RESUMEN
Climate warming and the feminization of populations due to temperature-dependent sex determination may threaten sea turtles with extinction. To identify sites of heightened risk, we examined sex ratio data and patterns of climate change over multiple decades for 64 nesting sites spread across the globe. Over the last 62 years the mean change in air temperature was 0.85°C per century (SD = 0.65°C, range = -0.53 to +2.5°C, n = 64 nesting sites). Temperatures increased at 40 of the 64 study sites. Female-skewed hatchling or juvenile sex ratios occurred at 57 of the 64 sites, with skews >90% female at 17 sites. We did not uncover a relationship between the extent of warming and sex ratio (r62 = -0.03, p = .802, n = 64 nesting sites). Hence, our results suggest that female-hatchling sex ratio skews are not simply a consequence of recent warming but have likely persisted at some sites for many decades. So other factors aside from recent warming must drive these variations in sex ratios across nesting sites, such as variations in nesting behaviour (e.g. nest depth), substrate (e.g. sand albedo), shading available and rainfall patterns. While overall across sites recent warming is not linked to hatchling sex ratio, at some sites there is both is a high female skew and high warming, such as Raine Island (Australia; 99% female green turtles; 1.27°C warming per century), nesting beaches in Cyprus (97.1% female green turtles; 1.68°C warming per century) and in the Dutch Caribbean (St Eustatius; 91.5% female leatherback turtles; 1.15°C warming per century). These may be among the first sites where management intervention is needed to increase male production. Continued monitoring of sand temperatures and sex ratios are recommended to help identify when high incubation temperatures threaten population viability.
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Tortugas , Animales , Femenino , Masculino , Razón de Masculinidad , Arena , Temperatura , Cambio ClimáticoRESUMEN
As climate-related impacts threaten marine biodiversity globally, it is important to adjust conservation efforts to mitigate the effects of climate change. Translating scientific knowledge into practical management, however, is often complicated due to resource, economic and policy constraints, generating a knowledge-action gap. To develop potential solutions for marine turtle conservation, we explored the perceptions of key actors across 18 countries in the Mediterranean. These actors evaluated their perceived relative importance of 19 adaptation and mitigation measures that could safeguard marine turtles from climate change. Of importance, despite differences in expertise, experience and focal country, the perceptions of researchers and management practitioners largely converged with respect to prioritizing adaptation and mitigation measures. Climate change was considered to have the greatest impacts on offspring sex ratios and suitable nesting sites. The most viable adaptation/mitigation measures were considered to be reducing other pressures that act in parallel to climate change. Ecological effectiveness represented a key determinant for implementing proposed measures, followed by practical applicability, financial cost, and societal cost. This convergence in opinions across actors likely reflects long-standing initiatives in the Mediterranean region towards supporting knowledge exchange in marine turtle conservation. Our results provide important guidance on how to prioritize measures that incorporate climate change in decision-making processes related to the current and future management and protection of marine turtles at the ocean-basin scale, and could be used to guide decisions in other regions globally. Importantly, this study demonstrates a successful example of how interactive processes can be used to fill the knowledge-action gap between research and management.
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Ecosistema , Tortugas , Animales , Conservación de los Recursos Naturales/métodos , Cambio Climático , BiodiversidadRESUMEN
Why females would mate with multiple partners and have multiple fathers for clutches or litters is a long-standing enigma. There is a broad dichotomy in hypotheses ranging from polyandry having benefits to simply being an unavoidable consequence of a high incidence of male-female encounters. If females simply give in to mating when it is too costly to avoid being harassed by males (convenience polyandry), then there should be a higher rate of mating as density increases. However, if females actively seek males because they benefit from multiple mating, then mating frequency, and consequently the incidence of multiple paternity of clutches, should be high throughout. To explore these competing explanations, here we review the incidence of multiple paternity for sea turtles nesting around the World. Across 30 rookeries, including all 7 species of sea turtle, the incidence of multiple paternity was only weakly linked to rookery size (r2=0.14). However, using high resolution at-sea GPS tracking we show that the specifics of movement patterns play a key role in driving packing density and hence the likely rate of male-female encounters. When individuals use the same focal areas, packing density could be 100× greater than when assuming individuals move independently. Once the extent of adult movements in the breeding season was considered so that movements and abundance could be combined to produce a measure of density, then across rookeries we found a very tight relationship (r2=0.96) between packing density and the incidence of multiple paternity. These findings suggest that multiple paternity in sea turtles may have no benefit, but is simply a consequence of the incidence of male-female encounters.
