Petra Lenz Publication Summaries

Escape behavior of planktonic copepods in response to hydrodynamic disturbances: high speed video analysis

Edward J. Buskey, Petra H. Lenz and Daniel K. Hartline

Mar. Ecol. Progr. Ser. 235: 135-146 (2002)

Abstract:

Planktonic copepods exhibit rapid escape behavior in response to hydrodynamic disturbances. Small disturbances of brief duration were produced by a piezoelectric transducer moving a small cylinder. The escape responses of free-swimming adult males and females of the copepods Acartia tonsa and A. lilljeborgii were recorded using high-speed video and quantified using computerized motion analysis techniques. Response latency, swimming speed, acceleration and turning rate during escape behavior were measured. Acartia spp. typically responded within 4 msto the hydrodynamic disturbance, giving multiple power strokes of the swimming legs. Each stroke and recovery was of ca. 7 ms duration with maximum speeds often exceeding 500 mm/s and minimum speeds between strokes rarely falling below 100 mm/s. Acceleration during initial escape usually exceeded 100 m/s^2. Escapes often began with rapid reorientation away from the source of the disturbance, with maximum turning rates of about 30 degrees/ms. Significant differences were found between the kinetics of escape responses of adult male and female copepods of each species, with males having greater maximum speeds and accelerations, and females having longer duration jumps. Significant differences were also found between the two species, for both males and females, with A. lilljeborgii exhibiting greater speeds and more rapid acceleration than the smaller A. tonsa.

Mechanoreceptors in calanoid copepods: designed for high sensitivity

Weatherby, T.M. and Lenz, P.H. (2000)

Arthropod Struct. Dev. 29: 275-288.

Article via Science Direct.

Abstract

Mechanoreceptors of the first antennae of the mesopelagic calanoid copepod, Pleuromamma xiphias, are critical for the detection of potential predators. These receptors exceed the physiological performance of other crustacean mechanoreceptors in sensitivity to relative water velocities as well as in frequency response. A study of these receptors was initiated to elucidate structure-function relationships. Morphologically, the receptors resemble arthropod scolopidial organs in the occurrence of a scolopale tube. However, the rigidity of the copepod receptors greatly exceeds that described for other crustaceans and as well as other arthropods. The scolopale tube completely encloses the distal dendrites and is firmly anchored to the cuticle. Microtubules are organized in register and arise from microtubule subfibers associated with crescent-shaped rods that extend from the basal body region to the setal socket. The distal dendrites are filled with a large number of cross-linked microtubules. Termination of the distal dendrites inside the lumen of the setae is gradual with firm anchoring to the cuticle. A likely mechanism for mechanotransduction would involve a linkage between individual microtubules and mechanically-gated channels in the dendritic membrane. The rigidity probably contributes to the high frequency sensitivity, and termination of the dendrite inside the seta rather than at its base (as in insects) increases the overall sensitivity of these receptors.

The need for speed. I. Fast reactions and myelinated axons in copepods

Petra H. Lenz, Daniel K. Hartline and April D. Davis

J. comp. Physiol. A 186: 337-345 (2000)

Full text via JCP

Abstract

A rapid and powerful escape response decreases predation risk in planktonic copepods. Calanoid copepods are sensitive to small and brief hydrodynamic disturbances: they respond with multiple nerve impulses to hydrodynamic disturbances produced by a vibrating sphere. Some species, such as Pleuromamma xiphias and Labidocera madurae, respond with very large spikes (1 to 4 mV), whereas maximum spike heights are an order of magnitude smaller in others, such as Undinula vulgaris and Neocalanus gracilis. A comparative study of the escape responses showed that all species reacted within 10 milliseconds of the initiation of a hydrodynamic stimulus. However, U. vulgaris and N. gracilis had significantly shorter reaction times (minimum reaction times: 1.5 and 1.6 msec) than the other two, P. xiphias (6.6 msec) and L. madurae (3.1 msec). Examination of the first antenna and the central nervous system using transmission electron microscopy revealed extensive myelination of sensory and motor and central axons in the two species with the shorter reaction times. Axons of the other two species resembled typical crustacean unmyelinated fibers. A survey of 20 calanoids revealed that none of the species in two of the more ancient superfamilies possessed myelin, but myelination was present in the species from three more recently evolved superfamilies. Myelin may be a major innovation in copepods, providing increased resistance to predator pressure and allowing penetration and survival in riskier environments.

