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ENDANGERED SPECIES RESEARCHEndang Species Res
Vol. 28: 235247, 2015doi: 10.3354/esr00684
Published online October 7
INTRODUCTION
During development, sea turtle hatchling sex isdirected by
temperature (Bull 1980, Mrosovsky &Yntema 1980, Girondot 1999).
In sea turtle species,male-biased sex ratios occur when nest
temperaturesare cooler (
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Endang Species Res 28: 235247, 2015
some turtle species (Georges at al. 2004, Girondot etal. 2010,
Telemeco et al. 2013a).
In addition to genetic variation and possible mater-nal effects,
environmental factors, such as sandalbedo (Hays et al. 2001),
shading and sun exposure(Standora & Spotila 1985), and moisture
from rainfall(Godfrey et al. 1996, Houghton et al. 2007) may
mod-ify nest sex ratios. A number of studies suggest thatthe hydric
environment, in combination with thethermal environment, influences
embryonic devel-opment and phenotype, including sex in turtles
(e.g.,Packard et al. 1987, 1989, Cagle et al. 1993, Finkler2006,
LeBlanc & Wibbels 2009, Wyneken & Lolavar2015). Moisture as
rainfall may impact the nest envi-ronment, affecting hatchling size
(McGehee 1990)and influencing hatchling sex (re viewed by Carthy
etal. 2003, Wibbels 2003). Heavy rainfall decreases gasdiffusion
throughout the nest (Miller et al. 2003),which can cause egg death
if extreme. Other sourcesof excess water, such as prolonged tidal
inundation(Ragotzkie 1959, Kraemer & Bell 1980) can also
causeembryo death.
Field studies suggest that higher moisture duringincubation
influences hatchling sex ratios in turtles.Godfrey et al. (1996)
found increased production ofmale hatchlings in green turtle
(Chelonia mydas) andleatherback turtle (Dermochelys coriacea) nests
dur-ing April and May, months with the most rainfall inSuriname.
Additionally, Matsuzawa et al. (2002)examined nests in Japan and
found sand tempera-ture increased as the rainy season ended; thus
mois-ture may influence the thermal environment of thenest.
Houghton et al. (2007) found high rainfall inGranada produced
unseasonably cool nest tempera-tures and interpreted these results
as likely shiftingleatherback sex ratios toward male-bias;
however,sex ratio verification in this study was lacking.Wyneken
& Lolavar (2015) found that loggerheadnests incubated in years
that were wetter than nor-mal and nests incubated in the lab under
hot and wetconditions produced more males than would beexpected
based on previous studies of sex ratio andincubation temperature
(e.g. Mro sovsky & Yntema1980, Mrosovsky 1988).
We measured how rainfall affects sand tempera-tures as it
travels down to nest depth, as moisture isan environmental factor
that can change nest tem-peratures. We also investigated the
relationshipsamong rainfall amounts, loggerhead nest tempera-tures,
and loggerhead hatchling sex ratio samples ata southeastern Florida
nesting beach that has fe -male-biased sex ratios (Rogers 2013,
Wyneken &Lolavar 2015). The nesting beaches along Floridas
east coast are important because they produce themajority of the
loggerhead hatchlings entering theNorthwestern Atlantic Ocean (TEWG
2009). Thus, itis important to understand how environmental
fac-tors, specifically temperature and rainfall, influencehatchling
sex ratios a component of life history thatcan influence future
reproduction.
MATERIALS AND METHODS
Sand and rainfall
To document the effects of rainfall on sand tempera-ture at
different depths, we placed Hobo Model U22dataloggers (accuracy
0.2C; Onset Computer) inthe sand at 3 locations on a nesting beach
in Boca Ra-ton, Florida, during July and August 2014. The
data-loggers were distributed throughout ~1.4 km of thebeach and
were no closer than 2 m from the nearestnest. We recorded
temperatures every 10 min for 30 d.
The dataloggers were buried at 3 different depths:5, 18, and 30
cm to create temperature profiles of thesand column above the level
that may directly influ-ence eggs. The dataloggers at 5 cm recorded
the tem-peratures of surface sand. The top eggs of a logger-head
nest in Boca Raton are frequently at 26 to 32 cm(J. Wyneken unpubl.
data). To help identify how tem-perature changes with depth, we
included datalog-gers at 18 cm, which is above upper nest depth
butbelow hottest surface sand, and at 30 cm to recordsand
temperatures at upper nest depth. Rain gauges(Stratus RG202M Metric
Long Term Professional Rainand Snow Gauge, accuracy 0.02 cm),
located 5 to12 m away from the dataloggers, re corded daily
rain-fall amounts at each location. The rainfall data weregraphed
in temporal synchrony with sand tempera-ture data for each depth.
Data were not normally dis-tributed and were compared using
Kruskal-Wallistests (Zar 1999).
Nest temperatures, rainfall and sex ratios
Loggerhead Caretta caretta nests laid on thebeaches of Boca
Raton, Florida, USA (26.1819 N,80.0410 W to 26.3828 N, 80.0675 W)
during the2010 to 2013 nesting seasons were marked (n = 9 to13
nests yr1) and instrumented with temperaturedataloggers. Nests were
sampled throughout theentire nesting season (April to October). The
nestingseason was partitioned into 3 categories: early (Aprilto
mid-June), middle (mid-June through July), or late
236
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Lolavar & Wyneken: Rainfall and sea turtle sex ratios
237
season (August through September). The eggs incu-bated in situ
to allow normal environmental factors toinfluence the sex
ratios.
Nest temperatures were recorded using Onset
Model U22 dataloggers. A datalogger was placedin the center of
each clutch (~45 cm) during nest deposition or a few hours
afterwards. Nest tempera-tures (accuracy 0.2C) were recorded every
10 minthroughout incubation. After the hatchlings
emerged,dataloggers were removed and downloaded. Tem-perature data
were recorded for the entire incuba-tion duration (d) of each nest.
We estimated the TSPfrom incubation duration in 2 ways: the middle
thirdof the incubation period (33 to 66%; TSP) and thelater portion
of the middle third (50 to 66%; TSPL).
During 2013, the datalogger from nest CC13-539was excavated by a
raccoon but was replaced after5 h. The thermal data were discarded
for that 5 hperiod plus 2 h after the datalogger was
repositionedand the nest cavity resealed with sand. One datalog-ger
malfunctioned so no temperature data wererecorded for nest
CC13-271. No hatchlings were col-lected from nest CC13-317;
however, temperaturedata and hatch and emergence success were re
-corded.
Local rainfall and weather data for the 2010 to 2013nesting
seasons (April to October) were obtainedfrom the South Florida
Water Management Districtsenvironmental database, DBHYDRO (SFWMD
2013),as well as the National Weather Service. Graphingrainfall
data in daily synchrony with incubation tem-perature data
identified rainfall effects on nest tem-peratures. Incubation
temperatures were temporallysynchronized with daily rainfall
records. We matchedthe rainfall data by day with each nests
incubationtemperature data for the same day so that shifts innest
temperatures associated with rainfall could beidentified. Each
nests TSP was estimated and thatportion of the temperature graph
was used to identifywhether rain cooling had had the potential to
impactsex ratios. The presumed loggerhead pivotal temper-ature
(~29.0C) and TRT (26.532C) were used toidentify relevant
temperatures and interpret results.
