Turtle embryos move to optimal thermal environments within the egg

A recent study demonstrated that the embryos of soft-shelled turtles can reposition themselves within their eggs to exploit locally warm conditions. In this paper, we ask whether turtle embryos actively seek out optimal thermal environments for their development, as do post-hatching individuals. Specifically, (i) do reptile embryos move away from dangerously high temperatures as well as towards warm temperatures? and (ii) is such embryonic movement due to active thermoregulation, or (more simply) to passive embryonic repositioning caused by local heat-induced changes in viscosity of fluids within the egg? Our experiments with an emydid turtle (Chinemys reevesii) show that embryos avoid dangerously high temperatures by moving to cooler regions of the egg. The repositioning of embryos is an active rather than passive process: live embryos move towards a heat source, whereas dead ones do not. Overall, our results suggest that behavioural thermoregulation by turtle embryos is genuinely analogous to the thermoregulatory behaviour exhibited by post-hatching ectotherms.     

A non-invasive method for quantifying patterns of torpor and activity under semi-natural conditions

Understanding thermal biology in heterothermic endotherms requires that we accurately quantify temporal patterns of torpor use and activity. In many studies this is done using open-flow respirometry or implanted temperature sensitive transmitters. Here we report a method to quantify torpor and activity in cavity living endotherms that does not require surgery or confinement in metabolic chambers. We used temperature dataloggers affixed inside nests to record nest temperatures (T_nest) as a proxy for body temperature. We constructed nests so that animals were in direct contact with dataloggers while at rest. Passive infrared motion detectors were used to determine when animals were active in their cages outside nests. We confirmed that the approach accurately quantifies torpor patterns using open-flow respirometry. This method may prove useful in studies addressing temporal patterns of torpor use under semi-natural conditions because it results in little disruption to animals.     

Some aspects of the metabolism of hibernating and recently aroused common dormouse Muscardinus avellanarius L. (Rodentia,Gliridae)

Summary A dormouse found in hibernation in its winter nest on January 26 was studied continously from February 5 until May 11 by recording ambient temperature, temperatures inside the nest ball and 5 cm from it, and by recording any possible motor activity. The first emergence from hibernaculum occurred on April 3 after which the animal was active each day with the exception of April 11, 13 and 14. Activity mainly occurred during evening and night hours and lasted on average 4 hrs (2–8 hrs) per day. Outside periods of activity the winter nest was consistently used as a place of shelter and for sleep.The ambient temperature ranged from-0.5° to 21.0°C being chiefly 1°C less the nestbox temperature. The difference between the nest-box and nest temperature was also about 1°C when the animal was inactive, thus clearly indicating torpidity. Steep increases in nest temperature, amounting to 14–18°C and raising nest temperature up to 30°C, were recorded on four occasions. This is interpreted as shallow torpor, since no activity occurred on these days.The spontaneous warming up from deep hypothermia to shallow torpor lasted on average 40 min (30–70 min), while the duration of passive cooling when returning to the hypothermic condition amounted to 5 hrs. In the weeks following continuous hibernation the dormouse alternated between activity, shallow torpor, and relatively deep torpor each day. The species should be considered as a true aestivator.     

The influence of hydric environments during egg incubation on embryonic heart rates and offspring phenotypes in a scincid lizard (Lampropholis guichenoti)

Extensive evidence shows that incubation conditions can affect phenotypic traits of hatchling reptiles, but the relative importance of thermal versus hydric factors, and the proximate mechanisms by which such factors influence hatchling phenotypes, remain unclear for most species. We incubated eggs of an Australian scincid lizard, Lampropholis guichenoti, at four different moisture contents ranging from -500 to 0 kPa. Drier substrates reduced water uptake of eggs and resulted in smaller hatchlings, but other phenotypic traits (incubation periods, hatchling sex, body proportions, running speeds, growth rates post-hatching) were not affected by the hydric environment during incubation. Contrary to our prediction, lower water uptake during incubation (and hence, presumably, more viscous blood) did not affect embryonic heart rates. Thus, as in many other squamate species, hatchling phenotypes and embryonic developmental rates of L. guichenoti are less sensitive to hydric conditions in the nest than to thermal regimes.     

