Biological Conservation 277 (2023) 109873
Available online 26 December 2022
0006-3207/© 2022 Elsevier Ltd. All rights reserved.
Neglecting cooler low-season nest protection could deprive sea turtle
populations of valuable hatchlings
Luis Angel Tello-Sahagún a, Cesar P. Ley-Quiñonez b, F. Alberto Abreu-Grobois c,
Jonathan R. Monsinjon d,1, Alan A. Zavala-Norzagaray b, Marc Girondot d, Catherine E. Hart b,*
a Estación Biológica Majahuas, Tomatlan, Jalisco, Mexico
b Instituto Politécnico Nacional, CIIDIR Unidad Sinaloa, Juan de Dios Bátiz Paredes No. 250, Col. San Joachin, C.P. 81101 Guasave, Sinaloa, Mexico
c Laboratorio de Genética y Banco de Información sobre Tortugas Marinas (BITMAR) Unidad Académica Mazatlán Instituto de Ciencias del Mar y Limnologia UNAM,
Mazatlán, Sinaloa, Mexico
d Université Paris-Saclay, CNRS, AgroParisTech, Ecologie Systématique et Evolution, 91190 Gif-sur-Yvette, France
A R T I C L E I N F O
Keywords:
Seasonality
Sex ratios
Fitness
Incubation
Lepidochelys olivacea
A B S T R A C T
Reproductive seasonality is present across species and phyla. Many species retain seasonal patterns even in
tropical regions where climatic variations may be less apparent. Environmental features and large-scale envi-
ronmental cues play a role in species seasonality and can have major effects on reproductive success. In or-
ganisms that present environmental sex determination, the season in which individuals reproduce has
consequences for their primary sex ratio. Here we looked at the possible effects on fitness and primary sex ratio
for the olive ridley sea turtle (Lepidochelys olivacea) when nesting during peak and low nesting seasons. In the
eastern Pacific, peak olive ridley sea turtle nesting occurs during the warmest months, which coincide with the
rainy season. Yet, as nesting takes place year-round, a small proportion of the nests laid during the dry part of the
season are exposed to contrasting environmental conditions. Most of the studies on Pacific coast sea turtles have
estimated sex ratios produced during the rainy, high abundance period when most conservation activities are
focused. Thus, dry-low season nests have on the whole, been overlooked. Here we compared sex ratios and
hatchling fitness for offspring produced during the dry and rainy seasons in 2015. We found that olive ridley
clutches incubated during the dry-low season were exposed to lower temperatures, yielded higher hatchling
success, mainly produced male offspring and larger, heavier hatchlings with better locomotor abilities. This
highlights that, for sea turtles, protecting nests outside of the peak nesting season may help future population
viability by yielding higher proportions of males with greater locomotor capacities and, thus, survival. Our re-
sults highlight the critical value of monitoring and protecting species during their entire reproductive period and
not concentrating all resources on the peak season to collect more data and protect a greater number of or-
ganisms. Our results suggest that monitoring low-season reproductive effort (nests in this case), albeit at much
lower densities, would be critical for understanding and possibly ensuring population viability and adaptation to
contemporary climate change and anthropogenic threats.
1. Introduction
Reproductive seasonality is present across species and phyla. Even in
tropical regions where climatic variations may be less apparent, many
species maintain some level of seasonal pattern. In marine species,
reproductive seasonality may be linked to marine productivity (Afán
et al., 2015),
local environmental
features, and large-scale
environmental cues.
In the eastern Pacific, peak olive ridley sea turtle (Lepidochelys oli-
vacea) nesting occurs during the warmest months, coinciding with the
rainy season from July to October (Hart et al., 2018; Morales-Mérida
et al., 2022). However, this species nests year-round, exposing the
comparatively small number of nests laid in the dry and cooler months
to environmental conditions that contrast with those of the majority of
* Corresponding author.
E-mail addresses: cleyq@ipn.mx (C.P. Ley-Quiñonez), alberto.abreu@ola.icmyl.unam.mx (F.A. Abreu-Grobois), anorzaga@ipn.mx (A.A. Zavala-Norzagaray),
marc.girondot@universite-paris-saclay.fr (M. Girondot), cehart03@gmail.com (C.E. Hart).
1 Present affiliation: Ifrermer, Indian Ocean Delegation, 97420 Le Port, La Reunion, France.
Contents lists available at ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/biocon
https://doi.org/10.1016/j.biocon.2022.109873
Received 22 September 2022; Received in revised form 27 November 2022; Accepted 16 December 2022
Biological Conservation 277 (2023) 109873
2
nests that incubate during the summer. For example, incubation tem-
perature and humidity are markedly different between the peak and low
abundance portions of the season. Temperature is one of the critical
factors for the successful embryonic development of sea turtles (Miller,
1985). However, turtle embryos have a narrow thermal tolerance range
between 25 ◦C and 35 ◦C (Howard et al., 2014), wherein the actual
temperature and the duration of exposure impact survival. Olive ridley
clutches can survive higher temperatures (>37.9 ◦C) but only over short
durations, with detrimental effects on hatchling emergence success and
locomotion performance (Maulany et al., 2012a). Olive ridley turtles,
which exhibit temperature-dependent sex determination (Mrosovsky
and Pieau, 1991; Broderick et al., 2000; Charruau and Hénaut, 2012),
present latitudinal variation in the reported pivotal temperatures, i.e., at
which we can expect 50 % of each sex within a clutch (e.g. Costa Rica:
30.5 ◦C ± 0.13 ◦C; Mexico: 30.16 ◦C ± 1.9 ◦C; Wibbels et al., 1998;
Abreu-Grobois et al., 2020). As the incubation temperature rises above
the pivotal within a sea turtle clutch, the proportion of females increases
to the point of producing all females. The opposite is true as the tem-
perature falls below the pivotal, and all-male production can occur in
the lower viable temperature scale. Additionally, rainfall is a factor that
varies significantly between seasons, especially in the tropics. Humidity
within the nest environment influences moisture uptake by embryos,
resulting in longer incubation durations and larger hatchlings (Delmas
et al., 2007) and may also affect the sex ratio through temperature
changes as a result of evaporation (Godfrey et al., 1996; Wyneken and
Lolavar, 2015; Sifuentes-Romero et al., 2018).
