Short-term resilience to climate-induced temperature increases for equatorial sea turtle populations.

Projection models are being increasingly used to manage threatened taxa by estimating their responses to climate change. Sea turtles are particularly susceptible to climate change as they have temperature-dependent sex determination and increased sand temperatures on nesting beaches could result in the 'feminisation' of hatchling sex ratios for some populations. This study modelled likely long-term trends in sand temperatures and hatchling sex ratios at an equatorial nesting site for endangered green turtles (Chelonia mydas) and critically endangered hawksbill turtles (Eretmochelys imbricata). A total of 1078 days of sand temperature data were collected from 28 logger deployments at nest depth between 2018 and 2022 in Papua New Guinea (PNG). Long-term trends in sand temperature were generated from a model using air temperature as an environmental proxy. The influence of rainfall and seasonal variation on sand temperature was also investigated. Between 1960 and 2019, we estimated that sand temperature increased by ~0.6°C and the average hatchling sex ratio was relatively balanced (46.2% female, SD = 10.7). No trends were observed in historical rainfall anomalies and projections indicated no further changes to rainfall until 2100. Therefore, the sex ratio models were unlikely to be influenced by changing rainfall patterns. A relatively balanced sex ratio such as this is starkly different to the extremely female-skewed hatchling sex ratio (>99% female) reported for another Coral Sea nesting site, Raine Island (~850 km West). This PNG nesting site is likely rare in the global context, as it is less threatened by climate-induced feminisation. Although there is no current need for 'cooling' interventions, the mean projected sex ratios for 2020-2100 were estimated 76%-87% female, so future interventions may be required to increase male production. Our use of long-term sand temperature and rainfall trends has advanced our understanding of climate change impacts on sea turtles.

Insights from an ancient gymnosperm lineage: ambient temperature and light and the timing of thermogenesis in cycad cones.

PREMISE: Although maintaining the appropriate mid-day timing of the diel thermogenic events of cones of the dioecious cycads Macrozamia lucida and M. macleayi is central to the survival of both plant and pollinator in this obligate pollination mutualism, the nature of the underlying mechanism remains obscure. We investigated whether it is under circadian control. Circadian mechanisms control the timing of many ecologically important processes in angiosperms, yet only a few gymnosperms have been studied in this regard. METHODS: We subjected cones to different ambient temperature and lighting regimens (constant temperature and darkness; stepwise cool/warm ambient temperatures in constant darkness; stepwise dark/light exposures at constant temperature) to determine whether the resulting timing of their thermogenic events was consistent with circadian control. RESULTS: Cones exposed to constant ambient temperature and darkness generated multiple temperature peaks endogenously, with an average interpeak-temperature period of 20.7 (±0.20) h that is temperature-compensated (Q10 = 1.02). Exposure to 24-h ambient temperature cycles (12 h cool/12 h warm, constant darkness) yielded an interpeak-temperature period of 24.0 (±0.05) h, accurately and precisely replicating the ambient temperature period. Exposure to 24-h photo-cycles (12 h light/12 h dark, constant ambient temperature) yielded a shorter, more variable interpeak-temperature period of 23 (±0.23) h. CONCLUSIONS: Our results indicate that cycad cone thermogenesis is under circadian clock control and differentially affected by ambient temperature and light cycles. Our data from cycads (an ancient gymnosperm lineage) adds to what little is known about circadian timing in gymnosperms, which have rarely been studied from the circadian perspective.

The ecological importance of the accuracy of environmental temperature measurements.

The implications of logger accuracy and precision are rarely considered prior to their application in many ecological studies. We assessed the accuracy and precision of three temperature data loggers widely used in ecological studies (Hobo®, iButton® and TinyTag®). Accuracy was highest in TinyTags (95% of readings were within 0.23°C of the true temperature) and lowest in HOBOs and iButtons (95% of were readings within 0.43°C and 0.49°C of the true temperature, respectively). The precision (standard deviation of the repeat measurements) was greatest in TinyTags (0.04°C), followed by iButtons (0.17°C) and then HOBOs (0.22°C). As a case study, we then considered how modelled estimates of sea turtle hatchling sex ratios (derived from temperature), could vary as a function of logger accuracy. For example, at 29°C when the mean sex ratio derived was 0.47 female, the sex ratio estimate from a single logger could vary between 0.40 and 0.50 for TinyTags and 0.29 and 0.56 for both HOBOs and iButtons. Our results suggest that these temperature loggers can provide reliable descriptions of sand temperature if they are not over-interpreted. Logger accuracy must be considered in future ecological studies in which temperature thresholds are important.

