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Tuning of chemoreceptor cells of the second antenna of the American lobster (Homarus americanus) with a comparison of four of its other chemoreceptor organs

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Summary

  1. 1.

    We determined the spectral tuning properties of 47 chemoreceptor cells of the antenna of Homarus americanus to amino acids and other compounds. Tests with 17 single compounds at 10-4 M showed 40 of 47 cells responded best to hydroxyproline, 4 cells to taurine and 3 cells to betaine. Mean tuning breadth (H-metric) doubled with 10 fold increase in concentration.

  2. 2.

    In hydroxyproline-best cells the mean threshold for hydroxyproline (Hyp) was found between 10-7 M and 10-8 M. An equimolar mixture of the 17 compounds generated a shallower stimulus-response function with thresholds similar to Hyp function (mixture suppression). Hyp-best cells were relatively narrowly tuned, often with arginine or leucine as second best stimuli.

  3. 3.

    Thus, physiologically the second antenna of H. americanus is a major chemoreceptor organ. It is more than any of the 5 chemoreceptor organs studied so far dominated by a single best-cell type (Hyp). Receptor cell composition of antennae resembles that of antennules more than legs or maxillipeds. Hyp-best cells in antennae and lateral antennules have similar tuning spectra.

  4. 4.

    Our cell tuning studies argue for independent receptors for all amino acids tested. We conclude that diversity of receptor cell tuning is created by cell-specific blends of receptors. At the organ level, differences in organ tuning result from different blends of receptor cells.

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References

  • Ache BW (1982) Chemoreception and thermoreception. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, vol 3. Neurobiology: Structure and function. Academic Press, New York, pp 369–398

    Google Scholar 

  • Atema J (1977) Functional separation of smell and taste in fish and Crustacea. In: Le Magnen J, MacLeod P (eds) Olfaction and taste VI. Information Retrieval Ltd, London, pp 165–174

    Google Scholar 

  • Atema J (1980) Smelling and tasting underwater. Oceanus 23:4–18

    Google Scholar 

  • Atema J (1985) Chemoreception in the sea: adaptations of chemoreceptors and behavior to aquatic stimulus conditions. Soc Exp Biol Symp 39:387–423

    Google Scholar 

  • Atema J (1988) Distribution of chemical stimuli. In: Atema J, Popper AN, Fay RR, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 29–56

    Google Scholar 

  • Atema J, Borroni PF, Johnson BR, Voigt R, Handrich LS (1989) Adaptation and mixture interactions in chemoreceptor cells: mechanisms for diversity and contrast enhancement. In: Laing DL, Cain W, McBride R, Ache BW (eds) Perception of complex smells and tastes. Academic Press, Sydney, NSW, pp 83–100

    Google Scholar 

  • Bauer U, Dudel J, Hatt H (1981) Characteristics of single chemoreceptive units sensitive to amino acids and related substances in the crayfish leg. J Comp Physiol 144:67–74

    Google Scholar 

  • Borroni PF, Handrich LS, Atema J (1986) The role of narrowly tuned taste cell populations in lobster (Homarus americanus) feeding behavior. Behav Neurosci 100:206–212

    Google Scholar 

  • Bruch RC, Rulli RD (1988) Ligand binding specificity of a neutral L-amino acid olfactory receptor. Comp Biochem Physiol 918:535–540

    Google Scholar 

  • Caprio J, Dudek J, Robinson JJ (1989) Electro-olfactogram and multiunit olfactory receptor responses to binary and trinary mixtures of amino acids in the channel catfish, Ictalurus punctatus. J Gen Physiol 93:245–262

    Google Scholar 

  • Carr WES, Derby CD (1986) Behavioral chemoattractants for the shrimp, Palaemontes pugio: identification of active components in food extracts and evidence of synergistic mixture interactions. Chem Senses 11:49–64

    Google Scholar 

  • Carr WES, Netherton JC, Milstead ML (1984) Chemoattractants of the shrimp, Palaemonetes pugio: Variability in responsiveness and the stimulatory capacity of mixtures containing amino acids, quaternary ammonium compounds, purines and other substances. Comp Biochem Physiol 77A:469–474

    Google Scholar 

  • Carter JA, Steele DH (1982) Attraction to and selection of prey by immature lobsters (Homarus americanus). Can J Zool 60:326–336

    Google Scholar 

  • Case J, Gwilliam GF (1961) Amino acid sensitivity of the dactyl chemoreceptors of Carcinides maenas. Biol Bull 127:428–446

    Google Scholar 

  • Coburn CA, Voigt R, Atema J (1988) High ammonium background does not affect response function of narrowly tuned chemoreceptor cells. Biol Bull 175:304–305

    Google Scholar 

  • Corotto F, Voigt R, Atema J (1992) Spectral tuning of chemoreceptor cells on the third maxilliped of the lobster, Homarus americanus. Biol Bull 183: (in press)

