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Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flow in ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics.

Geothermal energy provides an important resource in Antarctic marine ecosystems, exemplified by the recent discovery of large-sized chemosymbiotic vesicomyid bivalves (subfamily Pliocardiinae) in the Southern Ocean. These clams, which we identified as Archivesica s.l. puertodeseadoi, have been reported as dead shells in areas previously covered by Larsen A and B ice shelves (eastern Antarctic Peninsula) and as live animals from active hydrothermal sites in the Kemp Caldera (South Sandwich Arc) at depths of 852–1487 m. Before, A. puertodeseadoi was known only from its type locality in the Argentine Sea, so we considerably extend the range of the species. Observations taken by remotely operated vehicle (ROV) footage show that the clams can live buried in sediment, or epilithically on the surface of rocks in diffuse geothermal flow. Experimental respirometry was conducted at surface pressure on individual bivalves acclimated to either their habitat temperature (4 °C) or elevated temperature (10 °C). The range of standard metabolic rates, from 3.13 to 6.59 (MO2, μmol O2 h−1 g−1 dry tissue mass), is similar to rates measured ex situ for other species in this clade, and rates did not differ significantly between temperature groups. Taken together, these data indicate a range of ecophysiological flexibility for A. puertodeseadoi. Although adapted to a specialist mode of life, this bivalve exploits a relatively broad range of habitats in the Southern Ocean: within sulphidic sediments, epilithically in the presence of diffuse sulphidic flow, or in deep methane-enriched seawater trapped under ice.