Nests were monitored daily and the hatchlingsfrom the initial
major emergence were collected andbrought to the Florida Atlantic
University Marine Lab(Boca Raton, Florida, USA) where we
quasi-randomlyselected 10 morphologically normal
loggerheadhatchlings from each clutch for later sex ratio
sam-pling. We defined hatchlings as morphologically nor-mal by a
lack of scute, flipper or head abnormalities,weighing ~18 g and
having a flattened plastron. Thefirst major emergence was inferred
to consist of the
strongest hatchlings and those that might have thegreatest
chances of contributing to the population.The first major emergence
typically includes hatch-lings from a variety of positions in the
clutch (J.Wyneken unpubl. data). If fewer than 10
hatchlingsemerged, all of the available normal hatchlings
werecollected for the sex ratio sample. Nests were sampledfrom the
first, middle, and last quartiles of the seasonso the entire
nesting season was represented (2010,n = 117 hatchlings from 13
nests; 2011, n = 49 hatch-lings from 5 nests; 2012, n = 95
hatchlings from 11nests; 2013, n = 90 hatchlings from 10 nests). In
2011,just 9 nests provided hatchlings.
After the hatchlings emerged, nests were invento-ried for
success. Hatch success is defined as the per-centage of all eggs in
the nest that hatch, and emer-gence success is defined as the
percentage ofhatchlings that emerged from the nest. C.
carettaclutch size in Boca Raton averages 105 eggs per nest;the
hatch success is ~78% and average emergencesuccess is ~75% (J.
Wyneken unpubl. data). In somecases, sampling was not possible due
to temperaturedatalogger failure, nest losses to storms or
hatchlingsescaping before they could be collected.
To identify relationships among nest temperature,daily rainfall
amount and hatchling sex ratio, wegraphed daily rainfall in
temporal synchrony withincubation temperatures of each sampled
nest. Weempirically evaluated whether higher amounts ofrainfall
were associated with lower nest temperaturesand if that correlated
with higher male pro duction.Nest temperatures were summarized
graphically andas ranges during the estimated TSP. Comparisonswere
made using Kruskal-Wallis and Mann-Whitneytests.
Collected turtles were raised in the lab to 120 g,then sex was
identified laparoscopically (Wyneken etal. 2007). Sex ratios
reported are for the sample,which represents about 10% of the eggs
for eachnest. Following laparoscopic exam, the turtles werekept in
the lab for a minimum of 1 wk to ensure fullrecovery and then were
released offshore into theGulf Stream current. The Florida Atlantic
UniversityIACUC authorized the studies, which were permittedunder
Florida Marine Turtle Permit 073.
RESULTS
Sand temperatures and rainfall
Sand temperatures at the same depth, independentof turtle nests
and rainfall amounts, were compared
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Endang Species Res 28: 235247, 2015
at 3 locations for the same time period. Temperaturesat all
depths and locations experienced daily fluctua-tions associated
with diurnal heating and nocturnalcooling. However, the amplitude
of these fluctuationsdecreased with depth (Fig. 1). Sand
temperatures at5 cm and at 18 cm were not statistically different
atthe 3 locations (Kruskal-Wallis; H = 1.57, p > 0.05 at5 cm; H
= 1.91, p > 0.05 at 18 cm). However, sandtemperatures at 30 cm
differed among the 3 locations(Kruskal-Wallis; H = 8.85, p =
0.012). Mann-WhitneyU-tests indicated that sand temperatures at 30
cm inall locations differed from each other (Locations 1 vs.
2: H = 4.62; Locations 2 vs. 3: H = 4.01; Locations 1 vs.3: H =
9.85; p < 0.05 for each comparison). Tempera-tures of surface
sand increased and decreased morequickly than deeper sand. Sand
temperatures warmedup to ~44C at 5 cm, while sand at 18 cm and 30
cmwarmed to ~37C and ~34C, respectively. Similarly,cooling effects
from rain were also less extreme withdepth; mean sand temperatures
during heavy rainevents decreased to ~26C, 28C, and 29C at 5 cm,18
cm, and 30 cm, respectively.
Rainfall amounts among the 3 sample locationswere not
statistically different (Kruskal-Wallis; H =0.11, p > 0.05).
Sand temperatures decreased with sand depth atall locations
(Fig. 1) and were statistically differentamong the 3 depths at all
locations (Kruskal-Wallis;Location 1: H = 11.73, Location 2: H =
9.03, Location3: H = 6.76; p < 0.05 for each comparison). At
shal-lower sand depths, rainfall caused greater cooling.Periods
without rain or cloud cover caused greatersurface sand heating than
at deeper depths.
Average and standard errors of temperature oscil-lation ranges
associated with rainfall for all locationswere 11.47 1.1C (5 cm);
5.09 0.3C (18 cm); 2.89 0.3C (30 cm). A 27.4 cm rainfall event at
Location1 caused sand temperature at 5 cm depth to decreaseby
~10.5C, at 18 cm to decrease by ~4.9C, and at30 cm to decrease by
~3.1C (Fig. 1). After rainfall,temperature changes at all 3 depths
lasted roughlythe same amount of time (~4 d). Otherwise, therewere
few temperature differences among the samedepths at different
locations.
Hot nesting seasons: 2010 and 2011
The summer air temperatures in 2010 were recordhighs for coastal
regions to the north and south of oursite (West Palm Beach, Fort
Lauderdale and Miami);recorded temperatures ranged from 2 to 2.4C
abovenormal temperatures (NWS 2010). Periods withoutrain coincided
with rapid increases in nest tempera-ture concurrent with very warm
daily air tempera-tures. The 2010 rainy season lasted 141 d, 12 d
shorterthan the long-term average. Average wet seasonrainfall
ranges from 89 to 114 cm (35 to 45 inches),usually lowest over
coastal areas along both theAtlantic and Gulf coast (NWS 2012). The
2010 rain-fall amounts measured at the fixed sampling
stationsaveraged ~102 cm (~40 inches), although rainfallreaching
the nesting beach was lower by several cm.The 2010 rainy season was
characterized by littlecloud cover and widely varying rainfall
amounts
238
25
30
35
40
45
25
30
35
40
45
25
30
35
40
45
0
10 Jul
15 Jul
20 Jul
25 Jul
30 Jul
4 Aug
9 Aug
14 Au
g19
Aug
5
10
15
20
25
30
35
40
30 cm
5 cm
18 cm
Rai
nfal
l (cm
) S
and
tem
per
atur
e (
C)
Fig. 1. Impact of rainfall on sand temperature at 3 depths(5,
18, and 30 cm) from 3 loggerhead nesting beach locationsat Boca
Raton, Florida, from July 10 to August 19, 2014. Up-per 3 graphs
are sand temperatures: dark gray shows Loca-tion 1, light gray
shows Location 2, and medium gray showsLocation 3. Arrows identify
decreased sand temperaturewith greater rainfall. Bottom graph is
rainfall (in cm) at thesame locations and on the same dates as the
thermal data.Rainfall and sand temperature data at 5 and 18 cm at
differ-ent locations did not statistically differ; sand
temperatures
after rainfall differed significantly at different depths
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Lolavar & Wyneken: Rainfall and sea turtle sex ratios
(NWS 2010). The National Weather Service (NWS)characterized 2011
as having higher than normaltemperatures and 2011 was the warmest
calendaryear on record for West Palm Beach and Miami(north and
south of our site). The 2011 rainy season
was also shorter than average and lasted 133 d, 20 dless than
average (NWS 2011).
