Where do the embryos of Riftia pachyptila develop? Pressure tolerances, temperature tolerances, and buoyancy during prolonged embryonic dispersal

The giant vent tubeworm Riftia pachyptila releases slightly buoyant lipid-rich zygotes into the water column, where embryos develop and disperse for 21–25 days before they become ciliated larvae capable of controlling their position in the water column. If embryos rise too rapidly, either from their own buoyancy or by being entrained in a buoyant plume, they could encounter warmer temperatures or lower pressures than the embryos can tolerate. Likewise, if they are entrained among the tubes of the adults or in near-bottom currents, the embryos could encounter warm water and adverse chemical conditions. To determine the range of physiological tolerances for normal development of R. pachyptila, we examined survival of embryos at various combinations of pressure and temperature in the laboratory using small pressure vessels. We also used small incubation chambers deployed in and above tubeworm clusters at our study site on the East Pacific Rise. These served as an in situ comparison for the laboratory data. Temperatures were measured at each incubation site with temperature data loggers. The ambient temperature away from the vents at the study site was 2 °C, and the upper thermal limit for 50% normal development was 6 °C for embryos cultured in the pressure vessels and approximately 7 °C in situ. This limited temperature tolerance defines the embryos physiologically as “cold stenotherms”. In laboratory experiments conducted at 2 °C, embryos developed normally at the near-ambient vent pressure of 238 and also at 170 atm. Cleavage rates at 170 atm were much slower than at the higher pressure, however, suggesting that the embryos were probably near their low-pressure threshold. No development occurred at 100 or at 1 atm. During upward migration, embryos would encounter a pressure of 170 atm at a significantly greater depth (1700 m) than they would encounter a temperature of 6 °C, suggesting that embryonic survival should be pressure limited before temperature becomes a controlling factor. To determine the likelihood that these physiological stresses would be encountered during embryogenesis, we measured flotation rates of zygotes and early embryos. At ambient vent pressure (250 atm) and temperature, the zygotes rose at an average rate of 2 m day−1. As the embryos develop, they consume wax esters and therefore lose some buoyancy, but assuming a constant flotation of 2 m day−1 for 25 days, this would bring the embryos approximately 50 m off the bottom. If embryos were entrained in a buoyant plume however, they would reach a depth of slightly more than 2300 m (230 atm) before the plume becomes neutrally buoyant. In either case, the embryos would remain below the critical depth for normal development. Because development is inhibited at temperatures above 6–7 °C, it is unlikely that embryos are retained in or among the adult tubes.