The need for speed. II. Myelin in calanoid copepods

Tina M. Weatherby, April D. Davis, Daniel K. Hartline and Petra H. Lenz

J. comp. Physiol. A 186: 347-357 (2000)

Full text via JCP

The conduction speed of nerve impulses is greatly increased by myelin, a multilayered membranous sheath surrounding axons. Myelinated axons are ubiquitous among the vertebrates, but relatively rare among invertebrates. Electron microscopy of calanoid copepods using rapid cryofixation techniques revealed the widespread presence of myelinated axons. Myelin sheaths of up to 60 layers were found around both sensory and motor axons of the first antenna and interneurons of the ventral nerve cord. Except at nodes, individual lamellae appeared to be continuous and circular, without seams, as opposed to the spiral structure of vertebrate and annelid myelin. The highly organized myelin was characterized by the complete exclusion of cytoplasm from the intracellular spaces of the cell generating it. In regions of compaction, extracytoplasmic space was also eliminated. Focal or fenestration nodes, rather than circumferential ones, were locally common. Myelin lamellae terminated in stepwise fashion at these nodes, appearing to fuse with the axolemma or adjacent myelin lamellae. As with vertebrate myelin, copepod sheaths are designed to minimize both resistive and capacitive current flow through the internodal membrane, greatly speeding nerve impulse conduction. Copepod myelin differs from that of any other group described, while sharing features of every group.

Rapid jumps and bioluminescence elicited by controlled hydrodynamic stimuli in a mesopelagic copepod, Pleuromamma xiphias

Daniel K. Hartline, Edward J. Buskey and Petra H. Lenz

Biol. Bull. 197: 132-143 (1999)

Actively vertically migrating mesopelagic copepods are preyed upon by a wide variety of fishes and invertebrates. Their responses to predatory attacks include vigorous escape jumps and discharge of bioluminescent material. Escape jumps and bioluminescent discharge in the calanoid copepod, Pleuromamma xiphias were elicited by quantified hydrodynamic disturbances. Brief weak stimuli (peak water velocity 63 ą 21 ?m s-1) elicited weak (peak force 6.5 dynes) propulsive responses ("jumps") and no bioluminescence. Moderate stimuli (1580 ą 780 ?m s-1) produced strong propulsive responses consisting of long trains of coordinated powerstrokes by the four pairs of swimming legs ("kicks"). Peak forces averaged 42 dynes. Strong stimuli (5250 ą 3220 ?m s-1) were required to elicit both a jump and a bioluminescent discharge. In several cases, multiple stimuli were needed to evoke bioluminescence, given the limits on stimulus magnitude imposed by the apparatus. Repeated bioluminescent discharges could be evoked, but this responsiveness waned rapidly. Latencies for the jump response (mean = 13 ms) were considerably shorter than for the accompanying bioluminescent discharge (mean = 56 ms). The higher threshold for eliciting bioluminescent discharge compared to escape jumps suggests that the copepods save this defense mechanism for what is perceived to be a stronger threat.

Reaction times and force production during escape behavior of a calanoid copepod, Undinula vulgaris.

Petra H. Lenz and Daniel K. Hartline

Mar. Biol. 133: 249-258 (1999)

Effective escape behavior contributes to the success of copepods in planktonic communities. The kinematics of the escape was studied in tethered Undinula vulgaris (Calanoida) by analyzing the timing and magnitude of the powerstrokes to a precisely controlled sudden mechanical perturbation in the surrounding water. Copepods responded with rapid swims to water velocities of 36 to 86 um/sec. Reaction times were under 2.5 ms following stimulus onset. The time course of force exerted was complex but reproducible from stimulus to stimulus. Multiple powerstrokes ("kicks") were frequently observed in response to single stimuli. Time intervals of 5 milliseconds were observed between the end of one escape kick and the beginning of the next. U. vulgaris developed maximum forces of 40 to over 100 dynes during a rapid swim. The behavioral reaction times and intervals between multiple responses observed in this calanoid are among the shortest reported in aquatic invertebrates.

