Metabolic Rate

Cells need ATP to do their jobs but they only contain a limited store of ATP. When the demand for energy is high, as under intense activity, the ATP stores of cells are rapidly exhausted. Take a clawed frog for instance. The muscle cells the leg of this aquatic frog contain enough ATP for about 100 muscle contractions which is enough to swim a distance of about 1.4 meters. To swim further, the cells must synthesize ATP from molecules such as sugars, amino acids, and fatty acids. Cells make ATP through the process of cellular respiration. We can break down cellular respiration into two series of steps. The first series of steps occurs in the cytoplasm and without oxygen being present. This is the glycolysis and it produces 2 moles of ATP per mole of glucose. The other series of steps occurs in the mitochondrion. The last mitochondrial step, is the oxidative phosphorylation which requires oxygen and produces the most ATP: 34 moles of ATP per mole of glucose. The citric acid cycle (aka  the Krebs cycle), also occures in the mitochondrion and produces two moles of ATP per mole of glucose. So overall, when oxygen is present, cellular respiration pumps out 38 moles of  ATP per mole of glucose.

Sometimes, the supply of oxygen cannot keep up with the demand for ATP. That may occur for instance under intense activity like sprinting. In such situation the first series of steps (glycolysis) are ramped up to meet the demand for ATP. Although glycolysis alone produces less ATP per mole of substrate than the whole process of cellular respiration, it does so at a much faster pace. Muscles fibers used for burst of activity, like the jumping muscles of frogs rely more on glycolysis to produce ATP. These so called white or fast twitch muscle fibers have fewer mitochondria that than so called red or slow-twicth muscle fibers which are associated with sustained activities and rely primarily on cellular respiration as the source of ATP. For instance the trunk muscles in male frogs sustain long period of calling and are made of slow-twitch muscle fibers.

Animals have different types of muscles Muscle associated with bursts of activity like the jumping leg muscles of frogs, tend to have a relatively high concentration anaerobic muscle fibers (white muscle fibers). Muscles associated with sustained activity, like the trunk muscles of a calling male frog have a high concentration of aerobic muscle fibers (red muscle fibers).

Aside from the occasional bursts of activity, amphibians and reptiles rely on aerobic metabolism for their routine activities so they must obtain oxygen from their environment to keep the cellular machinery going. Oxidative metabolism produces water and carbon dioxide.  The latter must be eliminated from the body or it will react with water to create carbonic acid and that’s a bad thing. The business of moving oxygen into the body and moving carbon dioxide outside the body is the focus of this section.

The amount of energy an animal uses can be estimated from the volume of oxygen it consumes or of carbon dioxide it excretes. In mammals and birds, the amount of energy necessary to maintain an organism alive is called the Basal Metabolic Rate (BMR). BMR can be measured from the rate of O₂ consumption (or CO₂ production) in a resting, non-digesting individual.  The same is true for ectotherms except that the rates of O₂ consumption and CO₂ production vary with body temperature. In ectotherms, the equivalent of the basal metabolic rate is called the Standard Metabolic Rate (SMR). The effect of body temperature on the SMR can be quantified by measuring how much O₂ consumption changes when the body temperatures changes by 10°C. This measure is called the Q10.

As we’ve seen, endothermy has a high energetic cost. The BMR of a mammal or a bird is 7 to 10 times greater than that of an amphibian or reptile of equivalent mass. That is when animals are at rest. The difference in energy expenditure between endotherms and ectotherms is much greater for active animals. Field active birds and mammals consume 12 to 20 times more energy than field active herps of comparable mass.  An important consequence of a high octane endothermic life is that less energy is channeled towards growth and reproduction.  Indeed, birds and mammals convert about 2% of the energy contained in their food into biomass compared to 40 to 80% in amphibians and reptiles. Amphibians and reptiles can thus thrive is environments with relatively low productivity.

Gas Exchange

For birds and mammals, the business of gas exchange is relatively straightforward. Oxygen exclusively comes from the atmosphere and it enters the blood through the lungs. Amphibians and reptiles, in contrast, have more ways to obtain oxygen and they can get it from the atmosphere as well as from the water.