In both years, several nests reached peak tempera-tures close to
3637C and produced live hatchlings(Table 1). All turtles sampled in
2010 and 2011 were
239
Year & Season Date laid Incubation TSP range TSPL range
Emergence, hatch % femalenest ID (duration, d) range (C) (C) (C)
success (%)
2010CC 10-2 E 10 May (49) 27.836.5 30.633.8 31.934.4 24,42 100CC
10-3 E 11 May (50) 28.335.9 30.233.9 31.033.7 44,59 100CC 10-4 E 15
May (54) 27.734.7 30.334.0 32.034.0 90,90 100CC 10-15 E 22 May (50)
29.335.3 31.434.8 33.734.0 33,37 100CC 10-16 E 22 May (51) 28.634.1
29.932.9 31.532.8 43,61 100CC 10-34 E 28 May (47) 30.135.9 32.835.2
33.934.9 61,71 100CC 10-37 E 28 May (47) 29.435.0 31.333.7
32.533.4CC 10-65 E 3 June (46) 30.335.3 32.733.9 33.033.5 58,65
100CC 10-121 M 16 June (47) 29.134.9 29.134.0 31.933.2 61,65 100CC
10-143 M 20 June (47) 29.435.5 29.434.3 33.633.9 47,47 100CC 10-221
M 28 June (48) 29.235.4 32.234.8 33.034.5 41,58 100CC 10-364 M 22
July (50) 30.735.0 30.735.0 33.733.9 43,43 100CC 10-389 M 26 July
(48) 30.034.6 30.034.6 32.434.1 59,62 100CC 10-420 L 6 Aug (49)
30.834.5 31.434.0 31.432.8 4,4 1002011CC 11-36 E 16 May (49)
27.635.0 30.132.9 31.032.6 44,49 100CC 11-40 E 18 May (49) 28.435.1
31.433.9 31.733.8 96,96 100CC 11-44 E 21 May (50) 29.734.7 31.134.2
31.833.7 98,98 100CC 11-237 M 21 June (52) 29.136.9 29.736.6
34.336.3 15,21 100CC 11-276 M 25 June (50) 27.736.5 32.135.6
33.434.9 49,67CC 11-284 M 26 June (52) 28.535.9 31.735.3 33.835.0
74,82 1002012CC 12-2 E 22 April (57) 0,87 0CC 12-4 E 26 April (61)
23.933.1 26.631.5 28.931.5 77,98 0CC 12-6 E 1 May (57) 24.434.6
26.632.6 28.932.6 0,97 100CC 12-11 E 3 May (57) 95,95 100CC 12-287
M 16 May (58) 79,91 100CC 12-295 M 16 May (58) 95,95CC 12-453 M 2
July (50) 77,78 100CC 12-547 M 8 July (47) 18,46 100CC 12-730 L 26
July (51) 24.833.5 28.233.5 28.233.5 0,99 100CC 12-745 L 30 July
(54) 27.733.9 27.733.9 27.733.9 95,95 100CC 12-749 L 31 July (52)
22.333.1 27.833.1 27.832.4 87,87 100CC 12-756 L 3 Aug (51) 27.533.9
27.533.3 29.033.3 58,58CC 12-775 L 8 Aug (50) 28.834.2 28.834.2
32.734.2 14,26 1002013CC 13-2 E 27 April (59) 24.134.6 27.530.8
27.530.8 87,91 12.5CC 13-7 E 2 May (56) 24.035.2 26.830.8 26.829.9
87,95 20CC 13-8 E 3 May (54) 23.435.3 26.930.6 27.029.8 19,92 0CC
13-9 E 3 May (56) 23.735.0 27.530.6 27.529.6 89,95 20CC 13-271 M 20
June (46) 46,76 100CC 13-317 M 26 June (53) 27.634.3 27.632.7
30.332.7 96,98CC 13-389 M 4 July (50) 27.335.3 28.133.0 30.733.0
29,61 100CC 13-452 M 11 July (52) 28.036.1 31.034.6 31.434.6 78,92
100CC 13-39 L 20 July (48) 28.835.9 30.135.9 31.135.9 76,77 100CC
13-574 L 25 July (49) 29.035.3 31.235.3 31.735.3 93,94 100CC 13-662
L 24 Aug (52) 28.133.4 28.133.0 28.932.0 33,64 90
Table 1. Loggerhead turtle Caretta caretta nest metrics for 2010
to 2013 nesting seasons in Boca Raton, Florida, USA. Boldedrows in
2012 and 2013 indicate nests with cooler incubation temperatures
that resulted in male-biased sex ratios. Temperatureranges are
expressed as minimum and maximum values. Seasons: E, early season
(April to mid-June); M, mid-season (mid-June through July); L, late
season (August through September). Duration: incubation duration in
days. Thermosensitive pe-riod is the middle third (3366%; TSP) or
the later portion of the middle third (5060%; TSPL) of the
incubation period
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Endang Species Res 28: 235247, 2015
females. Nest temperatures (Table 1) during theseyears, and
particularly during the TSP remained rel-atively high. In 2010 and
2011, nests experiencedtemperature differences between the TSP and
TSPLas temperatures continually increased. In both years,incubation
temperatures during the TSP and TSPLremained above the published
loggerhead pivotaltemperature (29C) and near or beyond the
upperboundary of the TRT. Temporally synchronized graphsof nest
temperatures and rainfall from 2010 showedthat just 1 nest
(CC10-121) experienced a large rain-fall event that impacted
temperatures during the TSP(Fig. 2). Nest CC10-121 reached its
lowest tempera-ture (29.10C) during the TSP after a rainfall event
of8.2 cm. This temperature was close to the estimatedpivotal
temperature but only lasted for ~3 h. Temper-atures rapidly
increased, returning to and exceedingprevious baseline temperatures
recorded during the~8.5 d prior to the rainfall event. Rainfall
events in2010 and 2011 were infrequent or small, so nest
tem-peratures changed little. Periods of little or no rainfallwere
associated with higher incubation temperatures(Fig. 2) than during
rainfall. In 2010, no hatchlingswere collected from nest CC10-37 so
there is norecorded sex ratio, hatch or emergence success forthis
nest.
During 2011, temperature data were available for6 early and
middle season nests (Table 1). Bothweather events and equipment
failures combined toreduce sample sizes. Five late season nests
were lostto storm tides, reducing the samples whose TSPs wereduring
the warmest part of the season. No hatchlingsfrom nest CC11-276
were collected so no sex ratiosample was acquired; however,
emergence and hatchsuccess were estimated upon nest inventory.
