other potential prey (e.g. other fish species, invertebrates).
In addition, differences in physical qualities of the beach plus individual clutch variation means that natural nests emerge at different times during the night within a range (Witherington et al. 1990) when the sand surface temperature has cooled sufficiently.
Survival across the hatchling season
The survival rate for hatchlings at Juno/Jupiter beaches did not vary across the season, although a definite trend was evident. In September, hatchlings experienced the lowest survival rate (87.5%), compared to 97% for August. This is an important observation because during the month of September I caught
30% more predatory fish in the angling component of the study, than in July or
21 August (Table 5). The most commonly caught species and trends in fish capture were similar to those observed at the hatchery site (Wyneken et al. 2000).
Table 5. A summary of catch-per-unit-effort (for predatory fish only) for each month of the study. Catch-per-unit-effort is in units of fish per hour.
Month July August September CPUE (fish/hour) 0.04 0.12 0.17
The high survival rate observed in this study is also interesting from the perspective of when the most hatchlings enter the water. The peak weeks for emergence during 2000 were from 14-31 August (300-400 nests/week). By
September at Juno and Jupiter beaches, 80% of hatchlings had already emerged and swam past predators in nearshore waters.
Angling results
The angling survey results suggest that loggerhead hatchlings are not an important prey item for shallow water predatory fish at Juno and Jupiter beaches.
Of 24 predatory fish caught during my study, only 1 individual catfish had recently consumed 4 hatchlings. In my study, since only 11 turtles out of 217 followed were taken by fish, and large predatory fish were seen in the water at the study site it appears that predatory fish do not specialize on loggerhead hatchlings and instead may take them opportunistically, at least at a natural beach.
Catch-per-unit-effort was low, even for the reef sites. Using a variety of baits and lures did not increase this value. Due to the low captures of fish on many of the nights, even though fish were known to be in the water, catch-per-unit-effort
22 analysis was not an effective means for this particular study because of the low total captures and high variability in the number of captures for each site.
Comparison of survival rates at natural nest sites and hatcheries
On a natural high-density nesting beach (Juno/Jupiter), a survival rate of 95% is very high in comparison with other such studies. Gyuris (1994) documented a mean survival rate of 69% for green turtle hatchlings leaving Heron Island,
Australia, and Wyneken et al. (2000) found a survival rate of 72% at a hatchery in
Hillsborough, Florida. Table 6 illustrates the differences seen in hatchling survival during this study and the study done at that hatchery site by Wyneken et al. (2000). Sixty km south of Juno/Jupiter, nest density at the hatchery was an order of magnitude higher than at Juno/Jupiter. The total length of the hatchery was ~0.1 km, and it contained ~600 nests. Most nests deposited on the same day are placed in close proximity at hatcheries. As a result they incubate under similar beach conditions and tend to hatch and emerge, at the same time.
Aquatic predators may be able to cue in on a hatchery site as one that spatially and temporally concentrates a predictable source of food. The same strategies for escaping predators that proved so successful for hatchlings at a natural beach may fail to help them survive at hatcheries. For hatchlings in the water off hatcheries, the advantage of being part of a group may be reduced, because a higher concentration of prey can attract and support higher concentrations of predators (Goodenough et al. 2001), if only seasonally. Nests are so concentrated at the hatchery that spatial and temporal variability is effectively eliminated. On adjacent stretches of beach, there are few or no sea turtle nests
23 (because they often have been relocated to hatcheries) and so predators appear to learn to exploit a very small area in the water off these sites. Resident predators may also become more concentrated spatially (Goodenough et al.
2001).
Table 6. Comparison of hatchery sites (Hillsboro hatchery) and natural high-density nesting beach sites (Juno and Jupiter beaches). ∗ The effective density was ~6000 nests/km, however the actual length of the hatchery was only 0.1 km, and represented a nest density an order of magnitude higher than the natural site.
Hatchery Natural site Nest density ~6,000 nests/km∗ 600 nests/km Length of beach 0.1 km 15 km Nearshore survival 71% 95%
The dilution effect (safety in numbers) for hatchlings is effective only as long as predators encounter small groups of prey as often as large groups of prey.