Recent studies have attempted to understand the role of humidity
during embryo development and how moisture affects phenotype and
sex determination. However, moisture and temperature are inter-
connected, and it can be difficult to isolate the individual effects that
these abiotic parameters have during embryogenesis. For example, male
hatchlings can be produced above pivotal temperature if there is suffi-
cient moisture (Wyneken and Lolavar, 2015) and temperature appears
to have a greater effect during the earlier stages of embryo development
and therefore sex determination (Sifuentes-Romero et al., 2018). Once
sex is determined and embryo growth becomes the dominant process,
moisture instead of temperature helps sustain higher rates of meta-
bolism and yolk utilization. Nevertheless, Gatto et al. (2021) found that
moisture had minimal effects on hatchling traits when they compared
hatchlings incubated under dry and wet conditions and thus tempera-
ture likely has a greater role in determining hatchling traits than
moisture.
These factors make sea turtles particularly vulnerable to climate
change (Fuller et al., 2013; Refsnider and Janzen, 2016) which is pre-
dicted to cause increased not only incubation temperatures but also sea
level (IPCC Intergovernmental Panel on Climate Change, 2007). Addi-
tionally, storms that are expected to become stronger and more frequent
will further impact and modify turtle nesting habitat (Hawkes et al.,
2009; Hawkes et al., 2013; Fuentes et al., 2010; Fuentes et al., 2011).
Nonetheless, a female turtle can influence reproductive success through
the choice of nesting location, nesting timing during the year, and depth
at which she lays her eggs (Booth and Freeman, 2006; Santidrián
Tomillo et al., 2017). However, even with plasticity of the nesting sea-
sonality (Patrício et al., 2019), sea turtles may have difficulty adapting
to rapid climate change (Hawkes et al., 2009; Tilley et al., 2019). Olive
ridleys may be the most adept of sea turtles to cope with environmental
change as a consequence of their multiple reproductive strategies and
flexibility in their nesting site fidelity (Tripathy and Pandav, 2007) and,
therefore, may be able to utilize sites that are less impacted by envi-
ronmental change, and which result in healthy offspring.
Phenotypical variation has been used to study how abiotic changes
affect hatchling fitness (Fisher et al., 2014; Liles et al., 2019; Ríos-Huerta
et al., 2021). In warmer nests, hatchlings hatch sooner and are smaller as
less yolk is converted into tissue (Booth et al., 2004). Smaller hatchlings
are slower during the crawl towards the ocean and during initial
displacement from coastal zones (Booth and Evans, 2011) when
compared with their larger counterparts. Furthermore, hatchlings must
be able to maintain a 24–72 h frenzied swimming period upon entering
the ocean. Larger hatchlings, which are stronger swimmers than smaller
individuals, could be more capable of avoiding the large aggregations of
predators offshore of the nesting beach Gatto et al., 2022. Turtles in poor
condition upon hatching have a reduced probability of avoiding pre-
dation (Wyneken and Salmon, 1992; Booth et al., 2004; Booth, 2009).
Since Mexico’s 1990 ban on sea turtle use and consumption, multiple
nesting beach conservation programs have been created to protect
clutches from illegal take and predation. However, with limited re-
sources, many cannot monitor nesting beaches year-round. For species
such as the olive ridley that nest along the Mexican Pacific, limits in
resources force conservation programs to focus on the rainy season
months when nesting is significantly higher (García et al., 2003), leaving
nests laid during the latter part of the nesting season without protection.
Dry season nests are often not protected or counted, leading to an
impression from regional reports that nesting does not occur or is
insignificant during this period. Registering dry season nesting could be
extremely important as their different abiotic conditions may affect
hatchling sex ratio, phenotype, and fitness. Also, as sea turtle nesting
seasons have been shown to shift in response to changes in ambient
temperatures (Weishampel et al., 2004; Pike et al., 2006; Witt et al.,
2010; Morales-Mérida et al., 2022), these behavioral changes may be an
adaptive strategy of the nesting turtles in response to climate warming.
Nevertheless, recent studies on Loggerhead turtles suggest contrasted
responses depending on the population (Almpanidou et al., 2018;
Monsinjon et al., 2019a). The drivers of sea turtles’ nesting phenology
are yet to be fully understood (Mazaris et al., 2013; Monsinjon et al.,
2019b), especially in the context of climate change (Patrício et al.,
2021).
Majahuas beach is part of the Playón de Mismaloya rookery, where
olive ridley turtles would nest in arribadas before the population
collapsed in the late 1970s due to the unsustainable commercial harvests
of nesting females. The rookery’s collapse resulted from a 99 % reduc-
tion in nesting females (Abreu-Grobois and Plotkin, 2008), and a
concomitant reduction in genetic diversity (Rodríguez-Zárate et al.,
2013). Despite conservation efforts starting in 1985 at Majahuas beach,
no arribada has taken place since the collapse. That said, the area’s
solitary olive ridley nesting density is high when compared with the
regional average (García et al., 2003). The local fishing cooperative
Roca Negra runs conservation activities in collaboration with other
community members to help protect nesting turtles. Members take turns
from June to November to conduct nightly beach patrols and relocate
sea turtle clutches to a protected beach hatchery. Once the eggs hatch,
they release the hatchlings into the ocean. Beach patrols are sporadic
from December to May and focus on locating leatherback (Dermochelys
coriacea) and green turtle (Chelonia mydas) nests that are occasionally
laid during the cooler months. Despite the long history of conservation
activities, no studies have occurred at the site, and information on the
number of adult females, and success of conservation activities have not
been assessed.
This study, which will be helpful to improve future conservation
strategies, aims at acquiring a better understanding of nest character-
istics and hatchling phenotypes outside of the peak season when nests
are not effectively protected from illegal take. Our goals were to 1)
monitor the number of nesting turtles during 12 months; 2) compare
incubation temperatures for nests incubated during the dry and rainy
seasons; 3) determine if hatching success varied between these two parts
of the season; 4) estimate sex ratios produced in monitored nests; 5)
determine if incubation season influenced hatchling fitness and pheno-
types; and, 6) discuss the conservation implications of the results.
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
3
2. Materials and methods
2.1. Study site
Majahuas beach is located in Jalisco state between 19◦50′41′′N
105◦22′40′′W and 19◦46′14′′N 105◦19′38′′W on the Pacific coast of
Mexico. Majahuas is the southernmost 11 km of the Playón de Mis-
maloya sea turtle sanctuary. A RAMSAR mangrove wetland backs the
beach.
The nesting season begins in June and extends into the following
year. Rains occur between June and November, with 80 % occurring
between July and October, while the dry period lasts up to 6 months,
from December to May. Mean annual rainfall is 748 mm ± 119 (585-
961 mm) varies between with a mean annual temperature of 24.9 ◦C
(12–35 ◦C). Mean monthly temperatures vary with a minimum from
14.8 ◦C to 22.9 ◦C and a maximum from 29.1 ◦C to 32.0 ◦C (Bullock,
1986).