  • Daniel PC, Derby CD (1991) Chemosensory responses to mixtures: A model based on composition of receptor cell types. Physiol Behav 49:581–589

    Google Scholar 

  • Derby CD (1982) Structure and function of cuticular sensilla of the lobster Homarus americanus. J Crust Biol 2:1–21

    Google Scholar 

  • Derby CD, Ache BW (1984) Electrophysiological identification of the stimulatory and interactive components of a complex odorant. Chem Senses 9:201–218

    Google Scholar 

  • Derby CD, Atema J (1982) The function of chemo- and mechanoreceptors in lobster (Homarus americanus) feeding behaviour. J Exp Biol 98:317–328

    Google Scholar 

  • Derby CD, Atema J (1988) Chemoreceptor cells in aquatic invertebrates: peripheral mechanisms of chemical signal processing in decapod Crustacea. In: Atema J, Popper AN, Fay RR, Tavolga WN (eds) Sensory biology of aquatic animals. Springer, New York, pp 365–385

    Google Scholar 

  • Derby CD, Harpaz S (1988) Physiology of chemoreceptor cells in the legs of the freshwater prawn, Macrobrachium rosenbergii. Comp Biochem Physiol 90A:85–91

    Google Scholar 

  • Devine DV, Atema J (1982) Function of chemoreceptor organs in spatial orientation of the lobster, Homarus americanus: differences and overlap. Biol Bull 163:144–153

    Google Scholar 

  • Fuzessery ZM, Childress J (1975) Comparative chemosensitivity to amino acids and their role in feeding activity of bathypelagic and littoral crustaceans. Biol Bull 149:522–538

    Google Scholar 

  • Fuzessery ZM, Carr WES, Ache BW (1978) Antennular chemosensitivity in the spiny lobster, Panulirus argus: studies of taurine sensitive receptors. Biol Bull 154:226–240

    Google Scholar 

  • Girardot M-N, Derby CD (1988) Neural coding of quality of complex olfactory stimuli in lobsters. J Neuropysiol 60:303–324

    Google Scholar 

  • Gleeson RA, Ache BW (1985) Amino acid suppression of taurine-sensitive chemoreceptor neurons. Brain Res 335:99–107

    Google Scholar 

  • Govind CK, Lang F (1981) Physiological identification and asymmetry of lobster claw closer motoneurones. J Exp Biol 94:329–339

    Google Scholar 

  • Hatt H (1984) Structural requirements of amino acids and related compounds for stimulation of receptors in crayfish walking leg. J Comp Physiol A 155:219–231

    Google Scholar 

  • Johnson BR, Ache BW (1978) Antennular chemosensitivity in the spiny lobster, Panulirus argus: Amino acids as feeding stimuli. Mar Behav Physiol 5:145–157

    Google Scholar 

  • Johnson BR, Atema J (1983) Narrow-spectrum chemoreceptor cells in the antennules of the American lobster, Homarus americanus. Neurosci Letters 41:145–150

    Google Scholar 

  • Johnson BR, Atema J (1986) Chemical stimulants for a component of feeding behavior in the common Gulf weed shrimp, Leander tenuicornis (Say). Biol Bull 170:1–10

    Google Scholar 

  • Johnson BR, Voigt R, Borroni PF, Atema J (1984) Response properties of lobster chemoreceptors: Tuning of primary taste neurons in walking legs. J Comp Physiol A 155:593–604

    Google Scholar 

  • Johnson BR, Merrill CL, Ogle RC, Atema J (1988) Response properties of lobster chemoreceptors: tuning of olfactory neurons sensitive to hydroxy-proline. J Comp Physiol A162:201–211

    Google Scholar 

  • Johnson BR, Voigt R, Merrill CL, Atema J (1991) Across-fiber patterns may contain a sensory code for stimulus intensity. Brain Res Bull 26:327–331

    Google Scholar 

  • Laverack MS (1962) Responses of cuticular sense organs of the lobster Homarus vulgaris (Crustacea). I. Hair-peg organs as watercurrent receptors. Comp Biochem Physiol 5:319–325

    Google Scholar 

  • Lindsey JE (1976) Contact chemoreceptor mechanisms in the California rock lobster, Panulirus interruptus (Randall). Ph D Thesis, University of California, Santa Barbara, California

    Google Scholar 

  • Mackie AM, Adron JW, Grant PT (1980) Chemical nature of feeding stimulants for the juvenile Dover sole, Solea solea (L). J Fish Biol 16:701–708

    Google Scholar 

  • MacMillan DL, Phillips BF, Coyne JA (1992) Further observations on the antennal receptors of rock lobsters and their possible involvement in puerulus stage navigation. Mar Behav Physiol 19:211–225

    Google Scholar 

  • Manahan DT (1990) Adaptations by invertebrate larvae for nutrient acquisition from seawater. Amer Zool 30:147–160

