Friday, February 14, 2014

The missing link in respiration: The Lungfish

By: Denver Coleman


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            Cory wrote an exceptional blog post about avian respiration and how these organisms push the boundary of efficient biological design. I want to take a step back and look at the development of atmospheric respiration in the animal kingdom.


As small children we are taught that the ocean is filled with a multitude of fish and invertebrates, like the mantis shrimp, and the land we live on is stocked full of lions, tiger and bears. Oh my! (One day that joke will get old, but today is not that day.) However, there is one animal that breaks free of this stereotypical taxonomic bond. These animals are too awesome to be restricted to one ecosystem. They are the masters of both the land and sea. They are… the Lungfish of the subclass Dipnoi. As its name implies these creatures are capable of living and breathing in water as well as on land. Lungfish utilize a modified gas bladder to store atmospheric oxygen, thereby turning it into a respiratory organ (Burggren 1988). They are so adapted to being a “fish out of water” that during drought conditions they can even enter a state of sleep known as aestivation for as long as four years while waiting for a drought to pass (Johansen 1968). This animal make Aquaman look like a little pansy. Since these animals can survive in both aquatic and terrestrial environments they have become a model organism for studying the tetrapod transition from sea onto land. In this article, we will explore the anatomy and physiology behind respiration and circulation in lungfish.

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Considered a living fossil, the lungfish has remained unchanged for over 400 million years and dates back to the Devonian era. This monophyletic group of freshwater fish can be found in tropical regions of Africa, South America and Australia (Graham 1997). They are considered the oldest air-breathing organisms that are still extant and some species like the Lepidosiren paradoxa have even developed mobile pelvic and pectoral fins to allow for movement across land (Bishop & Foxon 1967).

Living in some of the driest parts of the world can be tough on a fish. When the waters dry up, the Lungfish will digs itself into the mud by gulping down sediment and expelling it through its operculum (gill flap). It will then secrete gooey mucus from its body that completely encases its body in a slime sarcophagus. This is vaguely starting to sound like my high-school prom date. Inside this cocoon the Lungfish will enter a state of aestivation, characterized as a depressed metabolism and heart rate, a suppression of urine and an increase in the production of metabolites (Burggren & Johansen 1986; Fishman et al. 1992). The adaption for atmospheric inspiration allows the Lungfish to survive through the longest of drought seasons.


           If it isn’t already obvious, a fish shouldn’t be able to breath oxygen. If you have ever gone fishing you will remember the fish gulping down air as it is pulled from the water. Teleost gills are designed for the diffusion of oxygen in water and cannot properly function in the air. These guys will just drop on the deck and flop like a fish. SPONGEBOB SQUAREPANTS!  In order to better understand this weird mechanism behind a Lungfish’s breathing ability we need to look at its anatomical structures.

            It’s important to note that lungfish are not the only species to have developed the ability to inspire atmospheric oxygen. The evolution of aerial respiration has arisen in more than 70 of the 4,000 known genera of fish (Bertin 1958; Gans 1970). Fish have developed air breathing from multitude of organs, including the alimentary canal, pharynx, air bladder, and esophagus and the development of the air-breathing organs in Lungfish is considered relatively simple when compared to that of tetrapods (Johansen 1970).

The gas exchange of CO2 and O2 in Lungfish.
Johansen & Lenfant 1968
            A typical fish uses counter current exchange to acquire O2 and expel CO2. Water flows over the gills in the opposite direction as blood to allow for maximum extraction of O2 from water. In hypoxic environments a large stress is put on the organism to maintain a diffusive balance. Lungfish have developed lungs in order to maintain plasma O2 levels even in the presence of low oxygenated water.  In a study on Protopterus aethipicus, researchers used X-ray imagining to examine the mechanism behind gill and lung respiration (McMahon 1969). Researchers found that in an aquatic environment the P. aethipicus will utilize a combination of buccal pumping and opercula suctioning to transport water across its gills. Interestingly in the presence of air the animals will open its glottis at the back of its throat to expose its alimentary canal. This is seen as the action of swallowing surface oxygen. The opercular gill flaps are kept closed by the constrictor muscles to prevent oxygen from escaping over the gills (Burggren & Johansen 1986) and the animal will then close its mouth on the air and depress its buccal floor to force the oxygen into the air bladder. This swallowed air in the bladder comes in contact with the highly vascularized epithelial tissue and subsequent gas exchange can occur. This use of a primitive lung for respiration is often times secondary to the gills, but in some species aerial ventilation is required for survival. In adult Protopterus and Lepidosiren, at least 90% of O2 uptake occurs in the lungs (Burggren & Johansen1986). I guess this answers the question I asked as a child: Can a fish drown? Yes! Studies have shown P. aethipicus to be so dependent on its pulmonary respiration that blood O2 will remain unchanged even in the presence of hypoxic waters (Johansen & Lenfant 1968). Before the developmental importance of the ribs and diaphragm, scientists believe the earliest tetrapods utilized this this type of buccal-pressure-pumping (McMahon 1970). The Lungfish evolved this dual breathing mechanisms and therefore had to develop a similarly unique method of circulation.


