Variability in thermal tolerance of clutches from different mothers indicates adaptation potential to climate warming in sea turtles.

The current climate warming is a challenge to biodiversity that could surpass the adaptation capacity of some species. Hence, understanding the means by which populations undergo an increase in their thermal tolerance is critical to assess how they could adapt to climate warming. Specifically, sea turtle populations could respond to increasing temperatures by (1) colonizing new nesting areas, (2) nesting during cooler times of the year, and/or (3) by increasing their thermal tolerance. Differences in thermal tolerance of clutches laid by different females would indicate that populations have the potential to adapt by natural selection. Here, we used exhaustive information on nest temperatures and hatching success of leatherback turtle (Dermochelys coriacea) clutches over 14 years to assess the occurrence of individual variability in thermal tolerance among females. We found an effect of temperature, year, and the interaction between female identity and nest temperature on hatching success, indicating that clutches laid by different females exhibited different levels of vulnerability to high temperatures. If thermal tolerance is a heritable trait, individuals with higher thermal tolerances could have greater chances of passing their genes to following generations, increasing their frequency in the population. However, the high rate of failure of clutches at temperatures above 32°C suggests that leatherback turtles are already experiencing extreme heat stress. A proper understanding of mechanisms of adaptation in populations to counteract changes in climate could greatly contribute to future conservation of endangered populations in a rapidly changing world.

Temperature-Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance.

The adaptive significance of temperature-dependent sex determination (TSD) in reptiles remains unknown decades after TSD was first identified in this group. Concurrently, there is growing concern about the effect that rising temperatures may have on species with TSD, potentially producing extremely biased sex ratios or offspring of only one sex. The current state-of the-art in TSD research on sea turtles is reviewed here and, against current paradigm, it is proposed that TSD provides an advantage under warming climates. By means of coadaptation between early survival and sex ratios, sea turtles are able to maintain populations. When offspring survival declines at high temperatures, the sex that increases future fecundity (females) is produced, increasing resilience to climate warming. TSD could have helped reptiles to survive mass extinctions in the past via this model. Flaws in research on sex determination in sea turtles are also identified and it is suggested that the development of new techniques will revolutionize the field.

Climate change overruns resilience conferred by temperature-dependent sex determination in sea turtles and threatens their survival.

Temperature-dependent sex determination (TSD) is the predominant form of environmental sex determination (ESD) in reptiles, but the adaptive significance of TSD in this group remains unclear. Additionally, the viability of species with TSD may be compromised as climate gets warmer. We simulated population responses in a turtle with TSD to increasing nest temperatures and compared the results to those of a virtual population with genotypic sex determination (GSD) and fixed sex ratios. Then, we assessed the effectiveness of TSD as a mechanism to maintain populations under climate change scenarios. TSD populations were more resilient to increased nest temperatures and mitigated the negative effects of high temperatures by increasing production of female offspring and therefore, future fecundity. That buffered the negative effect of temperature on the population growth. TSD provides an evolutionary advantage to sea turtles. However, this mechanism was only effective over a range of temperatures and will become inefficient as temperatures rise to levels projected by current climate change models. Projected global warming threatens survival of sea turtles, and the IPCC high gas concentration scenario may result in extirpation of the studied population in 50 years.

High thermal tolerance of egg clutches and potential adaptive capacity in green turtles.

Climate warming threatens sea turtles, among other effects, because high temperatures increase embryo mortality. However, not all species and populations are expected to respond the same way because they could have different thermal tolerances and capacities to adapt. We tested the effect of incubation temperature on egg mortality in a population of green turtles (Chelonia mydas) previously suggested to be less affected by extreme climatic events than others. We (1) assessed the relationship between temperature and hatching success, (2) defined an optimal range of temperatures that maximized hatching success and (3) assessed the variability in the response to temperature among clutches laid by different mothers, which could allow adaptation. Hatching success was consistently high in green turtle clutches with a skew toward high values, with 50 % of clutches having a success above 94 %. Yet, it was mildly affected by temperature, declining at both low and high temperatures. The optimal range of mean incubation temperatures was between ~30.5 °C and 32.5 °C. Current mean temperatures (31.3 °C) fall within the middle of the optimal range, indicating a potential resilience to further rises in mean nest temperature. Hatching success was best described by nest temperature and the interaction between female identity and temperature. This last predictor indicated a variability in thermal tolerance among clutches laid by different mothers and therefore, a capacity to adapt. The studied population of green turtles seems to be less vulnerable than others to climate warming. Understanding how different populations could respond to increasing temperatures could help complete the picture on the potential effects of climate change on sea turtles.

