Charles D. Drewes

Escape Reflexes in Earthworms and Other Annelids

Escape or startle reflexes are characteristically seen in many representatives of the Phylum Annelida (segmented worms), a group that comprises the earthworms, aquatic oligochaetes, leeches, and marine bristle or polychaete worms. From the standpoint of defense, the escape reflex represents one of the most important components of a worm’s repertoire of locomotory behavior that, depending on the species, may also include undulating swimming or peristaltic creeping movements. The underlying control and coordination for all of these locomotory movements are carried out by the worm’s central nervous system, which consists of a dorsal brain in anterior segments and a ventral nerve cord, the latter being composed of a chain of segmentally arranged ganglia joined by longitudinal connectives.

Morphallaxis in an aquatic oligochaete, Lumbriculus variegatus: Reorganization of escape reflexes in regenerating body fragments

We describe functional and anatomical correlates of the reorganization of giant nerve fiber-mediated escape reflexes in body fragments of an aquatic oligochaete, Lumbriculus variegatus, a species that reproduces asexually by fragmentation. Since fragments from any axial position always regenerate short heads (seven or eight segments long) and much longer tail sections, segments originating from posterior fragments become transposed along the longitudinal axis and acquire, by morphallaxis, features of escape reflex organization that conform to their new anterior position. Using noninvasive electrophysiological recordings we have quantified, on a day-to-day and a segment-by-segment basis, the reorganization that occurs in sensory field arrangements of the medial (MGF) and lateral (LGF) giant nerve fibers, as well as changes in giant fiber conduction velocity and morphometry. Our results show that (1) posterior fragments, originally subserved by the LGF sensory field gradually become subserved by the MGF sensory field; (2) appropriate increases in the ratio of MGF:LGF cross-sectional area, perimeter, and conduction velocity accompany the reorganization in giant fiber sensory fields; and (3) sensory field reorganization can be repeatedly reversed by additional amputations. These results demonstrate that the functional organization of escape reflexes is highly plastic and that morphallaxis may result from the counterbalance of morphogenic influences localized within the anterior and posterior ends of regenerating body fragments.

Rapid escape reflexes in aquatic oligochaetes: variations in design and function of evolutionarily conserved giant fiber systems

SummaryThis study provides neuroanatomical and electrophysiological evidence that an arrangement of three dorsal giant fibers, functioning as two distinct and dichotomous conduction pathways, has been evolutionarily conserved within the three major orders of aquatic and terrestrial oligochaetes. The medial giant fiber (MGF), activated by afferents of anterior segments, initiates anterior shortening; whereas, the two lateral giant fibers (LGFs), activated in synchrony by afferents of posterior segments, initiate a different response (usually tail withdrawal). Notwithstanding these common features, the design and function of LGF systems differ considerably in aquatic and terrestrial groups. In posterior segments of aquatic species, LGFs are disproportionately larger and conduct faster than MGFs. This contrasts with posterior segments of earthworms in which LGFs are smaller and conduct slower than MGFs.In addition, in aquatic tubificids, a single LGF spike is sufficient to evoke rapid and complete tail withdrawal, whereas a pair of closely-spaced LGF spikes are needed to elicit posterior shortening in earthworms. The graded nature of earthworm escape seems appropriate for worms that burrow in relatively hard substrates and may frequently encounter inanimate stimuli that evoke meaningless giant fiber spiking. On the other hand, the all-or-none nature of the tubificid escape appears advantageous for relatively sedentary worms that are vulnerable to intense predation but reside in aqueous sediments where triggering of giant fiber spikes by non-threatening stimuli is infrequent.Our studies suggest that anatomical and physiological modifications of giant fiber pathways in aquatic and terrestrial worms have occurred during the evolution of oligochaete nervous systems. We hypothesize that differential predation pressures, together with fundamental differences in lifestyle and habitat, have led to this divergence in the structure and function of evolutionarily conserved sets of homologous giant interneurons.

Hindsight and Rapid Escape in a Freshwater Oligochaete

A novel escape reflex involving the posterior end of a freshwater oligochaete worm, Lumbriculus variegatus, is described. Electrophysiological recordings and videotape analysis from submersed, freely behaving worms show that either a moving shadow or sudden decrease in light intensity evokes repetitive spiking in lateral giant nerve fibers (LGFs) and rapid tail withdrawal when the worms posterior end is positioned at the airwater interface, to facilitate gas exchange. Because comparable electrical and behavioral response patterns occur in isolated posterior body fragments, but not in midbody or anterior fragments, we conclude that the LGF shadow-sensitivity is localized in posterior segments. Added support for this idea is provided by electron microscopic observations demonstrating the presence of candidate photoreceptor cells in the epidermis of posterior segments. These cells are invaginated distally to form a cavity (phaosome) filled with microvilli, and resemble the known photoreceptors in anterior s...

Autotomy reflex in a freshwater oligochaete, Lumbriculus variegatus (Clitellata: Lumbriculidae)

A novel apparatus was developed that induced segmental autotomy in the freshwater oligochaete, Lumbriculus variegatus. The apparatus delivered a quantifiable amount of focal compression to the dorsal body surface at a selected site along the worm. This resulted in a rapid and stereotyped autotomy sequence, beginning with formation of a lateral fissure in the body just anterior to the compression site. Formation of the fissure usually occurred 100– 200 ms after the onset of compression. Autotomy readily occurred in the absence of significant longitudinal tension at the autotomy site and in the absence of direct laceration of the body wall. Autotomy culminated in a complete, transverse separation and sealing of anterior and posterior body fragments with no apparent blood loss from either end. There was a direct relationship between the amount of compression and the probability of autotomy in both midbody and tail regions. However, there was a consistently greater probability of autotomy in tail versus midbody regions. Autotomy did not occur if the duration of compression was less than 77 ms. Autotomy responses were suppressed in dose-dependent manner by a 15 min treatment with nicotine prior to compression. In instances where compression just failed to induce autotomy there was no evidence of disruption of impulse conduction in giant nerve fibers. Rapid and clear-cut autotomy, in combination with this worm’s significant capacity for regeneration of lost segments, are adaptively significant strategies for surviving predatory attack.

Assessing sublethal neurotoxicity effects in the freshwater oligochaete, Lumbriculus variegatus

Abstract The sublethal neurotoxic and behavioral effects of five chemicals (4-aminopyridine, cadmium chloride, carbofuran, chloroform and diazinon) were examined in the freshwater oligochaete, Lumbriculus variegatus (Family Lumbriculidae), following short-term exposure by immersion. Noninvasive electrophysiological recordings of touch-evoked medial giant nerve fiber (MGF) spikes were obtained, before and after exposure, using printed circuit board recording grids. Neurotoxic effects included substantial, and reversible, decreases in MGF conduction velocity following exposure to all chemicals, except CdCl 2 . Reversible losses of MGF touch sensitivity occurred with exposure to chloroform and CdCl 2 . Hypersensitivity of the MGF to touch, accompanied by high-frequency spike trains and rebound spikes, occurred with exposure to 4-aminopyridine. Our approach provides a rapid and sensitive means of detecting and differentiating sublethal neurotoxic effects, in vivo, in this cosmopolitan benthic oligochaete.

Helical swimming and body reversal behaviors in Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae)

Two unusual locomotor behaviors (body reversal and helical swimming) are described and related to postembryonic body size in the freshwater oligochaete, Lumbriculus variegatus (Annelida: Clitellata: Lumbriculidae). Both behaviors occur as responses to tactile stimulation when worms are on smooth substrates that offer little or no traction or protection. Body reversal, evoked by touch to anterior segments, involves a stereotyped sequence of bending movements that effectively reverse head and tail positions in about 0.4 s in newly hatched worms and 0.6 s in juvenile and adult worms. Though little net shift in the body center occurs, reversal may optimize body positioning in preparation for swimming away from predatory threat. In contrast to reversal, swimming is evoked by touch to posterior segments and consists of a rapid, rhythmic sequence of helical body waves (frequency ≈9–11 Hz). Waves alternate between clockwise and counterclockwise helical orientations, with posterior passage of each wave providing forward thrust. Swim velocity and wave velocity increase with body size. Though total distance and duration of each swim episode is short (≈1–2 body lengths in < 2 s), swimming may be an important means of predator avoidance in the littoral environment of these worms.

In vivo neurotoxic effects of dieldrin on giant nerve fibers and escape reflex function in the earthworm, Eisenia foetida

Abstract Neurotoxicological effects of dieldrin were assessed in adult earthworms, Eisenia foetida , using noninvasive electrophysiological recordings of escape reflex activity. After 48 hr body surface exposure to aqueous suspensions of dieldrin, dose-dependent reductions in medial and lateral giant nerve fiber conduction velocities were seen within a concentration range of 1.4 to 288 ppm. At a high concentration (288 ppm) the decreases in velocity occurred in as little as 90 min, but at low concentrations decreases in velocity occurred much more gradually. Other physiological and behavioral effects of dieldrin treatment included (i) after-discharges of giant fibers following brief mechanical stimulation, (ii) spontaneous bursts of giant fiber spikes, (iii) reductions in the amplitude of giant fiber-mediated muscle potentials, (iv) tonic spasms involving end-to-end shortening and body stiffening, (v) ataxia, and (vi) reduction in body weight. Thus, the in vivo effects of dieldrin in earthworms are characterized by a diverse and complex set of physiological and behavioral symptoms. Possible mechanisms underlying these effects are discussed in relation to the generally accepted mode of dieldrin action on synaptic transmission.

Rhythmic motor outputs co-ordinating the respiratory movement of the gill plates of Limulus polyphemus

Abstract 1. 1. The rhythmic mechanical activity (respiratory movement) recorded from the gill plates of Limulus polyphemus was compared to the rhythmic electrical activity recorded from the ventral nerves and their branches in an isolated ventral nerve cord preparation. 2. 2. The rhythmic electrical activity is evoked following the termination of stimulation of the ventral nerve cord, and the duration of this activity is directly dependent upon the length of the stimulation. 3. 3. The mechanical and the electrical events occur in a sequential pattern from segment thirteen through segment nine. 4. 4. The mechanical activity of the respiratory movement is a direct result of the rhythmic motor output in the branches of the ventral nerves. 5. 5. Each opisthosomal ganglion, when isolated, is capable of maintaining a rhythmic output similar to the output of the intact ventral nerve cord preparation.

Neurobehavioral specializations for respiratory movements and rapid escape from predators in posterior segments of the tubificid Branchiura sowerbyi

The posterior end of the aquatic oligochaete, Branchiura sowerbyi (Tubificidae) protrudes above the sediments and is specialized to carry out several rhythmic respiratory movements. These include 1) waves of flexion by paired gill filaments on each posterior segment, 2) body undulations, and 3) rectal water pumping. Since execution of these behaviors renders the worms posterior end vulnerable to predation, appropriate neurobehavioral mechanisms have evolved that permit extremely rapid escape of tail segments into the sediments. Some of these mechanisms include 1) highly sensitive sensory apparatus for detecting substrate vibrations, water displacements, or touch, 2) large diameter and rapidly conducting lateral giant nerve fibers, and 3) adequacy of a single lateral giant fiber impulse for evoking an all-or-none longitudinal muscle contraction. The significance of these posterior respiratory and escape reflex specializations are discussed in relation to possible predator foraging strategies.