Journal of Conference Abstracts

Volume 1 Number 2


Sensory Neurobiology of Hydrothermal Vent Shrimp from the Mid-Atlantic Ridge

Steven C. Chamberlain Institute for Sensory Research and Dept. of Bioengineering & Neuroscience,

Syracuse, Univ. Syracuse, NY 13244, USA

Steve_Chamberlain@isr.syr.edu

Barbara-Anne Battelle The Whitney Laboratory, University of Florida, St. Augustine, FL 32086, USA

Erik D. Herzog Department of Biology, University of Virginia, Charlottesville, VA 22903, USA

Robert N. Jinks Institute for Sensory Research and Dept. of Bioengineering & Neuroscience,

Syracuse Univ., Syracuse, NY 13244, USA

Leonard Kass Department of Zoology, University of Maine, Orono, ME 04469, USA

George H. Renninger Biophysics Group, Department of Physics, University of Guelph, Guelph,

Ontario N1G 2W1, Canada

Introduction

Bresiliid shrimp used in this study were collected during RV Atlantis II cruise 129-6/7 using DSV Alvin. They included: Rimicaris exoculata from TAG and Snake Pit; ?Rimicaris (Snake Pit)-the small orange Rimicaris-from Snake Pit; Chorocaris chacei from Snake Pit; Chorocaris fortunata from Lucky Strike; ?Chorocaris(Broken Spur)-possibly Chorocaris fortunata-from Broken Spur; and Alvinocaris markensis from Snake Pit. Animals were fixed for anatomical study both at depth and on deck. Tissue samples from live animals were harvested and frozen for subsequent biochemical analysis. Live animals were used for on board electrophysiological study. We generally found that smaller animals arrived at the surface in better condition than large animals. The small orange ?Rimicaris (Snake Pit) had particularly good viability with a survival rate of 45% after 7 days in cooled (4°C to 6°C) unaerated aquaria. Although we took particular care to collect and fix animals at depth, we subsequently found that the retinal ultrastructure of animals fixed on deck was better preserved except for the mitochondria (O'Neill et al., 1995). We conclude that the divalent cations unavoidably contaminating our fixation solutions from ambient seawater caused the ultrastructural disruption we observed.

Vision

Following the initial discovery of the dorsal eye in R. exoculata (Van Dover et al., 1989; Pelli and Chamberlain, 1989), the investigation of vision in these shrimp was our primary goal. We were unable to record electrical visual responses to light from R. exoculata, C. chacei or ?Rimicaris (Snake Pit). We attribute this to the prior light exposure of the animals during collection rather than to any intrinsic difficulty of recording responses of the visual system, since we were easily able to record EKG responses from the heart and nerve impulses from the antennal nerves as described below. Subsequent efforts by Johnson et al. (1995) using animals collected in darkness suggest that the spectral sensitivity of the electroretinogram may match that measured for the retinal visual pigment (Van Dover et al., 1989).

Hydrothermal vent shrimp that live in swarms on the sides of chimneys, R. exoculata (O'Neill et al., 1995) and ?Rimicaris (Snake Pit) (Nuckley et al., 1996), have enlarged dorsal eyes with two lobes fused anteriorly across the midline. Those that have a more solitary lifestyle, C. chacei (Lakin et al., in prep.), C. fortunata (Kuenzler et al., submitted), ?Chorocaris (Broken Spur), A. markensis (Wharton et al., submitted), have enlarged, forward-facing, anterior eyes. At the cellular level, however, the retinas of all these shrimp except A. markensis (see below) are remarkably similar. A smooth cornea and corneal epidermis devoid of any dioptric structures abuts a massive array of photosensitive membrane formed by the tightly packed rhabdomeral segments of the photoreceptors. Behind the layer of microvillar rhabdom is a layer of white diffusing cells through which the very narrow cylindrical cell bodies of the photoreceptors penetrate to send their axons to the brain. Light-absorbing screening pigment in the photoreceptors is found only in the distal axon below the cell nucleus. Screening pigment cells are reduced to small ovoids along the inner margin of the white diffusing cells. The volume density of microvillar array in the rhabdomeral segments of the photoreceptors ranges from 75% to 85%; much higher than typically found in surface-dwelling invertebrates. Overall these morphological characteristics suggest specialization for the detection of extremely dim light at the expense of imaging capabilities.

A. markensis appears to be a special case. Although the anterior eyes are enlarged and have a prominent layer of white diffusing cells, examination of the retina reveals few if any photoreceptors. Some individuals have eyes completely devoid of photoreceptors while others show a few dozen in an apparent state of degeneration. We interpret these observations to indicate that A. markensis has gone blind because its lifestyle at the base of the mound places it far enough from the light source (the chimney throat) that it was unable to adapt its eye to utilize the extremely low levels of light there, is therefore below the 'quit point', and is thus in the process of losing its retina in successive generations.