Changes in mass of eggs of softshell turtless (Trionyx spiniferus) incubated under hydric conditions simulating those of natural nests

Rigid-shelled eggs of softshell turtles ( Trionyx spiniferus ) incubated at 29C under hydric conditions simulating those at the interior of natural nests (i.e. eggs not contacting the substrate) declined in mass during incubation owing to the continuous escape of water vapour to air trapped inside the chambers, with eggs incubated in relatively dry chambers declining more in mass than eggs held in relatively wet chambers. Eggs held under hydric conditions approximating those at the periphery of natural nests (i.e. eggs partly buried in the substrate) also declined in mass during incubation, but at lower rates than characterized eggs not contacting the substrate, indicating that absorption of liquid water from the substrate compensated for part of the water vapour escaping to the air inside the chambers. There was no relationship between hatching success and either the position of eggs in the chambers or the wetness of substrates, nor was there any variation among experimental groups in the size of hatchlings. Thus, development of embryos of Trionyx spiniferus seems not to be closely coupled with the hydric environment of the nest, a situation contrasting with that of embryos of those species of turtles producing pliable-shelled eggs.     

Parental food conditions affect sex-specific embryo mortality in the yellow-legged gull (Larus michahellis)

Different mortality of males and females during early post-hatching development in sexually size-dimorphic bird species is usually attributed to different nutritional requirements of the sexes, because mortality is mostly biassed toward the larger sex. We investigated whether sex-specific embryo mortality in the yellow-legged gull (Larus michahellis), a size-dimorphic seabird, depends on parental condition. To test this, we experimentally modified parental nutritional conditions by supplementary feeding of yellow-legged gulls during egg formation, to evaluate sex-biassed environmental sensitivity of gull embryos. We found that eggs were larger in supplemented clutches, but egg size did not affect embryo survival. Survival of male gull embryos was more related to parental food conditions than was survival of female embryos. Survival of male embryos in supplemented clutches was greater than in unsupplemented clutches whereas survival of female embryos was similar in both groups. Because size at hatching was similar in both sexes our results suggest that male phenotype disadvantage is not exclusively linked to the energy demands of size-dimorphic development at the embryo stage.     

Hummingbird incubation: Female attentiveness and egg temperature

Summary Incubating hummingbirds adjust nest attentiveness patterns in different habitats to permit both regulation of egg temperatures for embryonic development and foraging of the adult for positive energy balance. Anna's (Calype anna) and Black-chinned (Archilochus alexandri) Hummingbirds nesting in California chaparral left the nest six to nine times during each daylight hour. Eggs usually cooled only 3–6°C during absences but sometimes cooled up to 20°C during long absences. One Anna's Hummingbird became torpid for 4.5 h at night following a rainy day; the eggs survived cooling to 11°C and hatched two days later. A Costa's Hummingbird (Calypte costae) nesting in the California desert also left the nest several times per hour in early morning and late afternoon, but shaded the eggs almost continuously during the middle of the day. A Purple-crowned Fairy (Heliothryx barroti) in the warm lowland tropics of Panama left her eggs unattended for a few relatively long periods each day rather than many short periods as do temperate zone species. This pattern is typical of other tropical hummingbirds as well probably because equable ambient temperatures mean thermoregulation of eggs is not as critical a problem as it is in other habitats. In the temperate zone, hummingbirds exhibit behavioral adaptations (timing of reproduction, segmented foraging pattern) and physiological adaptations (torpor and hypothermia) for successful incubation. Embryonic development is successful even when egg temperatures fluctuate widely.     

