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Cohort-Dependent Sex Ratio Biases in the American Crocodiles (Crocodylus acutus) of the Tempisque Basin

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A male-biased sex ratio of 3:1 has been reported for a population of American crocodiles (Crocodylus acutus) in the Tempisque River Basin, Guanacaste, Costa Rica. If confirmed, this would constitute one of the largest male-biased sex ratios reported for any population of a member of the genus Crocodylus. Here, we examine the aforementioned population of C. acutus and report on sex ratios of hatchling, juvenile, and adult age classes within a sample of 474 crocodiles captured in the Tempisque Basin between May 2012 and June 2014. Hatchling sex ratio is exceptionally male biased (3.5:1), an imbalance that is maintained in juveniles but is reduced in adults (1.5:1). Mark–recapture data document that juvenile males disperse from the study site, potentially to avoid competition, a process that reduces male bias in the adult age class. An increased role of males in human–crocodile conflict may be a result of juvenile males dispersing to human-inhabited areas.
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Cohort-Dependent Sex Ratio Biases in the American Crocodiles
(Crocodylus acutus) of the Tempisque Basin
Christopher M. Murray
1
, Michael Easter
2
, Sergio Padilla
3
, Davinia B. Garrigo´s
4
,
Julia Ann Stone
1
, Juan Bolan˜os-Montero
5
, Mahmood Sasa
6
, and Craig Guyer
1
A male-biased sex ratio of 3:1 has been reported for a population of American crocodiles (Crocodylus acutus) in the
Tempisque River Basin, Guanacaste, Costa Rica. If confirmed, this would constitute one of the largest male-biased sex
ratios reported for any population of a member of the genus Crocodylus. Here, we examine the aforementioned
population of C. acutus and report on sex ratios of hatchling, juvenile, and adult age classes within a sample of 474
crocodiles captured in the Tempisque Basin between May 2012 and June 2014. Hatchling sex ratio is exceptionally male
biased (3.5:1), an imbalance that is maintained in juveniles but is reduced in adults (1.5:1). Mark–recapture data
document that juvenile males disperse from the study site, potentially to avoid competition, a process that reduces
male bias in the adult age class. An increased role of males in human–crocodile conflict may be a result of juvenile males
dispersing to human-inhabited areas.
SEX allocation and sex ratio theory have been a topic of
experimental and theoretical discussion among ecol-
ogists and evolutionary biologists for over a century
(Darwin, 1871; Du¨sing, 1883; Fisher, 1930). Critical to the
viability of sexually reproducing organisms is an adequate
proportion of both sexes, most classically modeled by Fisher
(1930). This model relies on competition for mates based on
the number of individuals of each sex and associated mating
prospects. Parents that produce the minority sex will have
increased fitness based on number of grandchildren pro-
duced and the minority sex will be selected for, thus
maintaining sex ratio equilibrium (Fisher, 1930). Numerous
variables, such as sex-linked drive (Hamilton, 1967), alter-
native fitness influences (Charnov et al., 1981), dispersal
(Bulmer, 1986), longevity (Eberhardt, 2002), operational
sampling (Gibbons, 1990), and sibling interaction (Uller,
2006) have been added to the basic Fisherian model to
explain unusual sex ratios observed in nature.
For organisms exhibiting environmental sex determina-
tion (ESD), abiotic cues determine patterns of steroid
production, which canalizes development toward one gender
or another (Valenzuela and Lance, 2004). Temperature-
dependent sex determination (TSD), the most common
mechanism of ESD, has obvious relevance to sex allocation
theory. TSD is likely selected for when the environment
produces the sex with the highest fitness in a highly variable
environment (Charnov and Bull, 1977; Warner and Shine,
2008). Further, temperature is thought to lead to differential
growth rates between sexes and, thus, different fitness
consequences (Bull and Charnov, 1989). However, sex ratios
of organisms with TSD are less self-correcting than those with
genotypic sex determination so that organisms with TSD may
experience altered sex ratios that undermine demographic
viability, a feature that may make them susceptible to
anthropogenic change (Doody et al., 2006).
All extant crocodilians exhibit TSD and members of the
genus Crocodylus produce viable offspring between 25 and
35uC, with males generated between 31 and 33.5uC and
females produced at all other temperatures in the viable
range (Lang and Andrews, 1994). With such a narrow male-
specific thermal window, it has been suggested that male
bias in clutches of crocodiles is difficult to produce in nature
(Thorbjarnarson, 1997; Lance et al., 2000). However, male-
biased sex ratios are known in crocodilian populations
(Thorbjarnarson, 1997). For example, American crocodile
(Platt and Thorbjarnarson, 2000) and Morelet’s crocodile
populations (Rainwater et al., 1998) in Belize as well as
a population of the American crocodile (Crocodylus acutus)
in the Tempisque Basin of Guanacaste, Costa Rica (3:1 male
bias; Bolan˜os-Montero, 2012) exhibit some of the strongest
male biases documented. Similarly, Charruau (2012) re-
ported a male bias in hatchling C. acutus in Banco
Chinchorro Biosphere Reserve, Mexico. However, the study
by Bolan˜os-Montero (2012) was based on limited sampling
in the Tempisque watershed and a biased sex ratio was not
found by Sa´nchez-Ramı´rez (2001) for the same area.
