Biol. Bull. 207: 77-79. (October 2004)
© 2004 Marine Biological Laboratory
The Projectile Tooth of a Fish-Hunting Cone Snail: Conus catus Injects Venom Into Fish Prey Using a High-Speed Ballistic Mechanism
Joseph R. Schulz*,
Alex G. Norton and
William F. Gilly
Hopkins Marine Station, Department of Biological Sciences, Stanford University, 120 Ocean View Blvd., Pacific Grove, California 93950
* To whom correspondence should be addressed at Department of Biology M-3, Occidental College, Los Angeles, CA 90041-3314. E-mail: jschulz{at}oxy.edu
Conus catus, a fish-hunting cone snail (Fig. 1A), delivers venom into its prey by means of a single-use radular tooth (Fig. 1B). The venom is composed of a potent mix of bioactive peptides that, when injected into a fish through the hollow harpoon-shaped tooth, causes tetanus of the body musculature, resulting in a rigid paralysis (1). Although peptide toxins in the venom have been extensively studied (2), the biomechanical mechanisms of tooth insertion and venom ejection have not been determined. Anatomical observations have led to the suggestion that the radular tooth is pushed into prey by muscles surrounding the proboscis lumen (3). In this paper we show that the radular tooth is not pushed directly by the muscles of the proboscis but rather is propelled by a high-speed ballistic mechanism.
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Figure 1. Mechanism of prey capture by Conus catus. (A) Left panel: The experimental arrangement for observing prey capture by C. catus (1.8 cm shell length, specimens collected on Kauai island, Hawaii). The proboscis extends down a trough in the recording chamber to sting the fish (F). (B) Right panel: Composite photomicrograph of the anterior and posterior sections of an isolated radular tooth. Most of the ligament (L) trailing from the base of the tooth has been omitted. (C) Left panels: Frames from a high-speed video clip of the feeding sequence (times in milliseconds before and after release of the tooth are indicated in the upper right of each panel). Scale bar, 350 µm. Microscopy employed transmitted light and water-immersion optics. Video was sampled at 1000 frames/s (Redlake Imaging, courtesy of Mark Denny, Stanford University). (C) Right panels: Sketches indicating the position of the radular tooth (white) in the proboscis (medium grey) occupying most of the proboscis lumen (light grey). F in all panels indicates the location of the fish at the end of the trough. An asterisk above the proboscis indicates the location of the radular tooth base. SP indicates the sensory papillae at the tip of the proboscis. Arrowheads indicate the location of the constriction inside the proboscis lumen. Arrows below the proboscis indicate the location of the largest of three barbs on the tooth. L indicates the ligament (dark grey, right panels). A collection of stills from a high-speed video (1000 fps) illustrating radular tooth ejection by Conus catus can be viewed as a video sequence at <www.mbl.edu/BiologicalBulletin/VIDEO/BB.video.html>. The radular tooth ligament flutters inside the proboscis after tooth ejection.
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Small specimens of Conus catus (Hwass, 1792; <3 cm shell length) have a translucent proboscis allowing radular tooth movements to be visualized in situ by using a combination of transmitted-light microscopy with water-immersion optics and high-speed video. Figure 1A illustrates the experimental arrangement. A fish was positioned at the end of a trough where video observations were made. The snail sought the prey by extending its proboscis down a narrow trough in a recording chamber. As the proboscis approaches the fish, hairlike sensory papillae are visible at its tip (Fig. 1C, SP in top panels). Prior to stinging prey, the radular tooth is not held at the end of the proboscis but is positioned with its point 730 µms (about half the length of the tooth) from the end of the proboscis. The tip of the proboscis then contacts the fish, sensing potential prey (Fig. 1C, second panel). The delay between the proboscis first touching the fish and tooth ejection ranged from 240 to 295 ms.
With the proboscis held stationary against the fish, the radular tooth is propelled against a constriction of the proboscis lumen (Fig. 1C, arrowheads in the third panels), presumably by pressurization of the fluid space behind the tooth. The slight movements of the radular tooth against the constriction during this "priming" step peak during the 4–5 ms prior to release of the tooth into the fish (Fig. 2). Priming was a consistent feature with a similar time course in 10 feeding sequences captured by high-speed video.