Wet nesting seasons: 2012 and 2013
The NWS characterized 2012 as cooler than 2010and 2011, with
temperatures near or below normalthrough November due to increased
cloud cover andheavy rain (NWS 2012). The 2012 rainy season
wasextremely wet during the summer, particularly insoutheast
Florida, partially due to the effects of Trop-ical Storms Debby and
Isaac and Hurricane Sandy.The 2012 rainy season began 1 wk earlier
than in2010 and 2011. Eastern Florida received near recordamounts
of rainfall from May to mid-October andthere was extensive cloud
cover. Eastern Palm BeachCounty, the location of our nests,
received 128 cm ofrain (SFWMD 2012). Average yearly rainfall of 114
to152 cm (45 to 60 inches) fell from May to October
(NWS 2012). The longer rainy season and greatercloud cover
provided a cooler incubation environ-ment for 2012 nests. Similar
to 2012, the 2013 nestingseason was wetter than normal with each
month ofthe rainy season featuring above normal rainfallamounts.
Isolated areas in southeast Florida experi-enced over 127 cm (50
in) of rain and most areasreceived 89 to 114 cm (35 to 45 inches)
(NWS 2013).May through July represented the wettest start to
therainy season in 45 yr (NWS 2013). This time periodcoincides with
the thermosensitive periods of most ofthe 2013 sampled nests.
In 2012, temperature data were collected from 4early and 5 late
season nests. Not all middle seasonnest temperatures were available
due to equipmentfailures. However, emergence and hatch successwere
measured for all nests, and sex ratios were sam-pled for 11 nests.
The first 2 nest samples (CC12-2and CC12-4) were 100% male. The
subsequent 9nests provided 100% female hatchling samples. Forall
sampled nests, incubation temperatures rangedfrom below the pivotal
temperature to near to orabove the upper TRT boundary. Temperature
datawere obtained for only one of the 100% male sam-ples, which had
nest temperatures during the esti-mated TSP averaging around the
pivotal tempera-ture (Table 1). During incubation of the 2
all-malesample nests, rainfall events were frequent but tendedto be
small. Just 2 rainfall events yielded more than6 cm (Fig. 2) and
resulted in nest cooling that rangedfrom 4.3 to 5.1C. Late season
nests ex perienced tem-peratures above the TRT. An 11.5 cm rainfall
eventon August 27, 2012, caused temperatures to drop to27 29C from
3334C for ~4 d toward the end ofseveral nests TSP (Fig. 2; CC12-730
and CC12-745).However, these nests quickly returned to
warmertemperatures, well above the pivotal temperature.All middle
season and late season nest samples in2012 were 100% female. Nests
without associatedsex ratio estimates were due to turtles escaping
beforethey could be collected.
In 2013, early season nests experienced cooler tem-peratures,
and hatchling samples were predomi-nantly male. The first 4 nests
of the season had highlymale-biased sample sex ratios (0 to 20%
female). Theremaining 6 nests were from middle and late parts ofthe
seasons; those samples were 100% female (5nests) and 90% female (1
nest, CC13-662). Early sea-son nest temperatures during the TSP
fluctuated1.52C around the pivotal temperature (Table 1).These
nests experienced cooler sand temperatures atthe beginning of their
incubation periods associatedwith a large rainfall event of ~14.3
cm. Two subse-
240
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Lolavar & Wyneken: Rainfall and sea turtle sex ratios
241
CC10-420
1 May
21 Ma
y10
Jun30
Jun 20 Jul
9 Aug
29 Au
g18
Sep
1 May
21 Ma
y10
Jun30
Jun 20 Jul
9 Aug
29 Au
g
15
12
9
6
3
0
15
12
9
6
3
0
CC10-65
CC10-121
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
35
32
29
26
23
CC10-4
CC11-237
CC11-284
CC11-40
CC11-44
2010 2011
Rai
nfal
l (cm
) N
est
tem
per
atur
e (
C)
Fig. 2. (above and next page) Nest temperatures and rainfall for
the 2010 to 2013 loggerhead turtle nesting seasons at Boca Ra-ton,
Florida. We selected temperature data for 4 example nests
representative of each nesting season (top 4 rows for eachyear).
Incubation temperatures measured in each nest are shown by the gray
plot lines. The red shading indicates the pub-lished transitional
range of temperatures (TRT) over which males and females may occur
in Florida (Girondot 1999). The verti-cal gray boxes denote the
predicted thermosensitive period (TSP) for each nest during which
embryonic sex is determined.
Rainfall (cm) by year for the same nesting season dates is shown
in the bottom row of graphs set
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Endang Species Res 28: 235247, 2015
quent rainfall events of ~8.4 cm and ~7.2 cm furthercooled early
season nests, dropping nest tempera-tures below 27C (Fig. 2).
Smaller amounts of rainand cloud cover throughout the early portion
of theseason likely also contributed to cooling. After early
season nest TSPs, fewer and smaller rainfall eventsoccurred and
temperatures quickly rose above thepivotal temperature and TRT.
Mid- and late seasonnests experienced temperatures above the
pivotaltemperature and TRT for the majority of their TSPs.
242
23
26
29
32
35 CC12-745
23
26
29
32
35 CC12-730
23
26
29
32
35 CC12-4
23
26
29
32
35 CC12- 6
23
26
29
32
35 CC13-7
23
26
29
32
35 CC13-452
23
26
29
32
35 CC13-662
0
3
6
9
12
15
23
26
29
32
35 CC13-2
0
3
6
9
12
15
2012 2013R
ainf
all (
cm)
Nes
t te
mp
erat
ure
(C
)16
Apr
4 M
ay22
May
9 Ju
n27
Jun
15 Ju
l2
Aug
20 A
ug7
Sep
25 S
ep13
Oct
26 A
PR16
May
5 JU
N25
JUN
15 JU
L4
AUG
24 A
UG13
SEP
3 OC
T
Fig. 2 (continued)
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Lolavar & Wyneken: Rainfall and sea turtle sex ratios
Late season nests also experienced high tempera-tures but a ~8.7
cm rainfall event and subsequentsmaller rainfall amounts led to
fluctuating tempera-tures rather than the steady increase
experienced byearly and middle season nests. Nest CC13-662
expe-rienced lower temperatures than other late seasonnests. During
its TSP, temperatures decreased to~28C and remained within the TRT
(Fig. 2).
DISCUSSION
Sand temperatures and rainfall
The findings from this study are important forunderstanding the
effects of weather and climate atthe beach surface vs. the nest
level. The low ampli-tude changes and cooler temperatures at the
deepersand position (upper nest level) suggest that theimpact of
increased air temperatures is lesser herethan for shallower sand.
Moreover, precipitationmust be greater to have an effect on deeper
sandcompared to sand near the surface. If turtles lay shal-lower
nests, the effects can, theoretically, be morepronounced than the
effects on deeper nests. Fur-ther, rainfall events cooled the upper
sand layersmore than deeper sand. Thus, there is a graded
influ-ence of moisture that is smallest at the level whereeggs
could be affected, should they be present.Larger variations among
sand temperatures at 5 cmcompared to 18 cm and 30 cm are consistent
with theobservation that the temperature variation of shal-lower
turtle nests tends to be greater (Spotila et al.1987) than in
deeper nests. Periods of little or no rainwere associated with
warmer sand temperatures atall depths.
Weather and sea turtle nest incubation season
In south Florida the loggerhead sea turtle nestingseason begins
in late April and ends approximatelyin August, so nests incubate
into October. The rainyseason is defined as the months of the year
whensouth Florida receives roughly 70% of its annual rain(NWS
2013); this usually spans May to October. Hur-ricane season is
roughly June to November. These 3ranges coincide, suggesting that
the rainy season,including the hurricane season, has the potential
toimpact sea turtle sex ratios. Low rainfall amountscontributed to
the lack of male hatchlings in our2010, 2011, and the majority of
2012 and 2013 sam-ples. However, early season nests in 2012 and
2013
had male-biased sex ratios; these nests experiencedcooler
temperatures from heavier precipitation in theearly portion of the
nesting season. Early seasonnests in all 4 years began incubation
at cooler tem-peratures that rapidly increased, likely due to
adecrease in rainfall as the season progressed.