Increased grey wolf diurnality in southern Europe under human-restricted conditions.

Wolves have been the archetype of wildlife persecution by humans for centuries all over the world, and still are heavily persecuted in some regions. Facultative diurnal/nocturnal wild mammals are known to become more nocturnal when persecuted. Conversely, little is known regarding the possibility of wolves becoming more diurnal if not persecuted. We took advantage of a 9-year natural experiment of restricted human access to a restored coal mine debris dump to study the daily activity patterns of wolves under conditions of infrequent human presence. Results were compared with a paired control site with frequent human use. Circadian wolf activity was monitored using camera traps (3 years in human-restricted site; 2 years in control). Additionally, data from two GPS-GSM-collared wolves monitored in a second control site were also analyzed. In our control sites, wolves were nearly inactive during daylight hours. In contrast, in the human-restricted site wolves extended their activity toward noon, with a daily activity peak between 10:00 and 12:00, and showed some activity throughout the entire circadian 2-h interval cycle considered. Wolves clearly had higher diurnality in the human-restricted area with 78% greater incidence of capture with remote cameras during the day than in the control site. We suggest that the shift toward increased diurnality was related to the loss of fear of humans. Evidence in support of this hypothesis comes from flight initiation distance (FID) data. Wolves showed relatively short FIDs when faced with a human observer (range 70-183 m) in broad daylight at the human-restricted site, but were so afraid of humans in the control site that we were unable to conduct FID trials there. Based on these results, we suggest that wolves may increase their diurnality in those European countries with currently increasing movement of human populations from rural to urban areas and that do not conduct lethal control of wolves. This would represent a historical landmark for a species that has been persecuted for many centuries. However, such behavioral shifts could bring new human-wolf conflicts that would require new policies.

Using Unmanned Aerial Systems (UAS) to assay mangrove estuaries on the Pacific coast of Costa Rica.

Mangrove forests, one of the world's most endangered ecosystems, are also some of the most difficult to access. This is especially true along the Pacific coast of Costa Rica, where 99% of the country's mangroves occur. Unmanned Aerial Systems (UAS), or drones, have become a convenient tool for natural area assessment, and offer a solution to the problems of remote mangrove monitoring. This study is the first to use UAS to analyze the structure of a mangrove forests within Central America. Our goals were to (1) determine the forest structure of two estuaries in northwestern Costa Rica through traditional ground measurements, (2) assess the accuracy of UAS measurements of canopy height and percent coverage and (3) determine whether the normalized difference vegetation index (NDVI) could discriminate between the most abundant mangrove species. We flew a UAS equipped with a single NDVI sensor during the peak wet (Sept-Nov) and dry (Jan-Feb) seasons. The structure and species composition of the estuaries showed a possible transition between the wet mangroves of southern Costa Rica and the drier northern mangroves. UAS-derived measurements at 100 cm/pixel resolution of percent canopy coverage and maximum and mean canopy height were not statistically different from ground measurements (p > 0.05). However, there were differences in mean canopy height at 10 cm/pixel resolution (p = 0.043), indicating diminished returns in accuracy as resolution becomes extremely fine. Mean NDVI values of Avicennia germinans (most abundant species) changed significantly between seasons (p < 0.001). Mean NDVI of Rhizophora racemosa (second most abundant species) was significantly different from A. germinans and dry forest dominant plots during the dry season (p < 0.001), demonstrating NDVI's capability of discriminating mangrove species. This study provides the first structural assessment of the studied estuaries and a framework for future studies of mangroves using UAS.

Are thermal barriers "higher" in deep sea turtle nests?