Daily Torpor in Free-Ranging Gray Mouse Lemurs (Microcebus murinus) in Madagascar

I aimed to determine when and under which seasonal environmental conditions gray mouse lemurs (Microcebus murinus), a small nocturnal primate species endemic to Madagascar, utilize daily torpor. Using temperature-sensitive radio collars, I measured skin temperature (T _sk ) of free-ranging mouse lemurs under natural conditions. My results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a ) during the dry season, but not during the rainy season. Mouse lemurs that remained normothermic had significantly lower body masses (mean: 59.7 g) than individuals that used torpor (mean: 80.2 g). Skin temperatures dropped to 20.9°C and the mean torpor bout duration is 10.3 h. The use of torpor on a given night varied among individuals, whereas the propensity for torpor did not differ significantly between males and females. I found no evidence that T _a can be used to predict whether mouse lemurs will remain normothermic or enter torpor. It appears that the most reliable indicator for the occurrence of torpor in free-ranging Microcebus murinus is time of the year, i.e., photoperiod.     

Energy expenditure increases during the active season in the small,free-living hibernator Muscardinus avellanarius

Little is known about strategies employed by small mammals to reduce energy expenditure during the summer. To understand whether ambient conditions impact euthermic energy demands in a small free-living hibernator, we measured metabolic rate of hazel dormice (Muscardinus avellanarius) in the field. Furthermore, we aimed to reveal which variables influence torpor use. Our results show that hazel dormice altered euthermic energy expenditure during summer but not as expected as a response to environmental conditions. Euthermic resting metabolic rate was lowest directly after emergence from hibernation and increased by about 95% until the end of August. A considerable part of this increase was presumably caused by the changing influence of gender and rain on energy demands during different months, variation in food quality and quantity, and reversible size changes of organs that had been atrophied during hibernation. Torpor use in hazel dormice occurred more frequently when it was colder, earlier during the day, and in lighter individuals. Torpor was used routinely in males and non-reproductive females. We show that torpor is used more frequently than previously suggested by studies that only used visual proof of torpor use by surveying nest boxes.     

Prey availability affects daily torpor by free-ranging Australian owlet-nightjars (Aegotheles cristatus)

Food availability, ambient temperatures (T(a)), and prevailing weather conditions have long been presumed to influence torpor use. To a large extent, this is based on measurements in the laboratory of animals placed on restricted diets and kept at low T (a). Information on the determinants of torpor employment in the field is limited. We assessed winter torpor by insectivorous, free-ranging Australian owlet-nightjars (Aegotheles cristatus; 22 birds, 834 bird-days over six winters). Birds in three habitats were investigated to test whether torpor use is affected by annual T(a), rainfall, and arthropod abundance. Owlet-nightjars entered daily torpor regularly at all sites. Torpor frequency, depth and bout duration were greatest during two periods with lower arthropod abundance, providing rare evidence of the link between food availability and torpor patterns of wild birds. Temporal organization of torpor was similar among sites, and nocturnal torpor was more frequent than previously reported. Our findings quantitatively demonstrate that reduced food resources affect torpor usage independently from T(a), and support the view that food availability is a primary ecological determinant of torpor use in the wild.     

Defining torpor in free-ranging bats: experimental evaluation of external temperature-sensitive radiotransmitters and the concept of active temperature

A variety of definitions involving body temperature (Tb), metabolic rate and behavior have been used to define torpor in mammals and birds. This problem is confounded in some studies of free-ranging animals that employ only skin temperature (Tsk), a measure that approximates but may not precisely reflect Tb. We assess the accuracy of Tsk in the context of a recent definition for torpor called active temperature. We compared the active temperatures of individual big brown bats (Eptesicus fuscus), which aggregate in cavities, with solitary, foliage-roosting hoary bats (Lasiurus cinereus). In captive big brown bats, we compared Tsk and core Tb at a range of ambient temperatures for clustered and solitary roosting animals, compared Tsk and Tb during arousal from torpor, and quantified the effect of flight on warming from torpor. Hoary bats had significantly lower active temperatures than big brown bats despite having the same normothermic Tsk. Tsk was significantly lower than Tb during normothermia but often greater than Tb during torpor. Flight increased the rate of warming from torpor. This effect was more pronounced for Tsk than Tb. This suggests that bats could rely on heat generated by flight muscles to complete the final stages of arousal. Using active temperature to define torpor may underestimate torpor due to ambient cooling of external transmitters or animals leaving roosts while still torpid. Conversely, active temperature may also overestimate shallow torpor use if it is recorded during active arousal when shivering and non-shivering thermogenesis warm external transmitters. Our findings illuminate the need for laboratory studies that quantify the relationship between metabolic rate and Tsk over a range of ambient temperatures.     

