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.     

Bet hedging in a warming ocean: predictability of maternal environment shapes offspring size variation in marine sticklebacks

Bet hedging at reproduction is expected to evolve when mothers are exposed to unpredictable cues for future environmental conditions, whereas transgenerational plasticity (TGP) should be favoured when cues reliably predict the environment offspring will experience. Since climate predictions forecast an increase in both temperature and climate variability, both TGP and bet hedging are likely to become important strategies to mediate climate change effects. Here, the potential to produce variably sized offspring in both warming and unpredictable environments was tested by investigating whether stickleback (Gasterosteus aculeatus) mothers adjusted mean offspring size and within‐clutch variation in offspring size in response to experimental manipulation of maternal thermal environment and predictability (alternating between ambient and elevated water temperatures). Reproductive output traits of F1 females were influenced by both temperature and environmental predictability. Mothers that developed at ambient temperature (17 °C) produced larger, but fewer eggs than mothers that developed at elevated temperature (21 °C), implying selection for different‐sized offspring in different environments. Mothers in unpredictable environments had smaller mean egg sizes and tended to have greater within‐female egg size variability, especially at 21 °C, suggesting that mothers may have dynamically modified the variance in offspring size to spread the risk of incorrectly predicting future environmental conditions. Both TGP and diversification influenced F2 offspring body size. F2 offspring reared at 21 °C had larger mean body sizes if their mother developed at 21 °C, but this TGP benefit was not present for offspring of 17 °C mothers reared at 17 °C, indicating that maternal TGP will be highly relevant for ocean warming scenarios in this system. Offspring of variable environment mothers were smaller but more variable in size than offspring from constant environment mothers, particularly at 21 °C. In summary, stickleback mothers may have used both TGP and diversified bet‐hedging strategies to cope with the dual stress of ocean warming and environmental uncertainty.     

Sand and nest temperatures and an estimate of hatchling sex ratio from the Heron Island green turtle (Chelonia mydas) rookery, Southern Great Barrier Reef

Sand and nest temperatures were monitored during the 2002–2003 nesting season of the green turtle, Chelonia mydas, at Heron Island, Great Barrier Reef, Australia. Sand temperatures increased from ∼ 24°C early in the season to 27–29°C in the middle, before decreasing again. Beach orientation affected sand temperature at nest depth throughout the season; the north facing beach remained 0.7°C warmer than the east, which was 0.9°C warmer than the south, but monitored nest temperatures were similar across all beaches. Sand temperature at 100 cm depth was cooler than at 40 cm early in the season, but this reversed at the end. Nest temperatures increased 2–4°C above sand temperatures during the later half of incubation due to metabolic heating. Hatchling sex ratio inferred from nest temperature profiles indicated a strong female bias.     

Adapt,move or die – how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade, more than 365 tropical stenothermal fish species have been documented moving poleward, away from ocean warming hotspots where temperatures 2–3 °C above long‐term annual means can compromise critical physiological processes. We examined the capacity of a model species – a thermally sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least 6 weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end‐of‐century predicted temperatures (i.e. 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long‐term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating poleward migration of species.     

Thermosensitive period of sex determination in the coral-reef damselfish <Emphasis Type="Italic">Acanthochromis polyacanthus</Emphasis> and the implications of projected ocean warming

Higher temperatures associated with climate change have the potential to significantly alter the population sex ratio of species with temperature-dependent sex determination. Whether or not elevated temperature affects sex determination depends on both the absolute temperature experienced and the stage of development at which the thermal conditions occur. We explored the importance of exposure timing during early development in the coral reef fish, Acanthochromis polyacanthus, by increasing water temperature 1.5 or 3 °C above the summer average (28.5 °C) at different stages of development. We also measured the effect of treatment temperature on fish size and condition, in order to gauge how the thermal threshold for sex-ratio bias may compare with other commonly considered physiological metrics. Increasing grow-out temperature from 28.5 to 30 °C had no effect on the sex ratio of offspring, whereas an increase to 31.5 °C (+3 °C) produced a strong male bias (average ~90%). The thermosensitive period for this species lasted between 25 and 60 d post hatching, with the bias in sex ratio greater the earlier that fish experienced warm conditions. Temperatures high enough to bias the sex ratio are likely to be seen first during late summer (January and February) and would affect clutches produced late in the breeding season. There was no change to fish condition in response to temperature; however, the two higher temperature treatments produced significantly smaller fish at sampling. Clutches produced early in the season could buffer the population from a skewed sex ratio, as their development will remain below the thermal threshold; however, continued ocean warming could mean that clutches produced earlier in the breeding season would also be affected in the longer term. A skewed sex ratio could be detrimental to population viability by reducing the number of females in the breeding population.     