Additionally, these previous studies were based on raw
counts (observed ratios of captures animals) of individuals
detected rather than accounting for segments of the
population that were undetected. Therefore, the aim of this
study was to use mark–recapture techniques to estimate
cohort-specific population sizes of each sex independently,
compare such estimates, and assess whether a male-biased
sex ratio characterizes the population of C. acutus in the
Tempisque River Basin.
MATERIALS AND METHODS
Study area.—All sampling for this study was performed in
Palo Verde National Park and adjacent localities in the
Guanacaste Province, in northwestern Costa Rica. Seven
sampling localities in the Tempisque River basin were used;
the Humedal, the Drain, the Bebedero River, Varillal
Lagoon, La Bocana, Nicaragua Lagoon, and the Tower Ponds
(Fig. 1). All sampling localities were restricted to the areas
1
Department of Biological Sciences, Auburn University, 331 Funchess Hall, Auburn, Alabama 36849; E-mail: (CMM) cmm0054@auburn.edu;
and (CG) guyercr@auburn.edu. Send reprint requests to CMM.
2
Everglades Holiday Park, 21940 Griffin Rd., Fort Lauderdale, Florida 33332; E-mail: m.easter05@gmail.com.
3
Palo Verde Biological Station, Organization for Tropical Studies, Guanacaste, Costa Rica; E-mail: sergio.padilla@ots.ac.cr.
4
Biodiversity and Evolutionary Biology ‘‘Cavanilles’’ Institute, University of Valencia, Valencia, Spain; E-mail: davinia.beneyto@uv.es.
5
Grupo Aqua Corporacion Internacional SA, Can˜ as, Guanacaste, Costa Rica; E-mail: crocacutus@gmail.com.
6
Instituto Clodomiro Picado, Facultad de Microbiologı´a, Universidad de Costa Rica, San Jose´, Costa Rica; E-mail: msasamarin@gmail.com.
Submitted: 3 November 2014. Accepted: 11 April 2015. Associate Editor: D. S. Siegel.
F2015 by the American Society of Ichthyologists and Herpetologists DOI: 10.1643/CE-14-186 Published online: July 31, 2015
Copeia 103, No. 3, 2015, 541–545
within or immediately surrounding Palo Verde National
Park and are part of the same Tempisque River Basin
population. The Humedal, Varillal Lagoon, La Bocana,
Nicaragua Lagoon, and Tower Ponds are seasonal wetlands
characterized by open expanses of Typha,Thalia, and
Eichhornia in the wet season (May to December). These
areas are void of water during the dry season (December to
May) when they are characterized by cracked mud with
patches of vegetation. The Drain is a permanent canal that
drains irrigation water from rice fields north of the National
Park to the Tempisque River 10 km to the southwest. This
canal is influenced both by tide and agricultural discharge.
The Bebedero River is a major tributary to the Tempisque
River that extends to the northeast from the Tempisque
River to near the town of Can˜as, Guanacaste Province, Costa
Rica. This river is tidally influenced toward the mouth where
it meets the Tempisque River 5 km north of the Gulf of
Nicoya.
Crocodile sampling.—American crocodiles were captured in
the Tempisque Basin between May 2012 and June 2014.
Crocodiles were captured by hand, breakaway snare pole, or
top-jaw rope. Sex (by cloacal examination of the genitalia),
snout to vent length (SVL), and total length (TL) were
recorded followed by creation of a permanent mark via tail
scute removal. Individuals were categorized into a cohort
based on size: hatchling (,35 cm), juvenile (35–180 cm),
and adult (.180 cm; modified from Platt and Thorbjarnar-
son, 2000). A sub-adult size class was not included because
any size cut-off between the juvenile and sub-adult cohort
was deemed an artificial threshold.
Sampling of hatchlings included 13 clutches (204
hatchlings) within which all individuals were known to
have been captured because we monitored the nests from
which they emerged and the number of viable eggs was
matched to the number of hatchlings captured (n56) or
because we discovered aggregated individuals soon after
hatching from unmonitored nests. The risk of hatchling
predation and capture detection existed at unmonitored
nests, but was minimized by our timing. We captured two,
seven, and four clutches in 2012, 2013, and 2014,
respectively. Two clutches in 2013 were captured in the
Bebedero River while the rest were captured along a 10 km
stretch of drainage canal along the northwest border of the
national park. Because hatchlings remain aggregated at nest
sites immediately after hatching and because we accounted
for all individuals known to have hatched from monitored
nests, we assume that sex ratios based on raw counts of
hatchlings are not biased by undetected individuals emerging
from unmonitored nests. A hatchling crocodilian was de-
termined to be male if the clitero-penis possessed all of the
following character states: bi-lobed structure, extensive
vascularization, and length extending the length of the vent
(Fig. 2; Allsteadt and Lang, 1995).