Effects of reproductive condition,roost microclimate,and weather patterns on summer torpor use by a vespertilionid bat

A growing number of mammal species are recognized as heterothermic, capable of maintaining a high‐core body temperature or entering a state of metabolic suppression known as torpor. Small mammals can achieve large energetic savings when torpid, but they are also subject to ecological costs. Studying torpor use in an ecological and physiological context can help elucidate relative costs and benefits of torpor to different groups within a population. We measured skin temperatures of 46 adult Rafinesque's big‐eared bats (Corynorhinus rafinesquii) to evaluate thermoregulatory strategies of a heterothermic small mammal during the reproductive season. We compared daily average and minimum skin temperatures as well as the frequency, duration, and depth of torpor bouts of sex and reproductive classes of bats inhabiting day‐roosts with different thermal characteristics. We evaluated roosts with microclimates colder (caves) and warmer (buildings) than ambient air temperatures, as well as roosts with intermediate conditions (trees and rock crevices). Using Akaike's information criterion (AIC), we found that different statistical models best predicted various characteristics of torpor bouts. While the type of day‐roost best predicted the average number of torpor bouts that bats used each day, current weather variables best predicted daily average and minimum skin temperatures of bats, and reproductive condition best predicted average torpor bout depth and the average amount of time spent torpid each day by bats. Finding that different models best explain varying aspects of heterothermy illustrates the importance of torpor to both reproductive and nonreproductive small mammals and emphasizes the multifaceted nature of heterothermy and the need to collect data on numerous heterothermic response variables within an ecophysiological context.     

Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications

Altricial mammals and birds become endothermic at about half the size of adults and presumably would benefit energetically from entering torpor at that time. Because little is known about torpor during development in endotherms, we investigated whether after the establishment of endothermic thermoregulation (i.e. the ability to maintain a high body temperature during cold exposure), Sminthopsis macroura, a small (∼25 g) insectivorous marsupial, is capable of entering torpor and whether torpor patterns change with growth. Endothermic thermoregulation was established when the nest young reached a body mass of ∼10 g, and they were capable of entering torpor early during development at ∼10–12 g, lending some support to the view that torpor is a phylogenetically old mammalian trait. Torpor bout length shortened significantly and the minimum metabolic rate during torpor increased as juveniles approached adult size, and consequently total daily energy expenditure increased steeply with age. Relationships between total daily energy expenditure and body mass during development of S. macroura (slope ∼1.3) differed substantially from the relationship between basal metabolism and body mass in adult endotherms (slope ∼0.75) suggesting that the energy expenditure–size relationship during the development differs substantially from that in adults under thermo-neutral conditions. Our study shows that while torpor can substantially reduce energy expenditure during development of endotherms and hence is likely important for survival during energy bottlenecks, it also may enhance somatic growth when food is limited. We therefore hypothesize that torpor during the development in endotherms is far more widespread than is currently appreciated.     

Lizards fail to plastically adjust nesting behavior or thermal tolerance as needed to buffer populations from climate warming

Although observations suggest the potential for phenotypic plasticity to allow adaptive responses to climate change, few experiments have assessed that potential. Modeling suggests that Sceloporus tristichus lizards will need increased nest depth, shade cover, or embryonic thermal tolerance to avoid reproductive failure resulting from climate change. To test for such plasticity, we experimentally examined how maternal temperatures affect nesting behavior and embryonic thermal sensitivity. The temperature regime that females experienced while gravid did not affect nesting behavior, but warmer temperatures at the time of nesting reduced nest depth. Additionally, embryos from heat‐stressed mothers displayed increased sensitivity to high‐temperature exposure. Simulations suggest that critically low temperatures, rather than high temperatures, historically limit development of our study population. Thus, the plasticity needed to buffer this population has not been under selection. Plasticity will likely fail to compensate for ongoing climate change when such change results in novel stressors.     