Hot nesting seasons: 2010 and 2011
In 2010 and 2011, temperatures remained abovethe upper boundary
of the TRT throughout the TSP,suggesting all-female samples should
occur (Fig. 2).Eggs cease embryonic diapause once they are
laid(Miller 1997, Miller et al. 2003, Rafferty & Reina2012). At
our site, sand temperature is near or abovethe pivotal temperature
at the time eggs are laid.Consequently, eggs resumed development
andremained well above the pivotal temperature formost of
incubation. We examined incubation temper-atures during both
estimates of the TSP by dividingincubation duration into 2 separate
categories: theentire middle third of incubation, TSP (3366%
ofincubation) and the later portion of the middle third,TSPL (5066%
of incubation). A previous study ofother turtle species suggested
the end of the TSPrange (Yntema stages 2327 of 30) is
particularlyimportant in sex differentiation based upon anincrease
in gonadal aromatase activity (Desvages etal. 1993) in embryos
incubated at 27 and 30.5C.Temperatures during the 2 TSP ranges
varied verylittle. Despite slight differences between portions
ofthe TSP, most of our nest temperatures during bothTSP estimates
remained above the pivotal tempera-ture as well as the upper TRT
boundary (except forvery brief temperature drops due to rainfall).
In 2010and 2011, temperatures remained above the upperboundary of
the TRT throughout the TSP, which issupported by all female samples
in these years(Fig. 2). Nests in 2010 and 2011 experienced
lessrainfall and warmer ambient temperatures, causingnest
temperatures to increase rapidly and constantlythroughout all nest
incubation periods. Thus, nesttemperatures during the TSPL in these
years tendedto be warmer compared to the entire TSP. In all 2010and
2011 nests, temperatures during TSPL wereabove the pivotal
temperature and mostly above theupper boundary of the TRT, in spite
of rainfall events(Table 1).
Laparoscopic identification of the turtles sex corre-sponded
with expectations based on sampled nesttemperatures. All 2010 and
2011 samples werefemales, which is consistent with the
particularly
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Endang Species Res 28: 235247, 2015
high nest temperatures and minimal effects of localrainfall
events. Although it is tempting to suggestthat even a brief
reduction in temperature mightimpact the clutch sex ratio, evidence
from this studysuggests that short duration temperature declinesare
unlikely to impact the sex ratio, at least whenoverall temperatures
are warm (e.g. nest CC10-121from the 2010 nesting season). Temporal
models ofnonlinear thermal effects on sex ratio, such asGeorges et
al. (1994) and Telemeco et al. (2013a),suggest that the daily
proportion of development ator above a given temperature likely
directs sex deter-mination rather than single brief periods of
tempera-ture change. The Georges et al. (1994) approach
alsoconsiders that development is faster at warmer tem-peratures
and slower at cooler temperatures. Conse-quently, isolated rainfall
may have little effect ondevelopment in warm fast-developing nests.
We con-clude that it is only multiple and/or prolonged rain-fall
events that may impact the sex ratios.
Periods without rain and with very warm daily airtemperatures
coincided with rapid increases in nesttemperature, particularly in
2010 and 2011. Ourresults are consistent with those of Segura &
Cajade(2010), who found that sand temperatures increasedwith
decreasing rainfall. Several of our nests reachedincubation
temperatures that are above reportedthermal maxima for sea turtle
nests. Extreme temper-atures, hot or cold, can disrupt embryonic
develop-ment (Bustard & Greenham 1968, McGehee 1979,Yntema
& Mrosovsky 1980, Telemeco et al. 2013b).Miller (1997) found
that Australian Caretta carettaeggs incubated at temperatures
>33C rarely hatch.The nests in the present study hatched when
temper-atures were higher, which suggests that Florida log-gerheads
may have a higher thermal threshold forsuccessful incubation.
However, hatch success gen-erally was lower in the warmest nests.
Hatchlingsfrom nests that reached 36 to 37C during the lasthalf of
development often died within a few hours ofescaping the nest (J.
Wyneken pers. observ.). Conse-quently, nests incubating during warm
dry yearstend to produce fewer hatchlings, and these are
predominately females. Past studies of other taxa(Trivers &
Willard 1973, Kruuk et al. 1999) suggestthat a greater proportion
of females should be pro-duced when conditions are unfavorable.
Bull &Charnov (1989) suggest that skewed primary sexallocation
results from sex differences in fitness gainsfrom the incubation
environment. They also predictthat the direction of a sex ratio
bias is often towardthe sex produced in the poorer environment.
Theconclusions of these studies are consistent with our
studys findings. Our results show a strong femalebias across
several extreme years, which were likelydirected proximally by the
strong temperature influ-ence on sex determination, as well as
ultimately byevolutionary implications of conditions unfavorablefor
successful development.
Rainfall and rainy season duration were less thanaverage in the
2010 and 2011 nesting seasons. The2010 rainy season had little
cloud cover and widely-varying rainfall, which likely contributed
to highbeach temperatures. For example, Palm Beach Inter-national
Airport, located 40 km to the north of our sitereceived only 63 cm
(25 in) of rain, while Palm BeachGardens (~58 km to the northwest)
received 113 cm(45 in). Local variation of rainfall amounts may
resultin differences in sex ratios among nesting beaches;however,
we did not detect such. The short 2011rainy season averaged ~91 cm
of rainfall over south-east Florida where our nests were
located.
Wet nesting seasons: 2012 and 2013
Nests in 2012 and 2013 experienced conditions thatdiffered from
2010 and 2011. Rainfall was greaterthan average in the 2012 and
2013 nesting seasonsand the consequences were reflected in
sampledhatchling sex ratios. The NWS characterized 2012 ascooler
than 2010 and 2011, with temperatures near orbelow normal through
November due to increasedcloud cover and heavy rain (NWS 2012). The
2012rainy season was extremely wet during the summer,particularly
in southeast Florida, partially due to theeffects of Tropical
Storms Debby and Isaac and Hur-ricane Sandy. The 2013 rainy season
was character-ized by high summer rainfall amounts with eachrainy
season month experiencing above normal rain-fall. Tropical Storm
Andrea was the 2013 tropical sys-tem to impact south Floridas
weather, which gaveindirect effects in early June as its widespread
rain-fall and clouds likely contributed to male productionin early
season nests.
Early nest incubation temperatures in 2012 and2013 remained
within or close to the TRT but middleand late season nests
experienced temperaturesabove the TRT. Early nests in 2012 and 2013
experi-enced frequent rainfall and cooler incubation tem-peratures,
which likely contributed to the productionof males in contrast to
previous years. As with mostbiological systems, turtle development
is slower atcooler temperatures (Yntema 1978, Georges et al.1994).