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Reproducción/fisiología , Tortugas/fisiología , Animales , Femenino , MasculinoRESUMEN
For species with temperature-dependent sex determination (TSD) there is the fear that rising temperatures may lead to single-sex populations and population extinction. We show that for sea turtles, a major group exhibiting TSD, these concerns are currently unfounded but may become important under extreme climate warming scenarios. We show how highly female-biased sex ratios in developing eggs translate into much more balanced operational sex ratios so that adult male numbers in populations around the world are unlikely to be limiting. Rather than reducing population viability, female-biased offspring sex ratios may, to some extent, help population growth by increasing the number of breeding females and hence egg production. For rookeries across the world (n = 75 sites for seven species), we show that extreme female-biased hatchling sex ratios do not compromise population size and are the norm, with a tendency for populations to maximize the number of female hatchlings. Only at extremely high incubation temperature does high mortality within developing clutches threaten sea turtles. Our work shows how TSD itself is a robust strategy up to a point, but eventually high mortality and female-only hatchling production will cause extinction if incubation conditions warm considerably in the future.
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Análisis para Determinación del Sexo , Razón de Masculinidad , Temperatura , Tortugas/fisiología , Animales , Cruzamiento , Femenino , MasculinoRESUMEN
The optimum path to follow when subjected to cross flows was first considered over 80 years ago by the German mathematician Ernst Zermelo, in the context of a boat being displaced by ocean currents, and has become known as the 'Zermelo navigation problem'. However, the ability of migrating animals to solve this problem has received limited consideration, even though wind and ocean currents cause the lateral displacement of flyers and swimmers, respectively, particularly during long-distance journeys of 1000s of kilometres. Here, we examine this problem by combining long-distance, open-ocean marine turtle movements (obtained via long-term GPS tracking of sea turtles moving 1000s of km), with a high resolution basin-wide physical ocean model to estimate ocean currents. We provide a robust mathematical framework to demonstrate that, while turtles eventually arrive at their target site, they do not follow the optimum (Zermelo's) route. Even though adult marine turtles regularly complete incredible long-distance migrations, these vertebrates primarily rely on course corrections when entering neritic waters during the final stages of migration. Our work introduces a new perspective in the analysis of wildlife tracking datasets, with different animal groups potentially exhibiting different levels of complexity in goal attainment during migration.
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Migración Animal , Tortugas , Algoritmos , Animales , Masculino , Mar MediterráneoRESUMEN
Population declines of vertebrates are common, but rebuilding marine life may be possible. We assessed trends in sea turtle numbers globally, building 61 time series of abundance extending beyond 2015, representing monitoring in >1200 years. Increases were widespread with significant upward trends, no significant change, and significant downward trends in 28, 28, and 5 time series, respectively. For example, annual nest numbers increased between 1980 and 2018 from around 4,000 to 16,000 for green turtles at Aldabra (Seychelles, Indian Ocean) and between 2008 and 2020 from around 500 to 35,000 for loggerhead turtles in Sal (Cape Verde, north Atlantic). However, conservation concerns remain. Major populations may experience declines, such as loggerhead turtles in Oman, while previous upward trends can be reversed, as with green turtles nesting at Tortuguero (Costa Rica, Caribbean). Further, decreases in abundance were evident in several leatherback turtle time series. These concerns show there is no room for complacency for sea turtle conservation.
