Metabolic responses to exhaustive exercise in larva, juvenile and adult lampreys (Geotria australis)

Karen Marshall

doi:10.60867/00000110

Understanding how exercise affects the biochemistry of fish has important implications for the fishing industry, as well as for those involved in aquaculture. Research into this area can also lead to increases in our understanding of health issues for humans and animals alike. One of the aims of this research study was to gain a better understanding of the biochemistry of lampreys; specifically, the anadromous Geotria australis—a Southern Hemisphere lamprey—which is sadly declining in abundance. G. australis is one of only five lamprey species representing the early agnathan (jawless) stage of vertebrate evolution found in Australasia. And, as I will be outlining in the following chapters, G. australis is a very remarkable lamprey. Chapter 1 is a literature review into the subject of fish and the biochemistry of exercise and outlines why this exciting area is so important. Chapter 2 describes the general methodology that I used in this research and is therefore relevant to all experimental chapters. Where there are specific differences in methodology, this has been outlined in that chapter. I examined the metabolic responses in larva, juvenile and adult lampreys (G. australis) subjected to exhaustive exercise, including the effects on lipid and carbohydrate metabolism. Most literature currently available on exercise physiology of lampreys deals with upstream adult lampreys and their glycogen requirements; therefore, I also examined the other two lifecycle stages: specifically, G. australis larval and juvenile animals, to fill this gap in lamprey knowledge. In Chapter 3, I investigated the metabolism of exercising larvae and juveniles to determine their reliance on aerobic and anaerobic metabolism during such activity. From my research, it was found that when stimulated to swim continuously at a moderate rate, the larvae of G. australis could only swim for approximately 20 min; whereas, the juveniles of this species, following similar swimming activity over the same period, did not become exhausted. Mean concentrations of muscle glycogen in larvae declined during exercise but returned to resting levels within 30 min of recovery, whereas those of the juveniles changed little during the corresponding periods. At the same time, muscle lactate concentrations of larvae rose markedly during exercise and the first 30 min of recovery, before declining significantly, while those of juveniles remained similar during and immediately after exercise. Calculations, using the glycogen and lactate concentrations immediately after exercise, suggested that during exercise glycogen is, to some extent, utilised anaerobically (approximately 24%) by larvae, but only aerobically by juveniles. Furthermore, since juveniles used only a small amount of glycogen, they presumably metabolised triacylglycerol aerobically to produce energy. Muscle glycerol-3-phosphate levels were far higher prior to and immediately after exercise in juveniles than in larvae and then declined precipitously. The above trends in muscle glycogen and lactate of larval G. australis parallels, to some degree, those recorded by other workers for upstream migrant Petromyzon marinus that had been exercised to exhaustion. I then, as outlined in Chapter 4, subjected adult upstream migrating G. australis lampreys to an exercise/recovery regime at the commencement and end of their 13-15-month non-trophic, upstream spawning migration. In early (immature) migrants and prespawning females, muscle glycogen was markedly depleted during exercise but became rapidly replenished. As muscle lactate rose during exercise and peaked 1–1.5 h into the recovery period, and therefore after muscle glycogen had become replenished, it cannot be the direct source for that replenishment. However, both plasma lactate and glycerol (but not muscle glycerol and glucose) rose sharply during exercise and then declined markedly during the first 0.5 h of recovery. They thus exhibited the opposite trend to that of muscle glycogen, implying that these limited pools of glycogenic precursors contribute to glycogen replenishment. Although plasma glucose rose following exercise and consequently could also be a precursor for muscle glycogen replenishment, it remained elevated even after muscle glycogen had become replenished. While resting prespawning females and mature males retained high muscle glycogen concentrations, this energy store became permanently depleted in females during spawning. In mature males, muscle glycogen remained high and lactate low during the exercise/recovery regime, whereas muscle glycerol declined precipitously during exercise and then rose rapidly. In summary, vigorous activity by G. australis is fuelled extensively by anaerobic metabolism of glycogen early in the spawning run and by prespawning females, but by aerobic metabolism of its energy reserves in mature males. In Chapter 5, I attempted to further elucidate how lipid, protein and glycogen metabolism contribute to generating the ATP required by G. australis during its very long, non-trophic upstream spawning migration. Energy is required for maintenance, swimming, the development of gonads and secondary sexual characters and spawning and post-spawning activities. Plasma and muscle metabolites were measured in animals subjected to an exercise-recovery regime at the commencement and completion of the spawning run. This study demonstrated that at all stages of the migration, plasma glucose and glycerol concentrations increased during exercise and then declined, whereas plasma FFAs exhibited the reverse trend. During exercise and recovery, alanine declined, and ammonia increased in the plasma of early migrants, while the opposite occurred in mature males. Following exercise, muscle alanine rose and then declined in early migrants but declined and then rose in mature males. The composite data emphasised that, while the same catabolic processes are employed by both sexes early in the migration, when animals are immature, they differ markedly between the sexes as they mature and then spawn, reflecting their different demands. Energy is supplied predominantly via anaerobic metabolism in early migrants, but by anaerobic and aerobic metabolism in prespawning females and by aerobic metabolism in mature males and senescent females. Although proteolysis is limited early in the migration, it is employed extensively during maturation and particularly by females, which undergo a substantial reduction in length in the lead-up to spawning. In Chapter 6, I outlined the conditions in which the G. australis were kept in the laboratory and the behaviour I observed over many years. The adults were caught soon after they had entered rivers on their non-trophic upstream migration and were maintained in the laboratory tanks for 13–15 months through to spawning. As the adult G. australis were susceptible to haemorrhagic septicaemia, they were treated prophylactically and maintained in aquaria supplied with a flow-through charcoal filtration system and UV steriliser. Air temperature and the light: dark regime was constantly adjusted to parallel those in the environment. Males developed the very large suctorial disc and gular pouch characteristic of maturity and both sexes matured at the same time as in the wild. While males frequently showed aggressive behaviour towards each other, the same male and female mated on several occasions. The male coiled around the female and, with his urogenital papilla close to the female’s cloaca, twisted and vibrated, leading to egg release. These eggs formed coagulated clusters as in the wild, with many progressing through to the eight-cell stage. Remarkably, numerous G. australis were still alive 95–392 days after the end of the short spawning period, and one male was still alive after a further 119 days. Postspawning survival would be facilitated inter alia by extensive proteolysis, reflected in a shortening of the body. The data in this research emphasised that G. australis is a highly atypical lamprey and provides invaluable information for conserving this declining species. In Chapter 7, I summarised my research findings and discussed future directions.

Metabolic responses to exhaustive exercise in larva, juvenile and adult lampreys (Geotria australis)

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