One defining feature of Peter Lutz's career was that he was fascinated by a wide range of animals and how they coped with environmental extremes,particularly hypoxia and anoxia. When he passed away in February 2005, his friends and colleagues wanted to celebrate his career and the diversity of his research interests. The four papers featured in this issue of The Journal of Experimental Biology touch on many aspects of how animals survive with little or no oxygen. They follow on from the major contributions that Peter Lutz made to the study of diving adaptations in sea turtles, and also to the understanding of the mechanisms of anoxic brain survival in the freshwater turtle.
It is because of the extraordinary ability of freshwater turtles to survive anoxia that they have been intensively studied as anoxic `model organisms'. Moving from the turtle brain to the turtle heart, Johannes Overgaard, Hans Gesser and Tobias Wang review how freshwater turtles' hearts cope during anoxia and hypoxia (p. 1687). During the cold winter months, turtles settle down on pond beds to see through the winter as ice forms on the surface above. Under these anoxic conditions, few animals would survive, but many turtles emerge from their overwintering unscathed. How do they keep their cellular energy levels high enough so that cells don't die, but not run down their precious energy supplies? Turtles have an arsenal of coping mechanisms at their disposal, from matching their energy use with the low amount of ATP produced by anaerobic metabolism, to relying on breakdown of the molecule phosphocreatine to top up ATP levels and using their shells to buffer against the acidic conditions.
Moving from turtles to fish, Tony Farrell discusses another cardiac response to low oxygen: hypoxic bradycardia, where heart rate slows down dramatically when oxygen is scarce(p. 1715). But what are the benefits to the fish? Researchers suspect that bradycardia benefits the heart muscle because blood is held within the heart for longer, giving oxygen more time to diffuse into the muscle. An unusual property of fish heart muscle allows them to extensively increase cardiac stroke volume – the volume of blood shifted out of the ventricle per heart beat – while maintaining cardiac output, the total volume of blood pumped each minute. Not only will this send enough blood to the body tissues, but also stretch the walls of the heart, further favouring oxygen diffusion, and allowing the fish to draw out as much oxygen as possible from the ever dwindling supply in venous blood. Bradycardia severe enough to reduce the heart's output and demand for ATP could also be beneficial if the heart has to temporarily perform without any oxygen and rely on glycolysis, something that Peter Lutz's favourite animal model, the turtle, are experts at. Farrell also highlights the intriguing possibility that some fishes lost the bradycardia response when they evolved air breathing: the circulatory design of fish means that air breathing during hypoxia raises oxygen partial pressure in venous blood and hence oxygen availability to cardiac tissues.
Low oxygen levels do more than just trigger a cardiac response; when the going gets tough animals slow down their metabolism, which can also occur if the temperature plummets or if food and water are scarce. As Kenneth and Janet Storey explain, hypometabolism caused by hypoxia is easiest to study, and the freshwater turtle is the experimental organism of choice for many researchers(p. 1700). Animals need to ensure that their cells have enough ATP to survive so hypometabolism is highly regulated. They both minimize and reprioritize their ATP use to sustain necessary processes such as ion pumping and largely shut off optional ones like protein synthesis. At the same time other processes swing into action to protect the cell, including antioxidants, which mop up damaging reactive oxygen species, and chaperone proteins and protease inhibitors that protect the cell's macromolecules. This ensures that the molecules stay stable and cells remain viable, ready for action when oxygen levels rise once more.
Meanwhile, some colourful newcomers to the field of hypoxia research have been introduced by Göran Nilsson, Jean-Paul Hobbs and SaraÖstlund-Nilsson (p. 1673). Tropical coral reefs are littered with hypoxic hotspots and the brightly coloured fishes that teem over the reefs have to be very adaptable to these conditions. At night, crevices in between corals become hypoxic since photosynthesis has stopped, however fish rely on these crevices to hide from predators. Fishes may also become trapped in hypoxic shallow pools when the tide goes out at night, and some are able to breathe air by absorbing oxygen through their skin when the coral becomes exposed. Another challenge faced by the males of some mouth-brooders is maximising clutch size,while still being able to swim and keep water flowing over the gills. While researchers have only just begun to scratch the surface of how these fish adapt to hypoxia, studying one of the most diverse vertebrate communities in the world means that researchers `can be certain that a wealth of respiratory adaptations remain to be discovered among coral-reef fishes', says Nilsson.
It is clear from the papers in this tribute that Peter Lutz's contributions to integrative physiology continue to inspire researchers studying animals in hypoxic environments. As Tony Farrell writes, `he sought answers to the question why...and had an infectious enthusiasm for science'. Nilsson is sure that Lutz would have joined him and his colleagues in their study of tropical fishes, continuing to challenge himself and others to make exciting discoveries.
