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Acidity enhances the effectiveness of active chemical defensive secretions of sea hares, Aplysia californica, against spiny lobsters, Panulirus interruptus

Journal of Comparative Physiology A volume 193, pages 1195–1204 (2007)Cite this article

Abstract

Sea hares such as Aplysia californica, gastropod molluscs lacking a protective shell, can release a purple cloud of chemicals when vigorously attacked by predators. This active chemical defense is composed of two glandular secretions, ink and opaline, both of which contain an array of compounds. This secretion defends sea hares against predators such as California spiny lobsters Panulirus interruptus via multiple mechanisms, one of which is phagomimicry, in which secretions containing feeding chemicals attract and distract predators toward the secretion and away from the sea hare. We show here that ink and opaline are highly acidic, both having a pH of ∼5. We examined if the acidity of ink and opaline affects their phagomimetic properties. We tested behavioral and electrophysiological responses of chemoreceptor neurons in the olfactory and gustatory organs of P. interruptus, to ink and opaline of A. californica within their natural range of pH values, from ∼5 to 8. Both behavioral and electrophysiological responses to ink and opaline were enhanced at low pH, and low pH alone accounted for most of this effect. Our data suggest that acidity enhances the phagomimetic chemical defense of sea hares.

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References

  • Bobkov YV, Ache BW (2003) Calcium sensitivity of a sodium-activated non-selective cation channel in lobster olfactory receptor neurons. J Neurophysiol 90:2928–2940

    PubMed  Article  CAS  Google Scholar 

  • Bobkov YV, Ache BW (2007) Intrinsically bursting olfactory receptor neurons. J Neurophysiol 97:1052–1057

    PubMed  Article  CAS  Google Scholar 

  • Carew TJ, Kandel ER (1977) Inking in Aplysia californica. I. Neural circuit of an all-or-none behavioral response. J Neurophysiol 40:692–707

    PubMed  CAS  Google Scholar 

  • Case J (1964) Properties of the dactyl chemoreceptors of Cancer antennarius Stimpson and C. productus Randall. Biol Bull 127:428–446

    Article  CAS  Google Scholar 

  • Cate HS, Derby CD (2001) Morphology and distribution of setae on the antennules of the Caribbean spiny lobster Panulirus argus reveal new types of bimodal chemo-mechanosensilla. Cell Tissue Res 304:439–454

    PubMed  Article  CAS  Google Scholar 

  • Cimino G, Gavagnin M (eds) (2006) Molluscs: from chemo-ecological study to biotechnological application. Progress in molecular biology. Marine molecular biotechnology, Springer, Berlin

  • Corotto F, Voigt R, Atema A (1992) Spectral tuning of chemoreceptor cells of the third maxilliped of the lobster, Homarus americanus. Biol Bull 183:456–462

    Article  Google Scholar 

  • Derby CD (1989) Physiology of sensory neurons in morphologically identified cuticular sensilla of crustaceans. In: Felgenhauer BE, Watling L, Thistle AB (eds) Functional morphology of feeding and grooming in Crustacea. AA Balkema, Rotterdam, pp 27–47

    Google Scholar 

  • Derby CD (1995) Single unit electrophysiological recording techniques from crustacean chemoreceptor neurons. In: Spielman AI, Brand JG (eds) CRC handbook on experimental cell biology of taste and olfaction: current techniques and protocols. CRC Press, Boca Raton, pp 241–250

    Google Scholar 

  • Derby CD (2000) Learning from spiny lobsters about chemosensory coding of mixtures. Physiol Behav 69:203–209

    PubMed  Article  CAS  Google Scholar 

  • Derby CD, Steullet P, Horner AJ (2001) The sensory basis to feeding behavior in the Caribbean spiny lobster Panulirus argus. Mar Freshw Res 52:1339–1350

    Article  Google Scholar 

  • Faulkner DJ (1992) Chemical defenses in marine molluscs. In: Paul VP (ed) Ecological roles of marine natural products. Comstock, Ithaca, pp 119–163

