Hagfish predatory behaviour and slime defence mechanism

Abstract

Hagfishes (Myxinidae), a family of jawless marine pre-vertebrates, hold a unique evolutionary position, sharing a joint ancestor with the entire vertebrate lineage. They are thought to fulfil primarily the ecological niche of scavengers in the deep ocean. However, we present new footage from baited video cameras that captured images of hagfishes actively preying on other fish. Video images also revealed that hagfishes are able to choke their would-be predators with gill-clogging slime. This is the first time that predatory behaviour has been witnessed in this family, and also demonstrates the instantaneous effectiveness of hagfish slime to deter fish predators. These observations suggest that the functional adaptations and ecological role of hagfishes, past and present, might be far more diverse than previously assumed. We propose that the enduring success of this oldest extant family of fishes over 300 million years could largely be due to their unique combination of functional traits.

Figure 1. Hagfish toothplates and slime pores.

(a) Eptatretus cirrhatus (726 mm TL, ca. 85 total slime pores), arrows show its first five (of 15) prebranchial and last five (of 13) caudal slime pores. ey, eye; fpb, first pair of barbels; spb, second pair of barbels; tpb, third pair of barbels; mo, mouth; sp, slime pores; ga, gill aperture; pcd, pharyngocutaneous duct; te, teeth; prt, posterior row of teeth; art, anterior row of teeth. Scale bar, 4 cm. (b) Protracted and everted dental plate, exposing keratinous teeth, which can grasp prey with biting forces that exceed some gnathostomes of similar size.

Figure 2. Hagfish slime as a defence mechanism against gill-breathing predators.

The seal shark Dalatias licha (a–c) and the wreckfish Polyprion americanus (d–f) attempt to prey on the hagfishes Eptatretus cirrhatus (a–c) and Eptatretus sp.2 (d–f), respectively. (a),(d), First, the predators approach their potential prey. (b),(e), Predators bite or try to swallow the hagfishes, but hagfishes have already projected jets of slime (arrows) into the predators' mouth. The slime secretion took less than 0.4 sec. (c),(f), Choking, the predators release the hagfishes and gag in an attempt to remove slime from their mouth and gill chamber. See Supplementary Video S1 for the full sequence of these events in action, along with other examples (Table 1).

Figure 3. Sequence of events in hagfish predation.

The slender hagfish Neomyxine sp.1 preys on the red bandfish Cepola haastii (see Supplementary Video S2 for the full sequence). The family Cepolidae, represented in the New Zealand region by a single endemic species, is known to have a burrowing behaviour, excavating a hole in a sedimentary bottom and emerging to feed on zooplankton. (a) Several individuals of Neomyxine sp.1 actively search a small area of sediment where a number of C. haastii burrows were observed. (b) Cepola haastii protrudes its head outside of the burrow. (c) Neomyxine sp.1 forces C. haastii out into the water column by invading its burrow. (d) Neomyxine sp.1 enters a burrow and makes contact with the prey. The subsequent intense activity of the posterior portion of the hagfish suggests that it starts to grasp the prey by repeatedly protracting and retracting its pair of bilaterally symmetric dental plates (see Fig. 1b). It then goes through a period of relative inactivity where it is hypothesized that it waits for the prey to die or become incapacitated before extracting it from the burrow. It is possible that during this time lag, the hagfish suffocates its prey by producing slime. (e) Neomyxine sp.1 with its anterior section buried in the sediment creates an overhand knot with its posterior section before extracting the prey. (f) Neomyxine sp.1 withdraws from the burrow with the posterior part of a C. haastii held by its toothplates, then swims away with its prey.