RESUMEN
Climate change is a clear and present threat to species survival. For species with temperature-dependent sex determination, including all sea turtles, it has been hypothesised that climate change may drive the creation of sex-ratio biases leading to population extinctions1. Through a global analysis across multiple species, we present the first direct empirical evidence for a demographic consequence of male scarcity in sea turtle populations, with a lower incidence of multiple paternity being found in populations with more extreme female-biased hatchling sex-ratio skews. For green turtles, when the female bias in hatchling sex ratio was >90%, the incidence of multiple paternity was low compared to other nesting sites, being 24.5% in the eastern Mediterranean (Cyprus), 36.4% on Redang Island (Malaysia) and 15.4% on the southern Great Barrier Reef (Heron Island, Australia) compared to higher values (range 61.1-91.7%) at other sites globally. These results suggest that a low incidence of multiple paternity may serve as a harbinger of future problems with egg fertility if males become even scarcer. Assessments of the incidence of multiple paternity at sites where adult males are expected to become scarce, such as Raine Island on the northern Great Barrier Reef in Australia, may help to identify when a lack of males raises the threat of local extinctions. In such cases, intervention to increase the production of male hatchlings may be needed.
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Tortugas , Animales , Femenino , Masculino , Razón de Masculinidad , Temperatura , Cambio Climático , FertilidadRESUMEN
Quantifying the extent to which animals detect and respond to human presence allows us to identify pressure (disturbance) and inform conservation management objectively; however, obtaining baselines against which to compare human impact is hindered in areas where human activities are already well established. For example, Zakynthos Island (Greece, Mediterranean) receives around 850,000 visitors each summer, while supporting an important loggerhead sea turtle rookery (~300 individuals/season). The coronavirus (COVID-19)-driven absence of tourism in May-June 2020 provided an opportunity to evaluate the distribution dynamics of this population in the absence (2020) vs. presence (2018 and 2019) of visitors using programmed unmanned aerial system (UAS) surveys. Ambient sea temperature transitioned from suboptimal for breeding in May to optimal in late June, with turtle distribution appearing to shift from shallow (to benefit from waters 3-5°C above ambient) to deeper waters in 2018 and 2019, but not 2020. The 2020 data set demonstrated that increased tourism pressure, not temperature, drives turtles offshore. Specifically, >50% of turtles remained within 100 m of shore at densities of 25-50 visitors/km, even when sea temperature rose, with 2018 and 2019 data supporting this trend. Reduced access to warmer, nearshore waters by tourism could delay the onset of nesting and increase the length of the egg maturation period between nesting events (internesting interval) at this site. A coastal refuge zone could be delimited in May-June where touristic infrastructure is minimal, but also where turtles frequently aggregate. In conclusion, sea turtles appear capable of perceiving changes in the level of human pressure at fine spatial and temporal scales and adjusting their distribution accordingly.
RESUMEN
Several cancer risk factors (exposure to ultraviolet-B, pollution, toxins and pathogens) have been identified for wildlife, to form a "cancer risk landscape." However, information remains limited on how the spatiotemporal variability of these factors impacts the prevalence of cancer in wildlife. Here, we evaluated the cancer risk landscape at 49 foraging sites of the globally distributed green turtle (Chelonia mydas), a species affected by fibropapillomatosis, by integrating data from a global meta-analysis of 31 publications (1994-2019). Evaluated risk factors included ultraviolet light exposure, eutrophication, toxic phytoplanktonic blooms, sea surface temperature, and the presence of mechanical vectors (parasites and symbiotic species). Prevalence was highest in areas where nutrient concentrations facilitated the emergence of toxic phytoplankton blooms. In contrast, ultraviolet light exposure and the presence of parasitic and/or symbiotic species did not appear to impact disease prevalence. Our results indicate that, to counter outbreaks of fibropapillomatosis, management actions that reduce eutrophication in foraging areas should be implemented.