Thermal tolerances are affected by the range of temperatures that species encounter in their habitat. Daniel Janzen hypothesized in his "Why mountain passes are higher in the tropics" that temperature gradients were effective barriers to animal movements where climatic uniformity was high. Sea turtles bury their eggs providing some thermal stability that varies with depth. We assessed the relationship between thermal uniformity and thermal tolerance in nests of three species of sea turtles. We considered that barriers were "high" when small thermal changes had comparatively large effects and "low" when the effects were small. Mean temperature was lower and fluctuated less in species that dig deeper nests. Thermal barriers were comparatively "higher" in leatherback turtle (Dermochelys coriacea) nests, which were the deepest, as embryo mortality increased at lower "high" temperatures than in olive ridley (Lepidochelys olivacea) and green turtle (Chelonia mydas) nests. Sea turtles have temperature-dependent sex determination (TSD) and embryo mortality increased as temperature approached the upper end of the transitional range of temperatures (TRT) that produces both sexes (temperature producing 100% female offspring) in leatherback and olive ridley turtles. As thermal barriers are "higher" in some species than in others, the effects of climate warming on embryo mortality is likely to vary among sea turtles. Population resilience to climate warming may also depend on the balance between temperatures that produce female offspring and those that reduce embryo survival.

Patterns of vertebrate biodiversity in a tropical dry and mangrove forest matrix / Patrones de biodiversidad de vertebrados en una matriz de bosque seco tropical y manglar

Introduction: Tropical dry forests and mangroves, two of the world's most endangered ecosystems, each host a different set of environmental conditions which may support unique assemblages of species. However, few studies have looked at the unique vertebrate biodiversity in regions where both habitats occur side-by-side. Objective: To assess the vertebrate diversity and patterns of habitat usage in a mangrove and tropical dry forest matrix in an unprotected region of Northwestern Costa Rica. Methods: The study was conducted in a 7 km2 matrix of mangrove and tropical dry forests between Cabuyal and Zapotillal bays in Northwestern Costa Rica, south of Santa Rosa National Park. From September 2017 to March 2018, we used 13 automatic camera traps over 1 498 trap days to capture species utilizing the region and assess their patterns of habitat usage both spatially and temporally. Results: Seventy vertebrate species from 42 families in 27 orders were detected, including several globally threatened species. Over half of all species were detected in only one habitat, particularly amongst avian (78 %) and mammalian (42 %) species. Tropical dry forests hosted the greatest number of unique species and supported a greater percentage of herbivores than mangrove or edge habitats, which were dominated by carnivorous and omnivorous species. Mean detections per camera trap of all species increased significantly from the coldest and wettest month (Oct) to the hottest and driest months (Jan & Feb) in tropical dry forests. Sample-based rarefaction analysis revealed that survey length was sufficient to sample the tropical dry forest and edge habitats, though mangroves require further sampling. Conclusions: Taxa found to utilize different forest types may utilize each for different stages of their life cycle, moving between areas as environmental conditions change throughout the year. General patterns of global biodiversity favoring carnivore and omnivore usage of mangrove forests was confirmed in our study.

Introducción: Los bosques secos tropicales y los manglares, dos de los ecosistemas más amenazados del mundo, albergan cada uno un grupo de condiciones ambientales que pueden albergar conjuntos únicos de especies. Sin embargo, pocos estudios han analizado la biodiversidad única de vertebrados en regiones donde ambos hábitats se encuentran uno al lado del otro. Objetivo: Evaluar la diversidad de vertebrados y los patrones de uso del hábitat en una matriz de manglar y bosque seco tropical en una región no protegida del noroeste de Costa Rica. Métodos: El estudio se realizó en una matriz de 7 km2 de manglares y bosques secos tropicales en las bahías de Cabuyal y Zapotillal en el noroeste de Costa Rica, al sur del Parque Nacional Santa Rosa. De septiembre 2017 a marzo 2018, utilizamos 13 cámaras trampa automáticas durante 1 498 días trampa para capturar especies que utilizan la región y evaluar sus patrones de uso espacial y temporal del hábitat. Resultados: Se detectaron 70 especies de vertebrados de 42 familias y 27 órdenes, incluidas varias especies amenazadas a nivel mundial. Más de la mitad de todas las especies se encontraron en un solo hábitat, particularmente aves (78 %) y mamíferos (42 %). Los bosques secos tropicales albergan el mayor número de especies únicas y sustentan un mayor porcentaje de herbívoros que los hábitats de borde de manglares, que estaban dominados u hospedados por especies carnívoras y omnívoras. Las detecciones promedio por cámara trampa de todas las especies aumentaron significativamente desde el mes más frío y húmedo (octubre) hasta los meses más cálidos y secos (enero y febrero) en los bosques secos tropicales. El análisis de rarefacción basado en muestras reveló que la duración del estudio fue suficiente para muestrear los hábitats de bosque seco tropical y de borde, aunque los manglares requieren más muestreo. Conclusiones: Se encontró que los taxones pueden usar varios tipos de bosque en las diferentes etapas de su ciclo de vida, moviéndose entre áreas a medida que las condiciones ambientales cambian a lo largo del año. En nuestro estudio se confirmaron patrones generales de la biodiversidad global que favorecen el uso de los bosques de manglar por parte de carnívoros y omnívoros.