Body temperature patterns before, during, and after semi-natural hibernation in the European ground squirrel

Ground squirrels undergo extreme body temperature fluctuations during hibernation. The effect of low body temperatures on the mammalian circadian system is still under debate. Using implanted temperature loggers, we recorded body temperature patterns in European ground squirrels kept in an enclosure under natural conditions. Although hibernation onset was delayed, hibernation end corresponded closely to that measured in a field population. Circadian body temperature fluctuations were not detected during deep torpor, but indications of circadian timing of arousal episodes at higher temperatures were found at the beginning and end of hibernation. One male exhibited synchronised arousals to a relatively constant phase of the day throughout hibernation. All animals first entered torpor in the afternoon. Daily body temperature fluctuations were decreased or distorted during the first days after hibernation. We hypothesise that hibernation may affect the circadian system by either decreasing the expression of the circadian oscillator, or by decreasing the amplitude of the circadian oscillator itself. possibly due to gradual, temperature dependent, internal desynchronisation. The latter mechanism may be beneficial because it might facilitate post-hibernation re-entrainment rates.     

Eggs in autumn: responses to declining incubation temperatures by the eggs of montane lizards

Facultative hatching in response to environmental cues may increase the viability of offspring, if the cue that stimulates hatching also predicts the negative consequences of delayed emergence. Declining incubation temperatures might provide such a cue for montane lizards, because eggs that fail to hatch before winter will perish in the nest. I tested this idea by incubating eggs of an alpine scincid lizard ( Bassiana duperreyi ) in the laboratory. For the first half of the incubation period the eggs were kept at nest temperatures typical of those experienced in summer in the field (daily cycle of 18 ± 7.5°C). I then transferred eggs at weekly intervals into cooler regimes (either 15 ± 7.5°C; or with daytime temperatures unchanged but dropping to 0°C overnight). Contrary to prediction, the eggs did not hatch early. However, transfer to lower temperatures caused only a relatively short delay in hatching, because of a virtual temperature-independence of developmental rates late (but not early) in incubation. Decreasing incubation temperatures also modified hatchling running speeds and post-hatching growth rates, even if the thermal decrease occurred only shortly before the usual time of hatching. These processes plausibly affect hatchling fitness in cold-climate reptiles, and might be adaptations to montane habitats. Alternatively, they may prove to be widespread in other (warmer-climate) reptile taxa, in which case no adaptive hypothesis need be proposed. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 71–77.     

Development of temperature regulation in the common white-toothed shrew, Crocidura russula

1. Body temperature and oxygen consumption were measured during the first month of postnatal life in two litters of Crocidura russula at four different ambient temperatures. 2. Body temperature in the nest varies from 30.5-35.0 degrees C during the first 10 days; afterwards it becomes more constant (35.5-37.0 degrees C). 3. First homoiothermic reactions occur on the 2nd day of life and become effective on the 4th day. 4. In the case of undernourished shrews, torpor is already developed on the 2nd day. 5. After the 7th day torpor is the obligatory reaction in cooling experiments. 6. This discontinuous development of temperature regulation is interpreted as typical for shrews capable of torpor.     

Cool birds: first evidence of energy-saving nocturnal torpor in free-living common swifts Apus apus resting in their nests

Daily torpor is a means of saving energy by controlled lowering of the metabolic rate (MR) during resting, usually coupled with a decrease in body temperature. We studied nocturnal daily torpor under natural conditions in free-living common swifts Apus apus resting in their nests as a family using two non-invasive approaches. First, we monitored nest temperature (T_nest) in up to 50 occupied nests per breeding season in 2010–2015. Drops in T_nest were the first indication of torpor. Among 16 673 observations, we detected 423 events of substantial drops in T_nest of on average 8.6°C. Second, we measured MR of the families inside nest-boxes prepared for calorimetric measurements during cold periods in the breeding seasons of 2017 and 2018. We measured oxygen consumption and carbon dioxide production using a mobile indirect respirometer and calculated the percentage reduction in MR. During six torpor events observed, MR was gradually reduced by on average 56% from the reference value followed by a decrease in T_nest of on average 7.6°C. By contrast, MR only decreased by about 33% on nights without torpor. Our field data gave an indication of daily torpor, which is used as a strategy for energy saving in free-living common swifts.     

