Article

Regional Warming and the Thermal Regimes of American Crocodile Nests in the Tempisque Basin, Costa Rica

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  • Scales and Tail of Ohio
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... Nests sampled at ENWR were composed of mud, which is atypical for American alligators. Although nests constructed primarily of mud is relatively common in other crocodilians [60,66], this was a novel documented behavior in the American alligator [46]. We did not observe functional redundancy across space (macro-scale) when atypical mud nests were included in analyses of beta diversity, perhaps indicating a possible effect of female reproductive plasticity on microbial nest composition. ...
... We hypothesize that alligator nest construction behavior draws bacterial taxa from the surrounding environments who then become entrapped within the nest structure. Bacterial taxa may have limited dispersal possibilities and are subject to assemblage filtering by the stable environment within the nest, relative to external environmental fluctuations [66,71]. Dispersal- showing that increased distance is positively correlated with assemblage dissimilarity [2,71]. ...
... The central egg chamber of alligator nests may be environmentally unique relative to the rest of the nest structure. The comparatively stable thermal oscillations within egg chambers of crocodilian nests [66] and/or the presence of the eggs, themselves, may provide a highly calcified substrate for bacteria to colonize [41], selecting for a subset of functional pathways found only in the egg chamber. We suggest future work examining microorganisms expressing these pathways and their functional role in alligator hatching success. ...
Article
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Understanding the ecological processes that shape species assemblage patterns is central to community ecology. The effects of ecological processes on assemblage patterns are scale-dependent. We used metabarcoding and shotgun sequencing to determine bacterial taxonomic and functional assemblage patterns among varying defined focal scales (micro-, meso-, and macroscale) within the American alligator (Alligator mississippiensis) nesting microbiome. We correlate bacterial assemblage patterns among eight nesting compartments within and proximal to alligator nests (micro-), across 18 nests (meso-), and between 4 geographic sampling sites (macro-), to determine which ecological processes may drive bacterial assemblage patterns within the nesting environment. Among all focal scales, bacterial taxonomic and functional richness (α-diversity) did not statistically differ. In contrast, bacterial assemblage structure (β-diversity) was unique across all focal scales, whereas functional pathways were redundant within nests and across geographic sites. Considering these observed scale-based patterns, taxonomic bacterial composition may be governed by unique environmental filters and dispersal limitations relative to microbial functional attributes within the alligator nesting environment. These results advance pattern-process dynamics within the field of microbial community ecology and describe processes influencing the American alligator nest microbiome.
... It is a federally threatened species that may be affected by ecosystem restoration projects, particularly those related to the greater Everglades and Florida Bay (Mazzotti et al., 2007a;Mazzotti et al., 2009). As documented across other crocodylian species (Thorbjarnarson, 1996;Cañas & Anderson, 2002;Piña, Merchant & Verdade, 2015), environmental changes within American crocodile nests can significantly affect the health and survival of the developing young (Lutz & Dunbar-Cooper, 1984;Mazzotti et al., 1986;Mazzotti, Kushlan & Dunbar-Cooper, 1988;Mazzotti, 1989;Charruau, 2012;Charruau, Hénaut & Álvarez Legorreta, 2013;Murray et al., 2016). Crocodylus acutus exhibits temperature-dependent sex determination (Murray et al., 2016;Charruau, Cantón & De la Cruz, 2017), and developing embryos are vulnerable to both flooding and desiccation (Mazzotti, Kushlan & Dunbar-Cooper, 1988;Kushlan & Mazzotti, 1989;Charruau, Thorbjarnarson & Hénaut, 2010). ...
... As documented across other crocodylian species (Thorbjarnarson, 1996;Cañas & Anderson, 2002;Piña, Merchant & Verdade, 2015), environmental changes within American crocodile nests can significantly affect the health and survival of the developing young (Lutz & Dunbar-Cooper, 1984;Mazzotti et al., 1986;Mazzotti, Kushlan & Dunbar-Cooper, 1988;Mazzotti, 1989;Charruau, 2012;Charruau, Hénaut & Álvarez Legorreta, 2013;Murray et al., 2016). Crocodylus acutus exhibits temperature-dependent sex determination (Murray et al., 2016;Charruau, Cantón & De la Cruz, 2017), and developing embryos are vulnerable to both flooding and desiccation (Mazzotti, Kushlan & Dunbar-Cooper, 1988;Kushlan & Mazzotti, 1989;Charruau, Thorbjarnarson & Hénaut, 2010). Therefore, monitoring microenvironmental conditions in the nest, especially temperature and moisture, is a critical component of conservation efforts focused on this species. ...
... Previous studies have successfully deployed similar data loggers with built in sensors and data storage (López-Luna et al., 2015;González-Desales et al., 2016;Murray et al., 2016). However, these projects did not experience the same apparent level of instrument loss (Charruau, 2012). ...
Article
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Several data loggers deployed to monitor temperature and humidity of Crocodylus acutus (American crocodile) nests in South Florida could not be located after hatching. One badly damaged data logger was retrieved, providing insight into the possible fate of the others. Using a taphonomic approach, we identified numerous indentations, consistent with crocodylian bite marks, and inconsistent with potential mammalian or squamate bites. It seems most likely that the data logger was damaged by the nesting C. acutus rather than during attempted nest predation. Estimated bite forces for reproductive age, female C. acutus exceed the predicted material properties of the data logger’s housing, suggesting that the bites were exploratory in nature. We suggest that data loggers be removed prior to hatching or permit remote data storage.
... There is a significant correlation of ambient air temperature with the timing of nesting (Joanen and McNease, 1989), importance of warmer water temperatures in triggering of spermatogenesis (Murphy, 1980) and during the incubation period, nest temperature plays a critical role in the rate of embryonic development, viability, body size and weight at hatching, abnormalities, and fitness and growth rates after hatching (Lance, 1987;Thorbjarnarson, 1989;Webb and Cooper-Preston, 1989;Janzen, 1994;Booth, 2006;Cadby et al., 2010;Parachu Marco et al., 2010). Further, nest temperature can be influenced by canopy cover, solar radiation, nest material, rainfall, nest depth and egg number and size (Charruau, 2012;Murray et al., 2016). However to date, studies on the effects of climate change on crocodilian biology have largely focused on the effect of temperature on sex determination, thermal regime of nests, duration of incubation period and size at hatching (Pina et al., 2003;Parachu Marco et al., 2010;Charruau, 2012;Elsey and Lang, 2014;Murray et al., 2016), but not on temperature's influence on date of hatching. ...
... Further, nest temperature can be influenced by canopy cover, solar radiation, nest material, rainfall, nest depth and egg number and size (Charruau, 2012;Murray et al., 2016). However to date, studies on the effects of climate change on crocodilian biology have largely focused on the effect of temperature on sex determination, thermal regime of nests, duration of incubation period and size at hatching (Pina et al., 2003;Parachu Marco et al., 2010;Charruau, 2012;Elsey and Lang, 2014;Murray et al., 2016), but not on temperature's influence on date of hatching. ...