However, as groups of prey grow larger, the dilution strategy can be more effective, but not when groups of prey become more predictable and predators are able to increase their numbers as well. The sheer density of nests concentrated in a small area like a hatchery results in high numbers of hatchlings leaving the beach and forming large predictable groups. The feeding rate of the predators then becomes higher. Fish are unlikely to leave such a stretch of beach rich in prey, and may remain in the area for the duration of the nighttime hours. It is therefore important when using hatcheries as a management and protection tool to take care not to concentrate the relocated nests in too small an area. Being able to rely on several small hatcheries instead of one large
24 hatchery could greatly reduce the risk for hatchlings leaving these areas
(Wyneken and Salmon 1997).
Application of survival rates to population models
An estimate of productivity (P = emergence success X clutch size X survival rate) was established for this beach (590,000 hatchlings). These hatchlings presumably escaped nearshore waters and entered the pelagic stage. Even though additional hatchlings may be taken by predators as they continue migration, the survival rate is expected to increase as turtles get older (Heppell et al. 2000). More than half a million hatchlings left Juno and Jupiter beaches during the summer of 2000. This study identifies Juno/Jupiter as one of the most important beaches for loggerhead nesting in the State of Florida, and it points to its critical role for recruitment of hatchlings in the US loggerhead population.
The successful management of marine species stocks holds many challenges, especially if the species are long-lived vertebrates such as sea turtles. Many parameters for long-lived endangered or threatened species are inherently difficult to assess (Musick 1999). The most fundamental aspects of their population structure, population size, recruitment, mortality and length of life are often poorly documented (Musick 1999). Due to these factors, management strategies and recovery plans for these species are difficult to evaluate because the effects of the strategies are not seen for many years, and perhaps decades.
Population modeling has been used as a tool to examine management and
25 conservation strategies, if only hypothetically. There are relatively few empirical
data for some life stages to incorporate into many sea turtle population models,
and the best “guesses” are used in order to move forward. Little by little, models
are improved as empirical data become available. The survival rate derived from
my study has applications for parameters currently used in population modeling
(Heppell et al. 2000). Because my study quantified the fate of hatchlings during
the first 15 minutes of the first year, there are some assumptions that can be
made to incorporate my survival rate into the first annual survival rate for pelagic
stage turtles. If 95% of all hatchlings survive the initial 15 minutes in the water
and 75% (rough estimate) of those survive the additional week it takes to reach
the Gulf Stream, where survival increases dramatically, then it is possible to use
the pelagic stage survival rate for the remainder of the first year. This rate is
currently assumed to be 50%. If these values are used, then perhaps the first
annual survival rate should be 0.95 X 0.75 X 0.5 = 35.6%, which is much less
than the published estimate of 67% (Crouse et al. 1987). This survival rate can
be used to adjust the fecundity for adult females by improving the accuracy of
estimates of female production. Fecundity incorporates the following
parameters: sex ratio, remigration interval, number of eggs per nest, number of nests per year, nest survival and nearshore survival. Production per female =
{(eggs x nests)/remigration interval) x sex ratio x nest survival x nearshore
survival = {(103 x 4)/4) x 1 x 0.84 x 0.95 = 82 hatchlings per female per year for
the study beach.
26 In addition, this information on its own is important because the survival rate at
the beginning of the migration (presumably the most dangerous time for
hatchlings) now has an empirical baseline for at least one major rookery. If I had
found survival to be only 50%, hatchlings would have to have an extremely high
survival rate after that initial 15 minutes, if they were to achieve a stable
population level. When developing models to be used in designing management
strategies, it is important to partition mortality seen at different beaches to look at
the proportional contribution of each beach to the entire population. This
partitioning of mortality can then be used in spatially explicit population models
now being developed and updated (Turtle Expert Working Group 2000).
