Escape behavior and escape circuit activation in juvenile crayfish during prey–predator interactions

Abstract

SUMMARY The neural systems that control escape behavior have been studied intensively in several animals, including mollusks, fish and crayfish. Surprisingly little is known, however, about the activation and the utilization of escape circuits during prey–predator interactions. To complement the physiological and anatomical studies with a necessary behavioral equivalent, we investigated encounters between juvenile crayfish and large dragonfly nymphs in freely behaving animals using a combination of high-speed video-recordings and measurements of electric field potentials. During attacks, dragonfly nymphs rapidly extended their labium, equipped with short, sharp palps, to capture small crayfish. Crayfish responded to the tactile stimulus by activating neural escape circuits to generate tail-flips directed away from the predator. Tail-flips were the sole defense mechanism in response to an attack and every single strike was answered by tail-flip escape behavior. Crayfish used all three known types of escape tail-flips during the interactions with the dragonfly nymphs. Tail-flips generated by activity in the giant neurons were predominantly observed to trigger the initial escape responses to an attack, but non-giant mediated tail-flips were often generated to attempt escape after capture. Attacks to the front of the crayfish triggered tail-flips mediated either by the medial giant neuron or by non-giant circuitry, whereas attacks to the rear always elicited tail-flips mediated by the lateral giant neuron. Overall, tail flipping was found to be a successful behavior in preventing predation, and only a small percentage of crayfish were killed and consumed.

Animal escapology II: escape trajectory case studies

“…Work using real predators confirms that attacks to the front of the crayfish triggered backwards-directed tail-flips mediated either by the medial giant neuron or by non-giant circuitry, whereas attacks to the rear elicited upwards-directed tail-flips mediated by the lateral giant neurons (Herberholz et al, 2004). In all these cases, the swimming trajectory in the vertical plane is mainly determined by the direction of the propulsive thrust generated by the tail flip.…”

“…Non giant-fibre escapes with longer latencies were also observed as a reaction to threats that develop gradually (in P. Domenici, J. M. Blagburn and J. P. Bacon crayfish P. clarkii) (Wine and Krasne, 1972;Edwards et al, 1999), and can result in straight escape, pitching or even somersaulting (in crayfish Cherax destructor) (Cooke and Macmillan, 1985). The longer latencies for non-giant escapes are more variable and have been attributed to the 'voluntary' nature of the tail-flips in which crayfish make decisions about the direction and angle of the response before the response is executed (Herberholz et al, 2004;Reichert and Wine, 1983;Wine and Krasne, 1972).…”

The Retrograde Spread of Synaptic Potentials and Recruitment of Presynaptic Inputs

“…The short latency of the LG escapes is critical for the animal's survival: when attacked by dragonfly nymphs, crayfish using LGmediated escape tailflips were more successful in avoiding capture than those using non-giant-mediated tailflips that have a slightly longer latency (Herberholz et al, 2004). We conclude that the role of the lateral excitatory network in reducing the latency of an LG-mediated escape is probably more adaptive than preserving spatial resolution for stimuli of this sort.…”

“…Attack by a predator on the crayfish's tailfan directly excites a population of primary sensory afferents that project centrally into the terminal abdominal ganglion (Edwards et al, 1999;Herberholz et al, 2004). Each half of the tailfan is mapped through five major nerves onto the major branches of the dendritic tree of the LG in a somatotopic manner, so that afferents at the center of the attack converge onto the tips of one or two of major branches (Antonsen and Edwards, 2003).…”

Comparing memory-forming capabilities between laboratory-reared and wildLymnaea: learning in the wild, a heritable component of snail memory

“…No significant differences were detected between treatments in other electrophysiological parameters measured (see Materials and methods). Laboratory vs wild snails (Healy and Hurly, 2004;Herberholz et al, 2004;Kim and Diamond, 2002;Martens et al, 2007b;Rundle and Bronmark, 2001;Shors, 2004;Shors, 2006) or environmental enrichment (Berardi et al, 2007;Fischer et al, 2007;Frick et al, 2003;Harburger et al, 2007;Irvine and Abraham, 2005;Martens et al, 2007b) to explain the cognitive variation within and between species. This second hypothesis suggests that the cognitive ability of an organism is dependent on what it experiences during its ontogeny, and it is this ontogenetic adaptation that determines the behavioral fitness of an organism.…”