... Much of the work on timing of crocodilian nesting has focused on the relationship between precipitation and wetland water levels, to nest flooding and food availability. Work on effects of temperature and nest behavior has focused on how changes in oviposition timing can modify offspring phenotypic characteristics affecting sex (Pina et al., 2003;Parachu Marco et al., 2010;Charruau, 2012;Simoncini et al., 2014;Elsey and Lang, 2014;Murray et al., 2016), post hatching patterns of thermoregulation (Lang, 1987), growth and survivorship (Joanen et al., 1987;Webb and Cooper-Preston, 1989;Pina et al., 2003;Parachu Marco et al., 2010), hatchling size (Lance, 1987;Parachu Marco et al., 2010) and to a lesser extent how temperature affects timing of reproduction. Murphy (1980) noted that adult alligators (Alligator mississippiensis) living in ponds artificially heated by effluent from a nuclear reactor produced sperm two weeks earlier than adults living in adjacent natural ponds and hypothesized this could prevent animals within the cooling pond from mating with animals from outside. ...
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Globally temperature of marine environments is on the rise and temperature plays an important role in the life-history of reptiles. In this study, we examined the relationship between sea surface temperature and average date of hatching for American crocodiles (Crocodylus acutus) over a 37-year period at two nesting sites, Everglades National Park and Florida Power and Light Turkey Point Power Plant site in southern Florida. Our results indicate that hatch dates are shifting 1.5 days earlier every two years and at half that rate for the Turkey Point site, and with every 1 °C degree increase in temperature, hatching occurs about 10 days earlier in the Everglades and 6 days earlier at Turkey Point. Our results on shifting hatch dates for American crocodiles provide further details about the impacts of temperature change on crocodile life history and suggest that increased temperature may affect their phenology.
... 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]. ...
... 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]. These results strongly suggest that the observed natural bias could result from the masculinizing effects of this synthetic androgen [139][140][141]. ...
... 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]. These results strongly suggest that the observed natural bias could result from the masculinizing effects of this synthetic androgen [139][140][141]. ...
... 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]. ...
... 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]. These results strongly suggest that the observed natural bias could result from the masculinizing effects of this synthetic androgen [139][140][141]. ...
... 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]. These results strongly suggest that the observed natural bias could result from the masculinizing effects of this synthetic androgen [139][140][141]. ...
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.
... This is one of multiple reports that describe recent male-biased crocodilian populations throughout Central America (Charruau et al., 2005;Escobedo-Galván, 2008). Specific to the Tempisque drainage, thermal data from nests demonstrate that the male-bias is not a function of temperature effects on hatchling sex determination (Murray et al., 2016b). Additionally, exposure of crocodilian eggs to MT generates male hatchlings when incubated at a temperature that should produce only female offspring (Murray et al., 2016a). ...
... Further, degradation of MT in the environment is rapid (Gupta and Acosta, 2004) potentially lending support for a bio-transporter. Our observation that yolk MT concentrations do not differ between wild eggs and those experimentally dosed with MT (Murray et al., 2016a) suggests that Palo Verde crocodile eggs contain MT at levels known to produce male offspring despite incubation at female-producing temperatures (Murray et al., 2016b). In fact, of 357 eggs monitored at Palo Verde, 225 were estimated to produce females and 132 were estimated to produce males, based on temperature alone (Murray et al., 2016b). ...
... Our observation that yolk MT concentrations do not differ between wild eggs and those experimentally dosed with MT (Murray et al., 2016a) suggests that Palo Verde crocodile eggs contain MT at levels known to produce male offspring despite incubation at female-producing temperatures (Murray et al., 2016b). In fact, of 357 eggs monitored at Palo Verde, 225 were estimated to produce females and 132 were estimated to produce males, based on temperature alone (Murray et al., 2016b). Data collected by Murray et al., 2016a suggests that 60% of the females would convert to males in the presence of MT. ...
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.
... Crocodile nests experience a daily cycle of temperature fluctuations ranging from 1 • C to 5 • C as a consequence of fluctuations in external environmental temperature (Murray et al., 2016). These fluctuations are believed to expose incubating eggs to higher effective pivotal temperature compared to nest's mean incubation temperature. ...
... But each egg experiences a different temperature fluctuation due to its location inside the nest and the depth of nest itself. Eggs in the top layer of the nest usually experience highest fluctuations being in closest proximity to external temperature whereas eggs in lower layer experience low fluctuations (Murray et al., 2016). ...
Article
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1. The gharial (Gavialis gangeticus) is a critically endangered, long-snouted crocodilian, endemic to the Indian sub-continent. Today, the species' distribution and numbers have reduced by more than 95% in all the large rivers where it was formerly abundant. Living upstream in a reservoir dammed in 1976, the Katerniaghat gharial population has continued to nest along the Girwa River, subject to seasonal flooding in recent decades. In 2010, a natural flood upstream in Nepal resulted in a permanent reduction in the mainstream river flow. As a consequence of reduced flow, the formerly open sand banks and mid-river islands have converted gradually to riverbanks with woody vegetation. Coincident with the increased vegetation growth, gharial nesting sites and nest numbers declined by more than 40% by 2018. 2. In an attempt to reverse the observed decline in nesting, we intervened with vegetation removal (VR) in 2019 and sand addition (SA) in 2020, to augment available nesting opportunities at previous and potential nesting locations. 3. The number of nests increased with SA (n = 36 in 2020) but decreased with VR (n = 19 in 2019), relative to the prior year without intervention (n = 25 in 2018). Furthermore, hatching success increased significantly to 93% with SA, compared to 63% in VR. Creating an artificial sand bank required approximately one-third work hours and cost much less than removing vegetation. Substrate temperatures in and around nests approximated the viable incubation range (29-33.5 • C) when vegetation is absent, but were lower in sites covered with woody vegetation and/or dense, high grass. 4. Our study indicates that gharial will respond favourably to newly created sand banks that provide open, sandy riverside nesting areas, in contrast to cut-over sites with dense vegetation removed. 5. Finally, we note that this strategy of augmenting nesting sites is only an interim attempt to solve the 'nesting site' dilemma for the river-adapted gharial. Landscape-level solutions related to resumption of seasonal flooding, and particularly natural flow regimes that are dynamic, rather than steady, will likely be needed to avoid local extirpation of gharial in river‐reservoir habitats.
... The nearby Tempisque Basin harbors a rapidly expanding population of American crocodiles (Crocodylus acutus) that exhibits a male-biased sex ratio (Bolaños-Montero, 2012; Murray et al., 2015). Hatchling sex ratios from this population do not match the ratios predicted by clutch thermal regimes and this sex ratio bias differs among clutches, with some clutches being male-biased and others not (Murray et al., 2016). Here, we test the potential for MT to produce male crocodilian embryos at female-producing temperatures and histologically analyze organizational effects of urogenital development from MT exposure during the experimental assay. ...
... Crews (1996), in a review of TSD mechanisms, notes the production of male-biased clutches in turtles as a result of exogenous application of the non-aromatizable dihydrotestosterone. The male-biased sex ratio documented in the Tempisque Basin, Costa Rica appears unrelated to nest thermal regimes (Murray et al., 2016). However, MT utilized by local tilapia farms is capable of acting as a potent androgen yielding male-biased sex ratios at hatching. ...