For juveniles we used Bailey’s triple catch method (Bailey,
1951, 1952) to estimate gender-specific population size and,
thus, sex ratio. This method allowed us to estimate the
number of males and females by adjusting for individuals
not detected during our sampling. This algorithm assumes
an open population with variable gain and survival and
requires three sampling events with at least 20 captures per
event (Donnelly and Guyer, 1994). Each sampling event
represented a complete survey of the area, with one event
occurring in 2013 (January–May) and two events occurring
in 2014 (January–March and April–June). Separate estimates
for population size, loss rate, and gain rate were calculated
for male and female juveniles. Because the sample of adults
yielded few recaptures, unlike the juvenile cohort, we used
raw counts to characterize sex ratio of this cohort.
A G-test was used to assess differences in proportion of
males among cohorts and to test deviation from a 1:1 sex
ratio. A runs test for non-randomness was used to assess any
bias in the pattern of capture of males and females in the
field.
RESULTS
A total of 474 American crocodiles were captured during our
study. Analysis for raw count data provides G-test results
that indicate a significant difference in the sex ratio among
cohorts (G 550.828, df 52, P5,0.01). The hatchling
cohort exhibits a sex ratio of nearly 80%male, while
juvenile and adult cohorts both exhibit 60%male sex ratios.
Across all cohorts we recover a 2.2:1 male-biased sex ratio.
When data for juveniles were adjusted for undetected
individuals, we recovered a 3.4:1 male-biased sex ratio
overall, an imbalance that differs from the expected 1:1
sex ratio (G 5103.05, df 51, P5,0.001). The sex ratio
differed marginally among cohorts (G 55.447, df 52, P5
0.07; Fig. 3). The hatchling and juvenile cohorts consisted of
nearly 80%males, while the adult cohorts consisted of
approximately 60%males.
Our juvenile sex ratio was based on population estimates
associated with the second capture interval (N
1
; Table 1).
These values differ markedly from the female-biased pattern
indicated by juvenile raw counts. Vital demographic rates of
change for juvenile females indicated a positive growth rate
for this component of the population, with gains due to the
combined effects of growth of hatchlings and immigration
being sufficient to counteract losses due to the combined
effects of mortality and emigration. Vital rates of change for
juvenile males indicated a negative growth rate for this
component of the population, with gains due to the
combined effects of growth of hatchlings and immigration
being insufficient to counteract losses due to the combined
effects of mortality and emigration. Losses were more similar
for male and female juveniles than were gains, which were
Fig. 1. Map of the study area in Guanacaste, Costa Rica. Region shown
includes Palo Verde National Park and the Tempisque River Delta.
Seven sampling areas are noted: (Drain [A], Varialle Lagoon [B],
Humedal [C], La Bocana [D], Nicaragua Lagoon [E], Tower ponds [F], Rio
Bebedero [G]).
542 Copeia 103, No. 3, 2015
reduced in males relative to females (Table 1). We found no
significant runs of either sex in our capture records (Z 5
–0.447, P50.327; Table 1); thus, non-random sampling of
sexes is rejected.
DISCUSSION
Our data document a male-biased sex ratio in the Palo Verde
National Park (Tempisque Basin) population of Crocodylus
acutus. The extent of this bias is extreme at hatching,
becoming reduced for adults. Our data for juveniles provide
evidence for how such an extreme male bias is adjusted
over time. Of particular interest is our documentation that
juvenile males exhibit a negative population growth rate,
likely caused by dispersal of this stage from the Tempisque
sampling localities, and no immigration of juvenile males to
the population. Juvenile females, apparently, have balanced
rates of immigration and emigration that maintain a positive
population growth rate for this segment of the population.
Based on raw counts of individuals captured, juvenile
females were more numerous than juvenile males. This
suggests either that migration of juvenile males is extensive
and immediate, that males are more adept at avoiding
capture, or that both processes are operating. Our data for
adults are limited because recaptures are too low to account
for undetected animals and the important parameters of an
open population. However, if our raw counts accurately
reflect the real adult sex ratio, then increased dispersal or
mortality of males beyond the juvenile stage does not
appear to be occurring. If anything, immigration of
juveniles to the study site to retain a male bias in detected
adults may be indicated by our data.
The extent of male bias in our hatchling cohort is
unprecedented in crocodilian populations. Charruau
(2012) reported male-biased sex ratios at birth for American
crocodiles at a site in Mexico, but there only 66%of
hatchlings were male, a percentage closer to that of adults at
the Tempisque population. Because the sex of our hatch-
lings was determined by visual inspection of the relative size
of developing genitalia, our extreme male bias might result
from misidentification of sex. However, we argue that this is
unlikely, based on a sample of ten hatchlings that were
Fig. 2. Clitero-penis (CTP) examples depicting conservative sex determination of hatchlings based on the number of lobes, vascularization, and
relative length. Female exhibiting small vascularized nub (A); female exhibiting small non-vascularized nub (B); female exhibiting single-lobed
vascularized projection (C); male exhibiting bi-lobed vascularized projection that extends the length of the cloacal opening (D, E).
