Venom kinematics during prey capture inConus: the biomechanics of a rapid injection system

Abstract

high-speed video. Using light, fluorescence and transmission electron microscopy (TEM), we assessed the composition and function of specific tissues crucial for prey capture. Our integrative experimental approach offers a more comprehensive understanding of this well-developed mechanism in Conus.Kinematic studies of the mollusc-hunting C. pennaceus indicate that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey capable of rapid escape responses. Conus pennaceus SUMMARY Cone snails use an extensile, tubular proboscis as a conduit to deliver a potent cocktail of bioactive venom peptides into their prey. Previous studies have focused mainly on understanding the venom's role in prey capture but successful prey capture requires both rapid physiological and biomechanical mechanisms. Conus catus, a fish-hunting species, uses a high-speed hydraulic mechanism to inject its hollow, spear-like radular tooth into prey. We take an integrated approach to investigating the biomechanics of this process by coupling kinematic studies with morphological analyses. Taking advantage of the opaque venom and translucent proboscis of a mollusc-hunting juvenile cone snail, Conus pennaceus, we have determined that a high-speed prey capture mechanism is not unique to cone species that hunt fish prey. Two morphological structures were found to play crucial roles in this process. A constriction of the lumen near the tip of the proboscis, composed of tall epithelial cells densely packed with microfilaments, impedes forward movement of the radular tooth prior to its propulsion. Proximal to the constriction, a muscular sphincter was found to regulate venom flow and pressurization in the proboscis. In C. pennaceus, the rapid appearance and flushing of venom within the proboscis during prey capture suggests a mechanism involving the delivery of a discrete quantity of venom. The interplay between these elements provides a unique and effective biomechanical injection system for the fast-acting cone snail venom peptides. Supplementary material available online at

Developmental modularity and phenotypic novelty within a biphasic life cycle: morphogenesis of a cone snail venom gland

“…In many neogastropods, the midoesophageal gland is elaborated as the gland of Leiblein, which may manufacture digestive enzymes and even phagocytize food material [32]. The venom gland of cone snails is a pinnacle of specialization for the mid-oesophageal gland, where the ventral module of the developing foregut has become a hollow, spaghetti-shaped organ for synthesizing hyperdiverse neurotoxic peptides that are delivered to prey by a mechanism that is still only partially understood [8]. The developmental process that generates this long, narrow gland in C. lividus corresponds remarkably well with the 'stripping away' hypothesis for evolutionary derivation of the Conus venom gland that Amaudrut [29] proposed over 100 years ago.…”

“…Nevertheless, the feeding specializations of Conus and other conoideans extend well beyond those of most predatory gastropods [5]. Cone snails use a highly modified radular tooth, shaped like a hollow harpoon [6], and a ballistic mechanism [7,8] to inoculate their prey with a cocktail of small peptide neurotoxins that rapidly immobilize the prey (reviewed in [9]). The neurotoxins, which typically block ion channels and neurotransmitter receptors in neuronal cell membranes, and have been extensively studied for potential medical applications [9][10][11], are secreted by a long, narrow venom gland extending from the foregut.…”

Deep Venomics Reveals the Mechanism for Expanded Peptide Diversity in Cone Snail Venom

“…The success of this strategy relies on the deployment of potent toxins targeted to the nervous system and musculature of the prey using a specialized radula tooth (3). This hollow harpoon-like structure delivers venom deep into the prey's flesh, where it can enter the circulatory system and interact with nerves to induce rapid paralysis (4,5). It is not surprising that human envenomations resulting from certain cone snail stings are potentially lethal (e.g.…”

Venom Variation during Prey Capture by the Cone Snail, Conus textile

“…Our analyses of injected venom from a mollusc-hunting cone snail establish that, along with an elaborate venom injection system [13], [28], the composition of prey-injected peptides changes during single feeding events. Further investigations into the physiological effects of the various peptides on their diverse prey, their detailed expression patterns within the venom duct and the biomechanics of venom delivery will help to complete the mechanistic picture of prey capture.…”

“…textile venom ducts indicate that venom peptides are secreted in specific regions along the length of the duct [17], [18], [27] which may explain the compositional differences noted in multiple injections during single feeding events. Studies on the biomechanics of prey capture in the mollusc-hunter, Conus pennaceus , indicate that discrete amounts of venom are injected into prey [28]. First injections might be more prominent in peptides found in regions of the duct proximal to its insertion into the mid-esophagus and later injections composed of peptides found in more distal regions near a large muscular venom bulb connected to the end of the duct.…”