The first terrestrial animals were true pioneers. Having heaved themselves out of their swampy homes onto dry land, they were finally able to take full advantage of the metabolic benefits of unfettered access to an abundant oxygen supply. But what advantages could this oxygen bonanza provide for fish eggs laid out of water? Michael Wells, Andy Turko and Patricia Wright from the University of Guelph explain that so long as the developing fish embryos remain moist, they should develop faster than their aquatic counterparts, thanks to the enriched oxygen. However, no one had ever systematically compared the metabolic trade-offs when fish eggs develop in water and air. Explaining that the amphibious fish mangrove rivulus is equally happy laying its eggs in and out of water and that the fish are capable of self-fertilization – producing batches of genetically identical eggs – Wright and her colleagues set about assessing the benefits of a terrestrial versus aquatic start in life for fish embryos.
Suspecting that an abundant oxygen supply would improve the fish's fecundity, Wells measured the egg production of adult rivulus in water and on land and found that the terrestrial fish produced almost three times as many eggs as the fish in water. In addition, the eggs that were exposed to air developed faster than the aquatic eggs, with 95% reaching a stage where they could hatch after 15 days, compared with 45% in aquatic eggs. And when Wells compared how much oxygen the two sets of embryos consumed, he was impressed to see that the air-reared eggs consumed 44% less oxygen than the submerged embryos, in addition to retaining larger egg-yolk reserves. Next, Wells tested the fish's activity levels as they wafted oxygen-laden fluid in their eggs with their gill covers (opercula) and noticed that early in development (7 days after egg release) the water-reared embryos moved their opercula far more than the air-reared eggs. And when the air-reared eggs were returned to water, their metabolic rate and movement increased significantly, ‘Supporting the hypothesis that Kryptolebias marmoratus [mangrove rivulus] embryos use micro-environment manipulation to maintain oxygen uptake,’ the team says. They also calculated the metabolic cost of the opercular movements when the 30-day-old air-reared eggs were returned to water, discovering that the embryos consumed 64% more oxygen than embryos that were more static. And when the team compared the body size and survival of the embryos after they developed into adults, they found no ill effects of the different starts in life, showing that oxygen availability in the earliest life stages had little effect on the fish's long-term development.
The air-reared fish eggs seemed to benefit from their oxygen-rich start in life, developing faster while preserving their limited reserves for use after hatching. And Wright says, ‘Terrestrial rearing is energetically more favourable and, by extension, the energy savings may have provided the selective pressure favouring the evolution of terrestriality’.