[corrected 5/20/99]

Physiological and behavioral studies of escape responses in calanoid copepods

Daniel K. Hartline, Petra H.Lenz, and Christen M. Herren

Mar. Fresh. Behav. Physiol. 27: 199-212 (1996)

Copepods are among the more numerous and diverse of zooplankton groups in aquatic ecosystems. Inhabiting a pelagic environment with little cover, they are subject to intense predation pressure. Thus their abilities to detect and escape from potential predators is a major factor in their success. Owing to their small size (mm), their sensory capabilities have not, until recently, been investigated with the tools of sensory physiology. Much might be learned about copepod survival mechanisms and evolutionary pressures through application of such techniques. In this paper we describe electrophysiological approaches for monitoring sensory discharges from the first antennae of calanoid copepods. Nerve impulses can be recorded extracellularly from both mechanoreceptors and putative chemoreceptors. "Giant" spikes (mV) with unusual characteristics are found in Augaptiloids and Centropagoids, but not more recently diverging calanoid groups. There are two such giant antennal mechanoreceptor units (GAMs) in each antenna. These originate in the sensory setae of each distal tip. They are sensitive to very small (<10 nm) hydrodynamic signals, including abrupt displacements and sinusoidal vibrations. Their frequency range for oscillatory stimuli is unusual for aquatic arthropods, extending up to and above 2 kHz. Behavioral studies in the shallow-water calanoid Labidocera madurae show that rapid escape reactions can be triggered by the same types of disturbances as elicit firing in the GAMs. Sensitivities as low as 4 nm were found at frequencies of ca. 900 Hz. Behavioral sensitivities over a range of frequencies are similar to those measured physiologically and suggest that firing of the GAMs is capable of triggering escape behavior. It may be that even a single nerve impulse can elicit the reaction in these animals.

Mechanoreception in zooplankton first antennae: electrophysiological techniques

Donald V. Gassie, Petra H. Lenz, Jeannette Yen and Daniel K. Hartline

Bulletin of Marine Science 53(1): 96-105 (1993)

We describe methods for delivering calibrated mechanical displacements to antennal mechanoreceptors in zooplankton while simultaneously recording related neural traffic. Mechanosensory neural responses to small water displacements (0.01-1 um) were studied over a wide frequency range (30 to > 3000 Hz). Receptors could be localized and properties (thresholds, phase locking, habituation) examined. These methods have been tested on calanoid copepod first antennae (antennules), but may be suitable for other preparations. Extracellular recordings are made by holding the animal in stainless steel forceps and raising it into a layer of mineral oil, leaving one of the first antennae projecting into the underlying sea water. Nerve impulse traffic is recorded between the forceps and a chlorided silver wire in the seawater. Antennae are stimulated by water displacements produced by a vibrating sphere attached to either an electromagnetic or piezoelectric transducer. A fiberoptic sensor continuously monitors displacement. A computer-controlled waveform generator and amplifier drive the transducer with various frequencies, amplitudes and waveforms. The amplified sensor output and neural activity are digitized for later analysis.

Mechanoreception in marine copepods: electrophysiological studies on the first antennae

Jeannette Yen, Petra H. Lenz, Donald V. Gassie and Daniel K. Hartline

J. Plankton Res. 14(4):495-512 (1992)

Neural activity was recorded extracellularly at the base of the first antenna in 15 marine copepods. Controlled mechanical stimuli were delivered with a vibrator driven by a waveform generator. Many species exhibited responses characterized by a large number of small spikes, while others were characterized by the presence of a small number of large units. Two bay species, Labidocera madurae and Acarfia fossae , exhibited large units that could be easily distinguished from the background activity of smaller units. In these species, the antennal receptors fired short latency (>5 ms) trains of one to several impulses in response to a brief mechanical stimulus and sustained trains to a prolonged sinusoidal stimulus. They were extremely sensitive to small displacements and sensitivity increased with stimulus frequency. The receptors responded to stimuli between 40 and 1000 Hz and receptors required displacement velocities of 20 um s-1 or more to fire. Displacements as small as 10 nm were capable of triggering spikes. With an increase in the amplitude of the displacement, a decrease in the latency and an increase in the number of units recruited and/or firing frequency was recorded. Phase-locking to oscillatory stimuli was observed over a frequency range of 80-500 Hz. Neural activity increased in response to bending of individual setae. Setae appear innervated and structurally constrained to movements in specific directions. These experiments suggest that (i) some copepod setal receptors may be more nearly velocity detectors than purely displacement sensors, (ii) they may be capable of sensing closely spaced stimuli, (iii) the patterns of response may code for intensity and duration of the stimulus, and (iv) receptors may be capable of supplying directional information.