Spatial Ecology of Asian Water Monitors Adjacent to a Sea Turtle Nesting Beach.

Nest predation is the main cause of hatching failure for many turtle populations. For green turtles (Chelonia mydas) nesting at Chagar Hutang in Redang Island, Malaysia, Asian water monitors (Varanus salvator) are a potential nest predator. However, no studies have documented the space use of this species in coastal habitat adjacent to a sea turtle nesting beach to assess its potential impact on turtle nests. Here, we used Global Positioning System (GPS) data loggers to quantify space use of Asian water monitors in order to establish the extent to which they use sea turtle nesting areas. Asian water monitors had a diurnal activity pattern and spent most of their time in rain forest habitat behind the sea turtle nesting beach. The home range occupied by Asian water monitors varied between 0.015 and 0.198 km2 calculated by the Kernel Brownian Bridge method. The space use patterns of individual Asian water monitors varied between individuals. Two males had relatively small home ranges, whereas one male and the female had a relatively large home range. Because tracked Asian water monitors in this study rarely visited the sea turtle nesting areas, it is probable that only a few individuals are responsible for opening nests.

Thermogenic respiratory processes drive the exponential increase of volatile organic compound emissions in Macrozamia cycad cones.

An important outcome of plant thermogenesis is increased emissions of volatiles that mediate pollinator behaviour. We investigated whether the large increase in emissions, mainly the monoterpene ß-myrcene (>90%), during daily thermogenic events of Macrozamia macleayi and lucida cycad cones are due solely to the influence of high cone temperatures or are, instead, a result of increased respiratory rates during thermogenesis. We concurrently measured temperature, oxygen consumption and ß-myrcene emission profiles during thermogenesis of pollen cones under typical environmental temperatures and during experimental manipulations of cone temperatures and aerobic conditions, all in the dark. The exponential rise in ß-myrcene emissions never occurred without a prior, large increase in respiration, whereas an increase in cone temperature alone did not increase emissions. When respiration during thermogenesis was interrupted by anoxic conditions, ß-myrcene emissions decreased. The increased emission rates are not a result of increased cone temperature per se (through increased enzyme activity or volatilization of stored volatiles) but are dependent on biosynthetic pathways associated with increased respiration during thermogenesis that provide the carbon, energy (ATP) and reducing compounds (NADPH) required for ß-myrcene production through the methylerythritol phosphate (MEP) pathway. These findings establish the significant contribution of respiration to volatile production during thermogenesis.

Synchronous activity lowers the energetic cost of nest escape for sea turtle hatchlings.

A potential advantage of group movement in animals is increased locomotion efficiency. This implies a reduced energetic cost for individuals that occur in larger groups such as herds, flocks and schools. When chelonian hatchlings hatch in the underground nest with finite energy for their post-hatching dispersal phase, they face the challenge of minimizing energetic expenditure while escaping the nest. The term 'social facilitation' has been used to describe the combined digging effort of sea turtle hatchlings during nest escape. Given that in a normal clutch, a substantial part of the energy reserve within the residual yolk is used by hatchlings in the digging out process, a decreased cohort size may reduce the energy reserve available to cross the beach and sustain the initial swimming frenzy. This hypothesis was experimentally tested by varying cohort size in hatchling green turtles (Chelonia mydas) and measuring energy expenditure during the nest escape process using open-flow respirometry. The energetic cost of escaping through 40 cm of sand was calculated to vary between 4.4 and 28.3 kJ per individual, the cost decreasing as the number of individuals in the cohort increased. This represents 11-68% of the energy contained in a hatchling's residual yolk at hatching. The reduced energetic cost associated with large cohorts resulted from both a lower metabolic rate per individual and a shortened nest escape time. We conclude that synchronous digging activity of many hatchlings during nest escape evolved not only to facilitate rapid nest emergence but also to reduce the energetic cost to individuals.

Temperature, field activity and post-feeding metabolic response in the Asian house gecko, Hemidactylus frenatus.

