Thermal Adaptation - Basking

Reptiles are ectothermic animals and rely on external heat sources to regulate their internal temperature (Bogert 1949). This suggests that their means of thermoregulation is primarily behavioural, other than obvious physical structures affecting heat transfer such as skin type/thickness, and skin colour. These physical structures likely contribute to thermoregulation of reptiles in conjunction with behavioural adaptations, but will not be discussed in this post. The primary focus of this blog post is to evaluate the environmental conditions that reptiles are subject to, and discuss the adaptations that enable the effective operation of biological systems within reptiles. An understanding of the adaptations allowing the survival of reptiles in their habitat enables inference into past, present and future evolutionary patterns.

(Fig.1 - Thermoregulation time for reptiles of varying weights)

Reptiles regardless of species or size tend to share common behavioural thermoregulation patterns. Most activity is recorded in the morning with the rising sun (finding an appropriate position and substrate to bask upon), with decrease of activity or normal foraging/resting behaviour from approximately mid-day onwards. This was found in the lace monitor (Varanus varius), which would emerge from shelter and bask in morning sun until reaching 35-36°C, then reduce activity to forage and return to shelter (Seebacher 2004). The 2004 study by Seebacher also found variances in basking time between reptiles of varying weights; the five kilogram lace monitor required over 90 minutes to reach body temperature equilibrium, where a small lizard (0.01kg) required less than 15 minutes (Fig. 1). This is significant in determining the costs of achieving thermal preference, in that the risk of predation increases if basking time increases (Blouin-Demers & Weatherhead 2001). The time in which reptiles reach their thermal preferences is varied throughout species and weights, but the techniques used work the same. It would make logical sense that larger reptiles which take longer to behaviourally thermoregulate have evolved with different adaptations to deal with costs of thermoregulation (predation, oxygen availability, energy costs) than those which can achieve optimum internal temperature relatively quickly and easily.

Reptiles rely on behavioural thermoregulation (basking) in the early hours of the day to maintain optimal internal temperature (Bogert 1949). Basking in the morning enables reptiles to spend the remainder of the day engaging in routine activities (foraging, mating etc.) which require energy and warm, active cells. Larger reptiles require more time basking, presenting risks such as predation, energy loss, and dehydration. However, it is likely that larger reptiles have evolved with very different defense mechanisms to smaller ones to compensate for the cost-benefit scenarios present in reptilian ecological communities.

References:

Blouin-Demers, G. Weatherhead, P. 2001, ‘Thermal ecology of Black Rat Snakes (Elaphe Obsoleta) in a thermally challenging environment’, Ecology, Vol. 82, No.11, pp. 30125-3043

Bogert, C. 1949, ‘Thermoregulation in Reptiles, A Factor in Evolution’, Evolution, Vol. 3, No. 3, pp. 195-211

Seebacher, F. Shine, R. 2004, ‘Evaluating Thermoregulation in Reptiles: The Fallacy of the Inappropriately Applied Method’, Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, Vol. 77, No. 4, pp. 688-695

Figures:

Fig.1 - Seebacher, F. Shine, R. 2004, ‘Evaluating Thermoregulation in Reptiles: The Fallacy of the Inappropriately Applied Method’, Physiological and Biochemical Zoology: Ecological and Evolutionary Approaches, Vol. 77, No. 4, page 690

Thermal Adaptation - Heat Acclimation in Plants

The survival and reproduction of plants is dependent on availability of water, nutrients and sunlight. Increased environmental temperature can put significant pressures on plants, affecting osmoregulation and photosynthetic ability of the cells (Berry & Bjorkman 1980). Plants inhabiting hot climates possess adaptations to the impacts of heat stress (excessive water loss, chlorosis, increased respiration) (McWilliam & Naylor 1967). Physiological stress in plants as a result of temperature reduces reproductive and individual growth. This blog post will discuss some adaptations allowing plant survival in high temperatures. 