2.2. Nest collection and incubation
Nightly nest monitoring by the fishing cooperative Roca Negra
recorded 1954 nests in 2015, from which data were collected. Nests
were protected via relocation to a hatchery (see below and Sosa-Cornejo
et al., 2022) to avoid illegal take of eggs, predation, and erosion. We
selected 86 nests at random (dry season: N = 40; rainy season: N = 46) to
monitor incubation temperature and hatching success. Of these nests, 51
hatched and the sex ratio was estimated for these clutches. Phenotype
and fitness tests were conducted on the hatchlings from 38 nests (dry
season: N = 28 nests; rainy season: N = 10 nests).
Nests were collected during nightly beach patrols by either locating
the recently laid nest via tracks or by encountering the nesting turtle and
retrieving her nest. On encountering a female, we waited until she
entered a trance-like state before taking morphometric measurements.
Curved carapace length (CCL) and curved carapace width (CCW) were
taken using a metric tape marked in 0.1 cm intervals. CCL was measured
from the nuchal scute to the posterior tip of the supracaudal scute, and
CCW from the widest part of the carapace with the tape following the
curvature.
On locating a nest, the top egg was checked to make sure that the
characteristic white spot on the surface of the eggshell, indicating that
the embryo had begun development, was absent before proceeding. The
eggs were carefully removed from the egg chamber and counted. Nest
depth was measured by placing a pole across the top of the mouth of the
nest, and the distance was taken from the pole to the bottom of the nest
chamber. For each nest, we recorded the beach section and zone where it
was laid (Intertidal (beach face to the berm) = A, Open beach (the berm
to the vegetation line) = B, and Beach (vegetation line to the dune) = C).
Eggs were transferred to a plastic bag and transported to the hatchery, 2
km from the southern end of Majahuas beach using a quad bike. Only
newly laid clutches were used for temperature, phenotype and fitness
tests and were identified by the female turtle being observed on the
beach or her tracks being fresh in the receding tideline. Care was taken
to limit vibrations during transport, and transport from the nest chamber
to the hatchery in less than an hour.
Between February and May 2015 patrols were carried out on foot due
to mechanical problems with the quad bike. This resulted in shorter
patrols during the dry season. Each nest was reconstructed using a
manual tree planter to achieve a standardized depth of 45 cm, and then
the nest chamber was formed by hand to imitate the shape of a natural
nest made by a female turtle. Eggs were transferred into the artificially
dug chamber, and a temperature logger (HOBO UA-001-08, Onset USA)
was placed in the center of each clutch before the eggs were covered
with sand. Temperature loggers measured 5.8 × 3.3 × 2.3 cm and were
programmed to register the hourly temperature (accuracy of ±0.5 ◦C).
Meteorological observations (daily maximum, minimum, and mean
air temperature and precipitation) were obtained from the Universidad
Autonoma de Mexico’s Biological Research Center in Cuixmala, Jalisco
from 1 January 2015 to 31 December 2015 (located 55 km from Maja-
huas beach).
2.3. Hatchling phenotype and fitness
Phenotype and fitness tests were carried out on hatchlings from 38
clutches. We selected 20 hatchlings at random upon emergence to
partake in fitness tests and for morphological measurements. When
hatching success was too low to provide a total of 20 hatchlings, we used
those that were available. Supplementary Table 2 states the number of
hatchlings studied from each nest. Hatchlings were weighed using an
electronic balance (±0.1 g), and their straight carapace length (SCL),
straight carapace width (SCW), and carapace depth were measured
using an electronic caliper (±0.1 mm). Tests to measure crawling speed
(cm s− 1) were carried out at night and recorded by measuring the time
each hatchling took to crawl along a raceway of 3 m, 100 mm wide, dug
into the hatchery’s sand. We assigned hatchlings that failed to move
within 300 s of being placed on the raceway to a failed to crawl category.
We installed a LED light at one end of the raceway, and care was taken to
ensure that the track was flat. The time taken for hatchlings to self-right
themselves was measured by placing the turtle upside down on its
carapace and taking the time it took to right itself. This was repeated six
times for each hatchling, with a 5 s rest period between attempts. If an
individual did not self-right themselves in 60 s, the failure was recorded,
and they were given a 5 s rest period on their plastron before the next
attempt (maximum of 6 attempts). After the tests, hatchlings were
returned to the container with their siblings and released into the ocean.
2.4. Sex ratio estimation
Of a total of 86 nests with temperature data, 35 failed to hatch.
Therefore, we estimated sex ratio for the remaining 51 clutches
(Table 1). We used the R package embryogrowth v.8.4 (Girondot, 2022)
to account for the effects of varying field temperatures on the dynamics
of embryonic development. The thermal reaction norm of embryo
growth was estimated according to the method of Girondot and Kaska
(2014). Then the thermosensitive period (TSP) dates when gonad dif-
ferentiation occurred were identified for each nest (Girondot et al.,
2018). To do so, we estimated the thermal reaction norm for growth rate
from our nest temperature time series (n = 51 nests, Table 1) and SCL
measurements (mean = 40.51 mm ± SD = 2.03): we fitted the 4-param-
eter equation using maximum likelihood and refined the confidence
intervals using Bayesian MCMC following the method described in
Girondot and Kaska (2014). With this, growth-weighted mean incuba-
tion temperatures during the TSP (Fuentes et al., 2017) were estimated
for each nest and sex ratios derived using the thermal reaction norm for
the species (Abreu-Grobois et al., 2020). We estimated the sex ratio
thermal reaction norm with data from the literature at constant incu-
bation temperatures (McCoy et al., 1983; Dimond, 1985; Wibbels et al.,
1998; Castheloge et al., 2018), we fitted the logistic equation using
maximum likelihood, and refined the confidence intervals using
Bayesian MCMC following the method described in (Abreu-Grobois
et al., 2020). Sex ratio estimates are presented as mean ± SE.
2.5. Statistical analysis
Reported statistics are arithmetic means ± standard deviation (SD).
All statistical tests were conducted using Minitab® 18.1 (Minitab Inc.,
State College, Pennsylvania, USA). Kolmogorov-Smirnov test was used
as a normality test. ANOVA with Tukey’s method was conducted to
examine mean differences among neonate fitness data obtained. A sta-
tistical test based on Pearson’s product-moment correlation coefficient
was used to evaluate the size of the adult females with number of eggs
and hatching size, and the effect of the incubation temperature on
hatchling morphology and locomotor performance. Levels of
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
4
Table 1
Summary for data from 86 olive ridley clutches with ranges of incubation temperatures (n = 86 clutches) and estimated sex ratios as proportion of males (n = 51
clutches).
Field
code
Season
Starting incubation
date
Incubation duration
(d)
Clutch
size
Hatching
success
Fitness
tests
% >
34 ◦C
% <
26 ◦C
Mean ◦C ± SD
(range)
Sex
ratio
MJ 1
Dry
18 Feb
61.2
79
21.5
Yes
0.0
4.8
28.2 ± 1.6
(23.2–31.2)
0.99
MJ 2
Dry
18 Feb
60.6
87
100
Yes
0.0
4.6
28.9 ± 2.1
(23.6–32.9)
0.98
MJ 3
Dry
18 Feb
59.8
100
85
Yes
0.0
4.8
28.8 ± 2.1
(23.7–32.9)
0.98
MJ 4
Dry
16 Feb
59.2
104
100
Yes
0.0
5.1
28.7 ± 2.3
(23.2–33.2)
0.98
MJ 5
Dry
16 Feb
59.8
93
90.3
Yes
0.0
6.6
28.2 ± 2.2
(22.9–32.7)
0.99
MJ 6
Dry
16 Feb
58.8
103
100
Yes
0.0
5.0
29.0 ± 2.3
(22.2–33.6)
0.98
MJ 7
Dry
16 Feb
59.8
85
94.1
Yes
0.0
4.8
28.9 ± 2.2
(23.3–33.3)
0.98
MJ 8
Dry
16 Feb
58.0
96
87.5
Yes
0.0
4.9
28.6 ± 2.3
(22.8–33.3)
0.98
MJ 9
Dry
16 Feb
59.8
77
15.6
Yes
0.0
6.6
27.7 ± 1.6
(23.1–30.5)
0.99
MJ 10
Dry
16 Feb
59.0
92
97.8
Yes
0.0
4.9
28.8 ± 2.1
(24.0–32.8)
0.97
MJ 11
Dry
19 Feb
59.3
157
96.2
Yes
1.7
7.0
29.0 ± 2.8
(20.1–34.3)
0.93
MJ 12
Dry
22 Feb
–
101
0
No
0.0
8.2
27.3 ± 1.1
(22.3–29.7)
–
MJ 13
Dry
22 Feb
59.9
87
66.7
Yes
0.0
6.6
28.3 ± 1.9
(20.6–31.5)
0.96
MJ 14
Dry
24 Feb
64.2
74
50.0
Yes
0.0
8.4
28.2 ± 1.9
(20.4–31.1)
0.97
MJ 15
Dry
24 Feb
58.8
123
96.7
No
0.0
6.4
28.8 ± 2.4
(24.0–33.1)
0.95
MJ 16
Dry
25 Feb
57.0
94
83.0
Yes
0.0
5.9
28.8 ± 2.3
(23.1–32.9)
0.93
MJ 17
Dry
25 Feb
58.5
96
89.6
Yes
0.0
5.1
29.2 ± 2.3
(23.9–33.7)
0.88
MJ 18
Dry
25 Feb
57.5
84
98.8
Yes
0.7
4.9
29.2 ± 2.5
(24.2–34.6)
0.89
MJ 19
Dry
25 Feb
60.0
113
88.5
Yes
0.0
4.6
28.8 ± 1.8
(24.4–32.0)
0.94
MJ 20
Dry
25 Feb
59.3
97
96.9
Yes
0.0
5.1
29.2 ± 2.4
(23.9–33.2)
0.89
MJ 21
Dry
03 Mar
62.1
102
71.6
Yes
0.0
6.1
29.3 ± 2.3
(23.6–32.4)
0.77
MJ 22
Dry
02 Mar
58.2
77
53.2
Yes
0.0
8.4
28.6 ± 2.2
(23.4–32.1)
0.91
MJ 23
Dry
03 Mar
–
78
0
No
0.0
12.1
27.6 ± 1.7
(22.4–30.6)
–
MJ 24
Dry
04 Mar
61.0
92
91.3
Yes
0.0
7.9
28.7 ± 2.1
(23.5–32.0)
0.87
MJ 25
Dry
04 Mar
55.0
112
98.2
Yes
0.0
6.7
29.2 ± 2.3
(23.4–32.9)
0.77
MJ 26
Dry
04 Mar
55.1
79
81.0
Yes
0.0
5.5
29.2 ± 2.1
(24.3–32.4)
0.76
MJ 27
Dry
04 Mar
55.2
112
97.3
Yes
0.0
5.3
29.5 ± 2.3
(23.9–33.2)
0.66
MJ 28
Dry
04 Mar
62.0
83
92.8
Yes
0.0
3.2
29.6 ± 1.9
(25.3–32.5)
0.67
MJ 29
Dry
05 Mar
–
111
0
No
0.0
6.8
28.3 ± 1.6
(23.3–30.8)
–
MJ 30
Dry
05 Mar
61.2
78
62.8
Yes
0.0
6.3
28.8 ± 1.7
(23.3–31.3)
0.83
MJ 31
Dry
19 Mar
51.9
89
88.8
Yes
0.0
0.2
30.3 ± 1.6
(25.0–32.9)
0.26
MJ 32
Dry
21 Mar
53.8
106
97.2
No
0.0
0.0
29.8 ± 1.7
(26.3–32.7)
0.62
MJ 33
Dry
21 Mar
53.8
64
60.9
No
0.0
0.2
29.9 ± 1.9
(25.5–33.3)
0.53
MJ 34
Dry
21 Mar
53.8
103
98.1
No
0.0
0.2
29.9 ± 1.9
(25.5–33.3)
0.53
MJ 35
Dry
21 Mar
55.1
85
98.8
No
0.0
0.2
29.4 ± 1.7
(24.5–32.5)
0.73
MJ 36
Dry
21 Mar
56.2
128
99.2
No
0.5
0.3
29.5 ± 2.1
(25.1–34.3)
0.76
(continued on next page)
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
5
Table 1 (continued )
Field
code
Season
Starting incubation
date
Incubation duration
(d)
Clutch
size
Hatching
success
Fitness
tests
% >
34 ◦C
% <
26 ◦C
Mean ◦C ± SD
(range)
Sex
ratio
MJ 37
Dry
21 Mar
55.3
86
91.9
No
0.0
0.4
28.9 ± 1.8
(25.8–32.4)
0.83
MJ 38
Dry
22 Mar
–
86
0
No
0.0
0.5
28.6 ± 1.1
(25.0–30.1)
–
MJ 39
Dry
22 Mar
52.2
76
89.5
No
0.0
0.2
29.5 ± 1.7
(24.6–32.6)
0.67
MJ 40
Dry
22 Mar
50.3
107
93.5
Yes
0.0
0.2
30.1 ± 1.9
(24.2–33.4)
0.50
MJ 41
Rainy
03 June
–
112
0
No
48.9
0.0
33.8 ± 1.7
(29.4–36.4)
–
MJ 42
Rainy
02 Jun
46.9
92
56.5
41.7
0.1
33.5 ± 1.6
(29.5–36.0)
0.03
MJ 43
Rainy
02 Jun
–
81
0
No
5.5
0.0
32.3 ± 1.1
(30.0–34.2)
–
MJ 44
Rainy
02 Jun
–
98
0
No
0.0
0.0
32.1 ± 1.0
(30.2–33.6)
–
MJ 45
Rainy
03 Jun
47.0
123
62.6
No
0.1
0.0
32.0 ± 1.2
(29.6–34.1)
0.01
MJ 46
Rainy
10 Jun
–
80
0
No
46.7
0.0
33.7 ± 1.7
(28.8–36.5)
–
MJ 47
Rainy
10 Jun
50.5
121
92.6
No
7.6
0.0
32.3 ± 1.3
(29.7–35.2)
0.01
MJ 48
Rainy
20 Jun
–
90
0
No
51.1
0.0
33.6 ± 1.7
(23.6–35.6)
–
MJ 49
Rainy
20 Jun
45.2
109
96.3
Yes
1.6
0.8
31.7 ± 1.4
(23.6–34.1)
0.41
MJ 50