Additionally, it has been recognized that we should be managing for at least 4
different subpopulations of loggerheads (Turtle Expert Working Group 2000), due
to genetic information obtained from turtles in 5 regions. Assessing population
trends for individual subpopulations will be needed to protect the smaller and
declining subpopulations. One of the research recommendations suggested by
TEWG (2000), is the quantification of empirically derived parameters, which will
help define annual survival rate of different age classes of turtles. The empirical
information I have collected can be incorporated into a better population model,
at least for one subpopulation – SE Florida, which is incidentally the largest of the
4 subpopulations.
Conclusions
In conclusion, risk to hatchlings from nearshore predators is very low at Juno and
Jupiter beaches. Hatchling survival nearshore is similar across the season. This
27 stretch of beach is uniformly risky for hatchlings swimming over different bottom substrates – and much less risky than hatchery sites. Recruitment to the pelagic stage was approximately 590,000 loggerhead hatchlings for the year 2000.
Finally, the survival of loggerheads in Florida may well depend on high density nesting beaches such as this one which is able to produce hundreds of adult turtles over time. The data described not only document the importance of this small beach to the recovery of loggerhead populations but at a fundamental level provide much needed baseline productivity data. My data are the first to quantify the initial risk to hatchlings from a natural loggerhead rookery and the production once hatchlings have crossed the first nearshore reef. Such data will assist managers in the development of more sound conservation strategies by improving the data going into the population and simulation models used to formulate those recovery plans, as well as assisting nesting beach managers with the development of sound beach management policies. If predation on hatchlings is significantly higher near hatcheries than at a natural beach, perhaps we should thoroughly examine these policies to reduce the amount of anthropogenic mortality source associated with placing hatcheries in places where survival of hatchlings will be very low.
28 Appendix 1A. Fish catch summary for the duration of the season. The effort spent (in hours) was calculated by taking the number of surfcasting rods and multiplying that by the number of hours spent angling. All species caught are listed; numbers in parentheses indicate multiple captures of one fish species.
Date Site Type Effort Species Caught 6/12/00 Sand 1 3 None 6/17/00 Sand 2 2 None 6/19/00 Trans 2 9 None 6/20/00 Sand 1 2.25 None 6/21/00 Trans 1 6 D. argenteus, H. parrai, A. surinamensis 6/23/00 Sand 1 7.5 None 6/25/00 Sand 1 7.5 None 6/28/00 Trans 1 6 L. griseus 6/29/00 Trans 2 6 L. griseus (3) 7/7/00 Sand 1 6 None 7/11/00 Trans 1 4.5 L. griseus 7/12/00 Sand 1 12 L. griseus, C. brevipinna 7/13/00 Trans 1 12 C. crysos 7/18/00 Trans 1 12 None 7/19/00 Sand 2 18 None 7/21/00 Trans 2 7.5 None 7/25/00 Trans 2 11 None 7/28/00 Sand 2 8 None 8/2/00 Reef 1 9 None 8/4/00 Reef 2 6 None 8/7/00 Sand 1 6 None 8/14/00 Reef 2 9 L.griseus (2), D. argenteus, H. parrai (2), C. undecimalis, G. cirratum, A. surinamensis 8/16/00 Trans 2 9 D. argenteus 8/17/00 Trans 1 9 D. argenteus, A. surinamensis (2), L. griseus 8/21/00 Reef 1 13 H. parrai, L. griseus, A. surinamensis (2), Family Muraenidae (2) 8/25/00 Trans 2 6 A. felis (2) 8/30/00 Reef 2 6 None 9/1/00 Reef 1 11 C. hippos, A. surinamensis, L. griseus 9/6/00 Sand 1 9 None 9/11/00 Trans 2 9 A. felis 9/18/00 Trans 2 5.9 G. cirratum, E. saurus 9/24/00 Reef 1 8.75 None 9/26/00 Sand 2 9 A. felis 10/06/00 Sand 1 6 E. saurus, C. crysos, P. saltatrix (3) 10/19/00 Trans 2 6 None 10/20/00 Reef 2 6 A. felis (3) Total 283.9
29 Appendix 1B. All fish species seen (snorkeling) or caught (angling) during my study. Site bottom substrate is indicated by: R=reef, S=sand, and T=transitional
Scientific Name Common Name Site Type Snorkel Fish Holocanthus ciliaris Angelfish T X Sphyraena barracuda Barracuda RT X Kyphosus sectatrix Bermuda chub TR X Anisotremus surinamensis Black margate TR X X Caranx crysos Blue runner TS X Acanthurus coeruleus Blue tang TR X Pomatomus saltatrix Bluefish S X Thalassoma bifasciatum Bluehead R X supermale Centropomus undecimalis Common snook TR X X Caranx hippos Crevalle jack R X Acanthurus chirurgus Doctorfish TR X Mycteroperca microlepis Gag grouper R X Lutjanus griseus Gray snapper RTS X X Acanthurus randalli Gulf surgeonfish R X Arius felis Hardhead catfish TS X Elops saurus Ladyfish TS X Lutjanus synagris Lane snapper TR X Haemulon album Margate R X Family Muraenidae Moray eel R X X Mugil cephalus Mullet T X Strongylura marina Needlefish R X Ginglymostoma cirratum Nurse Shark TR X X Acanthurus bahianus Ocean surgeon TR X Scarus coerleus Parrotfish TR X Liopropoma rubre Peppermint bass R X Harengula spp. Pilchards T X Diodon hystrix Porcupinefish R X Anisotremus virginicus Porkfish TR X Sparisoma rubripinne Redfin parrotfish R X Haemulon parrai Sailor’s choice TR X X Diplectrum formosum Sand perch RT X Lutjanus apodus Schoolmaster R X Abudefduf saxatilis Sergeant major TR X Echeneis naurcrates Sharksucker T X Archosargus probatocephalus Sheepshead R X Diplodus argenteus Silver porgy TR X X Chaetodipterus faber Spadefish TR X Carcharhinus brevipinna Spinner shark S X Diplodus holbrooki Spottail R X Elops atlanticus Tarpon R X Caranx bartholomaei Yellow jack R X Ocyurus chrysurus Yellowtail snapper R X
30 Appendix 2. Statistical analysis and results.
Power Tests
Sites P0 P1 n Power Average all .678 .9495 217 1 sites .99 .9495 217 .9668 Rock sites .678 .9189 74 1 .99 .9189 74 .9381 Sand sites .678 .9565 69 1 .99 .9565 69 .6686 Transition .678 .973 74 1 .99 .973 74 .3994
Key: P0: null proportion, percentage of hatchlings surviving P1: what was observed, percentage of hatchlings surviving n: sample size Power: the validity of the test, over 0.8 is optimal
Sample size was sufficient to accurately assess survival. As there was no significant difference in survival over 3 site types, all samples were pooled. Whether I test that 99% of hatchlings survive or 67.8% survive (taken from life tables and population models), the power is high, ranging from .9668 to 1. Therefore the proportion of hatchlings surviving to 15 minutes is accurately estimated at 94.95%.
Power analysis was done using a program located at this website (University of Iowa): http://www.math.uiowa.edu/~rlenth/Power/ Dr. R. Lenth [email protected]
Survival by site type
Chi-square analysis of survival rates among sample site types; sand, reef, and transitional.
H0: Hatchling survival ratios will not differ among sand, reef and transitional site types. H1: Hatchling survival ratios will differ among sand, reef, and transitional site types.
31
Sand Reef Transitional Total Survived Observed 66 68 72 206 Expected 65.5 70.25 70.25 Taken Observed 3 6 2 11 Expected 3.5 3.75 3.75 Totals 69 74 74 217
ΣΧ2 = 0.0038 + 0.0721 + 0.0436 + 0.0714 + 1.35 + 0.8167 = 2.3576
2 Χ critical = 5.99 degrees of freedom = (columns –1)(rows – 1) = 2*1 = 2
Therefore, accept the null hypothesis that the sample ratios are equal. There are no differences among sample site types, with regard to survival of hatchlings in the water.
Caution: The chi-square test requires that: (a) data are discrete and nominal. (b) when there are only 2 categories, no expected value may be less than 5.
For my data, this second assumption is not met, and all 3 of the expected values in the second row (turtles taken by predators) are <5.