Fig. 1 - Diagram showing processes of photosynthesis and respiration in plant cells
(Morholt & Brandwein)

Plant respiration is the oxidization of glucose in the mitochondrial organelles of plant cells, resulting in production of carbon dioxide (CO²) and water (Fig. 1). Global circulation models (GCM) have suggested that increased environmental temperature increases respiration in plants, resulting in water loss of leaves and roots, photosynthetic inhibition of leaves, and weakened roots (especially with increased soil temperature) (Atkin et al 2005). Increased respiration would also increase atmospheric CO², contributing to the existing greenhouse effect. Atkin et al (2005) contradicted GCM and found that increased environmental temperature does not always result in increased plant respiration and adaptations exist to balance regular CO² production with increased environmental temperature. These adaptations are both intra-cellular and physiological, depending on the species concerned and the niche conditions for its habitat.

Fig. 2 - Representation of the temperature response of respiration in warm-grown (Hot), cool-grown (Cold) and warm grown type plants acclimated to cooler and hotter temperatures
(Atkin et al 2005)

Desert plants reduce respiration and water loss by reducing surface area of leaves. Plants inhabiting Death Valley, California, retained photosynthetic ability up to 43°C before experiencing damage to the chloroplast membranes (Seemann et al 1984). Atkin et al (2005) found that some plants can regulate concentration/amount of enzymes involved in plant respiration, and vary mitochondrial protein concentration, thus changing rates of respiration. Simplified, this means cold-adapted plants can increase respiration with increased temperature, and warm-adapted plants can decrease respiration to reduce water loss and CO² output (Fig.2). This would balance the production of CO² by plants in the atmosphere. However, the ratio of cold-adapted plants to warm-adapted plants in global populations would impact total vegetative CO² output.

Plants inhabit areas of highly varied temperature, light and water availability in different global biomes. This post has listed some plant survival adaptations, as well as impacts of increased temperature on plants and the world. The likely increase in global temperature is an effect of anthropogenic increase in CO² emissions. Studies have shown that plants can somewhat modify respiration and osmoregulation as a result of temperature increase, and these processes may impact the effects of global warming.

References:

Atkin, O. Bruhn, D. Hurry, V. Tjoelker, M. 2005, ‘The hot and the cold: unravelling the variable response of plant respiration to temperature’, Functional Plant Biology, Vol. 32, pp 87-105

Berry, J. Bjorkman, O. 1980, ‘Photosynthetic response and adaptation to temperature in higher plants’, Annual Review of Plant Biology, Vol. 31, pp 491-543

McWilliam, J.R. Naylor, A.W. 1967, ‘Temperature and Plant Adaptation; Interaction of Temperature and Light in the Synthesis of Chlorophyll in Corn’, Plant Physiology, Vol. 42, pp 1711-1715

Seemann, J. Berry, J. Downton, W. 1984, ‘Photosynthetic Response and Adaptation to High Temperature in Desert Plants: A Comparison of Gas Exchange and Fluorescence Methods for Studies of Thermal Tolerance’, Plant Physiology, Vol. 75, No. 2, pp 364-368

Figures:

Figure 1 - E. Morholt, P.F. Brandwein, (date unknown), A Sourcebook for the Biological Sciences

Figure 2 - Atkin, O. Bruhn, D. Hurry, V. Tjoelker, M. 2005, ‘The hot and the cold: unravelling the variable response of plant respiration to temperature’, Functional Plant Biology, Vol. 32, page 88 (Fig.1)

Thermal Adaptation - Increased Bill Size

Endothermic organisms regulate their body temperature by balancing metabolic heat production with heat exchange in their environment (Tattersall et al 2009). Toucans (family Ramphastidae) are endothermic, and have been studied in nature for their large bill size in comparison to body size. Early explanations for large bill size included mating, feeding purposes, and territorial defense (Tattersall et al 2009; Hughes 2014). Techniques of convective heat loss have been discussed previously in this blog, such as gular fluttering, sweating and increased surface area of ears in elephants (comments). This blog post will discuss the growth and thermoregulatory ability of the toucan’s bill, and evaluate its primary ecological function.