Article
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Effects of xenobiotics can be organizational, permanently affecting anatomy during embryonic development, and/or activational, influencing transitory actions during adulthood. The organizational influence of endocrine-disrupting contaminants (EDC's) produces a wide variety of reproductive abnormalities among vertebrates that exhibit temperature-dependent sex determination (TSD). Typically, such influences result in subsequent activational malfunction, some of which are beneficial in aquaculture. For example, 17-αmethyltestosterone (MT), a synthetic androgen, is utilized in tilapia farming to bias sex ratio towards males because they are more profitable. A heavily male-biased hatchling sex ratio is reported from a crocodile population near one such tilapia operation in Guanacaste, Costa Rica. In this study we test the effects of MT on sexual differentiation in American alligators, which we used as a surrogate for all crocodilians. Experimentally, alligators were exposed to MT in ovo at standard ecotoxicological concentrations. Sexual differentiation was determined by examination of primary and secondary sex organs post hatching. We find that MT is capable of producing male embryos at temperatures known to produce females and demonstrate a dose-dependent gradient of masculinization. Embryonic exposure to MT results in hermaphroditic primary sex organs, delayed renal development and masculinization of the clitero-penis (CTP).
... Crocodiles have some plasticity in terms of where they deposit their nests with respect to distance from water, depth of the clutch, and whether the nest is in sun or shade (Platt and Thorbjarnarson, 2000;Charruau, 2012;Balaguera-Reina et al., 2015). However, this behavioral plasticity may not be enough to mitigate increases in temperature brought about by climate change (Murray et al., 2016). The only study done on nest temperatures in Florida was performed on sand beach nests and marl creek nests in northeastern Florida Bay by Lutz and Dunbar-Cooper (1984). ...
Article
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Nesting ecology of American crocodiles (Crocodylus acutus) in Florida has been both positively and negatively influenced by anthropogenic and natural factors since the species was placed on the federally endangered species list in 1975. This includes a shift in nesting sites and an expansion of nesting to anthropogenic habitat. Using a 50-year record of monitoring data (1970-2020), we assessed factors influencing nesting ecology (number of nests, nest morphology, success rate, and habitat use) from a total of 3,013 nests recorded across South Florida. We detected a change in nesting success rate, increasing from 61% in the 1970's to near 90% since 2010. Our hot spot analysis illustrates that nesting sites in northeastern Florida Bay and Flamingo/Cape Sable (Everglades National Park) were important for American crocodiles. Anthropogenic habitats, such as canals provided vital habitat nesting in areas such as Flamingo/Cape Sable (Everglades National Park), Turkey Point Power Plant, and Crocodile Lake National Wildlife Refuge for the current Florida population. Environmental parameters suspected to affect nesting success have shown an increasing trend over the past 50 years and minimum temperature and rainfall, during the summer season, are correlated with increased nesting success and temporal variation across South Florida. The adaptive capacity that American crocodiles exhibited in Florida gave the species advantages to face changes in climate and landscape over the last 50 years, however, it does not imply that the adaptive capacity of the species to face these changes (evolutionary potential) cannot reach a limit if changes continue. Here, we document C. acutus nesting ecology population responses to ecosystem restoration efforts in Florida; and further demonstrate the value of protecting and restoring habitat to support recovery of listed species.
... Dinets (2013) Wet season hatching (yes, no) Magnusson and Campos (2010) Incubation duration (short, medium, long, extralong) Thorbjarnarson (1996) (2012) Hatching stimulus (signal calling, vibration) Garrick and Lang (1977) Nesting season (wet, dry) Murray et al. (2016) Clutch frequency (1, 2) Murray et al. (2016) Clutch size (small, medium, large) Thorbjarnarson (1996) Clutch mass (small, medium, large) Thorbjarnarson (1996) Mating vocals (none, roar, bellow, buzz, moan) ...
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Crocodilians comprise an ancient and successful lineage of archosaurs that repeatedly raises questions on how they survived a mass extinction and remained relatively unchanged for ~100 million years. Was their success due to the change‐resistant retention of a specific set of traits over time (phylogenetic conservatism) or due to flexible, generalist capabilities (e.g., catholic diets, phenotypic plasticity in behavior), or some combination of these? We examined the evolution of reproductive ecology and behavior of crocodilians within a phylogenetic perspective, using 14 traits for all 24 species to determine whether these traits were phylogenetically constrained versus (ecologically) convergent. Our analysis revealed that the ancestral crocodilian was a mound nester that exhibited both nest attendance and defense. Nesting mode exhibited 4–5 transformations from mound to hole nesting, a convergence of which habitat may have been a driving factor. Hole nesters were more likely to nest communally, but this association may be biased by scale. Although there were exceptions, mound nesters typically nested during the wet season and hole nesters during the dry season; this trait was relatively conserved, however. About two‐thirds of species timed their nesting with the wet season, while the other third timed their hatching with the onset of the wet season. Nest attendance and defense were nearly ubiquitous and thus exhibited phylogenetic conservatism, but attendance lodging was diverse among species, showing multiple reversals between water and burrows. Collectively, our analysis reveals that reproductive trait evolution in crocodilians reflects phylogenetic constraint (nest attendance, nest defense), ecological convergence (seasonal timing of nesting, nest attendance lodging), or both (mode of nesting). Some traits (e.g., communal nesting and mode of nesting) were autocorrelated. Our analysis provides a framework for addressing hypotheses raised for why there has been trait convergence in reproductive ecology and behavior in crocodilians and why some traits remained phylogenetically conserved. Our analysis reveals that reproductive trait evolution in crocodilians reflects phylogenetic constraint (nest attendance, nest defense), ecological convergence (seasonal timing of nesting, nest attendance lodging), or both (mode of nesting). Our analysis provides a framework for addressing hypotheses raised for why there has been trait convergence in reproductive ecology and behavior in crocodilians and why some traits remained phylogenetically conserved.
... For example, diel variation in temperature predictably decreases with depth below the sun-heated ground surface, such that eggs laid deeper in a nest will develop at less variable temperatures than do shallower eggs in some turtles [11,12]. Mean incubation temperatures also may shift; for example eggs at upper and central locations of the nest were consistently warmer than were the base and side of the nest in sea turtles [13][14][15], as well as in freshwater turtles [11,12] (electronic supplementary material, figure S1a). Temperature clines within a nest depend upon a range of attributes both of the substrate and the nest cavity; for example, as a consequence of thermal variation at various depths beneath the soil surface [16]. ...
Article
Natural nests of egg-laying birds and reptiles exhibit substantial thermal variation, at a range of spatial and temporal scales. Rates and trajectories of embryonic development are highly sensitive to temperature, favouring an ability of embryos to respond adaptively (i.e. match their developmental biology to local thermal regimes). Spatially, thermal variation can be significant within a single nest (top to bottom), among adjacent nests (as a function of shading, nest depth etc.), across populations that inhabit areas with different weather conditions, and across species that differ in climates occupied and/or nest characteristics. Thermal regimes also vary temporally, in ways that generate differences among nests within a single population (e.g. due to seasonal timing of laying), among populations and across species. Anthropogenic activities (e.g. habitat clearing, climate change) add to this spatial and temporal diversity in thermal regimes. We review published literature on embryonic adaptations to spatio-temporal heterogeneity in nest temperatures. Although relatively few taxa have been studied in detail, and proximate mechanisms remain unclear, our review identifies many cases in which natural selection appears to have fine-tuned embryogenesis to match local thermal regimes. Developmental rates have been reported to differ between uppermost versus lower eggs within a single nest, between eggs laid early versus late in the season, and between populations from cooler versus warmer climates. We identify gaps in our understanding of thermal adaptations of early (embryonic) phases of the life history, and suggest fruitful opportunities for future research.