Thus, only multiple and/or prolonged rainfallevents may impact the
sex ratios. Slow early develop-
244
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Lolavar & Wyneken: Rainfall and sea turtle sex ratios
ment may also have caused us to misidentify the TSPso that it
occurred later than we expected (see Giron-dot et al. 2010),
although that did not seem to be thecase. The 2012 and 2013 early
season nests experi-enced frequent periods of cooling throughout
theestimated TSP and hatchling samples were stronglymale biased
(Table 1, Fig. 2).
In 2012, a large rainfall event of 11.5 cm, followedby numerous
smaller rainy periods, caused late sea-son nest temperatures to
decline and remain withinthe TRT and near the pivotal temperature.
However,all resulting lower temperatures occurred after
theestimated TSP and thus likely did not affect sexratios. In 2013,
mid-season nests experienced fre-quent rainfall before the TSP
which lowered nesttemperatures to ~27C; however, for the remainder
ofincubation (including the TSP) little rain fell andclutch
temperatures rapidly increased above 35C(Fig. 2). Late season nests
in 2013 also experiencedhigh temperatures but a ~8.7 cm rainfall
event andsubsequent smaller rainfall amounts led to
fluctuatingtemperatures rather than the steady increase
experi-enced by early and middle season nests. The last nestof the
season (CC13-662) experienced lower temper-atures than other late
season nests. During its TSP,temperatures decreased to ~28C and
remainedwithin the TRT (Fig. 2). These lower temperatureslikely
explain its 90% female sex ratio compared tothe 100% female sex
ratios of the middle and otherlate season nests. However, by
sampling ~10% of theclutch on average (13% or more of the
emergenthatchling), we cannot rule out that some of our sam-ples
may be biased. In 2012, all sampled nests experi-enced temperatures
below the pivotal temperatureduring TSPL except for nest CC12-775,
the last sam-pled nest of the season, which was relocated after
theTSP to a higher and drier location due to the threat ofTropical
Storm Isaac. This nest experienced thewarmest temperatures of the
season, which likelyprevented nest cooling during periods of rain.
Similarto past years, all 2012 nests experienced temperaturesabove
the TRT but heavy rainfall events kept hightemperatures brief (Fig.
2). During TSPL, early 2013nests experienced temperatures below the
pivotaltemperature and never exceeded the upper boundaryof the TRT,
while mid- and late season nests ex -ceeded both the pivotal
temperature and the TRT.The last sampled nest of the season
experienced fluc-tuating temperatures that fell below the pivotal
tem-perature but remained within the TRT during TSPL.
Loggerhead nesting habits may also contribute tothe high female
sex bias of their nests. Loggerheadturtles tend to nest in the
middle of the beach (sea-
ward of the dune foot; Wood & Bjorndal 2000), conse-quently
their nests are seldom shaded, and theirnests are relatively
shallow. Loggerheads nesting inGreece tend to nest away from the
water and closeto, but not beyond, the vegetation line (Hays
&Speakman 1993). All sampled nests in the presentstudy were
seaward of the vegetation line but variedin proximity to the high
tide line. A nests distancefrom the water may also influence
incubation condi-tions. Sands higher and further away from the
watertend be warmer and have less moisture (Hays &Speakman
1993, Wood & Bjorndal 2000). Conse-quently, nests closer to the
water may be moister,which can impact the way they respond to
changingtemperature. Our study highlights the effects thatrainfall
has on nest temperature because it is oftencool and because once
sand is moist it requires moreheat energy to raise the temperature
than drier sandsdue to higher specific heat capacity and thermal
iner-tia from increased water content (Idso et al. 1975a,Reginato
et al. 1976, Lakshmi et al. 2003).
Studies quantifying the effect of rainfall on nestshave been
inconsistent in their findings. Jourdan &Fuentes (2013) suggest
that manually wetting nestsmay not reduce sand temperatures in hot
areas. Theyreport that sprinkling nests with water during theday
actually increased sand temperatures. However,Naro-Maciel et al.
(1999) reported that 2 h of sprin-kling decreased nest temperature
by ~1C. Conse-quently, the effects may vary with specific local
con-ditions, including rainfall amount and duration.
While sex determination in sea turtles is primarilydirected by
temperature (Bull 1980, Mrosovsky &Yntema 1980, Standora &
Spotila 1985, Wibbels2003, reviewed in Valenzuela & Lance
2004), thespecific re sponse mechanisms to temperature
remainelusive. Here we focus on the relationships amongnest
temperature, factors that modify temperatureeffects, and hatchling
sex ratios. An understanding ofthe impact of rainfall on the nest
temperature and sexratios is important because it identifies key
responsesby developing eggs that eventually impact sea
turtleproduction. Increasing air temperatures increaseevaporation,
which leads to greater precipitation insome regions (IPCC 2007).
The IPCC reports thataverage global temperatures have increased,
andalong with that, so has average global precipitation.However,
there is large variation among regions. It isparticularly important
to understand what changes intemperature and precipitation imply
for species thatrely upon them. In addition, understanding
theimpacts of increased rain and temperature togetherare necessary
to implement appropriate manage-
245
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Endang Species Res 28: 235247, 2015
ment strategies. Based upon the relationship wefound between
nest temperatures and heavy vs.sparse rainfall, future studies on
hatchling sex ratiosrelative to environment should include effects
of bothmoisture and temperature. Understanding the im -pact of
rainfall as well as temperature may allow biol-ogists not only to
better predict hatchling sex ratiobiases but also to anticipate the
effects of changingtemperature and precipitation on sex ratios.
Acknowledgements. We thank E. Frazier, R. Murphey, andJ. Nambu,
who guided A.L.'s participation in The NationalScience Foundation
Undergraduate Research & MentoringProgram (#0829250). Grants to
J.W. from the Disney World-wide Conservation Fund, SaveOurSeas
Foundation, Nelli-gan Sea Turtle Fund, and personal funds supported
this pro-ject. This study would not have been possible without
thegenerous help of Gumbo Limbo Nature Centers Sea
TurtleSpecialists, L. Bachler, M. Rogers, K. Rusenko, B. Tezak,
andN. Warraich. S. Libreros, R. Garcia, S. Epperly, F. Janzen, M.J.
Saunders, M. Salmon and an anonymous reviewer pro-vided
constructive criticism that improved this manuscript.
LITERATURE CITED
Blair K (2005) Determination of sex ratios and their
relation-ship to the nest temperature of loggerhead sea
turtle(Caretta caretta, L.) hatchlings produced along
thesoutheastern Atlantic coast of the United States. MS the-sis,
Florida Atlantic University, Boca Raton, FL
Bull JJ (1980) Sex determination in reptiles. Q Rev Biol 55:
321
Bull JJ (1985) Sex ratio and nest temperature in turtles:
com-paring field and laboratory data. Ecology 66: 11151122
Bull JJ, Charnov EL (1989) Enigmatic reptilian sex
ratios.Evolution 43: 15611566
Bustard RH, Greenham P (1968) Physical and chemical fac-tors
affecting hatching in the green sea turtle, Cheloniamydas (L.).