Because the expected values are <5, this indicates that the second row is not actually a variable in itself, there are just not enough non-survivors to make this a valid variable. I redid the chi-square analysis using only the survivors. This is a more valid test. Results are below.
Sand Reef Transitional Total Survived Observed 66 68 72 206 Expected 68.67 68.677 68.67
ΣΧ2 = 0.104 + 0.007 + 0.161 = 0.272
2 Χ critical = 5.99 degrees of freedom = (columns –1)(rows – 1) = 2*1 = 2
Therefore, accept the null hypothesis that the sample ratios are equal. There are no differences among sample site types, with regard to survivors only.
32
Survival by month
Chi-square analysis of survival by month is shown below. Again, the problem of expected values below 5 will make this a simplified chi-square to test only for survivors.
H0: Hatchling survival ratios did not differ among months of the hatchling season. H1: Hatchling survival ratios did differ among months of the hatchling season.
July August September Total Survived Observed 74 97 35 206 Expected 68.67 68.677 68.67
July 74/77 tested August 97/100 tested September 35/40 tested
2 The value of the Χ is 16.51. The critical value is 5.99 with 2 degrees of freedom. This makes the survival dependent on month (accept H1), however the sampling effort was not equal in all months. If the data are converted to percentages, there is no significant difference seen among months. To confirm this finding, I transformed the data (Box et al. 1978) and tested the proportions pairwise, using 3 t-tests. Fisher’s Exact Test was also used. The results were not significant.
Site Type Reef Sand Transition Original value 92 96 97 Transformed value 82 87 89
Reef vs. Sand p-value: 0.795 Sand vs. Transition p-value: 0.642 Reef vs. Transition p-value: 0.887
T-tests were done using the program located on the following website: http://home.clara.net/sisa/t-test.htm
Fisher’s Exact Test
Table (61, 13, 66, 8) p-value: 0.346 Table (61, 13, 60, 9) p-value: 0.494 Table (60, 9, 66, 8) p-value: 0.797
Website analysis: http://www.matforsk.no/ola/fisher/htm
Therefore ratios of survival by month are equal, and I accepted the null hypothesis. Hatchling survival did not depend on month.
33 Natural beach vs. hatchery
Chi-square analysis of survival rates between a hatchery site in Broward County and a natural beach (Juno/Jupiter).
H0: Hatchling survival ratios did not differ between a hatchery site and a natural beach site. H1: Hatchling survival ratios did differ between a hatchery site and a natural beach site.
Hatchery Juno/Jupiter Total Survived Observed 102 206 308 Expected 120.5 184.1 Taken Observed 40 11 55 Expected 21.5 32.9 Totals 142 217 363
ΣΧ2 = 2.8 + 2.6 + 15.9 + 14.6 = 35.9
2 Χ critical = 3.84 degrees of freedom = (columns –1)(rows – 1) = 1*1 = 1
Therefore, do not accept the null hypothesis that the ratios are equal. The survival rate depends on the location and so the results are significant. Hatchling survival does depend on the location. The proportion of hatchlings surviving was less at the hatchery.
34 Appendix 3: Listed below are the predation events for 217 hatchling loggerheads as they migrated from the beach (15 minute period). A total of 206 survived. Site type is noted, along with piscine predator, whenever identified. Some of the fish included in the unknown predator category are suspected to have been tarpon or snapper, but the fish were not seen to get a positive identification.
Number of Turtles Site Type Date Predator 2 hatchlings Sand 1 7/11/00, 7/13/00 Tarpon 1 hatchling Sand 1 7/13/00 Shark 1 hatchling Reef 1 8/1/00 Tarpon 5 hatchlings Reef 1&2 8/11/00, 8/31/00, Unknown predator 9/23/00 1 hatchling Transitional 2 9/15/00 Tarpon 1 hatchling Transitional 2 9/15/00 Unknown predator
35 Literature Cited
BJORNDAL, K. A., BOLTEN, A. B., and MARTINS, H. R. 2000. Somatic growth model of juvenile loggerhead sea turtles Caretta caretta: duration of pelagic stage. Marine Ecol. Prog. Ser. 202:265-272
BOOTH, J., and PETERS, J. A. 1972. Behavioural studies on the green turtle (Chelonia mydas) in the sea. Anim. Behav. 20:808-812
BOX, G. E. P., HUNTER, W. G., and HUNTER, J. S. 1978. Statistics for experimenters. John Wiley and Sons, Inc. New York, NY.