Conservation status of fish and marine invertebrate of rocky reefs and sandy substrates in two unprotected bays of the Papagayo Gulf, Costa Rica / Estado de conservación de peces e invertebrados marinos de arrecifes rocosos y zonas arenosas en dos bahías desprotegidas del Golfo de Papagayo, Costa Rica

Introduction: North Pacific Costa Rica is generally considered rich in marine habitats and species. However, some areas are subject to fishing pressures that could degrade ecosystems. The Gulf of Papagayo comprises protected and unprotected areas with various degrees of impact. Objectives: Our aim was to evaluate the conservation status of fish and invertebrate communities in rocky reefs and sandy areas in two unprotected bays of the Gulf of Papagayo. Methods: The study was conducted at Cabuyal and Zapotillal Bays, south of Santa Rosa National Park. From December 2017 to April 2018, a total of thirty-five transects were done parallel to the coast at 3-10 m depth. We identified fish and invertebrate species and estimated biomass by trophic group in fish, and density in invertebrates. Results: We found a high number of species of fish (81) and invertebrates (70) in rocky reefs, which indicates a biodiverse ecosystem, but few species of fish in sandy areas. Species composition differed between the two bays. Density of juvenile fishes was high in Zapotillal Bay, suggesting that the area could be important for recruitment and breeding. Fish biomass was higher in sandy areas than in rocky reefs and all trophic groups had lower biomass than in other unprotected areas of the region. On average, reef fish biomass was 1.57 ± 0.67 (s.e.) t ha-1, similar to previous reports for Costa Rican North Pacific. By trophic group, piscivorous and planktivorous had the highest biomass in sandy areas and piscivorous and carnivorous in rocky reefs. Mean coral cover was low with 4.09 % ± 2.51 (s.e.), similar to previously reported for the region. Conclusions: Cabuyal and Zapotillal Bays in the Gulf of Papagayo are biodiverse in fish and invertebrates. However, the area may be impacted by local fisheries and other human activities, affecting fish and invertebrate populations, and coral formations. Our study fills some gaps in knowledge of marine biodiversity in the Gulf of Papagayo that can contribute to the conservation of marine life in North Pacific Costa Rica.

Introducción: El Pacífico Norte de Costa Rica generalmente se considera rico en hábitats y especies marinas. Sin embargo, algunas zonas están sujetas a presiones de pesca que pueden degradar los ecosistemas. El Golfo de Papagayo comprende zonas protegidas y desprotegidas con diversos grados de impacto. Objetivos: Nuestro objetivo fue evaluar el estado de conservación de las comunidades de peces e invertebrados en los arrecifes rocosos y las zonas arenosas de dos bahías desprotegidas del Golfo de Papagayo. Métodos: El estudio se llevó a cabo en las bahías de Cabuyal y Zapotillal, al sur del Parque Nacional Santa Rosa. Desde diciembre 2017 hasta abril 2018, se realizaron un total de 35 transectos paralelos a la costa entre 3-10 m de profundidad. Se identificaron especies de peces e invertebrados y se estimó la biomasa por grupo trófico en los peces, y la densidad en los invertebrados. Resultados: Encontramos un alto número de especies de peces (81) e invertebrados (70) en arrecifes rocosos, lo que indica un ecosistema biodiverso, pero pocas especies de peces en zonas arenosas. La composición de especies difirió entre las dos bahías. La densidad de peces juveniles fue elevada en la bahía de Zapotillal, lo que sugiere que la zona podría ser importante para el reclutamiento y la reproducción. La biomasa de peces fue mayor en zonas arenosas que en arrecifes rocosos y todos los grupos tróficos tuvieron menores biomasas que en otras zonas desprotegidas de la región. En promedio, la biomasa de peces de arrecifes fue de 1.57 ± 0.67 (s.e.) t ha-1, similar a lo reportado anteriormente en el Pacífico Norte de Costa Rica. Por grupo trófico, los piscívoros y planctívoros tuvieron la biomasa más alta en las zonas arenosas y los piscívoros y carnívoros en los arrecifes rocosos. La cobertura media de coral fue baja con 4.09 % ± 2.51 (s.e.), similar a la reportada anteriormente para la región. Conclusiones: Las bahías Cabuyal y Zapotillal en el Golfo de Papagayo son biodiversas en peces e invertebrados. Sin embargo, la zona puede verse afectada por las pesquerías locales y otras actividades humanas, lo que afecta a las poblaciones de peces e invertebrados y formaciones coralinas. Nuestro estudio llena algunos vacíos de conocimiento de la biodiversidad marina en el Golfo de Papagayo que pueden contribuir a la conservación de la vida marina en el Pacífico Norte de Costa Rica.