Ecology 49: 269276
Cagle KD, Packard GC, Miller K, Packard MJ (1993) Effectsof the
microclimate in natural nests on development ofembryonic painted
turtles, Chrysemys picta. Funct Ecol7: 653660
Carthy RR, Foley AM, Matsuzawa Y (2003) Incubation envi-ronments
of loggerhead turtle nests: effects on hatchingsuccess and
hatchling characteristics. In: Bolten AB,Witherington BE (eds)
Loggerhead sea turtles. Smithson-ian Institution, Washington, DC, p
144153
Desvages G, Girondot M, Pieau C (1993) Sensitive stages forthe
effects of temperature on gonadal aromatase activityin embryos of
the marine turtle Dermochelys coriacea.Gen Comp Endocrinol 92:
5461
Finkler MS (2006) Does variation in soil water contentinduce
variation in the size of hatchling snapping turtles(Chelydra
serpentina)? Copeia 769777
Georges A, Limpus C, Stoutjesdijk R (1994) Hatchling sex inthe
marine turtles Caretta caretta is determined by pro-portion of
development at a temperature, not daily dura-tion of exposure. J
Exp Zool 270: 432444
Georges A, Doody S, Beggs K, Young J (2004) Thermal mod-els of
TSD under laboratory and field conditions. In: Valenzuela N, Lance
V (eds) Temperature-dependent
sex determination in vertebrates. Smithsonian
InstitutionScholarly Press, Washington, DC, p 7989
Girondot M (1999) Statistical description of
temperature-dependent sex determination using maximum likeli-hood.
Evol Ecol Res 1: 479486
Girondot M, Ben Hassine S, Sellos C, Godfrey M, GuillonJM (2010)
Modeling thermal influence on animal growthand sex determination in
reptiles: being closer to the tar-get gives new views. Sex Dev 4:
2938
Godfrey MH, Barreto R, Mrosovsky N (1996) Estimating pastand
present sex ratios of sea turtles in Suriname. Can JZool 74:
267277
Hays G, Speakman J (1993) Nest placement by loggerheadturtles,
Caretta caretta. Anim Behav 45: 4753
Hays GC, Ashworth JS, Barnsley MJ, Broderick AC and oth-ers
(2001) The importance of sand albedo for the thermalconditions on
sea turtle nesting beaches. Oikos 93: 8794
Houghton JDR, Myers AE, Lloyd C, King RS, Isaacs C, HaysGC
(2007) Protracted rainfall decreases temperaturewithin leatherback
turtle (Dermochelys coriacea)clutches in Grenada, West Indies:
ecological implicationsfor a species displaying temperature
dependent sexdetermination. J Exp Mar Biol Ecol 345: 7177
Idso S, Jackson R, Reginato R, Kimball B, Nakayama F(1975a) The
dependence of bare soil albedo on soil watercontent. J Appl
Meteorol 14: 109114
IPCC (2007) Contribution of Working Group I to the
FourthAssessment Report of the Intergovernmental Panel onClimate
Change. Cambridge University Press, Cam-bridge
Jourdan J, Fuentes, MMPB (2013) Effectiveness of strategiesat
reducing sand temperature to mitigate potentialimpacts from changes
in environmental temperature onsea turtle reproductive output.
Mitig Adapt Strateg GlobChange 20: 121133
Kraemer JE, Bell R (1980) Rain-induced mortality of eggsand
hatchlings of loggerhead sea turtles (Caretta caretta)on the
Georgia coast. Herpetologica 36: 7277
Kruuk LE, Clutton-Brock TH, Albon SD, Pemberton JM,Guinness FE
(1999) Population density affects sex ratiovariation in red deer.
Nature 399: 459461
Lakshmi V, Jackson TJ, Zehrfuhs D (2003) Soil
moisturetemperature relationships: results from 2 field
experi-ments. Hydrol Processes 17: 30413057
LeBlanc AM, Wibbels T (2009) Effect of daily water treat-ment on
hatchling sex ratios in a turtles with tempera-ture-dependent sex
determination. J Exp Biol 311A: 6872
Matsuzawa Y, Sato K, Sakamoto W, Bjorndal K (2002) Sea-sonal
fluctuations in sand temperature: effects on theincubation period
and mortality of loggerhead sea turtle(Caretta caretta)
pre-emergent hatchlings in Minabe,Japan. Mar Biol 140:639646
McGehee MA (1979) Factors affecting the hatching successof
loggerhead sea turtle eggs (Caretta caretta). MS the-sis,
University of Central Florida, Orlando, FL
McGehee MA (1990) Effects of moisture on eggs and hatch-lings of
loggerhead sea turtles (Caretta caretta). Her-petologica 46:
251258
Miller JD (1997) Reproduction in sea turtles. In: Lutz PL,Musick
JA, Wyneken J (eds) The biology of sea turtles,Vol. II, CRC Press,
Boca Raton, FL, p 5181
Miller JD, Limpus CJ (1981) Incubation period and
sexualdifferentiation in the green turtle Chelonia mydas L. In:
Proceedings of the Melbourne Herpetological Sympo-sium. Zoological
Board of Victoria, Parkville, Victoria,p 6673
246
http://dx.doi.org/10.1007/s00227-001-0724-2http://dx.doi.org/10.1002/hyp.1275http://dx.doi.org/10.1038/20917http://dx.doi.org/10.1175/1520-0450(1975)014%3C0109%3ATDOBSA%3E2.0.CO%3B2http://dx.doi.org/10.1016/j.jembe.2007.02.001http://dx.doi.org/10.1034/j.1600-0706.2001.930109.xhttp://dx.doi.org/10.1006/anbe.1993.1006http://dx.doi.org/10.1002/jez.1402260317http://dx.doi.org/10.1139/z96-033http://dx.doi.org/10.1159/000280585http://dx.doi.org/10.1002/jez.1402700504http://dx.doi.org/10.1643/0045-8511(2006)6[769%3ADVISWC]2.0.CO%3B2http://dx.doi.org/10.1016/S0306-4565(01)00017-1http://dx.doi.org/10.1006/gcen.1993.1142http://dx.doi.org/10.2307/2390185http://dx.doi.org/10.2307/1934455http://dx.doi.org/10.2307/2409470http://dx.doi.org/10.2307/1939163http://dx.doi.org/10.1086/411613
-
Lolavar & Wyneken: Rainfall and sea turtle sex ratios
Miller JD, Limpus CJ, Godfrey MH (2003) Nest site selec-tion,
oviposition, eggs, development, hatching, andemergence of
loggerhead turtles. In: Bolton AB, Wither-ington BE (eds)
Loggerhead sea turtles. Johns HopkinsUniversity Press, Baltimore,
MD, p 125143
Mrosovsky N (1988) Pivotal temperature for loggerhead tur-tles
(Caretta caretta) from northern and southern nestingbeaches. Can J
Zool 66: 661669
Mrosovsky N (1994) Sex ratios of sea turtles. J Exp Zool 270:
1627
Mrosovsky N, Provancha J (1992) Sex ratio of hatchling
log-gerhead sea turtles: data and estimates from a 5-yearstudy. Can
J Zool 70: 530538
Mrosovsky N, Yntema CL (1980) Temperature dependenceof sexual
differentiation in sea turtles: implications forconservation
practices. Biol Conserv 18: 271280
Naro-Maciel E, Mrosovsky N, Marcovaldi MA (1999) Ther-mal
profiles of sea turtle hatcheries and nesting areas atPraia do
Forte, Brazil. Chelonian Conserv Biol 3: 407413
NWS (National Weather Service) (2010) 2010 Rainy SeasonUnderway.