Murray et al.—Crocodile sex ratio biases 543
identified as to sex at birth and then raised for a year at the
Palo Verde Biological Station. When re-examined a year
later, none of these individuals changed in status. The
extreme male bias at hatching might also result from
a biased sample of nests. However, hatchlings were captured
within a short time following emergence from their nests
during a time when nest mates remain aggregated. For
monitored nests the number of hatchlings captured corre-
sponded to the number of viable eggs known to be in the
nests. We assume this to also be true of unmonitored nests.
Further, the temporal and spatial disparity of the clutches
analyzed accounts for climatic bias within years as well as
spatial thermal variation between habitats. Therefore, the
only way that our count of hatchling males and females is
biased is if the pool of undetected nests produced a sex ratio
differing from our detected nests. Additionally, the window
of nest temperatures yielding male American crocodiles is
quite narrow (Thorbjarnarson, 1997; Lance et al., 2000),
making it unlikely that we selected nests within this narrow
window and missed others outside this range.
The demographic patterns that we document for juvenile
males and females are consistent with interpretations
inferred for other crocodilians. The territoriality of adult
male crocodilians has been used to suggest that juvenile
males disperse from the natal population to avoid compe-
tition (Thorbjarnarson, 1989; Platt and Thorbjarnarson,
2000), features consistent with our estimates of gain and
loss rates for juveniles (Fig. 4).
Across the entire population of Tempisque crocodiles, we
recovered a male bias that is as skewed as that reported by
Bolan˜os-Montero (2012) and far more skewed than that
reported by Sa´nchez-Ramı´rez (2001). The sampling of
Bolan˜os-Montero (2012) and Sa´ nchez-Ramı´rez (2001) may
have been inadvertently susceptible to location-based biases
or biases resulting from undetected individuals. Here, we
present increased sampling and mark–recapture analysis to
estimate animals not detected. The difference in observed
versus estimated sex ratios of juveniles is extreme and
renders strict observation-based counts unreliable. Dispersal
of juvenile males from the core sampling areas would have
likely resulted in an underestimation of males in the
population based on strict count sampling.
Negative perceptions of crocodiles have reached a critical
level in Costa Rica as a result of increased media coverage of
crocodile/human conflicts and/or an actual statistical in-
crease in attacks by crocodiles on humans (Valdelomar et al.,
2012). A unique male bias, to the extent described by
Bolan˜os-Montero (2012), is likely to contribute to this
negative perception. The demographics discussed here
indicate an expanding population, from a spatial perspec-
tive, that may lead to increased overlap with human-
inhabited areas and potential for human-induced conflict
such as feeding (Rainwater et al., 2011). Furthermore, if this
problem persists for generations then selection for more
aggressive males based on heightened reproductive compe-
tition may occur. Of utmost importance is an organized
collaborative effort to assess the demographics of Crocodylus
acutus along the Pacific versant of Costa Rica prior to
management action.
ACKNOWLEDGMENTS
We thank M. Mendonc¸a, M. Merchant, and T. Wibbels for
guidance and review, T. Connors, A. Blanco, V. Salvatico, F.
Bonilla, S. Bermudez, and J. Serrano for logistic support, and
MINAET, Vicerrectorı´a de Investigacio´ n Uni versidad de
Costa Rica, and the Organization for Tropical Studies for
permitting assistance and funding.
Table 1. Populations estimates, birth/immigration rates, death/
emigration rates, and population growth rates of males and females
in the juvenile cohort based on Bailey’s Triple Catch algorithm (top).
Bailey’s Triple Catch Males Females
Population size at time 1 (N
1
) 3106208.2 89671.8
Raw count 98 117
Birth/immigration rate (B
12
) 0.322 1.241
Death/emigration rate (D
01
) 0.565 0.752
Instantaneous birth/immigration
rate (b
12
)
–1.13 0.216
Instantaneous death/emigration
rate (d
01
)
0.833 1.39
Population growth rate (r) –0.586 0.073
Fig. 3. Cohort-specific sex ratios with juvenile cohort based on triple
catch algorithm estimates. Sample sizes do not include recaptures. G-
test results show independence in male frequency among cohorts (G 5
50.828, df 52, P5,0.01).
Fig. 4. Schematic depicting proposed demographics among cohorts of
the two sexes, showing emigration of juvenile males from
the population.
544 Copeia 103, No. 3, 2015
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Murray et al.—Crocodile sex ratio biases 545
... Sin embargo, hay estudios que muestran variabilidad en este parámetro (Lance et al. 2000). En el aligátor americano (Alligator mississippiensis), Lance et al. (2000) encontraron un sesgo hacia los machos en la cohorte de juveniles, mientras que en C. acutus, Murray et al. (2015) también encontraron un sesgo hacia los machos en la cohorte de neonatos de 3.5:1 entre 2012-2014. Este parámetro se modeló con diferentes valores en otros escenarios. ...