Thermally induced plasticity of body shape in adult zebrafish Danio rerio (Hamilton, 1822)

We examined the effect of temperature during the early development on the phenotypic plasticity of Danio rerio. The effect of temperature was examined during two different early developmental periods of 280°d (the product of days × temperature) each, 28‐308°d or 280‐560°d, by subjecting the experimental populations to three different water temperatures (22°C, 28°C, and 32°C). Before and after the end of the 280°d period of the different thermal exposure, all populations were cultured in standard temperature (28°C). Five to 10 months after exposure to the different thermal regimes, the body shape of the adults was analyzed by geometric morphometrics. In both ontogenetic windows and experimental repetitions, the results showed that developmental temperature and sex significantly affected the body shape of adult zebrafish. Thermally induced shape variation discriminated the fish that developed at 22°C from those developed at 28°C–32°C. In the early developmental period (DP1, 28–308°d postfertilization), dorsal, anal, and caudal fin structures differed between the animals that developed at 22°C and 28°C–32°C. In the later developmental period (DP2, 280–560°d postfertilization), caudal, anal, pectoral, and pelvic fins, as well as the gill cover and lower jaw, were affected when animals developed at different temperatures. These results show that thermal history during a short period of embryonic and larval life affects the body form of adult zebrafish with potentially functional consequences. Based on previous data on the effects of temperature on fish development, we suggest thermally induced muscle and bone remodelling as possible mechanism underlying the observed plasticity. J. Morphol., 2010. © 2010 Wiley‐Liss, Inc.     

Longevity and resistance to cold stress in cold‐stress selected lines and their controls in Drosophila melanogaster

Thermal environments can influence many fitness‐related traits including life span. Here, we assess whether longevity in Drosophila melanogaster can experimentally evolve as a correlated response to cold‐stress selection, and whether genotype‐by‐temperature and sex‐by‐temperature interactions are significant components of variation in life span. Three replicated S lines were cold‐stress selected and compared with their respective unselected controls (Clines) in the 16^th generation of thermal selection. Cold‐stress resistance exhibited a substantial direct response to selection, and also showed a significant interaction between sex and type of line. Mean longevity exhibited a significant interaction between adult test temperature (14 and 25 °C) and line (with suggestive evidence for increased longevity of S lines when tested at 14 °C), but there was no evidence for increased longevity in S lines at normal temperatures (i.e. 25 °C). Another temperature‐dependent effect was sex‐specific, with males being the longer lived sex at 25 °C but the less long‐lived sex at 14 °C. Additionally, we tested in an exploratory way the relationship between longevity and cold‐stress resistance by also measuring resistance to a prefreezing temperature before and after one generation of longevity selection at 14 °C (selection intensity, i = 1.47 for S lines, and 1.42 for C lines). In this longevity selection, we found that cold‐stress resistance increased by about 6% in S lines and 18% in C lines. However, taken together, the results indicate no simple relationship between longevity and cold‐stress resistance, with genotype‐by‐sex interactions in both traits. Temperature dependent interaction in longevity is apparent between S and C lines, and sex‐specific variation in mean longevity also depends on temperature.     

Growth and physiological responses in largemouth bass populations to environmental warming: Effects of inhabiting chronically heated environments