    Google Scholar 

  • Garm A (2004) Mechanical functions of setae from the mouth apparatus of seven species of decapod crustaceans. J Morphol 260:85–100

    PubMed  Article  Google Scholar 

  • Garm A, Høeg JT (2006) Ultrastructure and functional organization of mouthpart sensory setae of the spiny lobster Panulirus argus: new features of putative mechanoreceptors. J Morphol 267:464–476

    PubMed  Article  Google Scholar 

  • Garm A, Shabani S, Høeg JT, Derby CD (2005) Chemosensory neurons in the mouthparts of the spiny lobsters Panulirus argus and P. interruptus (Crustacea: Decapoda). J Exp Mar Biol Ecol 314:175–186

    Article  Google Scholar 

  • Gillette R, Saeki M, Huang R-C (1991) Defensive mechanisms in notaspid snails: acid humor and evasiveness. J Exp Biol 156:335–347

    Google Scholar 

  • Ginsburg DW, Paul VJ (2001) Chemical defenses in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites. Mar Ecol Prog Ser 215:261–274

    Article  CAS  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 PM, Willows AOD (1999) Defense in sea hares (Gastropoda, Opisthobranchia, Anaspidea): multiple layers of protection from egg to adult. Mar Fresh Behav Physiol 32:147–180

    Google Scholar 

  • Jordt S, Tominaga M, Julius D (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci USA 97:8134–8139

    PubMed  Article  CAS  Google Scholar 

  • Kamio M, Kicklighter C, Ko K-C, Nusnbaum M, Aggio J, Hutchins M, Derby CD (2007) Defense through chemoreception: an l-amino acid oxidase in the ink of sea hares deters predators through their chemical senses. Chem Senses 32:A37

    Google Scholar 

  • Kicklighter CE, Derby CD (2006) Multiple components in ink of the sea hare Aplysia californica are aversive to the sea anemone Anthopleura sola. J Exp Mar Biol Ecol 334:256–268

    Article  Google Scholar 

  • Kicklighter CE, Shabani S, Johnson PM, Derby CD (2005) Sea hares use novel antipredatory chemical defenses. Curr Biol 15:549–554

    PubMed  Article  CAS  Google Scholar 

  • Kinnel RB, Dieter RK, Meinwald J, Van Engen D, Clardy J, Eisner T, Stallard MO, Fenical W (1979) Brasilenyne and cis-dihydro-rhodophytin: antifeedant medium-ring haloethers from a sea hare (Aplysia brasiliana). Proc Natl Acad Sci USA 76:3576–3579

    PubMed  Article  CAS  Google Scholar 

  • Liu D, Zhang Z, Liman ER (2005) Extracellular acid block and acid-enhanced inactivation of the Ca2+-activated cation channel trpm5 involve residues in the S3-S4 and S5-S6 extracellular domains. J Biol Chem 280:20691–20699

    PubMed  Article  CAS  Google Scholar 

  • Nolen TG, Johnson PM (2001) Defensive inking in Aplysia spp.: multiple episodes of ink secretion and the adaptive use of a limited chemical resource. J Exp Biol 204:1257–1268

    PubMed  CAS  Google Scholar 

  • Nolen TG, Johnson PM, Kicklighter CE, Capo T (1995) Ink secretion by the marine snail Aplysia californica enhances its ability to escape from a natural predator. J Comp Physiol A 176:239–254

    Article  Google Scholar 

  • Prince J, Nolen TG, Coelho L (1998) Defensive ink pigment processing and secretion in Aplysia californica: concentration and storage of phycoerythrobilin in the ink gland. J Exp Biol 201:1595–1613

    PubMed  CAS  Google Scholar 

  • Steullet P, Dudar O, Flavus T, Zhou M, Derby CD (2001) Selective ablation of antennular sensilla on the Caribbean spiny lobster Panulirus argus suggests that dual antennular chemosensory pathways mediate odorant activation of searching and localization of food. J Exp Biol 204:4259–4269