RESUMEN
Species that have temperature-dependent sex determination (TSD) often produce highly skewed offspring sex ratios contrary to long-standing theoretical predictions. This ecological enigma has provoked concern that climate change may induce the production of single-sex generations and hence lead to population extirpation. All species of sea turtles exhibit TSD, many are already endangered, and most already produce sex ratios skewed to the sex produced at warmer temperatures (females). We tracked male loggerhead turtles (Caretta caretta) from Zakynthos, Greece, throughout the entire interval between successive breeding seasons and identified individuals on their breeding grounds, using photoidentification, to determine breeding periodicity and operational sex ratios. Males returned to breed at least twice as frequently as females. We estimated that the hatchling sex ratio of 70:30 female to male for this rookery will translate into an overall operational sex ratio (OSR) (i.e., ratio of total number of males vs females breeding each year) of close to 50:50 female to male. We followed three male turtles for between 10 and 12 months during which time they all traveled back to the breeding grounds. Flipper tagging revealed the proportion of females returning to nest after intervals of 1, 2, 3, and 4 years were 0.21, 0.38, 0.29, and 0.12, respectively (mean interval 2.3 years). A further nine male turtles were tracked for short periods to determine their departure date from the breeding grounds. These departure dates were combined with a photoidentification data set of 165 individuals identified on in-water transect surveys at the start of the breeding season to develop a statistical model of the population dynamics. This model produced a maximum likelihood estimate that males visit the breeding site 2.6 times more often than females (95%CI 2.1, 3.1), which was consistent with the data from satellite tracking and flipper tagging. Increased frequency of male breeding will help ameliorate female-biased hatchling sex ratios. Combined with the ability of males to fertilize the eggs of many females and for females to store sperm to fertilize many clutches, our results imply that effects of climate change on the viability of sea turtle populations are likely to be less acute than previously suspected.
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Cambio Climático , Periodicidad , Conducta Sexual Animal , Tortugas/fisiología , Migración Animal , Animales , Cruzamiento , Conservación de los Recursos Naturales , Femenino , Geografía , Masculino , Dinámica Poblacional , Factores Sexuales , Razón de MasculinidadRESUMEN
Sex-biased survival linked to anthropogenic threats places populations at risk. We show the utility of long-term multidecadal photo-identification (photo-id) combined with long-term high-resolution (Fastloc-GPS) satellite telemetry to investigate the links between mortality rates and patterns of movement for a wide-ranging, endangered marine vertebrate. Using a photo-identification database of 947 loggerhead turtles (Caretta caretta) compiled over 18 yr, we estimated greater annual survival rates of females (0.89; 95% confidence interval [CI] 0.87-0.90) compared to males (0.73; 95% CI 0.67-0.78). For males satellite-tracked across multiple breeding seasons, 100% (26 of 26) returned to the same breeding site, suggesting the calculated lower male survival rate was likely not due to emigration to breed elsewhere. 10,111 and 2,524 tracking days for males (n = 39 individuals) and females (n = 18 individuals), respectively, revealed different habitat-use patterns outside the breeding season: males tended to occupy foraging sites closer to shore and closer to breeding sites but, due to their generally annual breeding, compared to biennial breeding for females, males migrated further per year on average. These differences in movement patterns likely contribute to higher mortality in males through increased interaction with anthropogenic threats. Long-term identification coupled with tracking offers great promise for estimating the survival rates of other wide-ranging species.
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Especies en Peligro de Extinción , Tortugas , Migración Animal , Animales , Ecosistema , Femenino , Masculino , Estaciones del Año , TelemetríaRESUMEN
1. Reproductive fitness is often compromised at the margins of a species' range due to sub-optimal conditions. 2. Set against this backdrop, the Mediterranean's largest loggerhead sea turtle (Caretta caretta) rookery at Zakynthos (Greece) presents a conundrum, being at a very high latitude for this species, yet hosting a high concentration of nesting. 3. We used visual surveys combined with global positioning system (GPS) tracking to show that at the start of the breeding season, individuals showed microhabitat selection, with females residing in transient patches of warm water. As the sea warmed in the summer, this selection was no longer evident. 4. As loggerhead turtles are ectothermic, this early season warm-water selection presumably speeds up egg maturation rates before oviposition, thereby allowing more clutches to be incubated when sand conditions are optimal during the summer. 5. Active selection of warm waters may allow turtles to initiate nesting at an earlier date.