US Department of Commerce, NationalOceanic and Atmospheric
Administration, National Mar-ine Fisheries Service. National
Weather Service, WeatherForecast Office. Miami, FL.
www.srh.noaa.gov/ images/mfl/news/RainySeason2010.pdf (accessed 13
Jul 2013)
NWS (National Weather Service) (2011) South Florida DrySeason
Outlook 20112012. US Department of Com-merce, National Oceanic and
Atmospheric Administra-tion, National Marine Fisheries Service.
National Wea -ther Service, Weather Forecast Office. Miami, FL.
http://www.srh.noaa.gov/images/mfl/news/2011RainySeason-Summary.pdf
(accessed 21 Jul 2013)
NWS (National Weather Service) (2012) South Florida DrySeason
Outlook 20122013. US Department of Com-merce, National Oceanic and
Atmospheric Administra-tion, National Marine Fisheries Service.
National Wea -ther Service, Weather Forecast Office. Miami, FL.
www.srh.noaa.gov/images/mfl/news/DrySeasonOutlook1213.pdf (accessed
21 Jul 2013)
NWS (National Weather Service) (2013) South Florida DrySeason
Outlook 20132014. US Department of Com-merce, National Oceanic and
Atmospheric Administra-tion, National Marine Fisheries Service.
National Wea -ther Service, Weather Forecast Office. Miami, FL.
www.srh.noaa.gov/images/mfl/news/DrySeasonRelease2013.pdf (accessed
26 Mar 2014)
Packard GC, Packard MJ, Miller K, Boardman TJ (1987)Influence of
moisture, temperature, and substrate onsnapping turtle eggs and
embryos. Ecology 68: 983993
Packard GC, Packard MJ, Birchard GF (1989) Sexual
differ-entiation and hatching success by painted turtles
incu-bating in different thermal and hydric
environments.Herpetologica 45: 385392
Pieau C, Girondot M, Desvages G, Dorizzi M, Richard-Mercier N,
Zaborski P (1995) Temperature variation andsex determination in
reptilia. J Exp Med 13: 516523
Rafferty AR, Reina RD (2012) Arrested embryonic develop-ment: a
review of strategies to delay hatching in egg-lay-ing reptiles.
Proc R Soc B Biol Sci 279: 22992308
Ragotzkie R (1959) Mortality of loggerhead turtle eggs
fromexcessive rainfall. Ecology 40: 303305
Raynaud A, Pieau C (1985) Embryonic development of thegenital
system. In: Gans C, Billett F (eds) Biology of theReptilia. John
Wiley & Sons, New York, NY, p 149300
Reginato RJ, Idso S, Vedder J, Jackson R, Blanchard M,Goettelman
R (1976) Soil water content and evaporationdetermined by thermal
parameters obtained fromground based and remote measurements. J
Geophys Res81: 16171620
Rogers M (2013) Hatchling sex ratios and nest temperature-sex
ratio response of 3 South Florida marine turtle spe-cies (Caretta
caretta L., Chelona mydas L., and Der-mochelys coriacea V.). MS
thesis, Florida AtlanticUniversity, Boca Raton, FL
Segura LN, Cajade R (2010) The effects of sand temperatureon
pre-emergent green sea turtle hatchlings. HerpetolConserv Biol 5:
196206
SFWMD (South Florida Water Management District) (2013)DHYDRO.
www.sfwmd.gov
Spotila JR, Standora EA, Morreale S, Ruiz GJ (1987) Tem-perature
dependent sex determination in the Green tur-tle (Chelonia mydas):
effects on the sex ratio on a naturalnesting beach. Herpetologica
43: 7481
Standora EA, Spotila JR (1985) Temperature-dependent
sexdetermination in sea turtles. Copeia 3: 711722
Telemeco RS, Abbott KC, Janzen FJ (2013a) Modeling theeffects of
climate changeinduced shifts in reproductivephenology on
temperature-dependent traits. Am Nat181: 637648
Telemeco RS, Warner DA, Reida MK, Janzen FJ (2013b)Extreme
developmental temperatures result in morpho-logical abnormalities
in painted turtles (Chrysemyspicta): a climate change perspective.
Integr Zool 8: 197208
TEWG (Turtle Expert Working Group) (2009) An assess-ment of the
loggerhead turtle population in the west-ern North Atlantic. NOAA
Tech Memo NMFS-SEFSC-575
Trivers RL, Willard DE (1973) Natural selection of
parentalability to vary the sex ratio of offspring. Science 179:
9092
Valenzuela N, Lance V (eds) (2004) Temperature-dependentsex
determination in vertebrates. Smithsonian Institu-tion, Washington,
DC
Wibbels T (2003) Critical approaches to sex determination insea
turtles. In: Lutz PL, Musick JA, Wyneken J (eds) Thebiology of sea
turtles, Vol II. CRC Press, Boca Raton, FL,p 103134
Wood DW, Bjorndal KA (2000) Relation of temperature,moisture,
salinity, and slope to nest site selection in log-gerhead sea
turtles. Copeia 119128
Wyneken J, Lolavar A (2015) Loggerhead sea turtle environ-mental
sex determination: implications of moisture andtemperature for
climate change based predictions forspecies survival. J Exp Zool
(Mol Dev Evol) 323B:295314
Wyneken J, Epperly SP, Crowder LB, Vaughan J, Esper KB(2007)
Determining sex in post hatchling loggerhead seaturtles using
multiple gonadal and accessory duct char-acteristics. Herpetologica
63: 1930
Yntema CL (1978) Incubation times for eggs of the turtleChelydra
serpentina (Testudines: Chelydridae) at vari-ous temperatures.
Herpetologica 34: 274277
Yntema CL, Mrosovsky N (1980) Sexual differentiation inhatchling
loggerheads incubated at different controlledtemperatures.
Herpetologica 36: 3336
Zar JH (1999) Biostatistical analysis, 4th edn. Prentice
Hall,Upper Saddle River, NJ
247
Editorial responsibility: Mark Hamann,Townsville, Queensland,
Australia
Submitted: December 22, 2014; Accepted: June 15, 2016Proofs
received from author(s): September 10, 2015
http://dx.doi.org/10.1655/0018-0831(2007)63[19%3ADSIPLS]2.0.CO%3B2http://dx.doi.org/10.1002/jez.b.22620http://dx.doi.org/10.1643/0045-8511(2000)2000[0119%3AROTMSA]2.0.CO%3B2http://dx.doi.org/10.1126/science.179.4068.90http://dx.doi.org/10.1111/1749-4877.12019http://dx.doi.org/10.1086/670051http://dx.doi.org/10.2307/1444765http://dx.doi.org/10.1029/JC081i009p01617http://dx.doi.org/10.2307/1930045http://dx.doi.org/10.1139/z84-216http://dx.doi.org/10.2307/1938369http://dx.doi.org/10.1016/0006-3207(80)90003-8http://dx.doi.org/10.1139/z92-080http://dx.doi.org/10.1002/jez.1402700104http://dx.doi.org/10.1139/z88-098
cite26: cite10: cite21: cite32: cite17: cite3: cite28: cite12:
cite23: cite39: cite19: cite2: cite7: cite25: cite40: cite31:
cite16: cite1: cite27: cite38: cite22: cite18: cite5: cite13:
cite24: cite30: cite41: cite4: cite9: