In comparison with endotherms, ectotherms can be found in a diverse range of habitats across the globe however their dispersion is dependent on the access to sources of heat and there adaptation to their environment. The body temperature (Tb) of reptiles is affected by the surrounding environment from air/water temperatures /substratum they are in contact with. Thermoregulation occurs from behavioural responses to temperature (rather than the more passive thermoregulation found in amphibians) moving from different locations to find a more suitable climate. They are therefore termed poikilothermic, using a range of unique adaptations to survive in these diverse environments. Many species have a wider range of tolerance of temperature than what was originally perceived, a few of which can survive sub zero (Tb) such as the painted turtle or in contrast plus 40Â°C (Tb) such as the desert iguana (Dipsosaurus dorsalis). The mechanisms used by the species to survive in these environments is the main discussion point of this literature review.
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Compared to endotherms, the terrestrial ectotherm vertebrates are found in a diverse but a limited number of localities and dispersion is limited largely by their dependence on the external heat sources for thermal homeostasis and normal activity. (Spellerberg, 1973). Reptile distribution is affected by their tolerance to different environments as some species are specialists and others are generalists in habitat use. (Segura et al., 2007). Thermoregulation is maintained and altered by behaviour to find the required temperature which may be affected by functions such as feeding. Snakes actively adjust thermoregulatory behaviour to raise their body temperature during digestion (Tattersall et al., 2004).
Reptiles are poikilothermic and rely on their environment as a source of heat to raise the body temperature. Body temperature in reptiles is controlled via behavioural processes and these vary depending on the environment they are in. Basking is a typical behaviour exhibited by reptiles to raise body temperature and is typically exhibited around sunrise to initially warm the body to reach optimal performance. This can be a vulnerable time for reptiles as their movements are sluggish and slow however more primitive reptiles such as geckonids, iguanids, chameleonids and xantusids are able to change their body colour to increase the body temperature at a faster rate. The dark coloration observed frequently during morning basking in chameleons may serve to reduce the basking period and, hence, reduce time spent at suboptimal performance temperatures (Walton & Bennet., 1993). Optimal temperatures allow the reptile to function and metabolise however lower temperatures can slow these processes down. Typically the metabolic rate is 10% of the equivalent size endotherm, this is an example of the low cost energy needed to sustain an ectotherm.
Researchers have studied the role of the parietal eye, a third eye situated high in the centre of the head in certain reptile species such as Anolis carolinensis. Results suggest that the lizard parapineal plays a direct role in thermoregulation in addition to the indirect function as an illuminometer (Hutchison &.Kosh.,1974).
3.2 Surviving the Seas
Marine reptiles have a close association with water; in some species they only leave the water to lay eggs. Those that are sea bound do not regularly show typical basking, thermoregulatory behaviours. For example there are some species of marine turtle where there is no proof of behavioural thermoregulation. The Leatherback sea turtle (Dermochelys coriacea) can maintain body temperature (Tb) up to 18Â° C above that of the surrounding sea water (T-W) which allows leatherbacks to enter cold temperate waters and have the largest global range of any reptile. (Bostrom & Jones., 2007). Therefore marine turtles are actually able to maintain body temperatures without the need to bask because of the heat produced from the exertion of muscle contraction. However research of the loggerhead turtle showed that although spending 90% of their time underwater they did spend time at the surface. The timings of these surfacing have not shown evidence that it is connected to thermoregulatory behaviours although theories have been suggested such as the turtles dived through the thermocline to exploit prey of deeper water layers, and hence most likely returned to the surface with full stomachs. For ectothermic animals that live in temporally resource-sparse environments, thermoregulation for warmer body temperatures has been discussed as a means to maximise energy production in times when food is abundant (Hochscheid et al., 2009). Therefore they utilised the heat from the sun at the surface in increase digestion efficiency of the recent intake of food.
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The Yellow Bellied Sea Snake (Pelamis platurus) is an example of a sea snake which is adapted to swim through the water with its dorsally flattened tail used a paddle to move through the water. It is found in tropical waters and thermoregulates whilst in water. It shows some tolerance to colder waters however exhibits thermoregulatory behaviours; When a snake is basking at the water surface, the blackened upper portion of its body is emergent. This coloration would facilitate the absorption of solar energy (Graham et al., 1971). At cooler temperatures (around 18Â°C) the P.platurus rises to the surface where the waters are warmer and UV rays are at their strongest. In contrast when temperatures increase to 32Â°C it will dive to cooler waters to maintain the ideal temperature. Therefore, thermoregulation is controlled by regulating its depth in the water.