... En dicho análisis, el valor de mortalidad de cada cohorte es igual para ambos sexos, lo que hace la proporción sexual total de la población sea de 1:1. En otros estudios, las poblaciones pueden presentar un sesgo hacia los machos (Lance et al. 2000, Murray et al. 2015 o hacia las hembras (Mauger et al. 2012), pero también puede que no haya diferencia en proporción sexual en el número total de individuos de la población (Cedeño-Vásquez et al. 2006, Platt et al. 2011). ...
... La proporción sexual de individuos adultos es de 0.566 : 1 (machos : hembras). Este valor es muy variable entre poblaciones (Thorbjarnarson 1989), puede ser muy sesgado hacia las hembras (Sánchez 2001) o hacia los machos (Murray et al. 2015), e incluso puede que haya igualdad entre ambos sexos (Platt et al. 2011). El valor del modelo de línea base es similar al promedio de valores reportados para varios estudios en Florida (1:2) (Thorbjarnarson 1989). ...
Technical Report
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Análisis de Viabilidad de Poblaciones de una población hipotética del Pacífico de Costa Rica
... However, there are studies that show variability in this parameter (Lance et al. 2000). In the American alligator (Alligator mississippiensis), Lance et al. (2000) found a bias toward males in the juvenile cohort, while in C. acutus, Murray et al. (2015) also found a bias toward males in the neonatal cohort of 3.5: 1 between 2012-2014. This parameter was modeled with different values in other scenarios. ...
... In Soberón et al. (2000), the mortality value of each cohort is equal for both sexes, which makes the total sexual ratio of the population to be 1:1. In other studies, populations may be skewed towards males (Lance et al. 2000, Murray et al. 2015 or toward females (Mauger et al. 2012), but there may also be no differences in the proportion of sexes on the total number of individuals of the population (Cedeño-Vásquez et al., 2006, Platt et al., 2011. ...
... The sex ratio of adult individuals is 1:1.88 (males:females). This value is highly variable among populations (Thorbjarnarson 1989), can be very skewed towards females (Sánchez 2001) or towards males (Murray et al., 2015), and may even have no differences between both sexes (Platt et al. 2011). The value of the baseline model is similar to the average values reported for several studies in Florida (1: 2) (Thorbjarnarson 1989). ...
Technical Report
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This is a Population Viability Analysis of hypothetical Crocodile populations from the Pacific of Costa Rica
... A uniquely male-biased sex ratio of American crocodiles (Crocodylus acutus) in the Tempisque drainage of Costa Rica has been previously described (Bolaños-Montero, 2012;Murray et al., 2015). This is one of multiple reports that describe recent male-biased crocodilian populations throughout Central America (Charruau et al., 2005;Escobedo-Galván, 2008). ...
... Upon capture, sex was determined for individuals via inspection of the secondary sex organ. Individuals were diagnosed as male is the clitero-penis exhibited all of the following characteristics: bi-lobed structure, extensive vascularization, and length extending the length of the vent (Murray et al., 2015). ...
... Thus, 75% of eggs incubated at field temperatures known from Palo Verde would produce males in the presence of known levels of MT in the yolk. This value approaches the 80% male bias for hatchling crocodiles recorded at Palo Verde (Murray et al., 2015). ...
Article
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Endocrine-disrupting contaminants (EDC's) are well known to alter sexual differentiation among vertebrates via estrogenic effects during development, particularly in organisms characterized by temperature-dependent sex determination. However, substances producing androgenic effects typically lack potency when tested in laboratory settings and are virtually unstudied in field settings. Here, we assay levels of a synthetic androgen, 17α-methyltestosterone (MT), in a heavily male-biased population of American crocodiles in the Tempisque River Basin of Costa Rica based on the recent hypothesis that this chemical is an EDC in developing crocodilian embryos. The presence of MT was documented in all field-collected samples of egg yolk and in plasma of all age classes in among population of crocodiles. Hatchlings exhibited higher plasma MT concentrations (102.1 ± 82.8 ng/mL) than juveniles (33.8 ± 51.5) and adults (25.9 ± 20.8 ng/mL). Among populations, crocodiles captured in the Tempisque River (62.9 ± 73.7 ng/mL) were higher in MT concentration than those from Tarcoles (13.3 ± 11.4 ng/mL) and negative controls (0.001 ± 0.0002 ng/mL). A mechanism for the bio-transport of MT and its subsequent effects is proposed.
... American crocodile populations have been reported to have male-skewed sex ratios in some Costa Rican drainages, despite living under female-producing temperature regimes [138][139][140]. The levels of accumulated MT in all the field collected eggs and in the plasma of wild crocodile hatchlings were similar to those that found in experimentally masculinized hatchlings, even when eggs were exposed to a female-producing temperature [139]. ...
... Following a single meal of a diet containing both unlabeled and labeled (3H-and 14C-) 17MT, adult tilapia can accumulate MT in various tissues (adipose tissue was not analyzed in this study) [124]. At four and 21 days after the single [138][139][140] for the American Crocodile in Costa Rica, via the activation and inactivation of sulphate conjugates. Abbreviations: FPT, female-producing temperature. ...