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Ecosistema , Ambiente , Temperatura , Tortugas/fisiología , Animales , Femenino , Grecia , Biología Marina , Dinámica Poblacional , Agua de Mar/química , Tortugas/metabolismo , VientoRESUMEN
There have been efforts around the globe to track individuals of many marine species and assess their movements and distribution, with the putative goal of supporting their conservation and management. Determining whether, and how, tracking data have been successfully applied to address real-world conservation issues is, however, difficult. Here, we compile a broad range of case studies from diverse marine taxa to show how tracking data have helped inform conservation policy and management, including reductions in fisheries bycatch and vessel strikes, and the design and administration of marine protected areas and important habitats. Using these examples, we highlight pathways through which the past and future investment in collecting animal tracking data might be better used to achieve tangible conservation benefits.
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Conservación de los Recursos Naturales , Explotaciones Pesqueras , Animales , EcosistemaRESUMEN
We document a tendency for published estimates of population size in sea turtles to be increasing rather than decreasing across the globe. To examine the population status of the seven species of sea turtle globally, we obtained 299 time series of annual nesting abundance with a total of 4417 annual estimates. The time series ranged in length from 6 to 47 years (mean, 16.2 years). When levels of abundance were summed within regional management units (RMUs) for each species, there were upward trends in 12 RMUs versus downward trends in 5 RMUs. This prevalence of more upward than downward trends was also evident in the individual time series, where we found 95 significant increases in abundance and 35 significant decreases. Adding to this encouraging news for sea turtle conservation, we show that even small sea turtle populations have the capacity to recover, that is, Allee effects appear unimportant. Positive trends in abundance are likely linked to the effective protection of eggs and nesting females, as well as reduced bycatch. However, conservation concerns remain, such as the decline in leatherback turtles in the Eastern and Western Pacific. Furthermore, we also show that, often, time series are too short to identify trends in abundance. Our findings highlight the importance of continued conservation and monitoring efforts that underpin this global conservation success story.
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Conservación de los Recursos Naturales , Tortugas , Animales , Biodiversidad , Ecosistema , Densidad de Población , Dinámica PoblacionalRESUMEN
The marine turtle Caretta caretta is a widely distributed species that is facing critical population decline, especially in the Mediterranean rookeries. Molecular markers, such as mitochondrial DNA (mtDNA) sequences, are of great importance for the description and monitoring of turtle migratory populations. The complete sequence of the C. caretta mitochondrial genome is presented here. The genome comprises 16,440 base pairs, containing 37 genes (13 protein-coding genes, 22 tRNA genes, and 2 rRNA genes), and a control region, all organized similar to the majority of vertebrate mitogenomes. MtDNA length polymorphism and heteroplasmy were observed among, and within, individuals due to the variable size of a microsatellite repeat residing at the 3' end of the control region. The use of the above repeat as a marker for individual fingerprinting is discussed. Furthermore, phylogenetic analyses among Testudines based on complete mitogenomes, as well as among marine turtles based on partial mtDNA sequences, are considered.
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ADN Mitocondrial/genética , Genoma , Filogenia , Tortugas/genética , Animales , Secuencia de Bases , Cartilla de ADN , Reacción en Cadena de la Polimerasa , Tortugas/clasificaciónRESUMEN
Long distance migration occurs in a wide variety of taxa including birds, insects, fishes, mammals and reptiles. Here, we provide evidence for a new paradigm for the determinants of migration destination. As adults, sea turtles show fidelity to their natal nesting areas and then at the end of the breeding season may migrate to distant foraging sites. For a major rookery in the Mediterranean, we simulated hatchling drift by releasing 288 000 numerical particles in an area close to the nesting beaches. We show that the pattern of adult dispersion from the breeding area reflects the extent of passive dispersion that would be experienced by hatchlings. Hence, the prevailing oceanography around nesting areas may be crucial to the selection of foraging sites used by adult sea turtles. This environmental forcing may allow the rapid evolution of new migration destinations if ocean currents alter with climate change.