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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.
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Morelet’s crocodile (Crocodylus moreletii) and hybrid crocodiles (C. moreletii × acutus) are mound-nesting crocodilians found in the lowlands of northern and southern Belize, respectively. Nests of both crocodilians consist of large mounds of soil, vegetation, leaf litter, and in some cases sand. We here report on the fauna associated with nest mounds of C. moreletii and C. moreletii × acutus, and describe the associations between crocodiles and commensal fauna. Our data were collected during various ecological studies conducted from 1992 through 2000, and we examined 138 active (containing eggs) nests of C. moreletii and 11 active nests of C. moreletii × acutus. We noted the occurrence of at least 14 species of fauna associated with 45 (32.6%) C. moreletii and three (27.2%) C. moreletii × acutus nests. Nest-associated fauna included ants, bees, termites, turtles, squamates, birds, and mammals. Associations included five species dwelling within crocodile nest mounds, four species that deposited eggs in crocodile nest mounds, and five species nesting in close proximity to crocodile nests. Nest-associated fauna presumably benefit from the protection afforded by nest attendance and aggressive defence behaviour of female crocodiles, although these benefits have yet to be empirically established.
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Understanding the combined effects of anthropogenic impacts such as climate change and pollution on aquatic ecosystems is critical. However, little is known about how predicted temperature increases may affect the activity of endocrine disrupting compounds (EDCs), particularly in species with plasticity in sex determination. We investigated the effects of a concomitant increase in temperature and exposure to estrogenic EDCs on reproduction and development in an estuarine model organism (Menidia beryllina) across multiple generations. Parents (P) were exposed to environmental levels of the estrogenic insecticide bifenthrin or ethinylestradiol (EE2) at 22 °C and 28 °C for 14 days prior to the initiation of spawning trials. Embryos in the F1 generation were exposed to EDCs until 21 days post hatch (dph), reared to adulthood in clean water at elevated temperatures, and spawned. F1 sex ratios were significantly influenced by elevated temperature and EDCs, potentially altering adaptive development. We also observed fewer viable offspring and increased developmental deformities in the F1 and F2 generations, with a greater impact on F2 juveniles. These findings enhance our understanding of responses to EDCs in the context of climate change and may demonstrate heritable effects. Our study represents the first multigenerational assessment of elevated temperatures in combination with environmentally relevant concentrations of commonly detected endocrine disruptors in a model vertebrate species.
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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.
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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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Sex determination in animals is amazingly plastic. Vertebrates display contrasting strategies ranging from complete genetic control of sex (genotypic sex determination) to environmentally determined sex (for example, temperature-dependent sex determination). Phylogenetic analyses suggest frequent evolutionary transitions between genotypic and temperature-dependent sex determination in environmentally sensitive lineages, including reptiles. These transitions are thought to involve a genotypic system becoming sensitive to temperature, with sex determined by gene-environment interactions. Most mechanistic models of transitions invoke a role for sex reversal. Sex reversal has not yet been demonstrated in nature for any amniote, although it occurs in fish and rarely in amphibians. Here we make the first report of reptile sex reversal in the wild, in the Australian bearded dragon (Pogona vitticeps), and use sex-reversed animals to experimentally induce a rapid transition from genotypic to temperature-dependent sex determination. Controlled mating of normal males to sex-reversed females produces viable and fertile offspring whose phenotypic sex is determined solely by temperature (temperature-dependent sex determination). The W sex chromosome is eliminated from this lineage in the first generation. The instantaneous creation of a lineage of ZZ temperature-sensitive animals reveals a novel, climate-induced pathway for the rapid transition between genetic and temperature-dependent sex determination, and adds to concern about adaptation to rapid global climate change.
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Crocodilians normally incubate at temperatures >27oC. Stable temperatures >27oC are not naturally available in the tropical-rainforest habitat of Paleosuchus trigonatus. Most nests are placed at the side of, or on top of, termite mounds. Heat from the termite mound insulation by the nest material maintain the eggs at c 30oC (28.4-32.1oC). -from Authors
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Read the Feature Paper: Nest depth may not compensate for sex ratio skews caused by climate change in turtlesOther Commentaries on this paper: Chelonians in a changing climate: can nest site selection prevent sex ratio skews?; Revealing the links between climate and demography for reptiles with environmental sex determinationResponse from the authors: Experimental field studies of species' responses to climate change: challenges and future directions
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Mean daily temperature in natural nests of freshwater turtles with temperature dependent sex determination is a poor predictor of hatchling sex ratios when nest temperatures fluctuate. To account for this, a mathematical model has been developed on the assumption that hatchling sex depends on the daily proportion of embryonic development that occurs above the threshold temperature for sex determination rather than the proportion of time spent above the threshold. The model predictions are borne out by experiments using the marine turtle Caretta caretta. Average developmental rates, both overall and during the period that sexual differentiation is sensitive to temperature, are unaffected by diel fluctuations about the mean incubation temperature. Sex ratios, on the other hand, were affected by diel fluctuations and ranged from ca. 100% males under regimes 26 ± 0°C and 26 ± 3°C to 100% females for regimes 26 ± 7°C and 26 ± 8°C. These and intermediate sex ratios were in close agreement with model predictions. Demonstration of an impact of temperature on sex, while holding overall developmental rate constant, gives support to hypotheses invoking a direct role for temperature rather than alternative hypotheses invoking overall developmental rate as a more proximal influence on sex. The model explains why mean temperature is a poor predictor of hatchling sex ratios. It urges caution in using “hours above the threshold” for predicting sex ratios, because 1 hr at 1°C above the threshold will not be equivalent to 1 hr at 4°C above the threshold. It provides a general framework for integrating experiments at constant temperatures with those in the field or laboratory using fluctuating regimes. It provides greater scope for exploring how reptiles with temperature dependent sex determination might respond to climatic change or other disturbances to the incubation environment. And it provides an explanation of why secondary factors such a hydric conditions and oxygen potentials might influence hatchling sex, even if temperature acts directly to influence sex ratios rather than through its influence on overall developmental rate. © Wiley-Liss, Inc.
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In November 2004, a regional climate change workshop was held in Guatemala with the goal of analyzing how climate extremes had changed in the region. Scientists from Central America and northern South America brought long-term daily temperature and precipitation time series from meteorological stations in their countries to the workshop. After undergoing careful quality control procedures and a homogeneity assessment, the data were used to calculate a suite of climate change indices over the 1961-2003 period. Analysis of these indices reveals a general warming trend in the region. The occurrence of extreme warm maximum and minimum temperatures has increased while extremely cold temperature events have decreased. Precipitation indices, despite the large and expected spatial variability, indicate that although no significant increases in the total amount are found, rainfall events are intensifying and the contribution of wet and very wet days are enlarging. Temperature and precipitation indices were correlated with northern and equatorial Atlantic and Pacific Ocean sea surface temperatures. However, those indices having the largest significant trends (percentage of warm days, precipitation intensity, and contribution from very wet days) have low correlations to El Niño-Southern Oscillation. Additionally, precipitation indices show a higher correlation with tropical Atlantic sea surface temperatures.