3.2 Surviving the Heat
Reptiles low metabolic rate and various unique physiological attributes have enabled them to adapt to some of the harshest environments. One of those being high temperature habitats such as deserts. A variety of behaviours are exhibited by a range of reptiles all attempting to maintain a sufficient (Tb). Although deserts are hot throughout the day and can possibly reach temperatures of 50Â°C+ they can at night have temperatures that drop to sub zero temperatures, around -5Â°C in the Sahara. Therefore reptiles have a varied climate to contend with, including the need to maintain correct temperatures in extreme heat but also surviving the cold nights. This in turn means that sunrise is a prime time for reptiles to warm from the previous cold night. Many species have adaptations to thaw out faster such as a change in colour. The dark coloration observed frequently during morning basking in chameleons may serve to reduce the basking period and, hence, reduce time spent at suboptimal performance temperatures. (Walton &Bennett., 1993) This not only increases the (Tb) at a faster rate but also reduces the amount of time in the open reducing the chances of predation. This adaptation is seen in many primitive species such as geckonids, iguanids, and xantusids.
Many reptiles make use of burrows to escape the daytime temperatures and make use of mammalian burrows to seek cooler temperatures. These burrows act as a microclimate and allow the ectotherms to maintain a temperature whilst the external temperatures remain intolerable. Some species of lizard also adopt bipedal locomotion to sprint across hot sands, this behaviour allows the abdomen to be raised from the ground, removing its contact from the warm air emitted from the substratum. This behaviour is often accompanied by shuffling of the front feet while the animal moves forward, pushes the hottest sand aside and brings the body into contact with the cooler layers underneath. This behaviour pattern has repeatedly been observed in the desert iguana (Dipsosaurus dorsalis). (Schmidt-Nielsen,.1964). Other cooling techniques have been adopted linked with water loss. Water levels in reptiles in comparison with mammals are relatively similar or slightly higher. Although living in the desert means that water is usually scarce, it is believed that a considerable amount of water intake is from their carnivorous diet. One species ignores the scarcity of water and uses it as a source of thermoregulation. The Gila monster uses evaporative water loss (EWL) from its cloaca to reduce (Tb). (DeNardo., 2003) Cloacal EWL was extremely low and relatively constant between 20.5Â°C and35Â°C, but rose dramatically above 35Â°C. The results collated showed a direct affect of (Tb) decrease however it was corresponding with the level of dehydration of the reptile.
Krochmal & Bakken (2003), recently discovered a link between viper facial pits and thermoregulation. Environmental features subtend far larger solid angles and possess relatively larger temperature differences than do prey items, and they would therefore present a larger total thermal signal than would prey items. This would make environmental features more easily sensed than prey items by animals with a limited form of thermal detection. An ancestral, comparatively limited, ability to sense thermal radiation might therefore have been more useful for thermoregulation than for prey acquisition. Recently it has also been researched that these facial pits may have been originally for thermoregulation but over time have adapted for prey location as part of an evolutionary advancement.
3.3 Nocturnal species
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The thermal quality of diurnal refuges is important to the performance and survival of nocturnal reptiles. (Aguilar &Â Cruz.,2010). Depending on how warm the refuge is will directly affect their (Tb) and their performance during activity. Nocturnal reptiles are thigmothermic meaning they attain there heat from surrounding substratum rather than the sun's rays. Throughout the day the sun heats all the ground below it which is absorbed and at dusk these reptiles become active, absorbing heat from their environment. Nocturnal species are more tolerant to low temperatures in comparison with diurnal species. Nonbasking thigmotherms, which gain body heat by conduction, are generally less thermophylic and tolerate lower body temperatures than do heleotherms. (Templeton., 1970)
3.4 Surviving the Cold
Fig. 1. The survival rates of red eared turtles at sub zero temperatures at different lengths of time. From Churchill & Storey., 1992.Although more associated with hot climates, reptiles, in some species have acclimitised to living in colder environments. Species such as the European adder (Vipera berus), is distributed across most of temperate Eurasia and, being a cold-tolerant species, can be found in Fennoscandia north of the Arctic Circle (Carlsson,. 2004).Many examples of local distribution in regions with a relatively harsh climate suggest that these species owe their presence to patches where aspect and slope in combination with an appropriate substrate quality provide a particularly favourable microclimate. (Guisan & Hofer, 2003). Also that a study conducted presented evidence that reptiles are capable of adjusting their thermoregulatory behaviour in response to different thermal constraints. (Besson et al., 2010). Adaptations such as small size allows them to warm faster and hibernation enables them to be dormant throughout colder months. The adder was categorised as virtually non freeze tolerant capable of surviving only a short exposure not colder than approximately 4Â°C. Supercooling could play a role in winter survival but their precise choice of hibernation site is probably the most important. (Andersson & Johansson,. 2001).