The temperature–size rule in a rotifer is determined by the mother and at the egg stage

In most ectotherms, compared with development at low temperatures, development at high temperatures results in the acceleration of maturation, which in turn results in a smaller size (temperature–size rule, TSR). It is not known at which developmental stages this thermal response is determined. We exposed different life stages of the rotifer Lecane inermis to 15, 20, or 25 °C to determine whether the TSR in the F1 generation is governed by the thermal conditions experienced by the mothers (F0 generation) during their development, during egg production, or during the development of the eggs or hatchlings. We found that the adult size was affected by the thermal conditions experienced by the mothers and embryos, but not by the conditions during post-hatching growth. We suggest that the thermal plasticity producing the TSR in rotifers may reflect the joint impacts of a maternal effect and a direct effect of the environment during egg development. The two-point control of the TSR resembles the thermal determination of other biological phenomena, similar to the thermally determined sex determination in ectotherms. Our results contribute not only to better understanding the proximate mechanisms of TSR, but also to comprehending the general biological mechanisms of response to temperature, which is one of the most important ecological factors.     

THE THERMAL SIGNIFICANCE OF THE NEST OF THE SOCIABLE WEAVER PHILETAIRUS SOCIUS: SUMMER OBSERVATIONS

Extending a previous study of the thermal significance of the nest of the Sociable Weaver carried out during the winter, we measured temperature and humidity in the matrix and chambers of a large nest of this species in the Kalahari Gemsbok National Park, South Africa, during the austral summer of December 1973. Air temperatures outside the nest ranged from 16 to 33.5°C but temperatures in occupied chambers varied over a range of only 7 or 8°C and remained well within the zone of thermal neutrality for a passerine bird of this size. Compared to outside air temperatures, those within the nest matrix were lower during the day and higher at night. Thus, the nest ameliorates the effects of external temperatures and allows maintenance inside the chambers of a range of temperature favourable to the birds. In winter we found up to five roosting adults per chamber, with some chambers left empty. In the same nest in summer we found no more than two adults per chamber but virtually all chambers were occupied. The principal mechanism for maintaining chambers within the zone of minimal energetic cost is changes in the number of birds in the nest chambers at night. Humidity inside the occupied and unoccupied chambers was somewhat higher in the former but always less than that of outside air in both cases. Air movement through the desiccated nest materials causes uptake by these materials of most of the water vapour introduced by the birds, and this moisture is dissipated to the outside during the day so that the nest remains dry. The highly social and colonial habits of the birds and their year-round occupancy and maintenance of the nest favour a system of opportunistic breeding that may be initiated by rainfall at any season. Larger nests provide the most favourable environment for energy conservation and successful reproduction. Even the largest nests, however, do not prevent predation during the warm season by snakes such as the Cape Cobra, which may consume all the eggs and young in all the chambers of a large nest. The effects of such heavy predation may be offset by the birds' capability for breeding during times too cold for reptile activity. It seems likely that in smaller nests such as those on telephone poles, lack of predation would favour summer breeding while thermal problems would limit breeding success in winter. In larger nests, breeding success may be lower in summer because of predation and higher in winter when reptile predation is lacking and thermal problems are minimized by the nest structure. The large nest not only makes possible the success of the Sociable Weaver in desert areas, but the nest could only exist in such areas and the species' range is thereby restricted. Higher humidity and heavier rainfall would cause fermentation within the nest mass, loss of its thermoregulatory advantages, and ultimately its decomposition and destruction. Therefore, the unique nesting system of the Sociable Weaver appears to be initially self-reinforcing and ultimately self-limiting.