Temperature has significant effects on physiological activities and geographical distribution of ectotherms. The Asian house gecko Hemidactylus frenatus has become one of the most widely distributed reptiles in the world and is an invasive species in Australia. Since being introduced into northern Australia, Asian house geckos have spread rapidly and expanded into south-east Queensland and northern New South Wales. Despite their rapid spread, there have been few studies that address thermal adaptability of this species. In order to understand how temperature might limit the distribution and feeding behavior of H. frenatus we observed gecko foraging activities in the wild over the winter period, measured the temperature at which voluntary feeding ceases, and assessed the effect of temperature (30, 25, 20, and 18 °C) on post-feeding metabolic rate. Resting metabolic rate and post-feeding peak in metabolic rate decreased with low temperature, while the duration of elevated metabolic rate after feeding increased at lower temperature. The SDA coefficient (a ratio of the energy expended due to the post-feeding rise in metabolic rate to the energy contained within the meal) did not change systematically with ambient temperature. Field observations and voluntary feeding experiments showed that H. frenatus stop feeding when ambient temperature drops below 17 °C, so that persistent night time temperatures below 17 °C may be limiting the distribution of this species.

How well do embryo development rate models derived from laboratory data predict embryo development in sea turtle nests?

Development rate of ectothermic animals varies with temperature. Here we use data derived from laboratory constant temperature incubation experiments to formulate development rate models that can be used to model embryonic development rate in sea turtle nests. We then use a novel method for detecting the time of hatching to measure the in situ incubation period of sea turtle clutches to test the accuracy of our models in predicting the incubation period from nest temperature traces. We found that all our models overestimated the incubation period. We hypothesize three possible explanations which are not mutually exclusive for the mismatch between our modeling and empirically measured in situ incubation period: (1) a difference in the way the incubation period is calculated in laboratory data and in our field nests, (2) inaccuracies in the assumptions made by our models at high incubation temperatures where there is no empirical laboratory data, and (3) a tendency for development rate in laboratory experiments to be progressively slower as temperature decreases compared with in situ incubation.

Locomotor activity during the frenzy swim: analysing early swimming behaviour in hatchling sea turtles.

Swimming effort of hatchling sea turtles varies across species. In this study we analysed how swim thrust is produced in terms of power stroke rate, mean maximum thrust per power stroke and percentage of time spent power stroking throughout the first 18 h of swimming after entering the water, in both loggerhead and flatback turtle hatchlings and compared this with previous data from green turtle hatchlings. Loggerhead and green turtle hatchlings had similar power stroke rates and percentage of time spent power stroking throughout the trial, although mean maximum thrust was always significantly higher in green hatchlings, making them the most vigorous swimmers in our three-species comparison. Flatback hatchlings, however, were different from the other two species, with overall lower values in all three swimming variables. Their swimming effort dropped significantly during the first 2 h and kept decreasing significantly until the end of the trial at 18 h. These results support the hypothesis that ecological factors mould the swimming behaviour of hatchling sea turtles, with predator pressure being important in determining the strategy used to swim offshore. Loggerhead and green turtle hatchlings seem to adopt an intensely vigorous and energetically costly frenzy swim that would quickly take them offshore into the open ocean in order to reduce their exposure to near-shore aquatic predators. Flatback hatchlings, however, are restricted in geographic distribution and remain within the continental shelf region where predator pressure is probably relatively constant. For this reason, flatback hatchlings might use only part of their energy reserves during a less vigorous frenzy phase, with lower overall energy expenditure during the first day compared with loggerhead and green turtle hatchlings.

Influence of short-term temperature drops on sex-determination in sea turtles.

