Heart cockle shells transmit sunlight for photosynthesis using bundled fiber optic cables and condensing lenses

Abstract

AbstractMany animals convergently evolved photosynthetic symbioses, including two clades within the Bivalvia. Giant clams (Tridacninae) gape open to let light irradiate their symbionts, but heart cockles (Fraginae) can stay closed because sunlight passes through transparent windows in their shells. Here, we show that heart cockles (Corculum cardissaandspp., Cardiidae) use intricate biophotonic adaptations to transmit more than 30% of visible sunlight (400-700nm) while transmitting only 12% of potentially harmful UV radiation (300-400nm). Beneath each window, microlenses condense light to penetrate more deeply into the symbiont-rich tissue. In the shell windows, aragonite forms narrow fibrous prisms that are optically co-oriented perpendicularly to the shell surface. These bundled “fiber optic cables’’ project images through the shell with a resolution of >100 lines / mm. Further, parameter sweeps in optical simulations show that the observed size (~1μm wide), morphology (long narrow fibers rather than typical aragonite plates), and orientation (along the c-axis) of the aragonite fibers transmit more light than many other possible morphologies. Heart cockle shell windows are thus: (i) the first instance of fiber optic cable bundles in an organism to our knowledge; (ii) a second evolution of condensing lenses for photosynthesis, as in plant epidermal cells; and (iii) a photonic system that efficiently transmits visible light while protecting photosymbionts from UV radiation. The animals’ soft tissues and the symbionts are therefore protected from predation and light stress.Significance StatementPhotosymbiotic animals face a fundamental problem: they must irradiate their photosymbiotic symbionts without exposing their symbionts, or themselves, to predation and intense UV radiation. Reef-dwelling bivalves called heart cockles evolved an intricate biophotonic solution. Sunlight passes through clear windows in their shell, which are composed of aragonite fiber optic cable bundles and condensing lenses. This arrangement screens out UV radiation and allows the heart cockle to keep its shell closed. These intricate photonic adaptations are a novel solution to the evolutionary challenges of photosymbiosis: harnessing solar power while protecting against light stress and predation.