The toucan family (Ramphastidae) is entirely distributed in Neotropical areas, with most species inhabiting lowland tropical forests, where high daily temperatures and humidity is frequent (Hughes 2014). The toucan’s body is covered primarily by dense feathers, which remain slightly above environmental temperature, suggesting most areas of body mass are unsuitable for thermoregulation (Tattersall et al 2009). A 2014 study conducted on the development of physical structures relative to body mass, found that maxilla length and depth (upper part of bill) increases at a greater than isometric rate more than any other physiological structure (e.g. cranium length and width, sternum, synsacrum, femur and tibiotarsus) (Hughes 2014). A 2009 study found that the proximal region of the bill (closest to head) dissipated heat at lower environmental temperatures (>16°C - 25°C), with blood flow increasing to distal regions of the bill as temperatures rose toward 30°C and higher. This study also determined that heat loss from the bill can account for 25 – 400% of heat production in adult toucans, depending on environmental variables such as altitude, wind speed, ambient temperature etc. The thermoregulatory capabilities of the toucan bill also far surpass that of elephants ears’ estimated at a range of 9-91% of heat production (Tattersall et al 2009).

Toucans live in tropical ecosystems, with high humidity and high daily temperatures. Studies have shown they are dependent on rapid growth of the maxilla to dissipate heat (Hughes 2014). Their ability to control blood flow between proximal and distal regions of the beak enables relative homeostasis in a varied climate (Tattersall et al 2009). Toucans have evolved with large bill size in order to maintain optimal internal temperature, suggesting that thermoregulation is its primary function. However, this research does not disprove that mating, feeding or any other environmental pressures have selected for large bill size during the evolution of the toucan.

References:

Hughes, A. 2014, ‘Evolution of bill size in relation to body size in toucans and hornbills’, Zoologia, Vol. 31, pp. 256-263

Tattersall, G. Andrade, D. Abe, A. 2009, ‘Heat Exchange from the Toucan Bill Reveals a Controllable Vascular Thermal Radiator’, Science, Vol. 325, No. 5939, pp. 468-470

Thermal Adaptation - Torpor

Large areas of Australian woodlands are subject to bushfire, particularly eucalypt forests. Woodland forests comprise 67% of forest vegetation in Australia, with scrublands, shrub and mixed forest types dominating the northern and eastern coast (Fig. 1)(ERIN 2012 & ABARES 2013).  An estimated 39 million hectares of Australian forest was burnt from 2006 to 2011 (ABARES 2013). Animals inhabiting Australian woodlands must be well-adapted to frequent changes in environmental conditions in order to survive and successfully reproduce.

(Fig. 1 - Terrestrial Ecoregions of Australia (April 2012))

Bushfire is an important ecological process for the germination of native plants, soil nutrient cycling and removal of obstructive ground vegetation, including invasive weeds (IFA 2005). However, bushfire results in increased environmental temperature, and the potential death of native fauna. In the 1950’s, laboratory studies on thermoregulation of the short-beaked echidna (Tachyglossus aculeatus) found that body temperatures of 38°C resulted in fatalities (Brice et al. 2002). However, recent field studies have shown they are able to withstand ambient temperatures of above 40°C, as well as survive large bushfire events (Brice et al 2002 & Nowack et al 2016).

Echidnas survive bushfire and increased environmental temperature by seeking shelter, usually a log, cave or burrow, before entering a state of torpor.  Torpor significantly lowers metabolic rate, and reduces breathing and heart rate. This decrease in cardiovascular and metabolic activity results in effective loss of body temperature (Heldmaier et al 2004). Echidnas subjected to bushfire in Dryandra Woodland, south-east of Perth, reduced their body temperatures on average by 4°C as a result of behavioural sheltering and torpor (Nowack et al 2016). One individual reduced body temperature from over 30°C, to below 20°C for four days after the onset of bushfire. After a period of re-adjustment, body temperature returned to normal as measured within the week prior (Fig.2). Possibly the most important finding from this study was that none of the echidnas in the sample left their home range as a result of the bushfire, although one did die as a result of poor log choice (Nowack et al 2016).

(Fig. 2 -  Body temperature traces of the same echidna (a) 7 days before and (b) 7 days after the fire on 21 April)

The short beaked echidna enters a state of torpor as an adaptation to bushfire, and subsequent increase in environmental temperature. This adaptation is believed to have enabled their survival through global wildfire events, such as those caused by meteoroid impacts during the Cretaceous-Paleogene era, 65.5 million years ago (Nowack et al. 2016). Temperature variation and natural disasters will continue to occur, affecting all species on earth. Thermal adaptations like torpor have and will continue to benefit animals such as the short-beaked echidna as evolution continues over time.

