The structure and electrical activity of the tentacular apparatus of the ctenophore Mnemiopsis leidyi

Abstract

Ctenophores have garnered considerable interest in evolutionary biology due to molecular phylogenetic studies that have positioned Phylum Ctenophora as the sister taxon to all other animals. Mnemiopsis leidyi, one of the most studied ctenophore species, possesses a complex tentacular apparatus essential for feeding and likely mediating diverse sensory functions. This dissertation focuses on elucidating the morphological and bioelectrical properties of this critical organ system. In Chapter 1, I describe the previous and current state of understanding of this enigmatic organ and provide some background regarding the phylogenetic position of Phylum Ctenophora. In Chapter 2, we present a detailed morphological analysis of the tentacular apparatus, resolving prior ambiguities and proposing an updated model for tentilla dynamics, including growth, distribution, transport, and recycling mechanisms. Chapter 3 explores the ultrastructure of the tentacular bulb, identifying distinct functional regions and anatomical specializations, while also documenting the presence of presumed apoptotic cells that suggest that active cellular remodeling is ongoing. Chapter 4 establishes nine staging criteria for M. leidyi metamorphosis, capturing key morphological transitions in the tentacular apparatus, unexpected mechanisms of tentacle modulation and modification and revealing unexpected reverse developmental activity. Chapter 5 introduces the first extracellular recordings from the tentacular apparatus of M. leidyi, uncovering spontaneous, endogenous rhythmic electrical waves that propagate through the tentacular structure and across the epithelial surface. Lesion experiments reveal that multiple sources are likely to generate and support spontaneous firing, although the tentacular bulb likely acts as a central pacemaker or oscillator that coordinates and drives rhythmicity. Altogether, these related studies resolve longstanding uncertainties in the anatomy of M. leidyi’s tentacular apparatus and provide a structural and functional framework for future studies. My work offers novel insights into signal generation and coordination in this, the most common ctenophore in the Atlantic Basin. This work advances our understanding of the resiliency of the ctenophore nervous system and laying groundwork for future behavioral studies; it may also provide insight into the bases for the enormously invasive activity of this animal in the world’s coastal seas.