Rainy
21 Jun
46.5
97
88.7
50.9
0.2
33.7 ± 1.6
(23.9–35.9)
0.03
MJ 51
Rainy
26 Jun
–
80
0
No
5.7
0.0
32.0 ± 1.4
(28.4–34.3)
–
MJ 52
Rainy
26 Jun
–
103
0
No
53.9
0.0
33.5 ± 1.7
(27.8–36.6)
–
MJ 53
Rainy
02 Jul
44.9
93
71.0
Yes
38.4
0.0
33.3 ± 1.8
(28.8–37.1)
0.00
MJ 54
Rainy
02 Jul
–
107
0
No
74.7
0.0
34.6 ± 1.5
(29.8–36.6)
–
MJ 55
Rainy
02 Jul
45.3
91
42.9
Yes
16.2
0.0
32.6 ± 1.5
(28.3–34.9)
0.01
MJ 56
Rainy
02 Jul
–
126
0
No
74.3
0.0
34.5 ± 1.5
(29.3–36.6)
–
MJ 57
Rainy
05 Jul
45.2
98
28.6
Yes
37.1
0.0
33.2 ± 1.9
(28.1–36.5)
0.00
MJ 58
Rainy
05 Jul
–
57
0
No
73.4
0.0
34.5 ± 1.6
(28.6–36.6)
–
MJ 59
Rainy
05 Jul
49.1
106
12.3
Yes
11.5
0.0
32.6 ± 1.5
(27.9–35.1)
0.01
MJ 60
Rainy
05 Jul
–
87
0
No
63.6
0.0
34.1 ± 1.6
(28.1–36.2)
–
MJ 62
Rainy
14 Jul
–
54
0
No
75.5
0
34.5 ± 1.7
(28.2–36.4)
–
MJ 64
Rainy
14 Jul
–
80
0
No
79.9
0.0
34.7 ± 1.7
(28.1–36.4)
–
MJ 65
Rainy
14 Jul
46.2
105
13.3
Yes
0.0
0.0
32.1 ± 1.4
(27.9–33.8)
0.02
MJ 66
Rainy
14 Jul
–
77
0
No
80.1
0.0
34.8 ± 1.8
(28.3–36.7)
–
MJ 67
Rainy
14 Jul
48.1
109
24.8
Yes
0.0
0.0
32.1 ± 1.4
(27.4–34.0)
0.02
MJ 68
Rainy
14 Jul
–
108
0
No
81.0
0.0
34.8 ± 1.7
(28.3–36.9)
–
MJ 69
Rainy
14 Jul
–
111
0
No
3.6
0.0
32.5 ± 1.4
(27.9–34.4)
–
MJ 70
Rainy
14 Jul
–
69
0
No
82.5
0.0
34.7 ± 1.8
(26.1–36.9)
–
MJ 71
Rainy
23 Aug
–
100
0
No
29.3
0.0
33.1 ± 1.5
(29.0–35.9)
–
MJ 73
Rainy
24 Aug
–
87
0
No
30.6
0.0
33.2 ± 1.5
(29.0–36.0)
–
MJ 74
Rainy
24 Aug
44.7
86
68.6
Yes
30.1
0.0
33.1 ± 1.6
(28.9–36.2)
0.04
MJ 75
Rainy
24 Aug
45.2
56
92.9
Yes
43.3
0.0
33.8 ± 0.9
(26.2–36.1)
0.00
MJ 76
Rainy
24 Aug
–
92
0
No
33.8 ± 1.5
(29.1–37.1)
–
MJ 77
Rainy
24 Aug
46.0
68
19.1
Yes
28.4
0
0.02
(continued on next page)
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
6
significance are stated as p values.
2.6. Ethics statement
Sampling and behavior tests were covered by permits granted by
Mexico’s Dirección General de Vida Silvestre/Secretaría de Medio
Ambiente y Recursos Naturales (SEMARNAT) SGPA/DGVS/05366/15.
3. Results
3.1. Nesting
We recorded a total of 1954 nests over 12 months (1st January
2015–30th December 2015). Nesting occurred year-round, with the
highest levels recorded in October when the conservation project relo-
cated 605 nests to the beach hatchery and the lowest levels in May (n =
22 nests) (Fig. 1). The majority of nests (n = 1573, 80.5 %) were laid in
the rainy season while 19.5 % of nests (n = 381) occurred during the dry
season. Nesting was predominately on beach berm or zone B where 79.3
% of nests were laid (n = 1547 nests) (zone A: 7.3 %, 143 nests; zone C:
13.4 %, 261 nests). Proportionally, a greater number of nests were laid
in intertidal zone A during the dry season (9.0 % n = 34 nests) than
during the rainy season (6.9 % n = 109). We measured 25 nesting fe-
males and found that the mean curved carapace length (CCL) and width
(CCW) were 67.6 cm (range: 63–76 cm) and 73.8 cm (range: 68–82 cm),
respectively (Supplementary Table 1). There was no significant rela-
tionship between the size of the adult females and the number of eggs
laid (r = − 0.136; p > 0.05) or hatchling sizes (r = 0.273; p > 0.05).
3.2. Nest temperatures
We monitored temperature in 86 nests but could only estimate sex
ratios in 51 nests because the 35 others did not hatch (Table 1). Nest
temperatures presented significant seasonal differences (F(1,69) =
143.26; p < 0.001), with those incubated during the dry season
(29.09 ◦C ± 0.52) being a mean of 3.89 ◦C cooler than those incubated
in the rainy season (32.98 ◦C ± 0.58). The temperature within the 86
nests ranged between 20.1 ◦C and 38.5 ◦C. The most frequent temper-
ature interval for dry season nests was 27–28 ◦C with 24 % of recorded
values, while in the rainy season, the most frequent temperature interval
was 33–34 ◦C with 28 % of records (Fig. 2).