References:

Brice, P. Grigg, G. Beard, L. Donovan, J. 2002, ‘Heat tolerance of short-beaked echidnas (Tachyglossus aculeatus) in the field’, Journal of Thermal Biology, Vol. 27 pg 449 - 457

Department of Agriculture (ABARES), 2013, ‘Australia’s State of the Forests Report’, Five Yearly Report, Australian Government

Environmental Resources Information Network (ERIN) 2012, Department of Sustainability, Environment, Water, Population and Communities, Commonwealth of Australia, Australian Government

Heldmaier, G. Ortmann, S. Elvert, R. 2004, ‘Natural hypometabolism during hibernation and daily torpor in mammals’, Respiratory Physiology & Neurobiology, Vol. 141 pg 317–329

Institute of Foresters of Australia (IFA), 2005, ‘The role of fire in Australian forests and woodlands’, Forest Policy Statement 3.1, pg 1-3

Nowack, J. Cooper, C.E. Geiser, F. 2016, ‘Cool echidnas survive the fire’, Proceedings of the Royal Society B, Vol. 283, pg 1-8

Figures:

Figure 1: 

Environmental Resources Information Network (ERIN) 2012, Department of Sustainability, Environment, Water, Population and Communities, Commonwealth of Australia, Australian Government

Figure 2:
Nowack, J. Cooper, C.E. Geiser, F. 2016, ‘Cool echidnas survive the fire’, Proceedings of the Royal Society B, Vol. 283, pg 1-8

Thermal Adaptation - Cutaneous Water Transport

Internal body temperature is affected by the availability of water to the cells. Osmoregulation is the process of water transfer between cells, and as a direct impactor of body temperature, is closely linked to the thermoregulation of animals. Desert inhabitants are threatened by dehydration, and will perish without adaptations allowing them to access water found in plants, ground surface or underground. The thorny devil is a lizard inhabiting large areas of arid Australian land, where rainfall is irregular and surface water largely unavailable (Sherbrooke 1993). The adaptations that allow the thorny devil to access water, thus regulate internal temperature will be discussed in this post.

(Fig.1 - Thorny Devil (Moloch horridus) in walking stance)
(Clemente et al 2004)

The thorny devil has hygroscopic skin, allowing for accumulation of water to ‘stick’ to the skin surface. Spines and thorns on the skin increase surface area, aiding condensation of water. However, the thick scales it possesses for predatory protection are non-permeable, so an adaptation must have developed to allow transportation of water to the mouth. The thorny devil achieves transportation of water through interscalar channels on its back, in some cases ‘drawing’ water from its legs and stomach to the jaw. The channel is formed by the scale hinge joint that is interconnected with all scale hinges on the body, and composed of a very thin layer of keratin. Capillary forces fill the channels with water and physical pumping mechanisms of the jaw and upper body depress local water pressure, pulling water up through the channels toward the mouth (Sherbrooke 2005). The thorny devil can also access water by walking through wet spinifex and lying on wet substrates such as undersides of rocks. However wet vegetation and rocks are rare occurrences in the desert, so it depends predominantly on accumulation of water on the skin, and subsequent transport to the mouth through capillary channels.

(Fig.2 - Thorny Devil (Moloch horridus) in drinkning stance (A) and in process of jaw movement (B))
(Sherbrooke 1993)

The thorny devil is specifically adapted to living in extremely arid and dry conditions. Its ability to transport water along its capillary inter-scalar channels is gravity defying and fascinating. Extreme environmental conditions are correlated with complex adaptations, and the thorny devil is a perfect example of this. The evolution of species can be achieved in seemingly uninhabitable conditions, as long as genetic variation and enough time is available. 

References:

Sherbrooke, W.C 1993, Rain-drinking Behaviors of the Australian Thorny Devil (Sauria: Agamidae), Journal of Herpetology, Vol. 27, No. 3, pp. 270-275

Sherbrooke, W.C 2005, Functional morphology of scale hinges used to transport water: convergent drinking adaptations in desert lizards (Moloch horridus and Phrynosoma cornutum), Zoomorphology (2007) Vol. 126, pp. 89–102

Figures:

Fig.1: Clemente, C.J, Thompson, G.G, Withers, P.C, Lloyd, D. 2004, 'Kinematics, maximal metabolic rate, sprint and endurance for a slow-moving lizard, the thorny devil (Moloch horridus), Australian Journal of Zoology, Vol. 52, page 488