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Figure 2. Linear incremental movement (parallel to the chamber trough) of the radular tooth between the times indicated and the previous frame (1000 frames per second). 0 indicates the first frame after release of the radular tooth into the fish.
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During the final millisecond, the radular tooth is explosively propelled into the fish (Fig. 1C, fourth panels). This release step propels the base of the tooth (Fig. 1B, asterisk) to the tip of the proboscis, where it is tightly held by a ring of muscles. The minimum velocity of the tooth during release is approximately 3 ms–1, but the actual time course of tooth movement is clearly faster than the maximum recording rate employed (1000 frames per second, shutter speed 1/2000). This extremely rapid event exceeds the maximum velocity (2 ms–1) for discharge of the cnidarian nematocyst (4). Radular tooth release is one of the fastest known prey capture events and has a time course similar to that of the trap jaw response (0.33 to 1 ms) of the ant Odontomachus (5).
Immediately following impalement, the end of the proboscis loses its taper and swells with fluid, especially near the tip where a noticeable bulge appears (Fig. 1C, fourth panels). This fluid, which contains the venom peptides, enters an opening at the base of the tooth and is ejected from both the tip of the tooth and the beginning of the largest radular barb (data not shown and ref. 6,7). Onset of tetanus in the fish prey is seen within 50 ms of impalement.
By gripping the base of the radular tooth, the proboscis is able to retain control of the stung fish prey while retracting. The paralyzed fish is then engulfed whole, thus completing the feeding sequence. The ligament attached to the base of the radular tooth (Fig. 1C, L fourth panels) moves freely in the proboscis lumen following impalement and therefore apparently does not participate in grasping of the impaled tooth by the proboscis (see supplemental material described in the legend to Fig. 1).
The proboscis acts as a hydrostatic skeleton that allows for coordinated movements in the absence of skeletal structures (3). It is unclear how the proboscis generates the pressure necessary to propel the tooth into prey. One possibility is that the muscles of the proboscis contract the fluid-filled lumen to generate pressure. To explore this possibility, the dimensions of extended proboscises (length 9 to 13 mm) were used to estimate the pressure necessary to accelerate the radular tooth by contraction of the proboscis muscles [minimum acceleration (3000 ms–2) x proboscis fluid mass ÷ tooth base surface area = pressure (Pa)]. The minimum pressure necessary was estimated to be 28.2 kPa (0.278 atm). This value falls within the range of the 
10 to 40 kPa recorded as the intra-mantle pressure during escape jetting in the squid Loligo opalecsens (8,9,10), suggesting that it would be feasible for the proboscis muscles of Conus catus to generate the necessary pressure. Although coordinated contraction of the proboscis muscles was not noted during any of the recorded feeding sequences, the radular tooth moves only 1.4 mm during the final millisecond (Fig. 2), so these contractions may be slight. This differs considerably from escape jetting in squid in which mantle contractions are obvious because water mass within the mantle is lost as thrust. Generation of the necessary pressure within the snail’s proboscis may also involve contraction of the longitudinal muscles of the proboscis, and these would be more difficult to visualize.
In addition to retaining the radular tooth prior to the release step, the constriction of the proboscis lumen may also aid in the acceleration of the tooth by releasing elastic energy as the base of the tooth passes the stretched constriction. Further analysis of the tissues in this region of the proboscis will be required to determine whether this mechanism is possible.
Conus catus has evolved an effective biomechanical means of tooth ejection based on a ballistic prime-and-release mechanism. This mechanism probably involves contraction of the proboscis muscles to propel the radular tooth into unsuspecting prey and, in combination with a potent mix of venom peptides, makes this cone snail a highly effective predator of fast-moving prey.
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Acknowledgments
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We thank M. Denny, W.M. Kier, and an anonymous reviewer for valuable advice, M. O’Donnell for assistance with high-speed video; and A. J. Kohn for critical reading of an earlier version of this manuscript. This work was supported by a Kirschstein NIH postdoctoral fellow 5F32NS43938 (J.R.S.) and NSF grant IBN-0131788 (W.F.G.).
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Footnotes
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Received 28 April 2004; accepted 19 July 2004.
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