Within the hatchery, mid-nest depth temperatures were regularly
lower than atmospheric temperature, and tropical storms and hurricanes
caused occasional and drastic drops in nest temperatures (Supplemental
Fig. 1).
3.3. Hatchling morphology and locomotor performance
Mean incubation temperature within nests was found to be signifi-
cantly correlated with some of the hatchling morphological traits:
weight (r = − 0.36; p < 0.05), SCW (r = − 0.35; p < 0.05), carapace
depth (r = − 0.34; p < 0.05), and locomotor ability (run speed (r = 0.46;
p < 0.01)) (Supplementary Fig. 1).
Hatchling morphology was significantly affected by season, with dry-
season hatchlings presenting both larger SCL, (Dry: 40.62 mm ± 1.82;
Rainy: 40.15 mm ± 2.53; F(1,758) = 7.16; p = 0.008), SCW (Dry: 32.84
mm ± 1.714; Rainy: 32.12 mm ± 2.104; F(1,758) = 20.71; p < 0.001),
Table 1 (continued )
Field
code
Season
Starting incubation
date
Incubation duration
(d)
Clutch
size
Hatching
success
Fitness
tests
% >
34 ◦C
% <
26 ◦C
Mean ◦C ± SD
(range)
Sex
ratio
33.2 ± 1.5
(29.0–36.7)
MJ 78
Rainy
24 Aug
44.8
117
13.7
Yes
25.7
0
33.1 ± 1.6
(28.8–36.8)
0.03
MJ 79
Rainy
24 Aug
–
120
0
No
29.6
0.0
33.2 ± 1.5
(29.2–36.0)
–
MJ 98
Rainy
25 Sep
–
93
0
No
32.2
0.0
33.2 ± 1.8
(28.8–36.2)
–
MJ 99
Rainy
25 Sep
–
66
0
No
39.4
0.0
33.3 ± 1.8
(28.6–36.3)
–
MJ 100
Rainy
25 Sep
–
113
0
No
40.8
0.0
33.6 ± 2.0
(28.9–38.5)
–
MJ 101
Rainy
25 Sep
–
87
0
No
30.6
0.0
33.1 ± 1.6
(29.1–35.9)
–
MJ 103
Rainy
25 Sep
–
112
0
No
29.4
0.0
33.2 ± 1.5
(28.6–35.6)
–
MJ 105
Rainy
25 Sep
–
92
0
No
24.7
0.0
32.8 ± 1.6
(28.3–35.3)
–
MJ 106
Rainy
25 Sep
–
111
0
No
31.1
0.0
33.1 ± 1.7
(28.6–35.8)
–
MJ 107
Rainy
25 Sep
–
98
0
No
32.6
0.0
33.2 ± 1.6
(28.9–35.8)
–
MJ 108
Rainy
25 Sep
–
85
0
No
40.2
0.0
33.3 ± 1.7
(28.8–35.8)
–
MJ 110
Rainy
25 Sep
–
93
0
No
39.9
0.0
33.5 ± 1.6
(29.5–36.0)
–
Fig. 1. Temporal distribution during 2015 of Lepidochelys olivacea nests
monitored at Majahuas beach, Jalisco, Mexico.
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
7
and weight (Dry: 16.23 g ± 1.686; Rainy: 14.93 g ± 2.317; F(1,758) =
64.55; p < 0.001) compared to those hatched in the rainy season. Sig-
nificant differences in terrestrial locomotor performance were observed
between seasons (F(1,758) = 60.17; p < 0.001), with dry-season hatch-
lings having a faster mean crawl speed (0.97 cm s− 1 ± 0.594) compared
to those hatched in the rainy season (0.55 cm s− 1 ± 0.359). In addition,
rainy season hatchlings also presented a slower mean righting response
(3.33 s ± 2.11) than those hatched in the dry season (3.87 s ± 2.41;
F(1,758) = 04.641; p = 0.032) (Table 2). Overall hatching success was
52.7 % and presented a significant difference between dry season
hatchling success 74.3 % and rainy season hatchling success 24.2 %
(F(1,1952) = 38.08; p < 0.001). Data for each nest studied can be found in
Supplementary table 2.
3.4. Estimates of hatchling sex ratios
The nests incubated during the February–March dry season that
successfully hatched (n = 36) produced between 26 % to 99 % male
hatchlings, whereas those incubated during June–September rainy
season (hatched nests: n = 15) produced between 0 and 41 % males
(Fig. 3), but 14 of 15 nests were extremely female-biased (Table 1).
4. Discussion
4.1. Hatchling phenotype and fitness
Seasonal effects were present in our study with dry-season hatchlings
having superior locomotor abilities, larger body size, and weight than
their rainy-season counterparts. This is similar to other studies which
have looked at the effect of nest temperature and found that cooler nests
produce larger hatchlings (Booth et al., 2013; Maulany et al., 2012b;
Wood et al., 2014) that may be better equipped (larger carapaces and
flippers) to crawl and swim faster than their smaller counterparts from
warmer nests (Ischer et al., 2009; Rivas et al., 2019). The phenotype and
fitness advantages received from cooler incubation temperatures high-
light the importance of protecting dry season nests which occur when
nesting levels are low because these nests produce higher hatching
success. The resulting hatchlings may have an increased chance of sur-
vival because they may be quicker to exit predator-rich coastal waters
due to their larger size and better fitness characteristics. However, the
lower number of nests laid during the dry season increases the likelihood
of eggs and hatchlings being predated as there are fewer available to
satiate predators (Ims, 1990). However, hatchlings from nests with high
emergence success also have a higher chance of avoiding predators on
their natal beach during their crawl to the sea, as predators rarely
consume large numbers of hatchlings from an individual nest (Erb and
Wyneken, 2019).
Our study tested hatchlings that emerged from nests relocated to a
beach hatchery. However, the relocation of clutches to artificially
excavated nest chambers can affect hatchling fitness and phenotype
through modification of the nest microenvironment. Tanabe et al.
(2021) found that green turtle hatchlings from relocated nests were
Fig. 2. Temperature frequency registered in the center of hatched Lepidochelys
olivacea clutches during incubation in the hatchery at Majahuas beach.
Table 2
Mean temperature for 86 nests (40 in Dry season and 46 in Rainy season) and
mean phenotype measurements (straight carapace length (SCL: mm), straight
carapace width (SCW: mm), and weight (g)) and crawl speed and righting
response for olive ridley sea turtle hatchlings from 38 nests at Majahuas beach
by season (Dry: n = 28; Rainy: n = 10) in 2015.