All sea turtles exhibit temperature-dependent sex-determination, where warmer temperatures produce mostly females and cooler temperatures produce mostly males. As global temperatures continue to rise, sea turtle sex-ratios are expected to become increasingly female-biased, threatening the long-term viability of many populations. Nest temperatures are dependent on sand temperature, and heavy rainfall events reduce sand temperatures for a brief period. However, it is unknown whether these short-term temperature drops are large and long enough to produce male hatchlings. To discover if short-term temperature drops within the sex-determining period can lead to male hatchling production, we exposed green and loggerhead turtle eggs to short-term temperature drops conducted in constant temperature rooms. We dropped incubation temperature at four different times during the sex-determining period for a duration of either 3 or 7 days to mimic short-term drops in temperature caused by heavy rainfall in nature. Some male hatchlings were produced when exposed to temperature drops for as little as 3 days, but the majority of male production occurred when eggs were exposed to 7 days of lowered temperature. More male hatchlings were produced when the temperature drop occurred during the middle of the sex-determining period in green turtles, and the beginning and end of the sex-determining period in loggerhead turtles. Inter-clutch variation was evident in the proportion of male hatchlings produced, indicating that maternal and or genetic factors influence male hatchling production. Our findings have management implications for the long-term preservation of sea turtles on beaches that exhibit strongly female-biased hatchling sex-ratios.

Extreme rainfall events and cooling of sea turtle clutches: Implications in the face of climate warming.

Understanding how climate change impacts species and ecosystems is integral to conservation. When studying impacts of climate change, warming temperatures are a research focus, with much less attention given to extreme weather events and their impacts. Here, we show how localized, extreme rainfall events can have a major impact on a species that is endangered in many parts of its range. We report incubation temperatures from the world's largest green sea turtle rookery, during a breeding season when two extreme rainfall events occurred. Rainfall caused nest temperatures to drop suddenly and the maximum drop in temperature for each rain-induced cooling averaged 3.6°C (n = 79 nests, min = 1.0°C, max = 7.4°C). Since green sea turtles have temperature-dependent sex determination, with low incubation temperatures producing males, such major rainfall events may have a masculinization effect on primary sex ratios. Therefore, in some cases, extreme rainfall events may provide a "get-out-of-jail-free card" to avoid complete feminization of turtle populations as climate warming continues.

Temperature-dependent sex-biased embryo mortality in a bird.

Sex ratios have important evolutionary consequences and are often biased by environmental factors. The effect of developmental temperature on offspring sex ratios has been widely documented across a diverse range of taxa but has rarely been investigated in birds and mammals. However, recent field observations and artificial incubation experiments have demonstrated that the hatching sex ratio of a megapode, the Australian brush-turkey (Alectura lathami), varied with incubation temperature; more females hatched at high incubation temperatures and more males hatched at low temperatures. Here, we investigated the causes of this temperature-dependent sex-biasing system. Molecular sexing of chicks and embryos confirmed that male embryo mortality was greater at high temperatures while female embryo mortality is greater at low temperatures, with mortality in both sexes similar at intermediate incubation temperatures. Temperature-dependent sex-biased embryo mortality represents a novel mechanism of altering sex ratios in birds. This novel mechanism, coupled with the unique breeding biology of the brush-turkey, offers a potentially unparalleled opportunity in which to investigate sex allocation theory in birds.

Incubation temperature induced phenotypic plasticity in oviparous reptiles: Where to next?

It is now undisputable that incubation temperature induces different phenotypes (sex, body size, body shape, behavior, and locomotion performance) in many if not most oviparous reptiles. These incubation temperature induced differences in phenotype are assumed to result in differential fitness among hatchlings and therefore to play an important role in recruitment of hatchlings and persistence of reptile populations. However, the role of incubation temperature induced differences in hatchling phenotypes in determining hatchling fitness is still under explored and needs more empirical study. This information is especially needed when making predictions on how climate change and its associated nest warming may affect long term persistence of oviparous reptile populations. Curiously, the ontogenetic and physiological mechanisms responsible for incubation temperature induced differences in hatchling reptile locomotion performance are still unknown. In this article, I review the literature on incubation temperature induced differences in hatchling locomotion performance and summarize what is known about this phenomenon and its influence on hatchling fitness. I discuss how the anticipated detrimental effects on hatchling locomotion performance caused by increased nest temperature associated with climate warming could be ameliorated. I also explore the most likely physiological mechanisms underlying incubation temperature induced differences in hatchling locomotion performance and how these mechanisms might be induced. Finally, I highlight current knowledge gaps in our understanding of incubation temperature induced phenotypic plasticity and suggest directions for future research.

Temperature and the energetics of development in the house cricket (Acheta domesticus).