Pulmonary Gas Exchange

Amphibians

All reptiles and most amphibians have lungs as adults. As we have seen previously, amphibians  do not have a rib cage so they cannot ventilate their lungs like amniotes.  Inhalation in mammals  is achieved by expanding the volume of the thoracic cavity through the depression of the diaphragm, as well as through the contraction of the costal and intercostal muscles which pull on the ribs. The expansion of the thoracic cavity decreases the pressure inside the lungs which in turn draws in fresh air through the nose or mouth.  In other words the expansion of the thoracic cavity decreases the pressure inside the lungs favouring the movement of air from a zone of relative high pressure (outside) to a zone of relatively low pressure (inside).  This form of lung ventilation is called negative pressure ventilation. Exhalation, in contrast to inhalation, is a passive process. As the diaphragm and the costal and intercostal muscles relax, the volume of the thoracic cavity decreases and the stale air is pushed out of the lungs. Negative pressure lung ventilation is not possible in amphibians which lack a rib cage. Instead, amphibians pump air into their mouth through their nostrils, and then force it into their lungs using their throat.

If you watch a frog or a salamander for a few seconds, you will notice that the throat is constantly moving up and down.  This pumping of the buccopharyngeal area is the main way by which amphibians ventilate their lungs. Amphibians push air inside their lungs instead of sucking it in as mammals and reptiles do. This ventilation system is thus based on positive pressure instead of negative pressure.

Lung ventilation in amphibians is powered by the hyoid apparatus and its associated muscles. When the hyoid is depressed, the volume of the buccal cavity increases and fresh air is sucked in through the nostrils. The fresh air is held inside the mouth while the stale air leaves the lungs via the glottis and escapes through the nostrils. The nostrils are then shut by a valve and the hyoid is pushed up forcing the fresh air inside the lungs through the glottis. The two air masses mix in the mouth but because more fresh air is being drawn in than stale air is being released, about 80% of the air entering the lungs is fresh and 20% is re-breathe.

Lungless Salamanders

Some amphibians have given up on lungs altogether. All the members of the big family Plethodontidae lack lungs and rely almost exclusively on cutaneous respiration as adults.  Some plethodontids are aquatic or semi-aquatic like the genus Eurycea but many species are exclusively terrestrial like the genus Plethodon. Terrestrial lungless salamanders face an important trade-off between hydration and gas exchange and their distribution is limited to moist environments. These salamanders spend most of their time underground and only surface on cool and wet days.

As explained above, amphibians use their hyoid apparatus to force air into their lungs. The evolution of lunglessness in plethodontid salamanders has allowed some species to repurpose their hyoid apparatus into a feeding weapon. Some species of plethodontids, such as Hydromantes sp, have evolved the ability to literally shoot their hyoid outside of their mouth along with their sticky tongue but more on this in the unit on feeding.

Reptiles

Reptiles have a rib cage and, like mammals, they ventilate their lungs using negative pressure. The structures responsible for gas exchange in the reptilian lung are called faveoli (sing. faveolus). These structures are equivalent to mammalian alveoli.

Interestingly, locomotion interferes with gas exchange in lizards. Lizards bend side to side when they walk: a form of locomotion called lateral undulation.

The muscles used to bend the trunk during locomotion are also used to ventilate the lungs. This dual role creates a conflict between locomotion and lung ventilation. Moreover, the lateral bending increases the pressure in the lung on the concave side and decreases the pressure in the lung on the convex side causing air to flow between lungs with little ventilation through the trachea (see animation). These constraints, called Carrier constraints (after the biologist David Carrier), may explain why most lizards only move in small bursts.

Body elongation as seen in some squamates (including all snakes) as well as in caecilians, constrains the size and shape of organs. Lungs are no exception. In both snakes and caecilians the left lung is atrophied and non-functional. In most snakes the left lung is 1-2% of the size of the right lung. The right lung of snakes has two compartments. The vascular lung (anterior) and the saccular lung (posterior). The vascular lung is the site of gas exchange while the saccular lung appears to play a role in regulating ventilation and in controlling buoyancy.

The rib cage of turtles has evolved into a stiff shell that cannot change its volume so turtles cannot ventilate their lungs the same way other reptiles do. The turtle’s shell thus evolved in concert with an alternative and unique mode of lung ventilation. The lungs of turtles are sitting on top of the visceral mass (the gut) to which they are attached with stiff mesenteric tissues. This connection forms a non-muscular diaphragm of sort. The dorsal part of the lungs is  attached to the carapace by mesenteries. Using pairs of anterior (serratus and pectoralis) and posterior (abdominis) muscles, the turtle can push or pull on its gut which itself can push or pull the lungs.

During inhalation, the serratus muscle pulls the forelimb forward and outward which creates more space in the abdominal cavity. At the same time, the obliquus abdominis muscle pulls the gut towards which further increases the space inside the shell. These actions cause the gut to drop down, pulling the lungs with it. Pulling on the lungs increases their volume, causing the internal pressure to drop which in turns allows air to flow in. To exhale, the turtle contracts the pectoralis and tranversus abdominis which push the gut against the lungs, decreasing the lung volume and increasing internal pressure, forcing the stale air out.