Fig. 2: Sherbrooke, W.C 1993, Rain-drinking Behaviors of the Australian Thorny Devil (Sauria: Agamidae), Journal of Herpetology, Vol. 27, No. 3, page 272

Thermal Adaptation - Coral Symbiosis

The Great Barrier Reef (GBR) is an important environmental and economic asset to North Queensland. As a result of warming ocean temperatures, six coral bleaching events have occurred in the GBR since 1980 (Berkelmans 2001). Progression of coral bleaching in this ecosystem will affect countless marine species with negative economic impacts to tourism (Strasser et al 1999). This blog post will discuss the potential of thermally-resilient symbiotic algae in order to reduce coral bleaching in the GBR.

Coral is the foundation of the GBR, providing shelter, feeding and breeding grounds for many marine organisms. However due to increasing ocean temperatures, coral bleaching is occurring (Fig.1). A 2001 JCU study found that upper thermal limits of coral in the GBR were only 2-4°C higher than average summer temperature, and within 1°C of daily average temperatures during summer periods (Berkelmans 2001). The white colour is caused by the death of zooxanthellae (Symbiodinium), occurrent within the gastrodermic cells of the coral as a symbiotic relationship (Ban & Graham 2012). The physiology of bleaching is not fully understood but involves the production of oxygen radicals, which are highly corrosive and damage chloroplasts (Berkelmans 2001).

(Fig. 1 - Coral Bleaching events between 1994 and 1998 - dark spots represent reports of bleached coral, light spots represent reports of healthy coral)
(Berkelmans 2001)

Thermal adaptation of coral could be achieved by transplanting heat-resilient zooxanthellae. A 2004 study found that in Guam, corals of the genus Pocillopora associate with both Symbiodinium C and thermally resilient species ‘D’ (Rowan 2004). In a 2006 research project, coral nubbins containing Symbiodinium D were transplanted to Magnetic Island, North Keppel Island and Davies Reef. Magnetic and North Keppel islands experienced significant increases in zooxanthellae density and reductions in bleaching/death of coral. Corals exposed to 32°C in the Keppel control had no zooxanthellae, with more than 60% of corals bleached and the rest dead. After treatment, over 50% of corals in this area at 32°C were surviving with reduced bleaching and significant reduction in mortality (Fig. 2) (Berkelmans & Van Oppen 2006).

(Fig. 2 - Zooxanthellae density in corals before and after transplanting at North Keppel Island sites (bar graph), pie graphs represent coral status; (grey) healthy, (white), bleached and (black) dead) (Berkelmans & Van Oppen 2006)

Coral bleaching is a significant problem for the GBR. In 1998, 87% of 2900 reef systems were affected by at least moderate bleaching (Berkelmans 2001). Coral transplanting has increased zooxanthellae density, and reduced coral bleaching/mortality but only in 30 - 32°C conditions. The increased tolerance of Keppel corals with Symbiodinium D is only about 1 - 1.5°C (Berkelmans & Van Oppen 2006). Transplanting of corals with Symbiodinium D has resulted in increased thermal tolerance of corals, however application of this research as a thermal adaptation would only be effective temporarily as temperatures continue to rise. 

References:

Ban, S.S. Graham, N.A.J. 2012, ‘Relationships between temperature, bleaching and white syndrome on the Great Barrier Reef’, Coral Reefs, Vol. 32, pages 1–12

Berkelmans, R. 2001, ‘Bleaching, upper thermal limits and temperature adaptation in reef corals’, PhD thesis, James Cook University

Berkelmans, R. Van Oppen, M.J.H. 2006, ‘The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change’, Proceedings of The Royal Society of Biology, Volume 273, pages 2305-2312. 