The influence of rearing temperature on the energetics of development was investigated in house crickets (Acheta domesticus). Crickets raised at 25 degrees C grew slower (0.51 mg d(-1), dry mass basis) and took longer to develop (119 d) but obtained a greater adult body mass (61 mg, dry mass) than crickets reared at 28 degrees C (0.99 mg d(-1), 49 d, 48 mg). Total metabolic energy consumed during development at 25 degrees C (1351 J) was twice that at 28 degrees C (580 J) primarily because of the longer development period, and as a consequence the specific net cost of growth was much greater for crickets reared at 25 degrees C (22.1 kJ g(-1)) than 28 degrees C (11.9 kJ g(-1)).

Influence of incubation temperature on sea turtle hatchling quality.

Since the 1980s it has been known that incubation temperature influences the sex ratio of sea turtle hatchlings emerging from their nests, and there has been much speculation on how global climate change might threaten sea turtle populations by raising nest temperatures and causing highly female-biased hatchling sex ratios. More recently, studies have indicated that incubation temperature can also influence the size and locomotor performance of sea turtle hatchlings. Here I review recent studies that have explored the influence of incubation temperature on sea turtle hatchling quality in terms of hatchling morphology and locomotor performance. I also discuss the likely underlying mechanisms responsible for incubation temperature-induced differences in hatchling locomotor performance, and how an increase in nest temperature associated with global warming might affect recruitment of sea turtle hatchlings.

Who are the important predators of sea turtle nests at Wreck Rock beach?

Excessive sea turtle nest predation is a problem for conservation management of sea turtle populations. This study assessed predation on nests of the endangered loggerhead sea turtle (Caretta caretta) at Wreck Rock beach adjacent to Deepwater National Park in Southeast Queensland, Australia after a control program for feral foxes was instigated. The presence of predators on the nesting dune was evaluated by tracking plots (2 × 1 m) every 100 m along the dune front. There were 21 (2014-2015) and 41 (2015-2016) plots established along the dune, and these were monitored for predator tracks daily over three consecutive months in both nesting seasons. Predator activities at nests were also recorded by the presence of tracks on top of nests until hatchlings emerged. In addition, camera traps were set to record the predator activity around selected nests. The tracks of the fox (Vulpes vulpes) and goanna (Varanus spp) were found on tracking plots. Tracking plots, nest tracks and camera traps indicated goanna abundance varied strongly between years. Goannas were widely distributed along the beach and had a Passive Activity Index (PAI) (0.31 in 2014-2015 and 0.16 in 2015-2016) approximately seven times higher than that of foxes (PAI 0.04 in 2014-2015 and 0.02 in 2015-2016). Five hundred and twenty goanna nest visitation events were recorded by tracks but no fox tracks were found at turtle nests. Camera trap data indicated that yellow-spotted goannas (Varanus panoptes) appeared at loggerhead turtle nests more frequently than lace monitors (V. varius) did, and further that lace monitors only predated nests previously opened by yellow-spotted goannas. No foxes were recorded at nests with camera traps. This study suggests that large male yellow-spotted goannas are the major predator of sea turtle nests at the Wreck Rock beach nesting aggregation and that goanna activity varies between years.

Influence of incubation temperature on hatchling phenotype in reptiles.

Incubation temperature influences hatchling phenotypes such as sex, size, shape, color, behavior, and locomotor performance in many reptiles, and there is growing concern that global warming might adversely affect reptile populations by altering frequencies of hatchling phenotypes. Here I overview a recent theoretical model used to predict hatchling sex of reptiles with temperature-dependent sex determination. This model predicts that sex ratios will be fairly robust to moderate global warming as long as eggs experience substantial daily cyclic fluctuations in incubation temperatures so that embryos are exposed to temperatures that inhibit embryonic development for part of the day. I also review studies that examine the influence of incubation temperature on posthatch locomotion performance and growth because these are the traits that are likely to have the greatest effect on hatchling fitness. The majority of these studies used artificial constant-temperature incubation, but some have addressed fluctuating incubation temperature regimes. Although the number of studies is small, it appears that fluctuating temperatures may enhance hatchling locomotor performance. This finding should not be surprising, given that the majority of natural reptile nests are relatively shallow and therefore experience daily fluctuations in incubation temperature.

Incubation temperature, morphology and performance in loggerhead (Caretta caretta) turtle hatchlings from Mon Repos, Queensland, Australia.