Global analysis of the effect of local climate on the hatchling output of leatherback turtles.

The most recent climate change projections show a global increase in temperatures along with precipitation changes throughout the 21(st) century. However, regional projections do not always match global projections and species with global distributions may exhibit varying regional susceptibility to climate change. Here we show the effect of local climatic conditions on the hatchling output of leatherback turtles (Dermochelys coriacea) at four nesting sites encompassing the Pacific, Atlantic and Indian Oceans. We found a heterogeneous effect of climate. Hatchling output increased with long-term precipitation in areas with dry climatic conditions (Playa Grande, Pacific Ocean and Sandy Point, Caribbean Sea), but the effect varied in areas where precipitation was high (Pacuare, Caribbean Sea) and was not detected at the temperate site (Maputaland, Indian Ocean). High air temperature reduced hatchling output only at the area experiencing seasonal droughts (Playa Grande). Climatic projections showed a drastic increase in air temperature and a mild decrease in precipitation at all sites by 2100. The most unfavorable conditions were projected for Sandy Point where hatching success has already declined over time along with precipitation levels. The heterogeneous effect of climate may lead to local extinctions of leatherback turtles in some areas but survival in others by 2100.

Climate driven egg and hatchling mortality threatens survival of eastern Pacific leatherback turtles.

Egg-burying reptiles need relatively stable temperature and humidity in the substrate surrounding their eggs for successful development and hatchling emergence. Here we show that egg and hatchling mortality of leatherback turtles (Dermochelys coriacea) in northwest Costa Rica were affected by climatic variability (precipitation and air temperature) driven by the El Niño Southern Oscillation (ENSO). Drier and warmer conditions associated with El Niño increased egg and hatchling mortality. The fourth assessment report of the Intergovernmental Panel on Climate Change (IPCC) projects a warming and drying in Central America and other regions of the World, under the SRES A2 development scenario. Using projections from an ensemble of global climate models contributed to the IPCC report, we project that egg and hatchling survival will rapidly decline in the region over the next 100 years by ∼50-60%, due to warming and drying in northwestern Costa Rica, threatening the survival of leatherback turtles. Warming and drying trends may also threaten the survival of sea turtles in other areas affected by similar climate changes.

Embryonic death is linked to maternal identity in the leatherback turtle (Dermochelys coriacea).

Leatherback turtles have an average global hatching success rate of ~50%, lower than other marine turtle species. Embryonic death has been linked to environmental factors such as precipitation and temperature, although, there is still a lot of variability that remains to be explained. We examined how nesting season, the time of nesting each season, the relative position of each clutch laid by each female each season, maternal identity and associated factors such as reproductive experience of the female (new nester versus remigrant) and period of egg retention between clutches (interclutch interval) affected hatching success and stage of embryonic death in failed eggs of leatherback turtles nesting at Playa Grande, Costa Rica. Data were collected during five nesting seasons from 2004/05 to 2008/09. Mean hatching success was 50.4%. Nesting season significantly influenced hatching success in addition to early and late stage embryonic death. Neither clutch position nor nesting time during the season had a significant affect on hatching success or the stage of embryonic death. Some leatherback females consistently produced nests with higher hatching success rates than others. Remigrant females arrived earlier to nest, produced more clutches and had higher rates of hatching success than new nesters. Reproductive experience did not affect stage of death or the duration of the interclutch interval. The length of interclutch interval had a significant affect on the proportion of eggs that failed in each clutch and the developmental stage they died at. Intrinsic factors such as maternal identity are playing a role in affecting embryonic death in the leatherback turtle.