Blood Shunting in the Lungfish.
Szidon et al 1969
Teleost fish have a single circuit system that goes in sequential order from the heart to the gills to the systemic tissues and back to the heart. This type of circulation is simple and is able to support the basic demands of a fish. The Lungfish has developed a divergent circulatory system that can travel to either the gills or the lungs. This dichotomous circulation prevents the unused respiratory organ from becoming an oxygen sink that would steal oxygen from the circulation. To accommodate divergent circulation the Lungfish pumps blood through trabeculated grooves in its heart to prevent the mixing of oxygenated and deoxygenated blood (Szidon et al 1969; Icardo et al 2005). These animals can shunt blood through its spiral and ventrolateral grooves to flow to the appropriate respiratory organ (Johansen & Burggren 1980). Depending on its current environment the Lungfish can decide to bypass either the lungs or the gills based on their oxygen demands. This quick transitioning allows the animal to avoid predation by escaping into an adjacent environment.

            This exceptional ability of the lungfish to differentiate itself from the stereotypical fish model has given it an evolutionary advantage over non-air breathing fish. Air breathing has developed in a number of ways amongst fish, but it has developed most extensively in the Lungfish. These animals have remained in a flux between an aquatic and terrestrial environment for hundreds of millions of years, allowing it to exploit a unique niche in semi-xeric environments. They maintain their significance in scientific research because of their distinctive anatomical structures in the presence of a myriad of environmental stressors.

Everyone loves a Lungfish.
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Bertin, L. 1958. Organes de la respiration aerienne. Traite de Zoologie 13: 1363-1374.

Bishop, I.R., and E.H. Foxon. 1967. The mechanism of breathing in the South American Lungfish, Lepidosiren paradoxa: A radiological study. Journal of Zoology 154: 263-271.

Burggren, W.W. 1988. Cardiac design in lower vertebrates: What can phylogeny reveal about ontogeny.  Experientia 144: 919-930.

Burggren, W.W., and K. Johansen. 1986. Circulation and respiration in lungfishes Dipnoi. Journal of Morphology Supplement 1: 217-236.

Fishman, A.P., R.J. Galante, A. Winokur, and A.I. Pack. 1992. Estivation in the African lungfish. American Philosophical Society 136: 61-72.

Gans, C. 1970. Strategy and sequence in the evolution of the external gas exchangers of ectothermal vertebrates. Forma et Functio 3: 61-70.

Graham, J.B. 1997. Air-breathing fishes: Evolution, diversity and adaptation. San Diego, C.A. Academic Press, pp. 299.

Icardo, J.M., E. Brunelli, I. Perrotta, E. Colvée, and W.P. Wong. 2005. Ventricle and outflow tract of the African lungfish Protopterus dolloi. Journal of Morphology 265: 43-51.

Johansen, K. 1970. Air breathing in fishes. Fish Physiology 4th ed. New York, N.Y. Academic Press, pp. 361-411.

Johansen, K., and W. Burggren. 1980. Cardiovascular function in lower vertebrates: Hearts and heart-like oreans. New York, N.Y. Academic Press, pp. 61-117.

Johansen, K., and C. Lenfant. 1968. Respiration in the African lungfish, Protopterus aethiopicus: Control of breathing. The Journal of Experimental Biology 49: 453-468.

McMahon, B. 1969. A functional analysis of the aquatic and aerial respiratory movements of an African lungfish Protopterus aethiopicus, with reference to the evolution of the lung-ventilation mechanism in vertebrates. The Journal of Experimental Biology 5: 407-430.

McMahon, B. 1970. The relative efficiency of gaseous exchange across the lungs and gills of an African lungfish Protopterus aethiopicus. The Journal of Experimental Biology 52: 1-15.

Szidon, J.P., L. Sukhamay, M. Lev, and A.P. Fishman. 1969. Heart and circulation of the African Lungfish. Circulation Research 25: 23-38.

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