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This study uses the American Alligator (Alligator mississippiensis) to assess the use of reproductive allometry as a tool to infer crocodilian population marginality based on conformation to advantageous life-history strategies. It is hypothesized that reproductive allometry, a morphometric relationship between mother's size and her reproductive output, varies intraspecifically between populations and that this variation reflects population marginality based on size, stress, temporal exploitation, habitat fragmentation, and/or the presence of social hierarchy. This hypothesis is tested using relative comparisons of allometric correlation between a marginal population inundated with saline storm surge from Hurricane Ike in southeastern Texas and a hypothesized unstressed core population in southeastern Louisiana. Heterophil to lymphocyte ratios fail to falsify the hypothesis of a saline stressor. The number of significant morphometric correlations between various parameters, degree of correlation (RI, and slope of correlation between mother and her respective nest and clutch varied greatly between study sites. Reproductive allometry, as a measure of relative population marginality, may provide a cost effective way to prioritize management with local support for crocodilian taxa.
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Half of the 22 extant crocodilians show evidence of temperature-dependent sex determination (TSD). We examine evidence for TSD in 11 species by reviewing reports on five and presenting new data for six. The female-male pattern (FM; females at low temperature, males at high temperature) attributed to Alligator mississippiensis and Caiman crocodilus are here revised to be female-male-female (FMF; males at intermediate temperature, females at low and high temperatures). A similar pattern characterizes Crocodylus palustris, C. moreletii, C. siamensis, and Gavialis gangeticus based on new data; published accounts establish a FMF pattern in Crocodylus porosus, C. johnstoni, and C. niloticus. TSD apparently occurs in Paleosuchus trigonatus and Alligator sinensis, but patterns are not yet documented. In the well-studied species, the incubation temperatures for FM transitions are congruent, but MF transition temperatures differ among species. In A. mississippiensis, 100% males are produced over a range of constant incubation temperatures, whereas in C. johnstoni, only low proportions of males are produced at any constant temperature.
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Theoretical models suggest that in changing environments natural selection on two traits, maternal nesting behaviour and pivotal temperatures (those that divide the sexes) is important for maintaining viable offspring sex ratios in species with environmental sex determination (ESD). Empirical evidence, however, is lacking. In this paper, we provide such evidence from a study of clinal variation in four sex-determining traits (maternal nesting behaviour, pivotal temperatures, nesting phenology, and nest depth) in Physignathus lesueurii, a wide-ranging ESD lizard inhabiting eastern Australia. Despite marked differences in air and soil temperatures across our five study sites spanning 19° latitude and 1200m in elevation, nest temperatures did not differ significantly among sites. Lizards compensated for climatic differences chiefly by selecting more open nest sites with higher incident radiation at cooler sites. Clinal variation in the onset of nesting also compensated for climatic differences, but to a lesser extent. There was no evidence of compensation through pivotal temperatures or nest depth. More broadly, our results extend to the egg stage the life history prediction that behaviour is the chief compensatory mechanism for climatic differences experienced by species spanning environmental extremes. Furthermore, our study was unique in revealing that nest site choice influenced mainly the daily range in nest temperatures, rather than mean temperatures, in a shallow-nesting reptile. Finally, indirect evidence suggests that the cue used by nesting lizards was radiation or temperature (through basking or assessing substrate temperatures), not visual detection of canopy openness. We conclude that maternal nesting behaviour and nesting phenology are traits subject to sex ratio selection in P. lesueurii, and thus, must be considered among the repertoire of ESD species for responding to climate change.
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Climate change is expected to disrupt biological systems. Particularly susceptible are species with temperature-dependent sex determination (TSD), as in many reptiles. While the potentially devastating effect of rising mean temperatures on sex ratios in TSD species is appreciated, the consequences of increased thermal variance predicted to accompany climate change remain obscure. Surprisingly, no study has tested if the effect of thermal variance around high-temperatures (which are particularly relevant given climate change predictions) has the same or opposite effects as around lower temperatures. Here we show that sex ratios of the painted turtle (Chrysemys picta) were reversed as fluctuations increased around low and high unisexual mean-temperatures. Unexpectedly, the developmental and sexual responses around female-producing temperatures were decoupled in a more complex manner than around male-producing values. Our novel observations are not fully explained by existing ecological models of development and sex determination, and provide strong evidence that thermal fluctuations are critical for shaping the biological outcomes of climate change.
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In many animals, temperatures experienced by developing embryos determine offspring sex (e.g. temperature-dependent sex determination, TSD), but most studies focus strictly on the effects of mean temperature, with little emphasis on the importance of thermal fluctuations. In the jacky dragon (Amphibolurus muricatus), an Australian lizard with TSD, data from nests in the field demonstrate that offspring sex ratios are predictable from thermal fluctuations but not from mean nest temperatures. To clarify this paradox, we incubated eggs in a factorial experiment with two levels of mean temperature and three levels of diel fluctuation. We show that offspring sex is determined by an interaction between these critical thermal parameters. Intriguingly, because these two thermal descriptors shift in opposing directions throughout the incubation season, this interactive effect inhibits seasonal shifts in sex ratio. Hence, our results suggest that TSD can yield offspring sex ratios that resemble those produced under genotypic sex-determining systems. These findings raise important considerations for understanding the diversity of TSD reaction norms, for designing experiments that evaluate the evolutionary significance of TSD, and for predicting sex ratios under past and future climate change scenarios.
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SYNOPSIS. A study of common snapping turtles conducted from 1975 through 1992 in southeastern Michigan provided sufficient demographic data to examine how life history characteristics may constrain population responses of long-lived organisms. Females reached sexual maturity between 11 and 16 years of age. Minimum reproductive frequency was less than annual (0.85), and nest survivorship over 17 years ranged from 0 to 64% and averaged 23%. Survivorship of yearlings had to be estimated since hatchlings can pass through the mesh on traps. Actual survivorship of juveniles was over 0.65 by age 2 and averaged 0.77 between the ages of 2 and 12 years. Annual survivorship of adult females ranged from 0.88 to 0.97. A life table for the population resulted in a cohort generation time of 25 years. Population stability was most sensitive to changes in adult or juvenile survival, and less sensitive to changes in age at sexual maturity, nest survival or fecundity. An increase in annual mortality of 0.1 on adults over 15 years of age with no density-dependent compensation would halve the number of adults in less than 20 years. The results from the present study indicate that life history traits of long-lived organisms consist of co-evolved traits that severely constrain the ability of populations to respond to chronic disturbances. Successful management and conservation programs for long-lived organisms will be those that recognize that protection of all life stages is necessary. Without protection of adults and older juveniles, programs that protect nests and headstart hatchlings have a low probability of success. Carefully managed sport harvests of turtles or other long-lived organisms may be sustainable; however, commercial harvests will certainly cause substantial population declines
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SYNOPSIS. Egg size and nest site selection are two potential effects that can have a persistent influence on the phenotype of offspring. In this paper, I develop the maternal condition-dependent choice hypothesis for the maintenance of environmental sex determination. The hypothesis stipulates three conditions: 1) there must be variation in the maternal effect, 2) the variation in the maternal effect must influence fitness of the offspring differently between the sexes, and 3) female reproductive behavior is determined by her condition or how her condition will influence her offspring's fitness. Females with the ability to recognize environments that have a higher probability of producing the sex that would benefit the most from maternal condition will have an advantage. Using egg size as a maternal effect, I test this hypothesis in the diamondback terrapin, an emydid turtle with temperature-dependent sex determination. Terrapins have large variation in egg size among clutches and little variation within clutches. Egg mass is the primary determinant of hatchling mass and can result in as much as a three year difference in reaching minimum size of first reproduction in females, but may not affect age or size of first reproduction in males. Finally, terrapins select open nesting sites with warmer incubation conditions and place larger eggs there. Females place smaller eggs in cooler sites. Terrapin reproduction is consistent with the prediction of the maternal condition-dependent nest site choice hypothesis. The model and supporting data demonstrate how maternal effects can be an important factor to consider in studies of environmental sex determination.