Non-Pulmonary Gas Exchange

Gills

Amniotes do not have gills, but amphibians do. Most amphibians have gills only at the larval stage. Gills are external in larval salamanders but internal in frog tadpoles. In the latter, gills are ventilated by pumping water in the mouth and over the gills. The pumped water then exits through an opening called the spiracle.

In some species of salamanders, the gills are retained in adults. The retention of juvenile traits such as gills into adulthood is called paedomorphosis. Gills (and other larval traits) are retained in adults because their development slows down relative to the development of sexual traits. Therefore, the salamander matures while retaining some larval traits. This process, in which some body parts develop at a slower rate that sexual organs, is called neoteny. Neoteny is thus a way by which paedomorphosis is achieved. In salamanders like the mudpuppy (Necturus maculosus), the retention of gills and other larval traits is obligatory. In other words, mudpuppies can never undergo metamorphosis.  In contrast, some salamanders in the genus Ambystoma (including the Axolotl; Ambystoma mexicanum) can retain their gills into adulthood but these species may still metamorphose.

Cutaneous gas exchange

All amphibians use cutaneous gas exchange, but its importance varies among species. Cutaneous gas exchange accounts for 20-90% of oxygen uptake and for 30-100% of carbon dioxide excretion in amphibians.

Permeability to gases is inseparable from permeability to water so cutaneous gas exchange and water regulation are intrinsically linked in amphibians. How much a species relies on cutaneous gas exchange thus depends greatly on the availability of moisture in its habitat (see unit on osmoregulation).

Amphibians possess a network of respiratory capillaries near the surface of their skin. Depending on the species, 20 to 95% of the respiratory capillaries are found in the skin and skin capillaries can be more abundant than pulmonary capillaries. Gas diffusion through the skin (as through any respiratory surfaces) follows Fick’s law of diffusion. According to this law, the diffusion speed through the skin is a function of diffusion distance, the surface area of the skin exposed to diffusion, and the partial pressure gradient across the diffusion surface.

As we saw, the skin of amphibians is relatively thin which reduces the diffusion distance. Moreover, the skin capillaries of amphibians are in the epidermis (they are in the dermis in most vertebrates) which further reduces the diffusion distance. As thin as it is, the skin of amphibians is still 10 to 100 times thicker than lung epithelia so cutaneous gas exchange is much slower than pulmonary gas exchange. Moreover amphibians cannot activelt ventilate their skin the same way they can ventilate their lungs (see below).

Some species, such as the hellbender (Cryptobranchus alleganiensis) and the lake Titicaca frog (Telmatobius coleus), have large flaps of skin which increase the surface area of the skin exposed to water. These adaptations are found only in fully aquatic species because so much exposed surface area would lead to rapid water loss on land.

Both gills and lungs are paired with ventilation systems allowing “fresh” air or water to flow over them. The skin can only be ventilated through movement of either the animal itself or of the fluid over of the animal (e.g. wind, flowing water).  In the absence of such movements, the partial pressure of oxygen in the layer of fluid in direct contact with the animal will decrease as oxygen is consumed, resulting in a hypoxic boundary layer around the animal.  This may be particularly problematic for frogs and turtles hibernating in water. Submerged frogs have been observed to increase activity in response to hypoxia probably as a mean to disrupt the hypoxic boundary layer. Similarly, softshell turtles do “push-ups” during hibernation seemingly to ventilate their skin.

The importance of the cutaneous respiration in amphibians is apparent in their circulatory system. In other tetrapods, the de-oxygenated blood goes to the lungs via the pulmonary artery but in amphibians, it leaves the heart via the pulmocutaneous artery which sends it to both the lungs and the skin to be oxygenated. The pulmocutaneous artery splits into the pulmonary artery which goes to the lungs and the cutaneous artery which goes to the skin.  The skin circuit is however less efficient than the lung circuit because the oxygenated blood returning from the skin mixes with the de-oxygenated blood returning from the systemic circulation before entering the heart.

Amphibians have a so-called three-chambered heart with two atria and a single ventricle. In theory, a single ventricle should result in the mixing of the oxygenated and de-oxygenated bloods.  Amphibians however manage to minimize the mixing of bloods. It is not entirely clear how the oxygenated and de-oxygenated bloods are kept separate but it probably involves ridge like structures called trabeculae lining the ventricle.  The compartments formed by these ridges may trap the oxygenated and de-oxygenated bloods in separate areas. During a heart contraction, the ridges on the left side of the heart guide the oxygenated blood into a spiral valve which sends it to the systemic circulation. The de-oxygenated blood is directed by the spiral valve into the pulmocutaneous circulation.