Parameter
Season
Statistical
test
Dry
Rainy
Mean
± SD
Min–max
Mean
± SD
Min–max
Temperature
(◦C)
29.09
± 0.52
(a)
27.3–30.1
32.98
± 0.58
(b)
31.7–34.8
F(1,84) =
723.92; p
< 0.001
Hatching
Success (%)
74.2
± 2.97
(a)
0.000–100.0
24.1
± 3.56
(b)
0.00–92.70
F(1,1952) =
38.08; p <
0.001
SCL (mm)
40.62
±
1.823
(a)
34.00–47.50
40.15
±
2.535
(b)
30.00–49.00
F(1,758) =
7.16; p =
0.008
SCW (mm)
32.84
±
1.714
(a)
26.40–38.00
32.12
±
2.104
(b)
26.00–29.50
F(1,758) =
20.71; p <
0.001
Weight (g)
16.23
±
1.686
(a)
12.00–24.00
14.93
±
2.317
(b)
8.020–19.88
F(1,758) =
64.55; p <
0.001
Crawl Speed
(cm s− 1)
0.977
±
0.594
(a)
0.132–3.600
0.550
±
0.359
(b)
0.086–1.597
F(1,758) =
60.17; p <
0.001
Righting
Response
(s)
3.870
±
2.412
(a)
0.980–19.00
3.336
±
2.110
(b)
0.830–18.00
F(1,758) =
04.641; p
= 0.032
N.B.: The statistical test used is the analysis of variance (ANOVA); statistical test
data as mean ± SD followed by Tukey’s test in parentheses if significant dif-
ferences were found. Hatching success data in percentage.
Fig. 3. Sex ratio (male proportion) of the 51 Lepidochelys olivacea nests on
Majahuas Beach that hatched.
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
8
smaller, and less fit than those from in situ nests. However, as all the
nests compared in our study were relocated to the hatchery all hatch-
lings would have experienced the effects of relocation and therefore this
would not influence the observed difference between seasons.
Temperature is not the only factor that presents seasonal changes.
Hatchlings entering the sea at different times of the year can encounter
seasonal changes in oceanic circulation (Scott et al., 2017). Ocean cur-
rents can change in both intensity and direction (Portela et al., 2016).
Therefore, neonates hatching at different times can end up in vastly
different locations and be exposed to different conditions (Mansfield
et al., 2017). In Spring, along the Mexican Central Pacific, sea turtles
have been observed to aggregate in coastal upwelling areas and near
cyclonic gyres. Whereas in winter, colder water flowing from the
northwest into the oceanic zone causes thermal fronts where turtles
forage (Zepeda-Borja et al., 2017). These currents may move hatchlings
from coastal waters into oceanic waters and away from predators.
4.2. Rainfall and hurricane season
Moisture is vital in determining temperature regimes (Gatto et al.,
2021) and has been associated with an increase in male hatchling pro-
duction (Godfrey et al., 1996). However, rainwater filtering through
sand has been found to quickly match the ambient sand temperature
even at the top of loggerhead turtles (Caretta caretta) egg chambers
(Lolavar and Wyneken, 2017). Olive ridley turtles lay relatively shallow
nests exposed to greater daily fluctuations in temperatures but may also
increase the possibility of rainfall reaching and cooling the eggs through
evaporation. However, rainfall occurred during only 61 days (16.7 %) in
2015, and only 33.3 % (n = 41 d) of rainy season days and 12.1 % of dry
season days (n = 20 d). Therefore, the temperature is likely the principal
factor driving the differences in the sex ratios between rainy and dry
seasons. Rainfall was related to the number of storms with hurricane
season occurring from May 15th to November 30th in the Eastern North
Pacific (NHC), which coincides with peak olive ridley sea turtle nesting
activity. The 2015 storm season was particularly active, with 18 cy-
clones registered for the northern East Pacific, of which 13 were hurri-
canes, nine were major hurricanes, and three were tropical depressions
(Avila, 2016; Collins et al., 2016). Seven storms (Supplementary Fig. 2)
affected Majahuas nesting beach during this study. This resulted in the
loss of hundreds of nests due to beach erosion and wash-out of hatch-
eries. However, these storms also lower incubation temperatures, which
help lower sand temperature in some cases below pivotal temperature.
During August and much of September, the sand temperature remained
above 34 ◦C, which has been identified as the lethal superior incubation
temperature for some olive ridley populations (Maulany et al., 2012a).
For example, when the effects of Hurricane Kevin and Linda occurred
within the same week, a drop in mid-nest depth temperature of 3 ◦C
(35 ◦C to 32 ◦C) occurred, taking incubation temperatures out of lethal
limits.
4.3. Sex ratio
Dry season nests were estimated to produce mainly male clutches,
and males’ increased hatch rate and survival may help balance out
female-biased sex ratios at Majahuas beach. Sandoval Espinoza (2012)
estimated sex ratios for olive ridleys along the Mexican Pacific coast and
found that ratios varied greatly, with beaches in Jalisco (Chalacatepec
and Playon de Mismaloya) producing 23 % male sex ratios. For the
Mexican Pacific, they estimated that temperatures would have resulted
in male hatchlings throughout the study period (July-Dec 2010), with
31 % of males in September, 11 % in August, 17 % in October, 20 % in
November, and 19 % in December. They did not monitor temperatures
during the dry season. This is contrary to our results, where the 2015
high rainy season temperatures resulted in very low levels of male
hatchling production.
When we compare our results with those of a study in 1993 (Valadez
González et al., 2000) at a beach 5 km north of Majahuas we find similar
variations in sex ratio, with 100 % females produced in October and 100
% males in December. However, the overall sex ratio of 7:3 in the 1993
study is not the same as that found in Majahuas during our research. The
incubation period in 1993 (Valadez González et al., 2000) was 44 to 65
days, which is similar to our results where we recorded the most pro-
longed incubation duration in February (64.2 d) and the shortest in
August (44.7 d). However, the temperature registered in the La Gloria
beach hatchery ranged from 27 ◦C ± 0.10 (December) to 34 ◦C ± 0.36
(August), even when considering a higher temperature within nests due
to metabolic heat (Sandoval et al., 2011) the 1993 study nests would not
have experienced the extreme upper temperatures (max 38.5 ◦C) that we
registered within clutches. As expected from our 12-month study period,
we registered lower temperatures than in the La Gloria study, which did
not monitor temperature during the dry winter season. Although Vala-
dez González et al. (2000) only recorded the hatchery sand temperature
at 12-hour intervals at nest depth but not from within clutches, the study
allows us to compare our results with data taken two decades ago.