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Many studies suggest that global warming is driving species ranges poleward and toward higher elevations at temperate latitudes, but evidence for range shifts is scarce for the tropics, where the shallow latitudinal temperature gradient makes upslope shifts more likely than poleward shifts. Based on new data for plants and insects on an elevational transect in Costa Rica, we assess the potential for lowland biotic attrition, range-shift gaps, and mountaintop extinctions under projected warming. We conclude that tropical lowland biotas may face a level of net lowland biotic attrition without parallel at higher latitudes (where range shifts may be compensated for by species from lower latitudes) and that a high proportion of tropical species soon faces gaps between current and projected elevational ranges.
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Under temperature-dependent sex determination (TSD), temperatures experienced by embryos during development determine the sex of the offspring. Consequently, populations of organisms with TSD have the potential to be strongly impacted by climatic warming that could bias offspring sex ratio, a fundamental demographic parameter involved in population dynamics. Moreover, many taxa with TSD are imperiled, so research on this phenomenon, particularly long-term field study, has assumed great urgency. Recently, turtles with TSD have joined the diverse list of taxa that have demonstrated population-level changes in breeding phenology in response to recent climate change. This raises the possibility that any adverse impacts of climate change on populations may be alleviated by individual plasticity in nesting phenology. Here, we examine data from a long-term study on a population of painted turtles (Chrysemys picta) to determine whether changes in phenology are due to individual plasticity and whether individual plasticity in the timing of nesting has the capacity to offset the sex ratio effects of a rise in climatic temperature. We find that individual females show plasticity in the date of first nesting each year, and that this plasticity depends on the climate from the previous winter. First nesting date is not repeatable within individuals, suggesting that it would not respond to selection. Sex ratios of hatchlings within a nest declined nonsignificantly over the nesting season. However, small increases in summer temperature had a much stronger effect on nest sex ratios than did laying nests earlier in the season. For this and other reasons, it seems unlikely that individual plasticity in the timing of nesting will offset the effects of climate change on sex ratios in this population, and we hypothesize that this conclusion applies to other populations with TSD.
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In gonochoristic vertebrates, sex determination mechanisms can be classified as genotypic (GSD) or temperature-dependent (TSD). Some cases of TSD in fish have been questioned, but the prevalent view is that TSD is very common in this group of animals, with three different response patterns to temperature. We analyzed field and laboratory data for the 59 fish species where TSD has been explicitly or implicitly claimed so far. For each species, we compiled data on the presence or absence of sex chromosomes and determined if the sex ratio response was obtained within temperatures that the species experiences in the wild. If so, we studied whether this response was statistically significant. We found evidence that many cases of observed sex ratio shifts in response to temperature reveal thermal alterations of an otherwise predominately GSD mechanism rather than the presence of TSD. We also show that in those fish species that actually have TSD, sex ratio response to increasing temperatures invariably results in highly male-biased sex ratios, and that even small changes of just 1-2 degrees C can significantly alter the sex ratio from 1:1 (males:females) up to 3:1 in both freshwater and marine species. We demonstrate that TSD in fish is far less widespread than currently believed, suggesting that TSD is clearly the exception in fish sex determination. Further, species with TSD exhibit only one general sex ratio response pattern to temperature. However, the viability of some fish populations with TSD can be compromised through alterations in their sex ratios as a response to temperature fluctuations of the magnitude predicted by climate change.
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Some biologists embrace the classical view that changes in behavior inevitably initiate or drive evolutionary changes in other traits, yet others note that behavior sometimes inhibits evolutionary changes. Here we develop a null model that quantifies the impact of regulatory behaviors (specifically, thermoregulatory behaviors) on body temperature and on performance of ectotherms. We apply the model to data on a lizard (Anolis cristatellus) and show that thermoregulatory behaviors likely inhibit selection for evolutionary shifts in thermal physiology with altitude. Because behavioral adjustments are commonly used by ectotherms to regulate physiological performance, regulatory behaviors should generally constrain rather than drive evolution, a phenomenon we call the "Bogert effect." We briefly review a few other examples that contradict the classical view of behavior as the inevitable driving force in evolution. Overall, our analysis and brief review challenge the classical view that behavior is invariably the driving force in evolution, and instead our work supports the alternative view that behavior has diverse--and sometimes conflicting--effects on the directions and rates at which other traits evolve.
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Amphibians stand at the forefront of a global biodiversity crisis. More than one-third of amphibian species are globally threatened, and over 120 species have likely suffered global extinction since 1980. Most alarmingly, many rapid declines and extinctions are occurring in pristine sites lacking obvious adverse effects of human activities. The causes of these “enigmatic” declines remain highly contested. Still, lack of long-term data on amphibian populations severely limits our understanding of the distribution of amphibian declines, and therefore the ultimate causes of these declines. Here, we identify a systematic community-wide decline in populations of terrestrial amphibians at La Selva Biological Station, a protected old-growth lowland rainforest in lower Central America. We use data collected over 35 years to show that population density of all species of terrestrial amphibians has declined by ≈75% since 1970, and we show identical trends for all species of common reptiles. The trends we identify are neither consistent with recent emergence of chytridiomycosis nor the climate-linked epidemic hypothesis, two leading putative causes of enigmatic amphibian declines. Instead, our data suggest that declines are due to climate-driven reductions in the quantity of standing leaf litter, a critical microhabitat for amphibians and reptiles in this assemblage. Our results raise further concerns about the global persistence of amphibian populations by identifying widespread declines in species and habitats that are not currently recognized as susceptible to such risks. • conservation • long-term studies • tropical wet forest
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How will climate change affect species' reproduction and subsequent survival? In many egg-laying reptiles, the sex of offspring is determined by the temperature experienced during a critical period of embryonic development (temperature-dependent sex determination, TSD). Increasing air temperatures are likely to skew offspring sex ratios in the absence of evolutionary or plastic adaptation, hence we urgently require means for predicting the future distributions of species with TSD. Here we develop a mechanistic model that demonstrates how climate, soil and topography interact with physiology and nesting behaviour to determine sex ratios of tuatara, cold-climate reptiles from New Zealand with an unusual developmental biology. Under extreme regional climate change, all-male clutches would hatch at 100% of current nest sites of the rarest species, Sphenodon guntheri, by the mid-2080s. We show that tuatara could behaviourally compensate for the male-biasing effects of warmer air temperatures by nesting later in the season or selecting shaded nest sites. Later nesting is, however, an unlikely response to global warming, as many oviparous species are nesting earlier as the climate warms. Our approach allows the assessment of the thermal suitability of current reserves and future translocation sites for tuatara, and can be readily modified to predict climatic impacts on any species with TSD.