... American crocodile populations have been reported to have male-skewed sex ratios in some Costa Rican drainages, despite living under female-producing temperature regimes [138][139][140]. The levels of accumulated MT in all the field collected eggs and in the plasma of wild crocodile hatchlings were similar to those that found in experimentally masculinized hatchlings, even when eggs were exposed to a female-producing temperature [139]. ...
... Following a single meal of a diet containing both unlabeled and labeled (3H-and 14C-) 17MT, adult tilapia can accumulate MT in various tissues (adipose tissue was not analyzed in this study) [124]. At four and 21 days after the single [138][139][140] for the American Crocodile in Costa Rica, via the activation and inactivation of sulphate conjugates. Abbreviations: FPT, female-producing temperature. ...
Chapter
Tilapias are the second largest group of fish produced worldwide, due to their great plasticity and ideal aquaculture traits, particularly the Nile tilapia. On most tilapia farms, sex control is necessary to increase profitability, due to early and continuous reproduction and female mouth‐brooding, and to benefit from the males’ faster growth rate. This review presents the different ways to produce all‐male populations by genetic approaches, such as the use of YY males (or ZZ females in the blue tilapia), and hormonal or high temperature sex reversal treatments, presenting the advantages and drawbacks of each method, as well as protocols for their use. Androgen treatment is still the predominant means to generate monosex male offspring, due to its simplicity, efficiency and price. The hormone amounts currently used worldwide, and its consequences on biodiversity, are discussed, regarding the sustainability of tilapia farming and taking into account growing consumer awareness. Results regarding 17α‐methyltestosterone (MT) accumulation and the possible use of MT‐degrading bacteria are discussed. More sustainable alternative methodologies can be potentiated. Current research status on the sex‐determining loci in Nile, blue, Mozambique and black chin tilapias is presented. Finally, we show the available genetic and phenotypic sex markers that can accelerate progeny testing, rapidly identifying particular genotypes and phenotypes of interest such as YY males or ZZ females, as well as being important for selection programs.
... Few populations of C. acutus show biased adult sex ratios and when they do, the bias often seems to be towards males (Escobedo-Galván et al. 2011). Recent studies have detected male-biased hatchling sex ratios in C. acutus populations (Charruau 2012, Murray et al. 2015, which could threaten their survival. However, Murray et al. (2015) found that some population-dynamic parameters of C. acutus, such as juvenile male dispersal, could permit the transition from male-biased hatchling sex ratios to equilibrate adult sex ratios. ...
... Recent studies have detected male-biased hatchling sex ratios in C. acutus populations (Charruau 2012, Murray et al. 2015, which could threaten their survival. However, Murray et al. (2015) found that some population-dynamic parameters of C. acutus, such as juvenile male dispersal, could permit the transition from male-biased hatchling sex ratios to equilibrate adult sex ratios. It is however still unclear what will happen to island populations where juvenile dispersal is impossible or to populations with female-biased sex ratios. ...
... Regarding the size distribution of C. acutus individuals, the right negative skew in both TNP and BACORE coincides with that reported for other zones by Sánchez et al. (1996), Bolaños et al. (1997Bolaños et al. ( , 2019, Bolaños (2011aBolaños ( , 2011bBolaños ( , 2012aBolaños ( , 2012b, Murray et al. (2015), Orozco (2015), and Bolaños et al. (2019), the last one for the Central Caribbean. Population status of American crocodile and spectacled caiman Unlike C. crocodilus, whose individuals tend to be more social and to remain within the family unit of their distribution zones (Gorzula and Seijas 1989), it is known that C. acutus hatchlings are carried away by river currents soon after they hatch and continue to move along the river course until they establish their own living sites (Bolaños et al. 2019). ...