All nests protected during the study were relocated to a beach
hatchery. Beach hatcheries are commonly located at the point furthest
away from the tide line to protect clutches from erosion. Yet for species
such as olive ridley turtle that prefer to nest on the beach berm (Hart
et al., 2014), this upper dune environment presents significantly higher
temperatures and lower humidity than those closer to the ocean (Spotila
et al., 1987; Martins et al., 2022) this could have contributed to the high
female-biased sex ratios during the hotter rainy season. If a proportion of
nests could be left in situ during the rainy season, this would expose
them to a variety of microenvironments. That said, they would still be
exposed to the high levels of predation, illegal take and erosion that
threaten clutches on this beach.
In the context of contemporary climate change, female-biased sex
ratios could provide an advantage (Santidrián Tomillo and Spotila,
2020). However, if these primary sex ratios persist into adulthood, it is
possible that genetic erosion would occur as a result of decreased
effective population size, and this could become detrimental. Our results
suggest that low-season nests, which produce individuals of the rarer
sex, are critical for the long-term persistence of this population. That
said, male sea turtles have been found to reproduce more frequently
than females, and this may help balance the operational sex ratio on
breeding grounds (Hays et al., 2014). This, coupled with the olive rid-
leys’ behavioral plasticity in nesting (Bernardo and Plotkin, 2007),
migration, and foraging (Santos et al., 2019; Figgener et al., 2022) will
likely help olive ridleys adapt to environmental change.
4.4. Benefits of low-season nesting for females
Olive ridleys present high levels of multiple paternity (MP), and this
is especially prominent in arribada breeding populations, with 92 % of
clutches having two or more fathers (Jensen et al., 2006) and clutches
sampled at the arribada in Escobilla, Mexico having between two and
seven fathers (González-Cortés et al., 2021). Similar results at other
large sea turtle nesting sites led to the hypothesis that population size
has a dominant effect on MP (Jensen et al., 2006; Lee et al., 2018). In
contrast, at solitary nesting beaches, clutches shared 2 to 3 fathers
(Duran et al., 2015). High MP was observed at the beginning of the
arribada season, with each subsequent mass nesting event presenting
fewer sires per clutch (González-Cortés et al., 2021). As for solitary
nesting sites, in-water observations of mating near beaches are highest
between July and September (Plotkin et al., 1996), whereas Zepeda-
Borja et al. (2017) observed mating only during October.
Despite the high frequency of MP in sea turtles, polyandry appears to
be without fitness benefits for female turtles, and clutches with multiple
fathers may contain fewer eggs overall (Wright et al., 2013). In addition,
avoiding males has energy requirements that may exceed that of mating
(Lee et al., 2018). Therefore, females that nest in times of low abundance
are likely to encounter fewer males and benefit from a lower chance of
L.A. Tello-Sahagún et al.
Biological Conservation 277 (2023) 109873
9
multiple encounters with aggressive males (Jensen et al., 2006). How-
ever, Duran et al. (2015) reported that some solitary breeding pop-
ulations also present high levels of MP, which could result from the low
breeding and feeding site fidelity (Plotkin, 2010) and sea turtle females’
ability to store sperm over multiple years.
4.5. Implications for current conservation efforts
Concentrating effort and resources on peak nesting season conser-
vation and research may seem the best use of limited funds. However, in
our region, nests laid during peak nesting season have lower possibilities
of hatching than those in the low season due to lethally high tempera-
tures and beach erosion resulting from storms. When protected from
predation in hatcheries, the comparatively small number of nests laid in
the low season has higher hatch rates and produce a higher proportion of
male hatchlings, which are a rare occurrence during the high rainy
season. Although in 2015, the number of nests laid during the low
season represented just 19.5 % of overall nesting, they are of high
conservation value because they produce the rarer sex and could help
population viability. It is important to note that patrols between
February and May 2015 were limited due to mechanical problems with
the projects quad bike on which patrols are made of the 11 km beach.
This resulted in reduced monitoring capacity during the dry season;
therefore, nesting levels may have been higher than those reported here.
Despite this, our study highlights the fact that viable nests are laid year-
round and that these nests produce valuable male hatchlings. Of rele-
vance is that under current practices, most of these nests are left on the
beach without protection. Most of them (>65 %) are predated by rac-
coons, coatis, or humans during the first night after laying (LATS, per-
sonal observation). Methods exist to limit predation and include the use
of mesh (O’Connor et al., 2017; Nordberg et al., 2019) which could be
implemented to allow at least some nests to be protected in situ each
season and therefore experience distinct microenvironments that could
produce hatchlings of distinct sex ratio, phenotype, and fitness to the
hatchery. However, further work would be needed in the local com-
munity to avoid these nests being taken for illegal consumption.
5. Conclusion
Understanding how seasonality affects reproductive success and in-
fluences sex ratios and phenotype in species is vital to conservation,
especially for species identified as at particular risk of environmental
change. In recent years, attention has been placed on the effects of
climate change on primary sex ratios, offspring phenotype, and fitness in
reptiles due in part to environmental sex determination. For vulnerable
species, conservation projects may concentrate solely on the peak
reproductive season. However, for species such as sea turtles, this may
inadvertently favor the production of female hatchlings while leaving
the cooler male-producing nests without protection from illegal take by
humans and animal predation. Indeed, we found that clutches incubated
during the dry-low season also yielded higher hatchling success and
produced larger, heavier hatchlings with better locomotor abilities.
Although it may be tempting to concentrate limited funds on peak
season, winter nests are of high value in areas such as Majahuas beach,
where summer nests do not produce male offspring and are subject to
erosion due to tropical storms and hurricanes. Future research into other
environmental differences between seasons for species that reproduce
year-round or over many months with differing environmental condi-
tions, such as humidity and how this interacts with temperature in
natural nests, will be important for understanding how species may be
able to adapt to climate change through possible shifts in their principal
reproductive season.
CRediT authorship contribution statement
CEH and LATS conceived the study, participated in data collection
and analysis, and drafted the manuscript; CPLQ, AAZN, JM and FAAG
carried out the statistical analyses and wrote the manuscript; JM and MG
analyzed the sex ratio data. All authors gave final approval for
publication.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgments
We are grateful for the support provided by personnel from the
fishers’ cooperative Boca Negra (Cooperativa Pesquera Roca Negra)
during our time working on Majahuas beach. We thank Jasiel Noé
Juárez-Rábago for his help with the hatchling fitness tests and Estación
de Biologia Chamela UNAM for supplying meteorological data. We
thank two anonymous reviewers for their insightful and valuable com-
ments on the manuscript.
Funding
No funding was received for this research.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.biocon.2022.109873.
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