Rowan, R. 2004, ‘Thermal adaptation in reef coral symbionts’, Nature, Vol. 430, page 742

Strasser, R.J. Tsimilli-Michael, M. Pecheux, M. 1999, ‘Perpetual adaptation in a perpetually changing environment as a survival strategy of plants: a case study in foraminifers concerning coral reef bleaching’, Photosynthetica, Vol. 37, pages 71-85

Figures:

Figure 1: Berkelmans, R. 2001, ‘Bleaching, upper thermal limits and temperature adaptation in reef corals’, "Records of bleaching on the reef from 1994 to 1998", PhD thesis, James Cook University

Figure 2: Berkelmans, R. Van Oppen, M.J.H. 2006, ‘The role of zooxanthellae in the thermal tolerance of corals: a ‘nugget of hope’ for coral reefs in an era of climate change’, "Zooxanthella densityGs.e. (bars) and coral condition (pies) of coral nubbins", Proceedings of The Royal Society of Biology, Volume 273, page 2311

Thermal Adaptation - Behavioural Thermoregulation

An ectotherm is an organism with internal temperature that is similar to its external environment. Fish, reptiles and invertebrates are most prominent examples of ectotherms. The issue with ectothermy is that the increasing environment increases internal temperature, affecting physiology such as metabolism, circulation and reproduction (Speed et al. 2012). A change in body temperature by 1°C alters the rate of many physiological processes by 6–10% (Johnston & Bennett, 1996). For ectotherms to maintain optimal or preferred body temperature, they rely significantly on behavioural adaptations. This blog post will discuss the behavioural thermoregulation of ectothermic marine and freshwater fishes, and the trade-offs involved with this process.

   

The movement of fish species is dependent on many environmental variables. These include resource availability (prey), shelter from predation, oxygen availability, water currents, tidal movements etc. (Ward et al. 2010 & Speed et al. 2012). It is important when studying behavioural thermoregulation to ensure movement is directly caused by a need to alter environmental temperature, rather than a combination of other variables. This is difficult to achieve with fish species, considering that movement to warmer areas of water generally increases risk of predation. This presents a trade-off situation; growth, reproductive or survival related benefits from thermal refuge use must outweigh the risks and cost of refuge use for the strategy to make biological sense (Westhoff et al. 2014).

A 2012 study was conducted on the behavioural thermoregulation of reef sharks in areas of the Ningaloo Reef in Western Australia. It was found that on average, body temperatures of female blacktip reef sharks (Carcharhinus melanopterus) were consistently warmer than average (±SE) water temperature by 1.3 ± 0.57°C, as a result of behavioural thermoregulation (Speed et al. 2012). In 1978 a study was conducted on the sand goby (Pomatoschistus minutus) in Norway, an example of an extremely eurythermal fish (adapted to survive between 5 and 22°C.) Common for almost all the fish tested was a period of about 10 min immediately after transfer to the gradient trough when they hovered along the sides (Hesthagen, 1979). This period of time is inferred to be for the fish to determine its thermal preferendum, when provided with a range of different temperatures to select.

Behavioural thermoregulation is vital to the optimal growth and survival of aquatic and marine ectotherms. Studies of fish such as sharks (large scale predator) through to sand goby have shown that the majority of fish have a thermal preferendum, where growth and survival rates are at their best. However, the energy expended and risks involved with achieving thermal preferendum are varied greatly among species. The common ecological situation of risk vs reward is evident in behavioural thermoregulation.

References:

Hesthagen, I. H, 1979, ‘Temperature selection and avoidance in the sand goby, Pomatoschistus minutus (Pallas), collected at different seasons’,  Environmental Biology of Fish, Vol. 4, No. 4, pg 369-377

Johnston, I. A. & Bennett, A. F, 1996, ‘Animals and Temperature : Phenotypic and Evolutionary Adaptation’. Cambridge: Cambridge University Press.

Speed, C. W. Meekan, M. G. Field, I. C. McMahon, C. R. Bradshaw, C. J. A, 2012, ‘Heat-seeking sharks: support for behavioural thermoregulation in reef sharks’, Marine Ecology Progress Series, Vol. 463: pg 231–244

Ward, A. J. W. Hensor, E. M. A. Webster, M. M. Hart, P. J. B, 2010, ‘Behavioural thermoregulation in two freshwater fish species’, Journal of Fish Biology (2010) Vol. 76, pg 2287–2298  

Westhoff, J. T. Paukert, C. Ettinger-Dietzel, S. Dodd, H. Siepker, M, 2014, ‘Behavioural thermoregulation and bioenergetics of riverine smallmouth bass associated with ambient cold-period thermal refuge’, Ecology of Freshwater Fish 2016: Vol. 25, pg 72–85