    Google Scholar 

  • McClintock TS, Ache BW (1989) Hyperpolarizing receptor potentials in lobster olfactory receptor cells: implications for transduction and mixture suppression. Chem Senses 14:637–647

    Google Scholar 

  • Merrill CL, Voigt R, Atema J (1993) Reliability of chemoreceptor cell response. I. Intensity coding by pattern and response magnitude. J Comp Physiol A (in press)

  • Michel WC, McClintock TS, Ache BW (1991) Inhibition of lobster olfactory receptor cells by odor-activated potassium conductance. J Neurophysiol 65:446–453

    Google Scholar 

  • Moore PA, Atema J, Gerhardt GA (1991) Fluid dynamics and microscale odor movement in the chemosensory appendages of the lobster, Homarus americanus. Chem Senses 16:663–674

    Google Scholar 

  • Mopper K, Lindroth P (1982) Diel and depth variations in dissolved free amino acids and ammonium in the Baltic Sea determined by shipboard HPLC analysis. Limnol Oceanogr 27:336–347

    Google Scholar 

  • Sandeman DC (1982) Organization of the central nervous system. In: Atwood HL, Sandeman DC (eds) The biology of Crustacea, vol 3. Neurobiology: Structure and function. Academic Press, New York, pp 1–61

    Google Scholar 

  • Schmidt M, Gnatzy W (1987) Contact chemoreceptors on the walking legs of the shore crab, Carcinus maenas. In: Roper SD, Atema J (eds) Taste and Olfaction. Ann NY Acad Sci, pp 589–590

  • Schoonhoven LM (1987) What makes a caterpillar eat? The sensory code underlying feeding behavior. In: Chapman RF, Bernays EA, Stoffolano JG (eds) Perspectives in chemoreception and behavior. Springer, New York, pp 69–97

    Google Scholar 

  • Shepheard P (1974) Chemoreception in the antennule of the lobster, Homarus americanus. Mar Behav Physiol 2:261–273

    Google Scholar 

  • Smith DV, Travers JB (1979) A metric for the breadth of tuning of gustatory neurons. Chem Senses Flavor 4:215–229

    Google Scholar 

  • Spencer M (1986) The innervation and chemical sensitivity of single aesthetasc hairs. J Comp Physiol A158:59–68

    Google Scholar 

  • Tautz J, Masters WM, Aicher B, Markl H (1981) A new type of water vibration receptor on the crayfish Astacus leptodactylus antenna. 1. Sensory physiology. J Comp Physiol 144:533–542

    Google Scholar 

  • Tazaki K (1977) Nervous responses from mechanosensory hairs on the antennal flagellum in the lobster Homarus gammarus. Mar Behav Physiol 5:1–18

    Google Scholar 

  • Tazaki K, Shigenaga Y (1974) Chemoreception in the antenna of the lobster Panulirus japonicus. Comp Biochem Physiol 47A:195–199

    Google Scholar 

  • Tierney AJ, Atema J (1988) Behavioral responses of crayfish (Orconectes virilis and Orconectes rusticus) to chemical feeding stimulants. J Chem Ecol 14:123–133

    Google Scholar 

  • Tierney AJ, Voigt R, Atema J (1988) Response properties of chemoreceptors from the medial antennule of the lobster Homarus americanus. Biol Bull 174:364–372

    Google Scholar 

  • Vedel JP (1985) Cuticular mechanoreception in the antennal flagellum of the rock lobster Palinurus vulgaris. Comp Biochem Physiol 80A:151–158

    Google Scholar 

  • Wegert S, Caprio J (1991) Receptor sites for amino acids in the facial taste system of the channel catfish. J Comp Physiol A 168:201–211

    Google Scholar 

  • Weinstein A, Voigt R, Atema J (1990) Spectral tuning of lobster olfactory cells and their response to defined mixtures and natural food extracts. Chemical Senses 15:651–652

    Google Scholar 

  • Zeil J, Sandeman R, Sandeman D (1985) Tactile localization: The function of active antennal movements in the crayfish Cherax destructor. J Comp Physiol A157:607–617

    Google Scholar 

  • Zimmer-Faust RK, Tyre JE, Michel WC, Case JF (1984) Chemical mediation of appetitive feeding in a marine decapod crustacean: the importance of suppression and synergism. Biol Bull 167:339–353

    Google Scholar 

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  1. Boston University Marine Program, Marine Biological Laboratory, 02543, Woods Hole, MA, USA

    Rainer Voigt & Jelle Atema

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  1. Rainer Voigt
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  2. Jelle Atema
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Voigt, R., Atema, J. Tuning of chemoreceptor cells of the second antenna of the American lobster (Homarus americanus) with a comparison of four of its other chemoreceptor organs. J Comp Physiol A 171, 673–683 (1992). https://doi.org/10.1007/BF00194115

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