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All species of crocodilian that have been studied normally incubate their eggs at temperatures above 27°C. Stable temperatures above 27°C are not naturally available in the tropical-rainforest habitat of Paleosuchus trigonatus, and our investigations indicate that its nests are not warmed by the processes that have been suggested for nests of other species: insolation, rotting vegetation, and metabolic heat of embryos. Most nests of P. trigonatus are placed at the side of, or on top of, termite mounds. Heat from the termite mound and insulation by the nest material maintain the eggs at about 30°C (28.4-32.1°C).
Article
Maternal ability to match nest characteristics with environmental conditions can influence offspring survival and quality, and may provide a mechanism by which animals can keep pace with climate change. In species with temperature-dependent sex determination that construct subterranean nests, the depth of the nest may affect incubation temperatures, and thus offspring sex ratio. Maternal adjustment of nest depth may be a mechanism by which climate change-induced sex ratio skews could be prevented in globally imperiled taxa such as turtles. We experimentally manipulated nest depth within a biologically relevant range in nests of the model turtle species Chrysemys picta. We then quantified the effects of nest depth on incubation regime, offspring sex ratio and offspring performance. We found no effect of nest depth on six parameters of incubation regime, nor on resultant offspring survival, size or sex ratio. However, deeper nests produced hatchlings that weighed less, and were faster at righting themselves and swimming, than hatchlings from shallower nests. We suggest that cues used by females in adjusting nest depth are unreliable as predictors of future incubation conditions, and the adjustment in nest depth required to affect sex ratio in this species may be too great to keep pace with climate change. Therefore, maternal adjustment of nest depth seems unlikely to compensate for climate change-induced sex ratio skews in small-bodied, freshwater turtles.
Article
How are organisms responding to climate change? The rapidity with which climate is changing suggests that, in species with long generation times, adaptive evolution may be too slow to keep pace with climate change, and that alternative mechanisms, such as behavioural plasticity, may be necessary for population persistence. Species with temperature-dependent sex determination may be particularly threatened by climate change, because altered temperatures could skew sex ratios. We experimentally tested nest-site choice in the long-lived turtle Chrysemys picta to determine whether nesting behaviour can compensate for potential skews in sex ratios caused by rapid climate change. We collected females from five populations across the species′ range and housed them in a semi-natural common garden. Under these identical conditions, populations differed in nesting phenology (likely due to nesting frequency), and in nest depth (possibly due to a latitudinal cline in female body size), but did not differ in choice of shade cover over the nest, nest incubation regime, or in resultant nest sex ratios. These results suggest that choice of nest sites with particular shade cover may be a behaviourally plastic mechanism by which turtles can compensate for change in climatic temperatures during embryonic development, provided that sufficient environmental variation in potential nest microhabitat is available.
Article
We conducted a study of American Crocodile nesting ecology in coastal Belize from June 1996 to July 1997. Most nesting areas were found on elevated beach ridges composed of coarse sand. Shallow, brackish lagoons adjacent to nesting areas provide critical nursery habitat for hatchlings. The most significant nesting areas were found in the Turneffe Atoll. American crocodiles construct both hole and mound nests in Belize. Clutches are deposited during the last half of the dry season, from late March to early May. Mean clutch size is 22.3 ± 6.0 eggs. Hatching occurred from late June to mid-July, a period coinciding with the beginning of the wet season. Nesting success was high, and losses to predation and flooding were negligible. Females may defend nests from predators and excavate neonates at hatching, but otherwise parental care appears minimal. The protection of suitable nesting and nursery habitat is essential for the continued survival of the American crocodile in Belize.
Article
1.The potential for metabolic heating by embryonic reptiles to influence temperature-dependent sex determination (TSD) has not been examined in a controlled environment.2.In a laboratory experiment conducted within a single background environment, eggs of the American Alligator (Alligator mississippiensis) arranged in a small cluster (“clutch”) yielded a sex ratio (73% male) that differed appreciably from the sex ratio (15% male) in a matched set of eggs in an open arrangement.3.The apparent cause of the difference in sex ratio was metabolic heating, which caused much higher temperatures in the cluster than in the open arrangement.
Article
Summary1.  The high spatial and temporal variability of forest understorey light environments requires lengthy and/or extensive sampling in order to characterize it by direct measurement. As this is often impractical, a number of surrogate measures have been developed that estimate light availability from assessments of forest canopy structure.2.  The subjective crown illumination index developed by Clark & Clark (1992) was compared with Garrison's (1949) moosehorn and two new methods: (i) the crown illumination ellipses method, which compares the size of canopy gaps with a series of standard area ellipses printed on a transparent screen; and (ii) the canopy-scope that, like the moosehorn, uses an array of 25 dots printed on a transparent screen to assess canopy openness, but is more robust and portable, measuring the largest canopy gap visible from the point of measurement rather than canopy openness overhead.3.  The new measures were more highly correlated with canopy openness in the range 0–30%, measured from hemispherical photographs, than the crown illumination index, and showed lower levels of between-observer variability.4.  The canopy-scope has the potential to be widely used for the simple and rapid assessment of forest understorey light environments. It has the advantage of giving ratio scale measurements that can be used in parametric statistics. The crown illumination ellipses can be used to score the illumination of crowns that are above head height.
Article
Recent increases in global temperatures have affected the phenology and survival of many species of plants and animals. We investigated a case study of the effects of potential climate change on a thermally sensitive species, the loggerhead sea turtle, at a breeding location at the northerly extent of the range of regular nesting in the United States. In addition to the physical limits imposed by temperature on this ectothermic species, sea turtle primary sex ratio is determined by the temperature experienced by eggs during the middle third of incubation. We recorded sand temperatures and used historical air temperatures (ATs) at Bald Head Island, NC, to examine past and predict future sex ratios under scenarios of warming. There were no significant temporal trends in primary sex ratio evident in recent years and estimated mean annual sex ratio was 58% female. Similarly, there were no temporal trends in phenology but earlier nesting and longer nesting seasons were correlated with warmer sea surface temperature. We modelled the effects of incremental increases in mean AT of up to 7.5 1C, the maximum predicted increase under modelled scenarios, which would lead to 100% female hatchling production and lethally high incubation temperatures, causing reduction in hatchling production. Populations of turtles in more southern parts of the United States are currently highly female biased and are likely to become ultra-biased with as little as 1 1C of warming and experience extreme levels of mortality if warming exceeds 31C. The lack of a demonstrable increase in AT in North Carolina in recent decades coupled with primary sex ratios that are not highly biased means that the male offspring from North Carolina could play an increasingly important role in the future viability of the loggerhead turtle in the Western Atlantic.
Article
Current paradigms may substantially underestimate the complexity of reptilian sex determination. In previous work, we have shown that the sex of a hatchling lizard (Bassiana duperreyi, Scincidae) does not depend entirely on its genes (XX versus XY sex chromosomes); instead, low nest temperatures can override genotype to produce XX as well as XY males. Our experimental studies now add a third mechanism to this list: sex determination via yolk allocation to the egg. Within each clutch, the eggs that produce daughters are larger than those that produce sons. If (and only if) eggs are incubated at low temperatures, removing yolk from a newly laid egg turns the offspring into a male. Adding yolk from a larger (but not smaller) egg turns the recipient egg's offspring into a female. Remarkably, then, offspring sex in this species is the end result of an interaction between three mechanisms: sex chromosomes, nest temperatures, and yolk allocation.