CALDWELL, D. K. 1959. The loggerhead turtles of Cape Romain, South Carolina. Bulletin of the Florida State Museum 4:319-348
CARR, A., 1986. Rips, FADS, and little loggerheads. Bioscience 36:92-100
CROUSE, D. T., CROWDER, L. B., and CASWELL, H. 1987. A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology 68:1412-1423
DINGLE, H. 1996. Migration: the biology of life on the move. Oxford University Press. New York, NY.
FLETEMEYER, J. R. 1978. Underwater tracking evidence of neonate loggerhead sea turtles seeking shelter in drifting sargassum. Copeia 1978:148-149
FLORIDA MARINE RESEARCH INSTITUTE. 2001. Status and trends of Florida's sea turtles. http://www.floridamarine.org
FRAZER, N. B. 1986. Survival from egg to adulthood in a declining population of loggerhead turtles, Caretta caretta. Herpetologica 42:47-55
FRICK, J. 1976. Orientation and behaviour of hatchling green turtles (Chelonia mydas) in the sea. Anim. Behav. 24:849-857
GOODENOUGH, J., MCGUIRE, B., and WALLACE, R. A. 2001. Perspectives on animal behavior, 2nd edition. John Wiley and Sons, Inc. New York, NY.
GYURIS, E. 1994. The rate of predation by fishes on hatchlings of the green turtle (Chelonia mydas). Coral Reefs 13:137-144
HELFMAN, G. S. 1993. Fish behaviour by day, night and twilight In Behaviour of teleost fishes. Edited by T. J. Pitcher, Chapman and Hall, London, U.K. pp.494- 512
36 HEPPELL, S. S., CROWDER, L. B. and CROUSE, D. T. 1996. Models to evaluate headstarting as a management tool for long-lived turtles. Ecol. Appl. 6:556-565
HEPPELL, S. S. 1998. Application of life-history theory and population model analysis to turtle conservation. Copeia 1998:367-375
HEPPELL, S. S., CROWDER, L. B., and MENZEL, T. R. 1999. Life table analysis of long-lived marine species with implications for conservation and management. In Life in the slow lane: ecology and conservation of long-lived marine animals. Edited by J. A. Musick, American Fisheries Society Symposium 23, AFS, Bethesda, MD. pp. 137-148
HEPPELL, S. S., CROUSE, D. T., and CROWDER, L. B. 2000. Using matrix models to focus research and management efforts in conservation. In Quantitative methods for conservation biology. Edited by S. Ferson and M. Burgman, Springer-Verlag, New York, NY. pp. 148-168
HIRTH, H. F.1980. Some aspects of the nesting behavior and reproductive biology of sea turtles. Amer. Zool. 20:507
LOHMANN, K. J., WITHERINGTON, B. E., LOHMANN, C. M. F., and SALMON, M. 1997. Orientation, navigation and natal beach homing in sea turtles. In The biology of sea turtles. Edited by P. L. Lutz and J. A. Musick, CRC Press, Boca Raton, FL. pp. 107-135
LUTCAVAGE, M. E., PLOTKIN, P., WITHERINGTON, B. E., and LUTZ, P. L., 1997. Human impacts on sea turtle survival. In The biology of sea turtles. Edited by P. L. Lutz and J. A. Musick, CRC Press, Boca Raton, FL. pp. 387-409
MCNAUGHTON, S. J., and WOLF, L. L. 1979. General ecology, 2nd edition. Holt, Rinehart and Winston, New York, NY.
MILLER, J. D. 1997. Reproduction in sea turtles. In The Biology of Sea Turtles. Edited by P. L. Lutz and J. A. Musick, CRC Press, Boca Raton, FL. pp. 51-81
MROSOVSKY, N. 1968. Nocturnal emergence of hatchling sea turtles: control by thermal inhibition of activity. Nature 220:1338-1339
MUSICK, J. A. 1999. Life in the slow lane: ecology and conservation of long-lived marine animals. AFS Symposium 23. American Fisheries Society, AFS, Bethesda, MD.