Marine turtles are vulnerable to climate change because their life history and reproduction are tied to environmental temperatures. The egg incubation stage is arguably the most vulnerable stage, because marine turtle eggs require a narrow range of temperatures for successful incubation. Additionally, incubation temperature affects sex, emergence success, morphology and locomotor performance of hatchlings. Hatchlings often experience high rates of predation in the first few hours of their life, and increased size or locomotor ability may improve their chances of survival. Between 2010 and 2013 we monitored the temperature of loggerhead (Caretta caretta; Linnaeus 1758) turtle nests at Mon Repos Rookery, and used these data to calculate a mean three day maximum temperature (T3dm) for each nest. We calculated the hatching and emergence success for each nest, then measured the mass, size and locomotor performance of hatchlings that emerged from those nests. Nests with a T3dm greater than 34°C experienced a lower emergence success and produced smaller hatchlings than nests with a T3dm lower than 34°C. Hatchlings from nests with a T3dm below 34°C performed better in crawling and swimming trials than hatchlings from nests with a T3dm above 34°C. Thus even non-lethal increases in global temperatures have the potential to detrimentally affect fitness and survival of marine turtle hatchlings.

Physiological responses to prolonged aquatic hypoxia in the Queensland lungfish Neoceratodus forsteri.

The effects of moderate and severe hypoxia on air breathing frequency and respiratory properties of the blood of the Queensland (Australian) lungfish Neoceratodus forsteri were measured in fish exposed to these conditions for 14-22 days at 20 degrees C. Haemoglobin oxygen affinity increased after exposure to moderate hypoxia (PW(O(2)) = 60 mmHg), but did not increase further after exposure to severe hypoxia (PW(O(2)) = 40 mmHg). The P(50) of whole blood (20 degrees C, P(CO(2)) = 16.0 mmHg) fell from 22.0 +/- 1.5 mmHg in normoxic conditions to 19.0 +/- 1.0 mmHg in hypoxic conditions. Under both moderate and severe hypoxia, haematocrit, haemoglobin, blood lactate, and erythrocyte phosphate concentrations did not differ from normoxic values. The observed increase in haemoglobin oxygen affinity in response to aquatic hypoxia is typical of compensatory responses seen in obligate water breathers, but smaller. This suggests that the capacity of lungfish to respond to hypoxia by breathing air removes the necessity for further left-shifting of the oxygen equilibrium curve.

Kinematics of swimming and thrust production during powerstroking bouts of the swim frenzy in green turtle hatchlings.

Hatchling sea turtles emerge from nests, crawl down the beach and enter the sea where they typically enter a stereotypical hyperactive swimming frenzy. During this swim the front flippers are moved up and down in a flapping motion and are the primary source of thrust production. I used high-speed video linked with simultaneous measurement of thrust production in tethered hatchlings, along with high-speed video of free swimming hatchlings swimming at different water speeds in a swim flume to investigate the links between kinematics of front flipper movement, thrust production and swimming speed. In particular I tested the hypotheses that (1) increased swimming speed is achieved through an increased stroke rate; (2) force produced per stroke is proportional to stroke amplitude, (3) that forward thrust is produced during both the down and up phases of stroking; and (4) that peak thrust is produced towards the end of the downstroke cycle. Front flipper stroke rate was independent of water speed refuting the hypothesis that swimming speed is increased by increasing stroke rate. Instead differences in swimming speed were caused by a combination of varying flipper amplitude and the proportion of time spent powerstroking. Peak thrust produced per stroke varied within and between bouts of powerstroking, and these peaks in thrust were correlated with both flipper amplitude and flipper angular momentum during the downstroke supporting the hypothesis that stroke force is a function of stroke amplitude. Two distinct thrust production patterns were identified, monophasic in which a single peak in thrust was recorded during the later stages of the downstroke, and biphasic in which a small peak in thrust was recorded at the very end of the upstroke and this followed by a large peak in thrust during the later stages of the downstroke. The biphasic cycle occurs in ∼20% of hatchlings when they first started swimming, but disappeared after one to two hours of swimming. The hypothesis that forward thrust is produced during both the up and down stroke was only supported relatively rarely in hatchlings that exhibited the diphasic cycle, the majority of time forward thrust was only produced during the downstroke phase. The hypothesis that peak forward thrust is produced during the end of the downstroke was supported in both the monophasic and biphasic thrust producing stroke cycles.