Ectotherms are susceptible to increasing environmental temperatures associated with anthropogenic warming. Supra-optimum temperatures lead to declining aerobic capacity and can increase exposure to lethal temperatures, resulting in reduced performance. Although the capacity of phenotypic plasticity to minimize the effects of temperature on physiological processes is well studied, evidence of generational changes (e.g. transgenerational plasticity and rapid adaptation) in response to environmental warming is limited in natural populations. We investigated metabolism, growth, and thermal tolerance of largemouth bass (Micropterus salmoides) populations inhabiting thermally altered lakes (i.e. power plant cooling lakes) which have year-round elevated temperature regimes and exhibit supra-optimum temperatures on a yearly basis, and compared these traits with those in largemouth bass populations from ambient lakes. Largemouth bass from ambient and heated groups (n = 3 populations per group) were spawned in an ambient, common garden pond environment, then acclimated to either a normal summertime temperature (24 °C) or a supra-optimum temperature (30 °C). Fish from heated populations had significant reductions in the resting metabolic rate at both temperatures and markedly increased growth rates at 30 °C. By comparing pond-raised fish to fish removed directly from heated lakes, we showed that developmental plasticity played little role in establishing the metabolic rate. A lower resting metabolic rate contributed to an increase in the conversion efficiency of food to biomass of largemouth bass from heated lakes, regardless of temperature. Despite inhabiting heated lakes for many decades, neither critical thermal maximum nor minimum were altered in heated populations when raised in a common garden environment. These results suggest that largemouth bass can lessen sub-lethal effects of warming by altering physiological processes to reduce the impact of warming on aerobic scope and that these changes are generationally transient, but changes in maximum thermal tolerance in response to warming is limited to phenotypic plasticity.     

Thermal response of demersal and pelagic juvenile fishes from the surf zone during a heat‐wave simulation

Experimental measurements were collected in the laboratory to evaluate the maximum thermal limit and thermal plasticity of Neotropical juvenile fish with different life habitats (demersal and pelagic) from surf zone in response to a “heat‐wave experiment”. Trials were conducted using two temperature acclimations (T_a), including the current average temperature of Southeastern Brazil (T_a: 14 days at 25°C) and the “heat‐wave experiment” (T_a: 14 days at 30°C), simulating a heat‐wave event that occurs when the daily maximum temperature of more than five consecutive days exceeds the average maximum temperature by 5°C. Typical species of the surf zone were used: the demersal White sea catfish (Genidens barbus) and Gulf kingcroaker (Menticirrhus littoralis), and the pelagic fishes Great pompano (Trachinotus goodei) and Long‐fin mullet (Mugil brevirostris). The thermal range and plasticity values for the both life‐habitats species were verified through current and heat‐wave acclimation. The thermal tolerance at high temperatures (CT_max) of these species differed between T_a, habitat and species. Fish showed a species‐specific response to temperature increase, regardless of their habitat even under similar abiotic conditions. However, at the heat‐wave simulation, the demersal fish presented a greater thermal plasticity in relation to the pelagic fish. Despite the higher thermal tolerance when exposed to heat‐wave simulation, all fish species displayed a lower thermal edge safety that is markedly close to their maximum thermal limits.     

Genetic differences and phenotypic plasticity in body size between high- and low-altitude populations of the ground beetle Carabus tosanus

The body size of a univoltine carabid beetle Carabus tosanus on Shikoku Island, Japan, was clearly smaller in higher‐altitude populations (subspecies), which possibly represents incipient speciation. To explore the determinants of altitudinal differences in body size in this species, we studied the degree of phenotypic plasticity by conducting rearing experiments at two constant temperatures and examined genetic differences through interpopulation crosses. At 15 °C, C. tosanus had a longer developmental period and a shorter adult body than at 20 °C. Nevertheless, variation in body size due to temperature effects (phenotypic plasticity) was small compared to the interpopulation differences, which suggests substantial genetic differences between populations (subspecies) at different altitudes. In F₁ offspring from crosses between a low‐altitude (subspecies tosanus) and a high‐altitude population (subspecies ishizuchianus), adult body length was affected by the genotypes of both parents, with an interaction effect of parental genotype and offspring sex. Further analyses revealed that adult body length was affected by sex‐linked factors in addition to autosomal factors. These genetic differences in body size may have resulted from adaptations to different altitudes and may be important for the process of incipient speciation because body size differences could contribute to premating reproductive isolation.     