Supercooling is a physical process exhibited by a few reptiles and amphibians. It is usually a motionless state where the specimen is able to survive sub zero freezing conditions often including parts of the body freezing. The internal fluids and organs are protected with the association of the cryoprotectant glucose. (Costanzo et al.,1995). Glucose-6-dehydrogrenase,Â G6PDH was isolated from liver of the wood frog, Rana sylvatica, a freeze tolerant species that uses glucose as a cryoprotectant.(Dieni, & Storey.,. 2010) Evidence of this ability has been regularly shown in turtles such as the painted turtle (Chrysemys picta). Research indicated that hatchlings tolerated 24 hr of freezing at- 4Â°C and survived both fast and slow regimens of freezing and thawing. (Storey et al., 1988). Although some species of turtle have shown evidence of freezing it has been identified that the duration it withstands these temperatures has a critical effect of its survival (Fig 1.) However these theories of the physiological functions to undergoe supercooling aren't completely proven, further research is needed to provide answers on the role of cryoprotectants such as glucose. Studies could hold the key to the development of techniques for mammalian organ cryopreservation. (Storey et al.,1988).
Unlike other organisms such as mammals where sex determination is from the allelic combination from two gametes, reptiles' sex is determined by temperature. Which considering the diversity in environments can lead to complications. Egg laying reptiles are termed oviparous and temperature plays a fundamental role in sex determination. Loggerhead turtles undergo sex determination via temperature with warmer incubation temperatures producing more females and cooler temperatures producing more males (Witt et al., 2009). Oviparous reptiles are usually laid within burrows or nests where temperatures can be maintained. In thermally challenging environments, maternal oviposition behaviour constrained by the limited availability of suitable oviposition sites and maternal oviposition choice can inï¬‚uence egg survival. (Pike et al., 2006).
Vivparity is a means of embryonic development inside the body of the mother therefore giving birth to live young. As previously discussed sex is determined by temperature however the offspring are warmed by internal temperature. Pregnant females modify their thermoregulatory behaviour in many species of viviparous (live-bearing) reptiles, typically maintaining higher and more stable body temperatures at this time.Â (Shine., 2006). Therefore this female viviparous lizard Niveoscincus ocellatus can influence the sex of their offspring by modifying the amount of time spent basking during pregnancy (Wapstra., 2004). Viviparous reptiles are often found in the north and can withstand colder temperatures than oviparous reptiles due to the internal thermal regulation of the offspring. There are 3 species of snake in the UK, Natrix natrix helvetica, Coronella austriaca, Vipera berus. Vipera berus is viviparous and is found as far north as Scotland in comparison to Natrix natrix helvetica, Coronella austriaca which are oviparous. However they manage to combat the cold british climate by ovipositing in a thermally distinctive man-made microhabitat (manure heaps on farms). (LoÂ¨wenborg., 2010). These microhabitats such as compost heaps etc produce enough heat to maintain a temperature sufficient to incubate the eggs.
Fig 2. From Tinkle & Gibbons, 1977)
Studies on reptilian life-history evolution have emphasized the role of cold climates as a selective force for the evolution of viviparity, but have tended to neglect the many cold-climate reptiles that retain oviparity. (Shine.,1999) One example is the female Children's python (Antaresia childreni) which exhibits parental care of the eggs by coiling around the clutch. The tightness of these coils was dependent on the ambient humidity and temperature surrounding the eggs. Thus, python egg brooding postural adjustments are functionally significant to embryonic thermoregulation and water balance because these movements modulate and respond to these two important developmental variables. (Stahlschmidt & DeNardo., 2010). A similar behaviour of egg brooding was exhibited in the carpet python over an 8 week period however throughout this time, females were facultatively endothermic, maintaining high constant temperatures through shivering thermogenesis. (Pearson et al.,Â 2003).