For most reptiles, the lungs are the only site of gas exchange. Aquatic reptiles can however perform gas exchange via non-pulmonary routes. Both aquatic snakes and turtles use cutaneous gas exchange when in water. Cutaneous gas exchange is particularly important in hibernating turtles. In Ontario, the spiny softshell turtle (Apalone spiniferus) and the common musk turtle (Sternotherus odoratus) use cutaneous respiration extensively in winter. Spiny softshell turtles use their skin to uptake up to 38% of their O₂ and to excrete up to 95% of their CO₂. In the common musk turtle, the skin accounts for up to 26% of the O₂ uptake and up to 56% of CO₂ excretions. Both species also appear to have a third gas exchange surface inside their mouth. The tongue and pharynx of the common musk turtles have many heavily vascularized folds which have been suggested to play a role in gas exchange. Softshell turtles have a network of villiform processes which are, like the folds inside the mouth of musk turtles, heavily vascularized.

In aquatic turtles, the cloaca has side pockets called cloacal bursae which are mainly used as ballasts to regulate buoyancy.  In a handful of pleurodires (side-neck turtles) turtles however, these pockets have been co-opted into gas exchange organs. In those species, the cloacal bursae are lined with vascularized finger-like projections (papillae), which are themselves covered by smaller projections creating a large surface area for gas exchange. The cloacal bursae are ventilated with water by active pumping by the cloaca. Cloacal respiration appears to account for 48% of aquatic gas exchange in the Fitzroy River Turtle (Rheodytes leukops) and probably extend dive duration.

Cloacal gas exchange is often cited as important in overwintering turtles including species like the painted turtle. This claim is in fact unsubstantiated. North American turtles overwintering for months all belong the cryptodires sub-order of turtles and do not possess cloacal adaptations for gas exchange seen in some pleurodires. In fact, it has been shown that painted turtles cannot perform cloacal gas exchange. For more on widespread myth of “butt-breathing” in turtles, see this article.

References

Bonnan, M. F. (2016). The Bare Bones: An Unconventional Evolutionary History of the Skeleton (Life of the Past) (Illustrated ed.). Indiana University Press.

Carrier, D. R. (1987). The evolution of locomotor stamina in tetrapods: circumventing a mechanical constraint. Paleobiology, 13(3), 326–341. https://doi.org/10.1017/s0094837300008903

FitzGibbon, S., & Franklin, C. (2010). The importance of the cloacal bursae as the primary site of aquatic respiration in the freshwater turtle,Elseya albagula. Australian Zoologist, 35(2), 276–282. https://doi.org/10.7882/az.2010.016

Heiss, E., Natchev, N., Beisser, C., Lemell, P., & Weisgram, J. (2010). The Fish in the Turtle: On the Functionality of the Oropharynx in the Common Musk Turtle Sternotherus odoratus (Chelonia, Kinosternidae) Concerning Feeding and Underwater Respiration. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, 293(8), 1416–1424. https://doi.org/10.1002/ar.21185

Lőw, P., Molnár, K., & Kriska, G. (2016). Atlas of Animal Anatomy and Histology (1st ed. 2016 ed.). Springer.

Luchtel, D. L., & Kardong, K. V. (1981). Ultrastructure of the lung of the rattlesnake,Crotalus viridis oreganus. Journal of Morphology, 169(1), 29–47. https://doi.org/10.1002/jmor.1051690104

Olesen, S. P., de Saint-Aubain, M., & Bundgaard, M. (1984). Permeabilities of single arterioles and venules in the frog skin: A functional and morphological study. Microvascular Research, 28(1), 1–22. https://doi.org/10.1016/0026-2862(84)90025-6

Shelton, G., & Boutilier, R. (1982). Apnoea in Amphibians and Reptiles. Journal of Experimental Biology, 100(1), 245–273. https://doi.org/10.1242/jeb.100.1.245

Wikipedia contributors. (2020, December 11). Buccal pumping. Wikipedia. https://en.wikipedia.org/wiki/Buccal_pumping

Yokosuka, H., Murakami, T., Ishiyama, M., Yoshie, S., & Fujita, T. (2000). The Vascular Supply of the Villiform Processes in the Pharynx of the Soft-Shelled Turtle, Trionyx sinensis japonicus. A Scanning Electron Microscopic Study of Corrosion Casts. Archives of Histology and Cytology, 63(2), 193–198. https://doi.org/10.1679/aohc.63.193