The Gastropods that Breathe Black Smoke
Deep-sea hydrothermal vents are home to some of the most interesting species in the world, ones that are uniquely adapted to the dark, hot, mineral-rich waters. These self-contained ecosystems have given rise to many gastropods and bivalves of interest to evolutionary biologists like Dr. Julia Sigwart, who has made it her mission to understand how species respond and adapt to environmental perturbations in order that we may better understand and protect them. Dr. Sigwart uses Ocean Optics oxygen probes to measure the metabolic rates of mollusks as a cue to understanding their basic physiology.
Hydrothermal Vents and their Inhabitants
Hydrothermal vents most commonly arise when seawater seeps down between tectonic plates (called a subduction zone), only to be heated by the hot magma below, reemerging as heated water enriched with reduced compounds. As the hot hydrothermal water mixes with near-freezing seawater, sulfide mineral particulate forms, solidifying as they cool, often forming “black smoker” chimneys from black sulfide deposits.
Despite the heat and pressure of this environment, it is often teeming with life, dominated by a select number of species uniquely adapted to the harsh conditions. One inhabitant, the “scaly-foot” gastropod, Chrysomallon squamiferum, has hard, iron-coated scales on its foot, and has been found at only three small but disparate sites in the Indian Ocean. Another, the “hairy vent snail” Alviniconcha marisindica, has a shell covered in spikes and is found at some of the same hydrothermal vents. Both thrive by harnessing chemosymbiosis, deriving their energy and nutrients from symbiotic bacteria. The bacteria themselves are chemoautotrophs, deriving their energy from reactions with chemicals like hydrogen sulfide, methane and hydrogen and synthesizing all necessary organic compounds from carbon dioxide.
These two species, like many gastropods residing near hydrothermal vents, live in “Goldilocks zones” – regions that are not too hot and not too cold, and which offer just the right ocean chemistry. While they often live at temperatures of up to 40 °C, each species has its own unique tolerance for temperature and pH, thus inhabiting adjacent microhabitats on vent chimneys. Previous studies have found the closely related Alviniconcha hesseleri to have a very high metabolism and one of the most efficient symbioses among hydrothermal vent species[i]. Previous research on the anatomy of Chrysomallon squamiferum indicated it has very enlarged respiratory and circulatory systems, which may be adaptations to provide oxygen to its symbionts[ii]. Based on this, a team of scientists set out to determine whether routine metabolism and oxygen demand of Chrysomallon could be even higher than that of Alviniconcha, and to understand the influence of temperature conditions on the oxygen demand in both gastropods.
A Very Deep Dive
To reach the habitats of these deep-sea creatures depends on large-scale oceangoing research vessels equipped with specialized sampling equipment possible only through support from government. This particular expedition used a Japanese government research vessel called the Shinkai 6500, a manned submersible that can dive up to a depth of 6,500 m to study deep-sea environments. It is owned and run by the Japan Agency for Marine-Earth Science and Technology (JAMSTEC) and it is launched from the support vessel R/V Yokosuka, and can accommodate two pilots and one researcher in a space just 2.0 m across (walls are 73.5 mm thick, and made of titanium). Three thick view ports allow some visibility, though samples are generally retrieved using robotic arms. This particular cruise, number YK16-02E, took place from February 4 – March 2 2016, exploring hydrothermal vent fields in the central Indian Ocean.
Methods and Results
Live specimens of Alviniconcha marisindica were collected during four dives of Shinkai 6500 to depths of ~ 2 miles, at Kairei vent field and Edmond vent field; Chrysomallon squamiferum were also collected at Kairei vent field. A total of 125 subjects were measured over the course of the expedition, divided into three temperature groups so as to evaluate the impact of temperature on metabolism. The temperatures used were 24 °C, 16 °C and 10 °C.
Experiments were conducted using a NeoFox oxygen measurement system fitted with a FOSPOR-OR125 oxygen probe. The probe was inserted into a sealed measurement chamber containing a single animal subject, measuring oxygen levels at 1 second intervals. Six probes were used to allow simultaneous measurement of five experimental animals and one control (seawater only). Standard protocols for closed-chamber respirometry were applied, with chambers being placed into a water bath maintained at constant temperature. Use of a sealed chamber allowed the animal only a fixed amount of oxygen, which decreased during the experiment. The rate of decline (mg O2 / time / animal mass) provided an effective estimation for routine metabolism.
Shown here is an example recording of decreasing oxygen in a closed-chamber respirometry experiment by the gastropod Alviniconcha marisindica. Decline from normoxic conditions (100%) to 40% of available oxygen took approximately four hours at 16 °C. The slope of the shaded area selected was used as representative of metabolic rate.
While it is still too early in the data analysis process to draw conclusions about how metabolic rates for the two species compare, the group did find that the scaly-foot gastropod (Chrysomallon) maintains the same rate of oxygen consumption in different temperatures (10° C and 24° C). This is of interest because it defies the conventional wisdom that animals in hydrothermal vents live in very specific “Golidlocks zones” for each species. This is particularly surprising, given that these animals are ectothermic, i.e., their metabolism depends on outside temperature. A temperature range of 10-24°C would be a surprisingly broad range for a scaly foot gastropod to maintain the same activity level. Knowing that the scaly-foot has an enormous muscular heart relative to that of any other snail, it is possible that its highly developed circulatory system may help it to maintain oxygen metabolism in changing conditions.
As the team continues to analyze the data and specimens collected and supplement them with additional studies, the metabolism and adaptability of these amazing creatures in changing conditions will be better understood. Given that each species may exist in only a handful of unique locations across the world, the preservation of those habitats is key. While threatened by the risk of exploration and exploitation for deep-sea mining to extract rare minerals from the vent chimneys, we can only hope that a better understanding and appreciation of their unique metabolism will inspire protection such that we may continue to learn from them forever, and Ocean Optics is proud to be part of that effort.
[i] Childress, J. J., and P. R. Girguis. “The Metabolic Demands of Endosymbiotic Chemoautotrophic Metabolism on Host Physiological Capacities.” Journal of Experimental Biology 214.2 (2010): 312-25. Web.
[ii] Chen, C., et al. “The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’(Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system.” Frontiers in zoology 12.1 (2015): 1.
Special thanks to JAMSTEC for the 2016 photographs of the black smoker, scaly-foot and Shinkai 6500.