Article
Previous studies have shown that exogenous steroid hormones can affect sex determination in reptiles with temperature-dependent sex determination (TSD). These studies have also suggested that the sensitivity of TSD to exogenous steroids may vary with incubation temperature. The majority of these studies, however, have utilized incubation temperatures producing all males or all females in the control groups, rather than temperatures which produced mixed sex ratios in control groups. The goals of the current study were to examine the effects of steroids on sex determination in a turtle (Trachemys scripta) at temperatures which produced mixed sex ratios in the control groups. Collectively, the results of single-treatment experiments indicate that at incubation temperatures producing mixed sex ratios in control groups, (1) estradiol-17 beta, tamoxifen, norethindrone, and testosterone all showed a similar "type" of effect (i.e., feminizing) as in previous studies utilizing male-producing temperatures, (2) sex determination has significantly increased sensitivity to estradiol-17 beta in comparison to its effect at temperatures producing all males, and (3) sex determination is sensitive to the masculinizing effects of dihydrotestosterone (DHT) (in previous studies utilizing female-producing temperature DHT did not affect sex determination). Last, a set of double-treatment experiments was performed in which eggs received both estradiol-17 beta and DHT treatments. No significant increases in the production of males were detected. Significant increases in the production of females were detected, but only in the groups receiving the highest dosage of estradiol-17 beta (1.0 micrograms).(ABSTRACT TRUNCATED AT 250 WORDS)
Article
We compared incubation temperatures in nests (n=32) of the green turtle (Chelonia mydas) on Ascension Island in relation to sand temperatures of control sites at nest depth. Intrabeach thermal variation was low, whereas interbeach thermal variation was high in both control and nest sites. A marked rise in temperature was recorded in nests from 30% to 40% of the way through the incubation period and attributed to metabolic heating. Over the entire incubation period, metabolic heating accounted for a mean rise in temperature of between 0.07 degrees and 2.86 degrees C within nests. During the middle third of incubation, when sex is thought to be determined, this rise in temperature ranged between 0.07 degrees and 2.61 degrees C. Metabolic heating was related to both the number of eggs laid and the total number of hatchlings/embryos produced in a clutch. For 32 clutches in which temperature was recorded, we estimate that metabolic heating accounted for a rise of up to 30% in the proportion of females produced within different clutches. Previous studies have dismissed any effect of metabolic heating on the sex ratio of marine turtle hatchlings. Our results imply that metabolic heating needs to be considered when estimating green turtle hatchling sex ratios.
American crocodile (Crocodylus acutus) (Crocodylia: Crocodylidae) (Cuvier 1807) population status in the Great Tempisque Wetland
  • J R Bolaños-Montero
Bolaños-Montero, J.R., 2012. American crocodile (Crocodylus acutus) (Crocodylia: Crocodylidae) (Cuvier 1807) population status in the Great Tempisque Wetland. In: Crocodiles. Proceedings of the 21st Working Meeting of the IUCN-SSC Crocodile Specialst Group. IUCN: Gland, Switzerland, pp. 167-178.
D. is a professor at Auburn University interested in herpetology, biogeography and tropical ecology
  • Craig Guyer
Craig Guyer Ph.D. is a professor at Auburn University interested in herpetology, biogeography and tropical ecology.
Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change
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  • S B Power
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IPCC, 2013. Annex I: Atlas of Global and Regional Climate Projections. In: van Oldenborgh, G.J., Collins, M., Arblaster, J., Christensen, J.H., Marotzke, J., Power, S.B., Rummukainen, M., Zhou, T. (Eds.), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom, New York, NY, USA.
is a graduate student at Auburn University and soon to be a post-doctoral teaching fellow at Southeastern Louisiana University interested in physiological ecology, functional and diagnostic morphology and biogeographic and systematic philosophy
  • Christopher M D Murray Ph
Christopher M. Murray Ph.D. is a graduate student at Auburn University and soon to be a post-doctoral teaching fellow at Southeastern Louisiana University interested in physiological ecology, functional and diagnostic morphology and biogeographic and systematic philosophy.
R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing
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R Development Core Team. 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
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  • J Soley
  • I G Garcia
  • R M Araujo
  • A R Santos
  • V E Valle
  • M Brunet
  • L Aguilar
  • L Alvarez
  • M Bautista
  • C Castanon
  • L Herrera
  • E Ruano
  • J J Sinay
  • E Sanchez
  • G I H Oviedo
  • F Obed
  • J E Salgado
  • J L Vazquez
  • M Baca
  • M Gutierrez
  • C Centella
  • J Espinosa
  • D Martinez
  • B Olmedo
  • C E O Espinoza
Aguilar, E., Peterson, T.C., Obando, P.R., Frutos, R., Retana, J.A., Solera, M., Soley, J., Garcia, I.G., Araujo, R.M., Santos, A.R., Valle, V.E., Brunet, M., Aguilar, L., Alvarez, L., Bautista, M., Castanon, C., Herrera, L., Ruano, E., Sinay, J.J., Sanchez, E., Oviedo, G.I.H., Obed, F., Salgado, J.E., Vazquez, J.L., Baca, M., Gutierrez, M., Centella, C., Espinosa, J., Martinez, D., Olmedo, B., Espinoza, C.E.O., Nunez, R., Haylock, M., Benavides, H., Mayorga, R., 2005. Changes in precipitation and temperature extremes in Central America and northern South America, 1961–2003. J. Geophys. Res. – Atmos., 110.
D. is a biologist and the Palo Verde Biological Station director interested in herpetology, toxicology, ecology and physiology
  • Mahmood Sasa
  • Marin Ph
Mahmood Sasa Marin Ph.D. is a biologist and the Palo Verde Biological Station director interested in herpetology, toxicology, ecology and physiology.
  • E Aguilar
  • T C Peterson
  • P R Obando
  • R Frutos
  • J A Retana
  • M Solera
  • J Soley
  • I G Garcia
  • R M Araujo
  • A R Santos
  • V E Valle
  • M Brunet
  • L Aguilar
  • L Alvarez
  • M Bautista
  • C Castanon
  • L Herrera
  • E Ruano
  • J J Sinay
  • E Sanchez
  • G I H Oviedo
  • F Obed
  • J E Salgado
  • J L Vazquez
  • M Baca
  • M Gutierrez
  • C Centella
  • J Espinosa
  • D Martinez
  • B Olmedo
  • C E O Espinoza
Aguilar, E., Peterson, T.C., Obando, P.R., Frutos, R., Retana, J.A., Solera, M., Soley, J., Garcia, I.G., Araujo, R.M., Santos, A.R., Valle, V.E., Brunet, M., Aguilar, L., Alvarez, L., Bautista, M., Castanon, C., Herrera, L., Ruano, E., Sinay, J.J., Sanchez, E., Oviedo, G.I.H., Obed, F., Salgado, J.E., Vazquez, J.L., Baca, M., Gutierrez, M., Centella, C., Espinosa, J., Martinez, D., Olmedo, B., Espinoza, C.E.O., Nunez, R., Haylock, M., Benavides, H., Mayorga, R., 2005. Changes in precipitation and temperature extremes in Central America and northern South America, 1961-2003. J. Geophys. Res.-Atmos., 110.