RICHARDSON, J. I., and RICHARDSON, T. H. 1982. An experimental population model for the loggerhead sea turtle (Caretta caretta). In Biology and
37 conservation of sea turtles. Edited by K. A. Bjorndal, Smithsonian Institution Press, Washington, D.C. pp. 165-176
SALMON, M., and WYNEKEN, J. 1987. Orientation and swimming behavior of hatchling loggerhead turtles Caretta caretta L. during their offshore migration. J. Exp. Marine Biol. Ecol. 109:137-153
SALMON, M., WITHERINGTON, B. E., and ELVIDGE, C. D. 2000. Artificial lighting and the recovery of sea turtles in Florida, USA. In Sea turtles of the Indo- Pacific. Edited by N. J. Pilcher and G. Ismail, ASEAN Academic Press, London, UK. pp. 25-35
STANCYK, S. E. 1982. Non-human predators of sea turtles and their control. In Biology and conservation of sea turtles. Edited by K. A. Bjorndal, Smithsonian Institution Press, Washington, D.C. pp.19-38
STEEL, R. G. D., and TORRIE, J. H. 1980. Principles and procedures of statistics: a biometrical approach. McGraw Hill Publishers, New York, NY.
TURTLE EXPERT WORKING GROUP. 2000. Assessment update for the Kemp’s ridley and loggerhead sea turtle populations in the western north Atlantic. U.S. Dep. Commer. NOAA Tech. Mem. NMFS-SEFSC-444, Miami, FL.
VAN BUSKIRK, J., and CROWDER, L. B. 1994. Life-history variation in marine turtles. Copeia 1994:66
VINE, I. 1973. Detection of prey flocks by predators. J. Theor. Biol. 40:207-210
WITHAM, R. 1974. Neonate sea turtles from the stomach of a pelagic fish. Copeia 1974:548
WITHAM, R. 1980. The “lost-year” question in young sea turtles. Amer. Zool. 20:525-530
WITHERINGTON, B. E., BJORNDAL, K. A., and MCCABE, C. M. 1990. Temporal pattern of nocturnal emergence of loggerhead turtle hatchlings from natural nests. Copeia 1990:1165-1168
WITHERINGTON, B. E., and SALMON, M. 1992. Predation on loggerhead turtle hatchlings after entering the sea. J. Herp. 26:226-228
WITHERINGTON, B. E., and MEYLAN, A. 2001. Sea turtle nesting in Florida. Presented at the annual sea turtle permit holders of Florida meeting, Gainesville, FL, January 20, 2001
38 WITZELL, W. N., and BANNER, A. C. 1980. The hawksbill turtle (Eretmochelys imbricata) in Western Samoa. Bull. Mar. Sci. 30:571-579
WYNEKEN, J., and SALMON, M. 1997. Assessment of reduced density open beach hatcheries and “spread-the-risk strategies” in managing sea turtles on Hillsboro Beach, Florida. Technical report 97-04, Broward County Board of Commissioners. Ft. Lauderdale, FL
WYNEKEN, J. 2000. The migratory behavior of hatchling sea turtles beyond the beach. In Sea turtles of the Indo-Pacific. Edited by N. Pilcher and G. Ismail, ASEAN Academic Press, London, UK. pp. 121-142
WYNEKEN, J., SALMON, M., FISHER, L., and WEEGE, S. 2000. Managing relocated sea turtle nests in open-beach hatcheries. Lessons in hatchery design and implementation in Hillsboro Beach, Broward, County, Florida, USA. In Proceedings of 19th Annual Sea Turtle Symposium. Compiled by H. Kalb and T. Wibbels. US Dept. Commerce. NOAA Tech. Memo. NMFS-SEFSC-443
ZAR, J. H. 1986. Biostatistical analysis. Prentice Hall, Inc. Upper Saddle River, NJ.
39