    PubMed  CAS  Google Scholar 

  • Steullet P, Kruetzfeldt DR, Hamidani G, Flavus T, Ngo V, Derby CD (2002) Dual antennular chemosensory pathways mediate odor-associative learning and odor discrimination in the Caribbean spiny lobster Panulirus argus. J Exp Biol 205:851–867

    PubMed  Google Scholar 

  • Thompson TE (1960) Defensive adaptations in opisthobranchs. J Mar Biol Assoc UK 39:123–134

    Google Scholar 

  • Thompson TE (1983) Detection of epithelial acid secretions in marine molluscs: review of techniques and new analytical methods. Comp Biochem Physiol 74A:615–621

    Article  Google Scholar 

  • Thompson TE (1986) Investigations of the acidic allomone of the gastropod mollusc Philline aperta by means of ion chromatography and histochemical localization of sulphate and chloride ions. J Moll Stud 52:38–44

    Article  Google Scholar 

  • Thompson TE (1988) Acidic allomones in marine organisms. J Mar Biol Assoc UK 68:499–517

    Article  Google Scholar 

  • Tierney AJ, Atema J (1988) Amino acid chemoreception: effects of pH on receptors and stimuli. J Chem Ecol 14:135–141

    Article  CAS  Google Scholar 

  • Tominaga M, Julius D (2000) Capsaicin receptor in the pain pathway. Jpn J Pharmacol 83:20–24

    PubMed  Article  CAS  Google Scholar 

  • Tritt SH, Byrne JH (1980) Motor controls of opaline secretion in Aplysia californica. J Neurophysiol 43:581–594

    PubMed  CAS  Google Scholar 

  • van Weel PB, Christofferson JP (1966) Electrophysiological studies on perception in the antennulae of certain crabs. Physiol Zool 39:317–325

    Google Scholar 

  • van Weel PB, Correa LH (1967) Electrophysiological responses in the antennulae of Thalamita crenata Latreille and Procambarus clarkii Girard to certain stimuli. Zool Jb Physiol 73:174–185

    Google Scholar 

  • Wägele H, Klussmann-Kolb A (2005) Opisthobranchia (Mollusca, Gastropoda)—more than just slimy slugs. Shell reduction and its implications on defence and foraging. Front Zool 2:3 (BioMed Central)

    PubMed  Article  Google Scholar 

Download references

Acknowledgments

We thank Drs. Paul Katz and Manfred Schmidt for their comments on an earlier draft of the manuscript. Supported by NSF grant IBN-0324435 and 0614685, the Center for Behavioral Neuroscience under the STC Program of the NSF under Agreement No. IBN-9876754 and IBN-0322773, and the Georgia Research Alliance.

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Affiliations

  1. Department of Biology, Brains and Behavior Program, and Center for Behavioral Neuroscience, Georgia State University, Atlanta, GA, 30303, USA

    Shkelzen Shabani, Seymanur Yaldiz, Luan Vu & Charles D. Derby

  2. Department of Biology, Georgia State University, P. O. Box 4010, Atlanta, GA, 30302-4010, USA

    Shkelzen Shabani

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  1. Shkelzen Shabani
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  2. Seymanur Yaldiz
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  3. Luan Vu
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  4. Charles D. Derby
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Correspondence to Shkelzen Shabani.

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Shabani, S., Yaldiz, S., Vu, L. et al. Acidity enhances the effectiveness of active chemical defensive secretions of sea hares, Aplysia californica, against spiny lobsters, Panulirus interruptus . J Comp Physiol A 193, 1195–1204 (2007). https://doi.org/10.1007/s00359-007-0271-5

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  • DOI: https://doi.org/10.1007/s00359-007-0271-5

Keywords

  • Chemoreception
  • Ink
  • Opaline
  • pH
  • Phagomimicry