Article
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Along the Costa Rican Caribbean shoreline, it is possible to find two species of crocodilians, the American crocodile (Crocodylus acutus) and the spectacled caiman (Caiman crocodilus). This region can be divided geographically into three subregions: North, Central, and South Caribbean. We conducted this research in the North Caribbean, between October 6, 2018 and August 31, 2019. Specifically, we worked in the area lying between the Jalova Station of the Tortugero National Park (TNP) and Agua Dulce Lake situated in the northern tip of Machuca Island, at the mouth of the Colorado River inside the Barra del Colorado National Wildlife Refuge (BACORE), which includes other connecting wetlands as well (Sierpe River, Samay Lake). Overall, this study area had an approximate extension of 408 km2 characterized by large, wide and deep canals, as well as wetlands, meanders, and adjacent lakes. The sampling was performed along 10 segments that varied in length from 7.5 km up to 29.49 km, located in the nearby zones of TNP and BACORE. In these zones, nightly counts were carried out using dazzling lamps. Individuals of C. acutus and C. crocodilus were classified into eight and six body size classes, respectively (both with 50 cm intervals). A relative abundance of 0.55 crocodiles and 1.37 caimans per linear kilometer was estimated during these spotlight surveys. The capture of 39 caimans let us to estimate a ratio of 30 males to 9 females (3.3:1 M:F). In stark contrast, only 1 male and 1 female crocodile were captured. A total of 85 C. acutus and 205 C. crocodilus were observed. Regarding the number of caiman sightings in the TNP, a statistically significant difference was found (Χ2=5.62, p≤0.05) for the distribution by sizes between the zones of BACORE and TNP, whereas no such difference was found for C. crocodilus sightings (Z=–1.22, p≥0.222). Some segments had a higher probability of caiman occurrence than did others in the surveys performed during the monitoring period (X2=8.36, p≤0.05), especially the Jalova-Sierpe River, Caño Negro-Tortuguero, and Tortuguero-Samay Lake (Tortuguero subarea) segments. Ninety percent of the sightings occurred in the BACORE zone, and this was significantly different (Χ2=7.34, p≤0.026) from the studied subareas. The number of crocodile sightings in the Colorado River segment was significantly different and higher than the other segments (X2=7.28, p≤0.05). There was a significant statistical difference among the sizes in all areas of study (X2=5.529, p≤0.026). The abundance of C. acutus and C. crocodilus in the north Caribbean part is lower than in the central Caribbean part of Costa Rica, where this species could use the resources available in more urbanized areas.
... Unlike caimans, the quantity and size structure of the crocodiles observed did not come close to what was expected, considering existing populations under similar environmental conditions (De Sola, Velasco, Villaroel, & Colomine, 2004;Bolaños, 2012a;Murray et al., 2015). In this case, apart from the Matina River, the Caño California and Boca de Jalova, the crocodile is evidently absent in the whole area studied, with special mention to individuals with sizes greater than size class VI (≥ 3 m), different from that found by Sánchez et al. (1996), Bolaños (2012b) and Orozco (2015) for the Pacific. ...
Article
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American crocodile (Crocodylus acutus)(Reptilia:Crocodilidae) and caiman (Caiman crocodilus)(Reptilia:Alligatoridae) population status, in the Costarican Central Caribbean. Two species of crocodilians have been described in Costa Rica, american crocodile (Crocodylus acutus: Cuvier 1807), and caiman (Caiman crocodilus: Linnaeus 1758). In Costa Rica, data has been generated on both species, but populations in the Pacific have received more attention from researchers; due to the fact that the Pacific slope has a greater development, which brings greater social pressure on the attention of the incidents generated by the encounter between humans and crocodiles. This study, performed during 2017, was done in an area of approximately 400 km2, characterized by having a wide and dense network of water courses, which includes the Matina, Pacuare, Reventazón and Parismina rivers. In these rivers, an average of 25 kilometers were traveled from the coastline up stream to the interior of the territory, including the Tortuguero canals, and other water bodies that connect these rivers, as well as in the most important lagoons and secondary channels. Three repetitions were made per segment. A population of 1084 caimans and 503 crocodiles is estimated; for a relative abundance of 8.64 and 2.80 ind/Km respectively. Speaking of caimans, up to 12% of individuals of reproductive age were observed, while for crocodiles that number was only 2%. The presence of both species in the different places studied, turned out to be significantly different for crocodiles and for caimans (Kruskal-Wallis, p≤0,000). Likewise, the size distribution is similar for crocodiles reported in all environments (Kruskal-Wallis, p≤0.15), while for caimans it indicates that there is a different distribution for sizes, according to the environment in which they are found (Kruskal -Wallis, p≤0,000), with a bias against of the Pacuare and Matina rivers. It was possible to estimate a sex ratio of 1.25 and 0.83 males to females, in crocodiles and caimans respectively, with 9 and 11 captures in that same order, in individuals of recruits, juvenile and subadult sizes. The Matina River and the Jalova Lagoon are the two main sites for the observation of crocodiles, their abundances are lower than those reported for the Pacific of Costa Rica, in whereas caimans, with a more homogeneous distribution throughout the sampling area, have a relative abundance considerably more than that reported in Honduras (2.2 ind/km), but lower than the 12.5 reported forLa Rambla de Sarapiquí, in the Northern Zone of Costa Rica.
Article
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American Crocodile Crocodylus acutus has most recently been assessed for The IUCN Red List of Threatened Species in 2020. Crocodylus acutus is listed as Vulnerable under criteria A2cd.
Chapter
Wildlife is exposed to a diverse range of natural and man-made chemicals. Some environmental chemicals possess specific endocrine disrupting properties, which have the potential to disrupt reproductive and developmental process in certain animals. There is growing evidence that exposure to endocrine disrupting chemicals plays a key role in reproductive disorders in fish, amphibians, mammals, reptiles and invertebrates. This evidence comes from field-based observations and laboratory based exposure studies, which provide substantial evidence that environmental chemicals can cause adverse effects at environmentally relevant doses. There is particular concern about wildlife exposures to cocktails of biologically active chemicals, which combined with other stressors, may play an even greater role in reproductive disorders than can be reproduced in laboratory experiments. Regulation of chemicals affords some protection to animals of the adverse effects of exposure to legacy chemicals but there continues to be considerable debate on the regulation of emerging pollutants.