We have compared the retinal structure of these hydrothermal vent shrimp with that of prototypic surface-dwelling species, Palaemonetes vulgaris and P. pugio. These two species have stalked, spherical apposition compound eyes for pattern vision. If one supposes that hydrothermal vent shrimp have evolved from ancestors with similar compound eyes, the adaptations can be summarized as follows. The number of photoreceptors and ommatidia are the same; however, each photoreceptor has become much larger and the volume density of photosensitive membrane in the rhabdomeral segment is increased by 5 times or more. The quadripartite cuticular cones are completely absent, and in some cases the cone cells themselves are also absent. The reflecting pigment cells have formed a prominent matte reflecting screen of white diffusing cells behind the photoreceptors which gives the eyes of vent shrimp their distinctive white color; the screening pigment cells which give the eyes of surface-dwelling shrimp their black color have atrophied and moved inward. While the details of these adaptations are different from species to species, the overall pattern is essentially constant.

We find no structural evidence of ongoing cyclic rhabdom shedding or synthesis in the photoreceptors of any of the hydrothermal vent shrimp. Furthermore, the marked hypertrophy of the rhabdomeral segment and atrophy of the rest of the cell surely physically preclude any significant daily turnover of rhabdom. This is the first clear example of animals whose photoreceptors do not show robust daily shedding and synthesis of arrays of light-sensitive membranes (rod and cone disks or microvillar rhabdom), and we believe it is related to the absence of cyclic lighting in the animals' environment (see discussion in O'Neill et al., 1995).

Chemosensation

We made recordings of trains of action potentials from nerve fibers of all three antennal filaments in both R. exoculata and ?Rimicaris (Snake Pit). Most fibers were spontaneously active in excised preparations. Nerves from the antennal filaments contained fibers that responded to a variety of chemical stimuli including mixtures of amino acids and homogenates of bacteria collected from the vents. Some nerve fibers in each filament type showed responses to sodium sulfide; however, fibers in the second antennal nerve responded with trains of action potentials in a graded way to sulfide concentration. The sensitivity of these sulfide responses suggests that these shrimp may be able to sense naturally occurring sulfides in the hydrothermal vent environment. Subsequently, we examined the external morphology of the first and second antennae and observed numerous sensilla that have open pores at their tips and that are each innervated by 10 to 14 sensory dendrites. The density of sensilla on the second antenna of vent shrimp is 4 to 5 times greater than in a typical surface-dwelling Caridean shrimp (e.g. P. aztecus), suggesting an enhanced chemosensory capability. See Renninger et al. (1995) for details.

Taction

In addition to responses to chemical stimuli, tactile responses to brushing were recorded from nerve fibers from both the medial and lateral filaments of the first antenna and the second antenna in excised antenna preparations of ?Rimicaris (Snake Pit). One recording from a long second antenna revealed fibers whose activity was sensitive to bending the antenna, but not to brushing it.

Central Nervous System

Morphological, immunocytochemical and neurochemical studies of the central nervous system (CNS) are in progress. Dissections of the CNS in R. exoculata reveal an overall plan typical of decapod crustaceans. Atlases of the brains of R. exoculata (Davis et al., in prep.) and C. chacei (Freyman et al., in prep.) are nearly complete. Immunocytochemical localization of neurons in the brain of R. exoculata with antibodies to neurotransmitters revealed that the photoreceptors and optic nerve fibers may contain histamine and that the optic nerve fibers terminate exclusively in the first optic neuropil (lamina). Neurons with serotonin-like immunoreactivity form a significant part of the olfactory neuropil. Analysis of amino acids in the brains of R. exoculata and P. vulgaris by HPLC showed that the hydrothermal vent species had nearly four times the concentration of gamma-aminobutyric acid (GABA-frequently an inhibitory neurotransmitter) as did the surface species (Curra et al., 1996).

Acknowledgements

Supported in part by NSF grant BNS 91-11248 and NIH grant EY03446.

References

Curra, F.P., Brink, C., Jinks, R.N., Battelle, B.-A. & Chamberlain, S.C., Exp. Biol. `96 (in press) (1996).

Davis, B.R., Jinks, R.N., Battelle, B.-A., Herzog, E.D., Kass, L., Renninger, G.H. & Chamberlain, S.C., J. Morph. (in preparation).

Freyman, T.M., Jinks, R.N., Battelle, B-A., Herzog, E.D., Kass, L., Renninger, G.H. & Chamberlain, S.C., J. Morph. (in preparation).

Johnson, M.L., Shelton, P.M.J., Herring, P.J. & Gardner, S., BRIDGE Newsl. 8, 38-42 (1995).

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Pelli, D.G. & Chamberlain, S.C., Nature 337, 460-461 (1989).

Renninger, G.H., Kass, L., Gleeson, R.A., Van Dover, C.L., B-A. Battelle, Jinks, R.N., Herzog, E.D. & Chamberlain, S.C., Biol. Bull. 1890, 69-76 (1995).

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Wharton, D.N., Jinks, R.N., Battelle, B-A., Herzog, E.D., Kass, L., Renninger, G.H. & Chamberlain, S.C., J.M. B. A. (U.K.) (1996).


FARA-IR Mid-Atlantic Ridge Symposium
19th-22nd June 1996
Reykjavik, Iceland

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