Elevated temperature reduces survivorship and settlement of the larvae of the Caribbean scleractinian coral, Favia?fragum (Esper)

The effect of elevated seawater temperatures, such as those plaguing tropical seas during the summers of anomalously warm years, on early life stages of reef corals remains poorly studied. To redress this situation, survivorship of larvae of the brooding coral, Favia fragum, was studied in the laboratory, using both short term (48 h) and long term (156–191 h) exposures to 28, 29, and 31°C. Ability to settle when presented with induction substrates and survival after settlement, at the same exposure temperature and after reciprocal transfers to the other experimental temperatures, were also measured. No significant effect of temperature on survivorship was detected after 48 h of exposure, but larvae incubated for 156 h at the highest temperature (31°C) exhibited a 13% reduced survivorship compared to larvae at 28°C. Induction of settlement further increased mortality at the highest temperature (31°C); survivorship after settlement at 31°C was 27% lower than when larvae were simply maintained at the elevated temperature. These results indicate that elevated temperatures are more detrimental to coral larvae undergoing the developmentally complex settlement process than to the swimming planula stage. This may bode poorly for Caribbean corals with late summer reproductive seasons. Communicated by Ecology Editor Prof. Peter Mumby     

A potential tool to mitigate the impacts of climate change to the caribbean leatherback sea turtle

It is now well understood that climate change has the potential to dramatically affect biodiversity, with effects on spatio‐temporal distribution patterns, trophic relationships and survivorship. In the marine turtles, sex is determined by incubation temperature, such that warming temperatures could lead to a higher production of female hatchlings. By measuring nest temperature, and using a model to relate the incubation temperature to sex ratio, we estimate that Caribbean Colombian leatherback sea turtles currently produce approximately 92% female hatchlings. We modelled the relationship between incubation, sand and air temperature, and under all future climate change scenarios (0.4–6.0 °C warming over the next 100 years), complete feminization could occur, as soon as the next decade. However, male producing refugia exist in the periphery of smaller nests (0.7 °C cooler at the bottom than at the centre), within beaches (0.3 °C cooler in the vegetation line and inter‐tidal zone) and between beaches (0.4 °C higher on dark beaches), and these natural refugia could be assigned preferential conservation status. However, there exists a need to develop strategies that may ameliorate deleterious effects of climate‐induced temperature changes in the future. We experimentally shaded clutches using screening material, and found that it was effective in reducing nest temperature, producing a higher proportion of male hatchlings, without compromising the fitness or hatching success. Artificial shade in hatcheries is a very useful and simple tool in years or periods of high environmental temperatures. Nevertheless, this is only an emergency response to the severe impacts that will eventually have to be reversed if we are to guarantee the stability of the populations.     

Beneficial developmental acclimation in reproductive performance under cold but not heat stress

Thermal plasticity can help organisms coping with climate change. In this study, we analyse how laboratory populations of the ectotherm species Drosophila subobscura, originally from two distinct latitudes and evolving for several generations in a stable thermal environment (18 °C), respond plastically to new thermal challenges. We measured adult performance (fecundity traits as a fitness proxy) of the experimental populations when exposed to five thermal regimes, three with the same temperature during development and adulthood (15-15 °C, 18-18 °C, 25-25 °C), and two where flies developed at 18 °C and were exposed, during adulthood, to either 15 °C or 25 °C. Here, we test whether (1) flies undergo stress at the two more extreme temperatures; (2) development at a given temperature enhances adult performance at such temperature (i.e. acclimation), and (3) populations with different biogeographical history show plasticity differences. Our findings show (1) an optimal performance at 18 °C only if flies were subjected to the same temperature as juveniles and adults; (2) the occurrence of developmental acclimation at lower temperatures; (3) detrimental effects of higher developmental temperature on adult performance; and (4) a minor impact of historical background on thermal response. Our study indicates that thermal plasticity during development may have a limited role in helping adults cope with warmer - though not colder - temperatures, with a potential negative impact on population persistence under climate change. It also emphasizes the importance of analysing the impact of temperature on all stages of the life cycle to better characterize the thermal limits.     

The progeny production of a hymenopterous parasitoid,Apanteles sp. groupultor,as affected by temperature

Adults of the parasiteApanteles sp. groupultor were held unter constant temperatures (15, 20, 26, 30°C) each within ±1°C. Total progeny production was significantly greater at 26°C, averaging 85 per female and decreased at 15°C and 30°C. Mating behavior showed that both sexes were a polygamous. The range of constant temperature did not greatly alter the progeny sex ratio when female parent had been mated. At 15°C, male activity was adversely affected when both sexes were exposed to it without previous mating, resulting in a higher number of male progeny. A temperature of 26°C was the most appropriate for normal sex ratio.      

