Prey-Capture Strategies of Fish-Hunting Cone Snails: Behavior, Neurobiology and Evolution

Abstract

The venomous fish-hunting cone snails (Conus) comprise eight distinct lineages evolved from ancestors that preyed on worms. In this article, we attempt to reconstruct events resulting in this shift in food resource by closely examining patterns of behavior, biochemical agents (toxins) that facilitate prey capture and the combinations of toxins present in extant species. The first sections introduce three different hunting behaviors associated with piscivory: 'taser-and-tether', 'net-engulfment' and 'strike-and-stalk'. The first two fish-hunting behaviors are clearly associated with distinct groups of venom components, called cabals, which act in concert to modify the behavior of prey in a specific manner. Derived fish-hunting behavior clearly also correlates with physical features of the radular tooth, the device that injects these biochemical components. Mapping behavior, biochemical components and radular tooth features onto phylogenetic trees shows that fish-hunting behavior emerged at least twice during evolution. The system presented here may be one of the best examples where diversity in structure, physiology and molecular features were initially driven by particular pathways selected through behavior.

Figure 1

The eight putative lineages of fish-hunting cone snails, illustrated using the shells of the type species of each subgenus believed to be fish hunting.

Figure 2

The taser and tether strategy for prey capture. Shown on the left-hand panel is a specimen of Conus catus envenomating its fish prey. The cone snail extends its yellowish proboscis towards the fish (top left panel), and after it strikes the fish (second left panel from top), it immediately begins to retract its proboscis and the fish is tethered through the radular tooth (see text). Within a few seconds, the fish is tetanically paralyzed with very stiff fins (third left panel), and in this state, it is engulfed by the rostrum of the snail, where pre-digestion takes place (bottom left panel). In approximately two hours the snail will regurgitate the scales and the bones of the fish, as well as the one harpoon-like radular tooth that it used for injecting venom; all the softer parts of the envenomated fish go further down into the gut for complete digestion (taken from a video supplied by Professor Jason Biggs, University of Guam). The right-hand panel shows shells of different species and subgenera that have been directly observed to use the taser and tether fish-hunting behavior. The upper right-hand panel shows shells of species of cone snails in the subgenus Pionoconus (see Table I). Top row, left to right: Conus striatus (Oahu, Hawaii); Conus circumcisus (Olango Island, Philippines); Conus stercusmuscarum (Bohol Island, Philippines). Middle row, left to right: Conus consors, form turschi (Bali, Indonesia); Conus catus (Nuku Hiva, Marquesas Islands) and Conus monachus (Marinduque Island, Philippines). Bottom row: Conus striolatus (Cebu Island, Philippines) and Conus magus (Bicol Peninsula, Luzon Island, Philippines). Pionoconus is the subgenus that has most frequently been observed to envenomate their prey by the taser and tether strategy. Lower right-hand panel: cone snail species in other lineages of Conus directly observed to use the taser and tether strategy. Top: Conus bullatus, Textilia clade (Olango Island, Philippines). Middle row, left to right: Conus purpurascens (West Mexico) and Conus ermineus (Senegal, West Africa), both in the Chelyconus clade. Bottom: Conus obscurus, Gastridium clade (Oahu, Hawaii).

Figure 3

The net engulfment strategy. Shown are the two Conus species observed to use the net-hunting strategy, Conus geographus (left panels) and Conus tulipa (right panels). As soon as these species detect a fish, they extend and greatly expand their rostrum towards the fish. Conus tulipa has ciliary processes at the edges of its rostrum. The snails of both species always engulf the fish prey before they inject venom. Unlike the taser and tether strategy shown in Figure 2, they do not extend their proboscis outside the rostrum to envenomate prey. The ability of Conus geographus to engulf fish is in part due to the release of venom components into the water that cause both sensory deprivation and hypoglycemia (see text).

Figure 4

The strike and stalk strategy for prey capture. Shown is a specimen of Conus flavus envenomating its prey. Once the cone snail has detected the presence of a fish, it extends its strikingly striped proboscis and flails it around, resembling the arms of a brittle star. When the tip of the proboscis gets close to the fish, it stings the fish but does not tether it. After envenomating its prey, the snail (which was buried in the top panel) unburies itself and begins to follow the fish. Once the fish is immobilized, the snail engulfs it completely (bottom panel). Two instances of envenomation were observed for Conus flavus. In the first, there was apparently an insufficient amount of venom injected, and the snail followed the fish around for many minutes, but the fish never was completely immobilized. In the second, after envenomation the fish was immobilized quickly upon envenomation and began to tremble and stiffen its musculature. The snail engulfed it from the tail first. These observations suggest that these snails have some components of the lightning-strike cabal (described in the text for the taser and tether strategy).

Figure 5

Diversity of radular teeth in different lineages of fish-hunting cones (reproduced from Tucker & Tenorio, 2009). The radular teeth of the eight type species of piscivorous subgenera are shown. For the subgenera Phasmoconus and Gastridium where there is clearly a heterogeneity in radular tooth morphology, diverse types are shown. A. Conus ermineus (Chelyconus); B. Conus magus (Pionoconus); C. Conus bullatus (Textilia); D. Conus asiaticus (Phasmoconus — not type species); E. Conus radiatus (Phasmoconus); F. Conus geographus (Gastridium); G., H. Conus obscurus (Gastridium— not type species); I. Conus sulcatus (Asprella); J. Conus kinoshitai (Afonsoconus).

Figure 6

Phylogenetic tree. The portion of the Conus phylogenetic tree showing the eight subgenera believed to be fish hunting (in bold type). The subgenera indicated in dark triangles are confirmed to have at least one fish-hunting species from direct observation of envenomation. The triangles with stripes are the three lineages of putative fish-hunting cone snails where there has been no direct observation of prey capture. The white triangles are worm-hunting subgenera. The relationship of the piscivorous Conus lineages to molluskivorous and the most closely related vermivorous subgenera is shown. The numbers shown next to the fish-hunting lineages are the number of species in each lineage directly analyzed for molecular markers; the number in parenthesis is the number of additional species in that lineage estimated by Puillandre et al., 2014; for these additional species, no molecular data was available. For each of the fish-hunting subgenera, the shell of one species is shown: Asprella (Conus sulcocasteneus); Afonsoconus (Conus kinoshitai); Textilia (Conus dusaveli); Pionoconus (Conus floccatus); Embrikena (Conus pergrandis); Gastridium (Conus eldredi); Phasmoconus (Conus blanfordianus); Chelyconus (Conus purpurascens). We also show an example of a species observed to hunt fish in the primarily worm-hunting subgenus Tesseliconus (Conus tessulatus).

Figure 7

Diverse colored proboscis extended to hunt fish. The panels show six species of cone snails that extended their proboscis in response to the presence of a fish. The species shown are: Top panel, left, Conus consors; right, Conus flavus. Middle panel, left, Conus circumcisus; right, Conus monachus. Bottom panel, left, Conus purpurascens; right, Conus tessulatus. Conus consors, Conus circumcisus and Conus monachus are species in the subgenus Pionoconus (see Figures 1 and 6, and Table I). Conus flavus is in the subgenus Phasmoconus, while Conus purpurascens is in the subgenus Chelyconus. Conus tessulatus is not in one of the specialized fish-hunting subgenera; it belongs to the subgenus Tessuliconus, which is primarily worm hunting, but will opportunistically attack fish, although it is often unable to pierce fish skin (see text).