Article
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El cocodrilo americano (Crocodylus acutus) es una especie amenazada por la pérdida de hábitat y la caza ilegal. En el río Tempisque, Costa Rica, sus poblaciones se han recuperado considerablemente pero siguen siendo vulnerables porque su nicho y hábitat se traslapan con las actividades humanas, lo que genera un conflicto humano-cocodrilo (CHC) que se agrava por conocimientos populares erróneos. Este trabajo evalúa la percepción y el conocimiento popular sobre los cocodrilos mediante 336 encuestas en 11 pueblos de los cantones Carrillo, Santa Cruz y Cañas de Guanacaste. Además se analizó la relación entre la percepción de peligrosidad de los cocodrilos según el pueblo de residencia, la edad, el sexo, el grado académico y la ocupación de los encuestados. La población considera que en sus pueblos existen demasiados cocodrilos, que son peligrosos y agresivos. En general conocen poco sobre la biología de C. acutus, pero bastante sobre su comportamiento, estado de conservación y protección estatal. Las personas encuestadas creen necesario regular las poblaciones de cocodrilos, sugieren la eliminación o el traslado selectivo (las cuales tienen diversas implicaciones) y parecen dispuestos a cooperar en planes de manejo. Se insta a seleccionar pueblos clave para reforzar los programas de educación ambiental con contenidos sobre la biología de la especie, seguridad y prevención de CHC. A futuro, parece necesario establecer un plan de manejo pararegular las poblaciones de cocodrilos en algunos sitios específicos de la cuenca del río Tempisque. ABSTRACT Perception and popular culture about the crocodile (Crocodylus acutus) near Tempisque River, Guanacaste, Costa Rica. The American crocodile (Crocodylus acutus) is an endangered species due to habitat loss and illegal hunting. Its population has recovered significantly in the Tempisque River, Costa Rica; nevertheless, they are still vulnerable because their niche and habitat overlap human activities, which causes a human-crocodile conflict worsened by mistaken popular beliefs. We evaluated popular perception and knowledge with 336 surveys in 11 towns of Carrillo, Santa Cruz and Cañas, in Guanacaste. We also tested the relationships among residence, occupation, sex, age and educational grade and perception of danger. The inhabitants believe there is an excess of crocodiles near their towns, and the reptiles are considered dangerous and aggressive. Overall, they know little about the biology of C. acutus,but much about its behavior, conservation status and state protection. To regulate the crocodile population, they consider elimination or relocation necessary (both have different implications). They seem, however, willing to cooperate in management plans. It is important to choose key towns to strengthen existent environmental education programs with contents about the biology of the species, security, and conflict avoidance. In the near future, we recommend the establishment of a management plan to regulate crocodile population in some specific spots within the Tempisque River’s Basin.
Article
The American crocodile is the most widely distributed of the New World crocodiles, ranging from the southern tip of Florida, along both the Atlantic and Pacifi c coasts of southern Mexico, Central America, and northern South America, as well as the Caribbean islands of Cuba, Jamaica, and Hispaniola. The habitat of C. acutus consists largely of brackish water coastal habitats such as the saltwater sections of rivers, coastal lagoons, and mangrove swamps. However, populations are known from freshwater areas located well inland, including a number of reservoirs. A signifi cant population is known from Lago Enriquillo, a landlocked hypersaline lake situated 40 m below sea level in the arid southwestern Dominican Republic. The American crocodile is a relatively large species, with males reaching maximum lengths of 5-6 m, although some individuals may reach 7 m (Schmidt 1924; Medem 1981). Adult females are generally no more than 3-3.5 m TL, but individuals up to 4.4 m have been reported (Dominguez-Laso 2009). The species is characterized by the most reduced and irregular dorsal armor (osteoderms) of any crocodilian (Ross and Mayer 1983). Figure 2. Crocodylus acutus. Photograph: Jemeema Carrigan.
Article
A sequence of changes in vital rates observed as populations approach maximal levels has been used as the basis for a "paradigm" for population analysis. Previous work indicates that early survival decreases first, followed by lower reproductive rates; ultimately, adult female survival may decrease. "Sensitivity" of population growth rates, as measured by partial derivatives of an approximation to the Lotka-Leslie model, appears to follow the same sequence, suggesting that population regulation may follow that sequence. This may imply some evolutionary significance in the sequence. Thus, it may be possible to assess population status by measuring the vital rates, as shown in a number of examples reported here. Measuring vital rates in the field is subject to a variety of biases; hence, an analysis should include direct estimates of population trend. In the absence of complete data, suitable trend data might be used to estimate missing rates. Bootstrapping provides a simple way to obtain confidence intervals, and the delta method can be used to obtain components of variance and thus improve sampling. Various methods for studying trend are given, with examples and simple statistical tests.