Effects of global warming on sex ratios in fishes

In fishes, sex is determined by genetics, the environment or an interaction of both. Temperature is among the most important environmental factors that can affect sex determination. As a consequence, changes in temperature at critical developmental stages can induce biases in primary sex ratios in some species. However, early sex ratios can also be biased by sex-specific tolerances to environmental stresses that may, in some cases, be amplified by changes in water temperature. Sex-specific reactions to environmental stress have been observed at early larval stages before gonad formation starts. It is therefore necessary to distinguish between temperature effects on sex determination, generally acting through the stress axis or epigenetic mechanisms, and temperature effects on sex-specific mortality. Both are likely to affect sex ratios and hence population dynamics. Moreover, in cases where temperature effects on sex determination lead to genotype–phenotype mismatches, long-term effects on population dynamics are possible, for example temperature-induced masculinization potentially leading to the loss of Y chromosomes or feminization to male-biased operational sex ratios in future generations. To date, most studies under controlled conditions conclude that if temperature affects sex ratios, elevated temperatures mostly lead to a male bias. The few studies that have been performed on wild populations seem to confirm this general trend. Recent findings suggest that transgenerational plasticity could mitigate the effects of warming on sex ratios in some populations.     

Influence of temperature and photoperiod on embryonic development in the dragonfly Sympetrum striolatum (Odonata: Libellulidae)

Temperature and photoperiod play major roles in insect ecology. Many insect species have fixed degree‐days for embryogenesis, with minimum and maximum temperature thresholds for egg and larval development and hatching. Often, photoperiodic changes trigger the transfer into the next life‐cycle stadium. However, it is not known whether this distinct pattern also exist in a species with a high level of phenotypic plasticity in life‐history traits. In the present study, eggs of the dragonfly Sympetrum striolatum Charpentier (Odonata: Libellulidae) are reared under different constant and fluctuating temperatures and photoperiodic conditions in several laboratory and field experiments. In general, and as expected, higher temperatures cause faster egg development. However, no general temperature or light‐days for eyespot development and hatching are found. The minimum temperature thresholds are distinguished for survival (2 °C), embryogenesis (6 °C) and larval hatching (above 6 °C). Low winter temperatures synchronize hatching. Above 36 °C, no eyespots are visible and no larvae hatch. In laboratory experiments, light is neither necessary for eyespot development, nor for hatching. By contrast to the laboratory experiments, the field experiment show that naturally changing temperature and photoperiod play a significant role in the seasonal regulation of embryonic development. The post‐eyespot development is more variable and influenced by temperature and photoperiod than the pre‐eyespot development. This developmental plasticity at the end of the embryogenesis might be a general pattern in the Libellulidae, helping them to cope with variation in environmental conditions.     

Effect of temperature on immature development and longevity of two introduced opiine parasitoids on Bactrocera invadens

Temperature‐dependent development, parasitism and longevity of the braconid parasitoids, Fopius arisanus Sonan and Diachasmimorpha longicaudata Ashmed on Bactorcera invadens Drew Tsuruta & White, was evaluated across five constant temperatures (15, 20, 25, 30 and 35°C). Developmental rate decreased linearly with increasing temperature for both the parasitoid species. Linear and Brière‐2 nonlinear models were used to determine the lower temperature threshold at which the developmental rate (1/D) approached zero. For F. arisanus, lower thresholds to complete development estimated with the linear and nonlinear models were 10.1 and 6.9°C, respectively. The total degree‐days (DD) required to complete the development estimated by the linear model for F. arisanus was 360. In D. longicaudata, the linear and nonlinear models estimated lower thresholds of 10.4 and 7.3°C, respectively, and the total DD estimated was 282. In F. arisanus, percentage parasitism differed significantly across all temperatures tested and was highest at 25°C (71.1 ± 2.5) and lowest at 15°C (46.4 ± 1.4). Parasitoid progeny sex ratio was female biased at all temperatures except at 20°C. In D. longicaudata, percentage parasitism was highest at 20°C (52.2 ± 4.0) and lowest at 15°C (27.7 ± 2.5). Parasitoid progeny sex ratio was female biased and similar for all temperatures. Adult longevity of both parasitoids was shortest at 35°C and longest at 15°C, and females lived significantly longer than males at all temperatures tested. Our findings provide some guidance for future mass rearing and field releases of the two parasitoids for the management of B. invadens in Africa.